Optics InfoBase > Virtual Journal for Biomedical Optics > Volume 5 > Issue 10 > Page 11148
Fluorescence lifetime endoscopy using TCSPC for the measurement of FRET in live cells
Gilbert O. Fruhwirth, Simon Ameer-Beg, Richard Cook, Timothy Watson, Tony Ng, and Frederic Festy »View Author Affiliations
Gilbert O. Fruhwirth,1,2
Simon Ameer-Beg,1,2
Richard Cook,3
Timothy Watson,3
Tony Ng,1,2
and Frederic Festy3,*
1King’s College London, The Richard Dimbleby Department of Cancer Studies, Division of Cancer, Guy’s Medical School Campus, SE1 1UL, London, United Kingdom
2King’s College London, Randall Division of Cellular and Molecular Biophysics, Guy’s Medical School Campus, SE1 1UL, London, United Kingdom
3King’s College London, Dental Institute, Biomaterials Biomimetics and Biophotonics Research Group, SE1 9RT, London, United Kingdom
*Corresponding author: frederic.festy@kcl.ac.uk
Optics Express, Vol. 18, Issue 11, pp. 11148-11158 (2010)
http://dx.doi.org/10.1364/OE.18.011148
View Full Text Article
Enhanced HTML 
Acrobat PDF (1246 KB)
Abstract
Development of remote imaging for diagnostic purposes has progressed dramatically since endoscopy began in the 1960’s. The recent advent of a clinically licensed intensity-based fluorescence micro-endoscopic instrument has offered the prospect of real-time cellular resolution imaging. However, interrogating protein-protein interactions deep inside living tissue requires precise fluorescence lifetime measurements to derive the Förster resonance energy transfer between two tagged fluorescent markers. We developed a new instrument combining remote fiber endoscopic cellular-resolution imaging with TCSPC-FLIM technology to interrogate and discriminate mixed fluorochrome labeled beads and expressible GFP/TagRFP tags within live cells. Endoscopic-FLIM (e-FLIM) data was validated by comparison with data acquired via conventional FLIM and e-FLIM was found to be accurate for both bright bead and dim live cell samples. The fiber based micro-endoscope allowed remote imaging of 4 µm and 10 µm beads within a thick Matrigel matrix with confident fluorophore discrimination using lifetime information. More importantly, this new technique enabled us to reliably measure protein-protein interactions in live cells embedded in a 3D matrix, as demonstrated by the dimerization of the fluorescent protein-tagged membrane receptor CXCR4. This cell-based application successfully demonstrated the suitability and great potential of this new technique for in vivo pre-clinical biomedical and possibly human clinical applications.
© 2010 OSA
OCIS Codes
(170.2150) Medical optics and biotechnology : Endoscopic imaging
(170.2520) Medical optics and biotechnology : Fluorescence microscopy
ToC Category:
Medical Optics and Biotechnology
History
Original Manuscript: February 3, 2010
Revised Manuscript: March 31, 2010
Manuscript Accepted: April 13, 2010
Published: May 12, 2010
Virtual Issues
Vol. 5, Iss. 10 Virtual Journal for Biomedical Optics
Citation
Gilbert O. Fruhwirth, Simon Ameer-Beg, Richard Cook, Timothy Watson, Tony Ng, and Frederic Festy, "Fluorescence lifetime endoscopy using TCSPC for the measurement of FRET in live cells," Opt. Express 18, 11148-11158 (2010)
http://www.opticsinfobase.org/vjbo/abstract.cfm?URI=oe-18-11-11148
Sort: Author | Year | Journal | Reset
References
- P. Cotton, and C. Williams, Practical gastrointestinal endoscopy (Blackwell Science, 2003).
- K. Suhling, P. M. French, and D. Phillips, “Time-resolved fluorescence microscopy,” Photochem. Photobiol. Sci. 4(1), 13–22 (2005). [CrossRef]
- Z. Papagatsia, A. Tappuni, T. F. Watson, and R. J. Cook, “Single wavelength micro-endoscopy in non-surgical vascular lesion diagnosis & characterization,” J. Microsc. 230(2), 203–211 (2008). [CrossRef] [PubMed]
- R. El-Gazzar, M. Macluskey, and G. R. Ogden, “Evidence for a field change effect based on angiogenesis in the oral mucosa? A brief report,” Oral Oncol. 41(1), 25–30 (2005). [CrossRef]
- F. Festy, S. M. Ameer-Beg, T. Ng, and K. Suhling, “Imaging proteins in vivo using fluorescence lifetime microscopy,” Mol. Biosyst. 3(6), 381–391 (2007). [CrossRef] [PubMed]
- G. McConnell, J. M. Girkin, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, T. Ng, A. Banerjee, T. F. Watson, and R. J. Cook, “Time-correlated single-photon counting fluorescence lifetime confocal imaging of decayed and sound dental structures with a white-light supercontinuum source,” J. Microsc. 225(2), 126–136 (2007). [CrossRef] [PubMed]
- W. Becker, H. Hickl, C. Zander, K. H. Drexhage, M. Sauer, S. Siebert, and J. Wolfrum, “Time-resolved detection and identification of single analyte molecules in microcapillaries by time-correlated single photon counting,” Rev. Sci. Instrum. 70(3), 1835–1841 (1999). [CrossRef]
- T. W. J. Gadella, T. M. Jovin, and R. M. Clegg, “Fluorescence lifetime imaging microscopy (FLIM): Spatial resolution of microstructures on the nanosecond time scale,” Biophys. Chem. 48(2), 221–239 (1993). [CrossRef]
- C. Buranachai, D. Kamiyama, A. Chiba, B. D. Williams, and R. M. Clegg, “Rapid frequency-domain FLIM spinning disk confocal microscope: lifetime resolution, image improvement and wavelet analysis,” J. Fluoresc. 18(5), 929–942 (2008). [CrossRef] [PubMed]
- E. A. Jares-Erijman and T. M. Jovin, “FRET imaging,” Nat. Biotechnol. 21(11), 1387–1395 (2003). [CrossRef] [PubMed]
- T. Förster, “Intermolecular energy migration and fluorescence,” Ann. Phys. 2, 55 (1948). [CrossRef]
- L. Stryer, “Fluorescence energy transfer as a spectroscopic ruler,” Annu. Rev. Biochem. 47(1), 819–846 (1978). [CrossRef] [PubMed]
- T. Ng, A. Squire, G. Hansra, F. Bornancin, C. Prevostel, A. Hanby, W. Harris, D. Barnes, S. Schmidt, H. Mellor, P. I. Bastiaens, and P. J. Parker, “Imaging protein kinase Calpha activation in cells,” Science 283(5410), 2085–2089 (1999). [CrossRef] [PubMed]
- T. Ng, D. Shima, A. Squire, P. I. H. Bastiaens, S. Gschmeissner, M. J. Humphries, and P. J. Parker, “PKCalpha regulates beta1 integrin-dependent cell motility through association and control of integrin traffic,” EMBO J. 18, 3909–3923 (1999). [CrossRef] [PubMed]
- F. S. Wouters and P. I. Bastiaens, “Fluorescence lifetime imaging of receptor tyrosine kinase activity in cells,” Curr. Biol. 9(19), 1127–1130 (1999). [CrossRef] [PubMed]
- F. S. Wouters, P. J. Verveer, and P. I. Bastiaens, “Imaging biochemistry inside cells,” Trends Cell Biol. 11(5), 203–211 (2001). [CrossRef] [PubMed]
- S. Pelet, M. J. R. Previte, and P. T. So, “Comparing the quantification of Forster resonance energy transfer measurement accuracies based on intensity, spectral, and lifetime imaging,” J. Biomed. Opt. 11(3), 034017 (2006). [CrossRef]
- M. Parsons, J. Monypenny, S. M. Ameer-Beg, T. H. Millard, L. M. Machesky, M. Peter, M. D. Keppler, G. Schiavo, R. Watson, J. Chernoff, D. Zicha, B. Vojnovic, and T. Ng, “Spatially distinct binding of Cdc42 to PAK1 and N-WASP in breast carcinoma cells,” Mol. Cell. Biol. 25(5), 1680–1695 (2005). [CrossRef] [PubMed]
- M. Peter and S. M. Ameer-Beg, “Imaging molecular interactions by multiphoton FLIM,” Biol. Cell 96(3), 231–236 (2004). [CrossRef] [PubMed]
- M. Peter, S. M. Ameer-Beg, M. K. Y. Hughes, M. D. Keppler, S. Prag, M. Marsh, B. Vojnovic, and T. Ng, “Multiphoton-FLIM quantification of the EGFP-mRFP1 FRET pair for localization of membrane receptor-kinase interactions,” Biophys. J. 88(2), 1224–1237 (2005). [CrossRef]
- A. Schönle, M. Glatz, and S. W. Hell, “Four-dimensional multiphoton microscopy with time-correlated single-photon counting,” Appl. Opt. 39(34), 6306–6311 (2000). [CrossRef]
- R. R. Duncan, A. Bergmann, M. A. Cousin, D. K. Apps, and M. J. Shipston, “Multi-dimensional time-correlated single photon counting (TCSPC) fluorescence lifetime imaging microscopy (FLIM) to detect FRET in cells,” J. Microsc. 215(1), 1–12 (2004). [CrossRef] [PubMed]
- V. Calleja, S. M. Ameer-Beg, B. Vojnovic, R. Woscholski, J. Downward, and B. Larijani, “Monitoring conformational changes of proteins in cells by fluorescence lifetime imaging microscopy,” Biochem. J. 372(1), 33–40 (2003). [CrossRef] [PubMed]
- J. Requejo-Isidro, J. McGinty, I. Munro, D. S. Elson, N. P. Galletly, M. J. Lever, M. A. A. Neil, G. W. Stamp, P. M. French, P. A. Kellett, J. D. Hares, and A. K. Dymoke-Bradshaw, “High-speed wide-field time-gated endoscopic fluorescence-lifetime imaging,” Opt. Lett. 29(19), 2249–2251 (2004). [CrossRef] [PubMed]
- D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004). [CrossRef] [PubMed]
- I. Munro, J. McGinty, N. Galletly, J. Requejo-Isidro, P. M. P. Lanigan, D. S. Elson, C. Dunsby, M. A. Neil, M. J. Lever, G. W. Stamp, and P. M. French, “Toward the clinical application of time-domain fluorescence lifetime imaging,” J. Biomed. Opt. 10(5), 051403 (2005). [CrossRef] [PubMed]
- S. Kumar, C. Dunsby, P. A. A. De Beule, D. M. Owen, U. Anand, P. M. P. Lanigan, R. K. P. Benninger, D. M. Davis, M. A. Neil, P. Anand, C. Benham, A. Naylor, and P. M. French, “Multifocal multiphoton excitation and time correlated single photon counting detection for 3-D fluorescence lifetime imaging,” Opt. Express 15(20), 12548–12561 (2007). [CrossRef] [PubMed]
- K. Makrogianneli, L. M. Carlin, M. D. Keppler, D. R. Matthews, E. Ofo, A. Coolen, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, and T. Ng, “Integrating receptor signal inputs that influence small Rho GTPase activation dynamics at the immunological synapse,” Mol. Cell. Biol. 29(11), 2997–3006 (2009). [CrossRef] [PubMed]
- S. Prag, M. Parsons, M. D. Keppler, S. M. Ameer-Beg, P. Barber, J. Hunt, A. J. Beavil, R. Calvert, M. Arpin, B. Vojnovic, and T. Ng, “Activated ezrin promotes cell migration through recruitment of the GEF Dbl to lipid rafts and preferential downstream activation of Cdc42,” Mol. Biol. Cell 18(8), 2935–2948 (2007). [CrossRef] [PubMed]
- P. R. Barber, S. M. Ameer-Beg, J. Gilbey, L. M. Carlin, M. Keppler, T. Ng, and B. Vojnovic, “Multiphoton time-domain fluorescence lifetime imaging microscopy: practical application to protein–protein interactions using global analysis,” J. R. Soc. Interface 6(0), 93–105 (2009). [CrossRef]
- H. Morise, O. Shimomura, F. H. Johnson, and J. Winant, “Intermolecular energy transfer in the bioluminescent system of Aequorea,” Biochemistry 13(12), 2656–2662 (1974). [CrossRef] [PubMed]
- E. M. Merzlyak, J. Goedhart, D. Shcherbo, M. E. Bulina, A. S. Shcheglov, A. F. Fradkov, A. Gaintzeva, K. A. Lukyanov, S. Lukyanov, T. W. Gadella, and D. M. Chudakov, “Bright monomeric red fluorescent protein with an extended fluorescence lifetime,” Nat. Methods 4(7), 555–557 (2007). [CrossRef] [PubMed]
- A. J. Vila-Coro, J. M. Rodríguez-Frade, A. Martín De Ana, M. C. Moreno-Ortíz, C. Martínez-A, and M. Mellado, “The chemokine SDF-1alpha triggers CXCR4 receptor dimerization and activates the JAK/STAT pathway,” FASEB J. 13(13), 1699–1710 (1999). [PubMed]
- G. J. Babcock, M. Farzan, and J. Sodroski, “Ligand-independent dimerization of CXCR4, a principal HIV-1 coreceptor,” J. Biol. Chem. 278(5), 3378–3385 (2003). [CrossRef]
- R. Maeda-Mamiya, E. Noiri, H. Isobe, W. Nakanishi, K. Okamoto, K. Doi, T. Sugaya, T. Izumi, T. Homma, and E. Nakamura, “In vivo gene delivery by cationic tetraamino fullerene,” Procs. Nat. Acad. Sci. 107(12), 5339–5344 (2010). [CrossRef]
- C. LoPresti, H. Lomas, M. Massignani, T. Smart, and G. Battaglia, “Polymersomes: nature inspired nanometer sized compartments,” J. Mater. Chem. 19(22), 3576–3590 (2009). [CrossRef]
- H. Lomas, M. Massignani, K. A. Abdullah, I. Canton, C. Lo Presti, S. MacNeil, J. Du, A. Blanazs, J. Madsen, S. P. Armes, A. L. Lewis, and G. Battaglia, “Non-cytotoxic polymer vesicles for rapid and efficient intracellular delivery,” Faraday Discuss. 139, 143–159, discussion 213–228, 419–420 (2008). [CrossRef] [PubMed]
- H. Bar, I. Yacoby, and I. Benhar, “Killing cancer cells by targeted drug-carrying phage nanomedicines,” BMC Biotechnol. 8(1), 37 (2008). [CrossRef] [PubMed]
- T. Y. Lee, C. T. Lin, S. Y. Kuo, D. K. Chang, and H. C. Wu, “Peptide-mediated targeting to tumor blood vessels of lung cancer for drug delivery,” Cancer Res. 67(22), 10958–10965 (2007). [CrossRef] [PubMed]
- C. C. Fjeld, W. T. Birdsong, and R. H. Goodman, “Differential binding of NAD+ and NADH allows the transcriptional corepressor carboxyl-terminal binding protein to serve as a metabolic sensor,” Proc. Natl. Acad. Sci. U.S.A. 100(16), 9202–9207 (2003). [CrossRef] [PubMed]
- A. Cobos-Correa, J. B. Trojanek, S. Diemer, M. A. Mall, and C. Schultz, “Membrane-bound FRET probe visualizes MMP12 activity in pulmonary inflammation,” Nat. Chem. Biol. 5(9), 628–630 (2009). [CrossRef] [PubMed]
Abdullah, K. A.
Ameer-Beg, S. M.
Anand, P.
Anand, U.
Apps, D. K.
Armes, S. P.
Arpin, M.
Babcock, G. J.
Banerjee, A.
Bar, H.
Barber, P.
Barber, P. R.
Barnes, D.
Bastiaens, P. I.
Bastiaens, P. I. H.
Battaglia, G.
Beavil, A. J.
Becker, W.
Benham, C.
Benhar, I.
Benninger, R.
Benninger, R. K. P.
Bergmann, A.
Birdsong, W. T.
Blanazs, A.
Bornancin, F.
Bulina, M. E.
Buranachai, C.
Calleja, V.
Calvert, R.
Canton, I.
Carlin, L. M.
Chang, D. K.
Chernoff, J.
Chiba, A.
Chudakov, D. M.
Clegg, R. M.
Cobos-Correa, A.
Cook, R. J.
Coolen, A.
Cousin, M. A.
Davis, D.
Davis, D. M.
De Beule, P. A. A.
Diemer, S.
Doi, K.
Downward, J.
Drexhage, K. H.
Du, J.
Duncan, R. R.
Dunsby, C.
Dymoke-Bradshaw, A. K.
El-Gazzar, R.
Elson, D.
Elson, D. S.
Farzan, M.
Festy, F.
Fjeld, C. C.
Förster, T.
Fradkov, A. F.
French, P.
French, P. M.
Gadella, T. W.
Gadella, T. W. J.
Gaintzeva, A.
Galletly, N.
Galletly, N. P.
Gilbey, J.
Girkin, J. M.
Glatz, M.
Goedhart, J.
Goodman, R. H.
Gschmeissner, S.
Hanby, A.
Hansra, G.
Hares, J. D.
Harris, W.
Hell, S. W.
Hickl, H.
Homma, T.
Hughes, M. K. Y.
Humphries, M. J.
Hunt, J.
Isobe, H.
Izumi, T.
Jares-Erijman, E. A.
Johnson, F. H.
Jovin, T. M.
Kamiyama, D.
Kellett, P. A.
Keppler, M.
Keppler, M. D.
Kumar, S.
Kuo, S. Y.
Lanigan, P.
Lanigan, P. M. P.
Larijani, B.
Lee, T. Y.
Lever, J.
Lever, M. J.
Lewis, A. L.
Lin, C. T.
Lo Presti, C.
Lomas, H.
LoPresti, C.
Lukyanov, K. A.
Lukyanov, S.
Machesky, L. M.
Macluskey, M.
MacNeil, S.
Madsen, J.
Maeda-Mamiya, R.
Makrogianneli, K.
Mall, M. A.
Marsh, M.
Martín De Ana, A.
Martínez-A, C.
Massignani, M.
Matthews, D. R.
McConnell, G.
McGinty, J.
Mellado, M.
Mellor, H.
Merzlyak, E. M.
Millard, T. H.
Monypenny, J.
Moreno-Ortíz, M. C.
Morise, H.
Munro, I.
Nakamura, E.
Nakanishi, W.
Naylor, A.
Neil, M.
Neil, M. A.
Neil, M. A. A.
Ng, T.
Noiri, E.
Ofo, E.
Ogden, G. R.
Okamoto, K.
Owen, D. M.
Papagatsia, Z.
Parker, P. J.
Parsons, M.
Pelet, S.
Peter, M.
Phillips, D.
Prag, S.
Previte, M. J. R.
Prevostel, C.
Reavell, F.
Requejo-Isidro, J.
Rodríguez-Frade, J. M.
Sandison, A.
Sauer, M.
Schiavo, G.
Schmidt, S.
Schönle, A.
Schultz, C.
Shcheglov, A. S.
Shcherbo, D.
Shima, D.
Shimomura, O.
Shipston, M. J.
Siebert, S.
Siegel, J.
Smart, T.
So, P. T.
Sodroski, J.
Squire, A.
Stamp, G.
Stamp, G. W.
Stryer, L.
Sugaya, T.
Suhling, K.
Tadrous, P.
Talbot, C.
Tappuni, A.
Treanor, B.
Trojanek, J. B.
Verveer, P. J.
Vila-Coro, A. J.
Vojnovic, B.
Wallace, A.
Watson, R.
Watson, T. F.
Webb, S.
Williams, B. D.
Winant, J.
Wolfrum, J.
Woscholski, R.
Wouters, F. S.
Wu, H. C.
Yacoby, I.
Zander, C.
Zicha, D.
- H. Lomas, M. Massignani, K. A. Abdullah, I. Canton, C. Lo Presti, S. MacNeil, J. Du, A. Blanazs, J. Madsen, S. P. Armes, A. L. Lewis, and G. Battaglia, “Non-cytotoxic polymer vesicles for rapid and efficient intracellular delivery,” Faraday Discuss. 139, 143–159, discussion 213–228, 419–420 (2008). [CrossRef] [PubMed]
- K. Makrogianneli, L. M. Carlin, M. D. Keppler, D. R. Matthews, E. Ofo, A. Coolen, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, and T. Ng, “Integrating receptor signal inputs that influence small Rho GTPase activation dynamics at the immunological synapse,” Mol. Cell. Biol. 29(11), 2997–3006 (2009). [CrossRef] [PubMed]
- P. R. Barber, S. M. Ameer-Beg, J. Gilbey, L. M. Carlin, M. Keppler, T. Ng, and B. Vojnovic, “Multiphoton time-domain fluorescence lifetime imaging microscopy: practical application to protein–protein interactions using global analysis,” J. R. Soc. Interface 6(0), 93–105 (2009). [CrossRef]
- S. Prag, M. Parsons, M. D. Keppler, S. M. Ameer-Beg, P. Barber, J. Hunt, A. J. Beavil, R. Calvert, M. Arpin, B. Vojnovic, and T. Ng, “Activated ezrin promotes cell migration through recruitment of the GEF Dbl to lipid rafts and preferential downstream activation of Cdc42,” Mol. Biol. Cell 18(8), 2935–2948 (2007). [CrossRef] [PubMed]
- F. Festy, S. M. Ameer-Beg, T. Ng, and K. Suhling, “Imaging proteins in vivo using fluorescence lifetime microscopy,” Mol. Biosyst. 3(6), 381–391 (2007). [CrossRef] [PubMed]
- G. McConnell, J. M. Girkin, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, T. Ng, A. Banerjee, T. F. Watson, and R. J. Cook, “Time-correlated single-photon counting fluorescence lifetime confocal imaging of decayed and sound dental structures with a white-light supercontinuum source,” J. Microsc. 225(2), 126–136 (2007). [CrossRef] [PubMed]
- M. Parsons, J. Monypenny, S. M. Ameer-Beg, T. H. Millard, L. M. Machesky, M. Peter, M. D. Keppler, G. Schiavo, R. Watson, J. Chernoff, D. Zicha, B. Vojnovic, and T. Ng, “Spatially distinct binding of Cdc42 to PAK1 and N-WASP in breast carcinoma cells,” Mol. Cell. Biol. 25(5), 1680–1695 (2005). [CrossRef] [PubMed]
- M. Peter, S. M. Ameer-Beg, M. K. Y. Hughes, M. D. Keppler, S. Prag, M. Marsh, B. Vojnovic, and T. Ng, “Multiphoton-FLIM quantification of the EGFP-mRFP1 FRET pair for localization of membrane receptor-kinase interactions,” Biophys. J. 88(2), 1224–1237 (2005). [CrossRef]
- M. Peter and S. M. Ameer-Beg, “Imaging molecular interactions by multiphoton FLIM,” Biol. Cell 96(3), 231–236 (2004). [CrossRef] [PubMed]
- V. Calleja, S. M. Ameer-Beg, B. Vojnovic, R. Woscholski, J. Downward, and B. Larijani, “Monitoring conformational changes of proteins in cells by fluorescence lifetime imaging microscopy,” Biochem. J. 372(1), 33–40 (2003). [CrossRef] [PubMed]
- S. Kumar, C. Dunsby, P. A. A. De Beule, D. M. Owen, U. Anand, P. M. P. Lanigan, R. K. P. Benninger, D. M. Davis, M. A. Neil, P. Anand, C. Benham, A. Naylor, and P. M. French, “Multifocal multiphoton excitation and time correlated single photon counting detection for 3-D fluorescence lifetime imaging,” Opt. Express 15(20), 12548–12561 (2007). [CrossRef] [PubMed]
- S. Kumar, C. Dunsby, P. A. A. De Beule, D. M. Owen, U. Anand, P. M. P. Lanigan, R. K. P. Benninger, D. M. Davis, M. A. Neil, P. Anand, C. Benham, A. Naylor, and P. M. French, “Multifocal multiphoton excitation and time correlated single photon counting detection for 3-D fluorescence lifetime imaging,” Opt. Express 15(20), 12548–12561 (2007). [CrossRef] [PubMed]
- R. R. Duncan, A. Bergmann, M. A. Cousin, D. K. Apps, and M. J. Shipston, “Multi-dimensional time-correlated single photon counting (TCSPC) fluorescence lifetime imaging microscopy (FLIM) to detect FRET in cells,” J. Microsc. 215(1), 1–12 (2004). [CrossRef] [PubMed]
- H. Lomas, M. Massignani, K. A. Abdullah, I. Canton, C. Lo Presti, S. MacNeil, J. Du, A. Blanazs, J. Madsen, S. P. Armes, A. L. Lewis, and G. Battaglia, “Non-cytotoxic polymer vesicles for rapid and efficient intracellular delivery,” Faraday Discuss. 139, 143–159, discussion 213–228, 419–420 (2008). [CrossRef] [PubMed]
- S. Prag, M. Parsons, M. D. Keppler, S. M. Ameer-Beg, P. Barber, J. Hunt, A. J. Beavil, R. Calvert, M. Arpin, B. Vojnovic, and T. Ng, “Activated ezrin promotes cell migration through recruitment of the GEF Dbl to lipid rafts and preferential downstream activation of Cdc42,” Mol. Biol. Cell 18(8), 2935–2948 (2007). [CrossRef] [PubMed]
- G. J. Babcock, M. Farzan, and J. Sodroski, “Ligand-independent dimerization of CXCR4, a principal HIV-1 coreceptor,” J. Biol. Chem. 278(5), 3378–3385 (2003). [CrossRef]
- G. McConnell, J. M. Girkin, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, T. Ng, A. Banerjee, T. F. Watson, and R. J. Cook, “Time-correlated single-photon counting fluorescence lifetime confocal imaging of decayed and sound dental structures with a white-light supercontinuum source,” J. Microsc. 225(2), 126–136 (2007). [CrossRef] [PubMed]
- H. Bar, I. Yacoby, and I. Benhar, “Killing cancer cells by targeted drug-carrying phage nanomedicines,” BMC Biotechnol. 8(1), 37 (2008). [CrossRef] [PubMed]
- S. Prag, M. Parsons, M. D. Keppler, S. M. Ameer-Beg, P. Barber, J. Hunt, A. J. Beavil, R. Calvert, M. Arpin, B. Vojnovic, and T. Ng, “Activated ezrin promotes cell migration through recruitment of the GEF Dbl to lipid rafts and preferential downstream activation of Cdc42,” Mol. Biol. Cell 18(8), 2935–2948 (2007). [CrossRef] [PubMed]
- K. Makrogianneli, L. M. Carlin, M. D. Keppler, D. R. Matthews, E. Ofo, A. Coolen, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, and T. Ng, “Integrating receptor signal inputs that influence small Rho GTPase activation dynamics at the immunological synapse,” Mol. Cell. Biol. 29(11), 2997–3006 (2009). [CrossRef] [PubMed]
- P. R. Barber, S. M. Ameer-Beg, J. Gilbey, L. M. Carlin, M. Keppler, T. Ng, and B. Vojnovic, “Multiphoton time-domain fluorescence lifetime imaging microscopy: practical application to protein–protein interactions using global analysis,” J. R. Soc. Interface 6(0), 93–105 (2009). [CrossRef]
- G. McConnell, J. M. Girkin, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, T. Ng, A. Banerjee, T. F. Watson, and R. J. Cook, “Time-correlated single-photon counting fluorescence lifetime confocal imaging of decayed and sound dental structures with a white-light supercontinuum source,” J. Microsc. 225(2), 126–136 (2007). [CrossRef] [PubMed]
- T. Ng, A. Squire, G. Hansra, F. Bornancin, C. Prevostel, A. Hanby, W. Harris, D. Barnes, S. Schmidt, H. Mellor, P. I. Bastiaens, and P. J. Parker, “Imaging protein kinase Calpha activation in cells,” Science 283(5410), 2085–2089 (1999). [CrossRef] [PubMed]
- F. S. Wouters, P. J. Verveer, and P. I. Bastiaens, “Imaging biochemistry inside cells,” Trends Cell Biol. 11(5), 203–211 (2001). [CrossRef] [PubMed]
- F. S. Wouters and P. I. Bastiaens, “Fluorescence lifetime imaging of receptor tyrosine kinase activity in cells,” Curr. Biol. 9(19), 1127–1130 (1999). [CrossRef] [PubMed]
- T. Ng, A. Squire, G. Hansra, F. Bornancin, C. Prevostel, A. Hanby, W. Harris, D. Barnes, S. Schmidt, H. Mellor, P. I. Bastiaens, and P. J. Parker, “Imaging protein kinase Calpha activation in cells,” Science 283(5410), 2085–2089 (1999). [CrossRef] [PubMed]
- T. Ng, D. Shima, A. Squire, P. I. H. Bastiaens, S. Gschmeissner, M. J. Humphries, and P. J. Parker, “PKCalpha regulates beta1 integrin-dependent cell motility through association and control of integrin traffic,” EMBO J. 18, 3909–3923 (1999). [CrossRef] [PubMed]
- C. LoPresti, H. Lomas, M. Massignani, T. Smart, and G. Battaglia, “Polymersomes: nature inspired nanometer sized compartments,” J. Mater. Chem. 19(22), 3576–3590 (2009). [CrossRef]
- H. Lomas, M. Massignani, K. A. Abdullah, I. Canton, C. Lo Presti, S. MacNeil, J. Du, A. Blanazs, J. Madsen, S. P. Armes, A. L. Lewis, and G. Battaglia, “Non-cytotoxic polymer vesicles for rapid and efficient intracellular delivery,” Faraday Discuss. 139, 143–159, discussion 213–228, 419–420 (2008). [CrossRef] [PubMed]
- S. Prag, M. Parsons, M. D. Keppler, S. M. Ameer-Beg, P. Barber, J. Hunt, A. J. Beavil, R. Calvert, M. Arpin, B. Vojnovic, and T. Ng, “Activated ezrin promotes cell migration through recruitment of the GEF Dbl to lipid rafts and preferential downstream activation of Cdc42,” Mol. Biol. Cell 18(8), 2935–2948 (2007). [CrossRef] [PubMed]
- W. Becker, H. Hickl, C. Zander, K. H. Drexhage, M. Sauer, S. Siebert, and J. Wolfrum, “Time-resolved detection and identification of single analyte molecules in microcapillaries by time-correlated single photon counting,” Rev. Sci. Instrum. 70(3), 1835–1841 (1999). [CrossRef]
- S. Kumar, C. Dunsby, P. A. A. De Beule, D. M. Owen, U. Anand, P. M. P. Lanigan, R. K. P. Benninger, D. M. Davis, M. A. Neil, P. Anand, C. Benham, A. Naylor, and P. M. French, “Multifocal multiphoton excitation and time correlated single photon counting detection for 3-D fluorescence lifetime imaging,” Opt. Express 15(20), 12548–12561 (2007). [CrossRef] [PubMed]
- H. Bar, I. Yacoby, and I. Benhar, “Killing cancer cells by targeted drug-carrying phage nanomedicines,” BMC Biotechnol. 8(1), 37 (2008). [CrossRef] [PubMed]
- D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004). [CrossRef] [PubMed]
- S. Kumar, C. Dunsby, P. A. A. De Beule, D. M. Owen, U. Anand, P. M. P. Lanigan, R. K. P. Benninger, D. M. Davis, M. A. Neil, P. Anand, C. Benham, A. Naylor, and P. M. French, “Multifocal multiphoton excitation and time correlated single photon counting detection for 3-D fluorescence lifetime imaging,” Opt. Express 15(20), 12548–12561 (2007). [CrossRef] [PubMed]
- R. R. Duncan, A. Bergmann, M. A. Cousin, D. K. Apps, and M. J. Shipston, “Multi-dimensional time-correlated single photon counting (TCSPC) fluorescence lifetime imaging microscopy (FLIM) to detect FRET in cells,” J. Microsc. 215(1), 1–12 (2004). [CrossRef] [PubMed]
- C. C. Fjeld, W. T. Birdsong, and R. H. Goodman, “Differential binding of NAD+ and NADH allows the transcriptional corepressor carboxyl-terminal binding protein to serve as a metabolic sensor,” Proc. Natl. Acad. Sci. U.S.A. 100(16), 9202–9207 (2003). [CrossRef] [PubMed]
- H. Lomas, M. Massignani, K. A. Abdullah, I. Canton, C. Lo Presti, S. MacNeil, J. Du, A. Blanazs, J. Madsen, S. P. Armes, A. L. Lewis, and G. Battaglia, “Non-cytotoxic polymer vesicles for rapid and efficient intracellular delivery,” Faraday Discuss. 139, 143–159, discussion 213–228, 419–420 (2008). [CrossRef] [PubMed]
- T. Ng, A. Squire, G. Hansra, F. Bornancin, C. Prevostel, A. Hanby, W. Harris, D. Barnes, S. Schmidt, H. Mellor, P. I. Bastiaens, and P. J. Parker, “Imaging protein kinase Calpha activation in cells,” Science 283(5410), 2085–2089 (1999). [CrossRef] [PubMed]
- E. M. Merzlyak, J. Goedhart, D. Shcherbo, M. E. Bulina, A. S. Shcheglov, A. F. Fradkov, A. Gaintzeva, K. A. Lukyanov, S. Lukyanov, T. W. Gadella, and D. M. Chudakov, “Bright monomeric red fluorescent protein with an extended fluorescence lifetime,” Nat. Methods 4(7), 555–557 (2007). [CrossRef] [PubMed]
- C. Buranachai, D. Kamiyama, A. Chiba, B. D. Williams, and R. M. Clegg, “Rapid frequency-domain FLIM spinning disk confocal microscope: lifetime resolution, image improvement and wavelet analysis,” J. Fluoresc. 18(5), 929–942 (2008). [CrossRef] [PubMed]
- V. Calleja, S. M. Ameer-Beg, B. Vojnovic, R. Woscholski, J. Downward, and B. Larijani, “Monitoring conformational changes of proteins in cells by fluorescence lifetime imaging microscopy,” Biochem. J. 372(1), 33–40 (2003). [CrossRef] [PubMed]
- S. Prag, M. Parsons, M. D. Keppler, S. M. Ameer-Beg, P. Barber, J. Hunt, A. J. Beavil, R. Calvert, M. Arpin, B. Vojnovic, and T. Ng, “Activated ezrin promotes cell migration through recruitment of the GEF Dbl to lipid rafts and preferential downstream activation of Cdc42,” Mol. Biol. Cell 18(8), 2935–2948 (2007). [CrossRef] [PubMed]
- H. Lomas, M. Massignani, K. A. Abdullah, I. Canton, C. Lo Presti, S. MacNeil, J. Du, A. Blanazs, J. Madsen, S. P. Armes, A. L. Lewis, and G. Battaglia, “Non-cytotoxic polymer vesicles for rapid and efficient intracellular delivery,” Faraday Discuss. 139, 143–159, discussion 213–228, 419–420 (2008). [CrossRef] [PubMed]
- K. Makrogianneli, L. M. Carlin, M. D. Keppler, D. R. Matthews, E. Ofo, A. Coolen, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, and T. Ng, “Integrating receptor signal inputs that influence small Rho GTPase activation dynamics at the immunological synapse,” Mol. Cell. Biol. 29(11), 2997–3006 (2009). [CrossRef] [PubMed]
- P. R. Barber, S. M. Ameer-Beg, J. Gilbey, L. M. Carlin, M. Keppler, T. Ng, and B. Vojnovic, “Multiphoton time-domain fluorescence lifetime imaging microscopy: practical application to protein–protein interactions using global analysis,” J. R. Soc. Interface 6(0), 93–105 (2009). [CrossRef]
- T. Y. Lee, C. T. Lin, S. Y. Kuo, D. K. Chang, and H. C. Wu, “Peptide-mediated targeting to tumor blood vessels of lung cancer for drug delivery,” Cancer Res. 67(22), 10958–10965 (2007). [CrossRef] [PubMed]
- M. Parsons, J. Monypenny, S. M. Ameer-Beg, T. H. Millard, L. M. Machesky, M. Peter, M. D. Keppler, G. Schiavo, R. Watson, J. Chernoff, D. Zicha, B. Vojnovic, and T. Ng, “Spatially distinct binding of Cdc42 to PAK1 and N-WASP in breast carcinoma cells,” Mol. Cell. Biol. 25(5), 1680–1695 (2005). [CrossRef] [PubMed]
- C. Buranachai, D. Kamiyama, A. Chiba, B. D. Williams, and R. M. Clegg, “Rapid frequency-domain FLIM spinning disk confocal microscope: lifetime resolution, image improvement and wavelet analysis,” J. Fluoresc. 18(5), 929–942 (2008). [CrossRef] [PubMed]
- E. M. Merzlyak, J. Goedhart, D. Shcherbo, M. E. Bulina, A. S. Shcheglov, A. F. Fradkov, A. Gaintzeva, K. A. Lukyanov, S. Lukyanov, T. W. Gadella, and D. M. Chudakov, “Bright monomeric red fluorescent protein with an extended fluorescence lifetime,” Nat. Methods 4(7), 555–557 (2007). [CrossRef] [PubMed]
- C. Buranachai, D. Kamiyama, A. Chiba, B. D. Williams, and R. M. Clegg, “Rapid frequency-domain FLIM spinning disk confocal microscope: lifetime resolution, image improvement and wavelet analysis,” J. Fluoresc. 18(5), 929–942 (2008). [CrossRef] [PubMed]
- T. W. J. Gadella, T. M. Jovin, and R. M. Clegg, “Fluorescence lifetime imaging microscopy (FLIM): Spatial resolution of microstructures on the nanosecond time scale,” Biophys. Chem. 48(2), 221–239 (1993). [CrossRef]
- A. Cobos-Correa, J. B. Trojanek, S. Diemer, M. A. Mall, and C. Schultz, “Membrane-bound FRET probe visualizes MMP12 activity in pulmonary inflammation,” Nat. Chem. Biol. 5(9), 628–630 (2009). [CrossRef] [PubMed]
- Z. Papagatsia, A. Tappuni, T. F. Watson, and R. J. Cook, “Single wavelength micro-endoscopy in non-surgical vascular lesion diagnosis & characterization,” J. Microsc. 230(2), 203–211 (2008). [CrossRef] [PubMed]
- G. McConnell, J. M. Girkin, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, T. Ng, A. Banerjee, T. F. Watson, and R. J. Cook, “Time-correlated single-photon counting fluorescence lifetime confocal imaging of decayed and sound dental structures with a white-light supercontinuum source,” J. Microsc. 225(2), 126–136 (2007). [CrossRef] [PubMed]
- K. Makrogianneli, L. M. Carlin, M. D. Keppler, D. R. Matthews, E. Ofo, A. Coolen, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, and T. Ng, “Integrating receptor signal inputs that influence small Rho GTPase activation dynamics at the immunological synapse,” Mol. Cell. Biol. 29(11), 2997–3006 (2009). [CrossRef] [PubMed]
- R. R. Duncan, A. Bergmann, M. A. Cousin, D. K. Apps, and M. J. Shipston, “Multi-dimensional time-correlated single photon counting (TCSPC) fluorescence lifetime imaging microscopy (FLIM) to detect FRET in cells,” J. Microsc. 215(1), 1–12 (2004). [CrossRef] [PubMed]
- D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004). [CrossRef] [PubMed]
- S. Kumar, C. Dunsby, P. A. A. De Beule, D. M. Owen, U. Anand, P. M. P. Lanigan, R. K. P. Benninger, D. M. Davis, M. A. Neil, P. Anand, C. Benham, A. Naylor, and P. M. French, “Multifocal multiphoton excitation and time correlated single photon counting detection for 3-D fluorescence lifetime imaging,” Opt. Express 15(20), 12548–12561 (2007). [CrossRef] [PubMed]
- S. Kumar, C. Dunsby, P. A. A. De Beule, D. M. Owen, U. Anand, P. M. P. Lanigan, R. K. P. Benninger, D. M. Davis, M. A. Neil, P. Anand, C. Benham, A. Naylor, and P. M. French, “Multifocal multiphoton excitation and time correlated single photon counting detection for 3-D fluorescence lifetime imaging,” Opt. Express 15(20), 12548–12561 (2007). [CrossRef] [PubMed]
- A. Cobos-Correa, J. B. Trojanek, S. Diemer, M. A. Mall, and C. Schultz, “Membrane-bound FRET probe visualizes MMP12 activity in pulmonary inflammation,” Nat. Chem. Biol. 5(9), 628–630 (2009). [CrossRef] [PubMed]
- R. Maeda-Mamiya, E. Noiri, H. Isobe, W. Nakanishi, K. Okamoto, K. Doi, T. Sugaya, T. Izumi, T. Homma, and E. Nakamura, “In vivo gene delivery by cationic tetraamino fullerene,” Procs. Nat. Acad. Sci. 107(12), 5339–5344 (2010). [CrossRef]
- V. Calleja, S. M. Ameer-Beg, B. Vojnovic, R. Woscholski, J. Downward, and B. Larijani, “Monitoring conformational changes of proteins in cells by fluorescence lifetime imaging microscopy,” Biochem. J. 372(1), 33–40 (2003). [CrossRef] [PubMed]
- W. Becker, H. Hickl, C. Zander, K. H. Drexhage, M. Sauer, S. Siebert, and J. Wolfrum, “Time-resolved detection and identification of single analyte molecules in microcapillaries by time-correlated single photon counting,” Rev. Sci. Instrum. 70(3), 1835–1841 (1999). [CrossRef]
- H. Lomas, M. Massignani, K. A. Abdullah, I. Canton, C. Lo Presti, S. MacNeil, J. Du, A. Blanazs, J. Madsen, S. P. Armes, A. L. Lewis, and G. Battaglia, “Non-cytotoxic polymer vesicles for rapid and efficient intracellular delivery,” Faraday Discuss. 139, 143–159, discussion 213–228, 419–420 (2008). [CrossRef] [PubMed]
- R. R. Duncan, A. Bergmann, M. A. Cousin, D. K. Apps, and M. J. Shipston, “Multi-dimensional time-correlated single photon counting (TCSPC) fluorescence lifetime imaging microscopy (FLIM) to detect FRET in cells,” J. Microsc. 215(1), 1–12 (2004). [CrossRef] [PubMed]
- S. Kumar, C. Dunsby, P. A. A. De Beule, D. M. Owen, U. Anand, P. M. P. Lanigan, R. K. P. Benninger, D. M. Davis, M. A. Neil, P. Anand, C. Benham, A. Naylor, and P. M. French, “Multifocal multiphoton excitation and time correlated single photon counting detection for 3-D fluorescence lifetime imaging,” Opt. Express 15(20), 12548–12561 (2007). [CrossRef] [PubMed]
- I. Munro, J. McGinty, N. Galletly, J. Requejo-Isidro, P. M. P. Lanigan, D. S. Elson, C. Dunsby, M. A. Neil, M. J. Lever, G. W. Stamp, and P. M. French, “Toward the clinical application of time-domain fluorescence lifetime imaging,” J. Biomed. Opt. 10(5), 051403 (2005). [CrossRef] [PubMed]
- J. Requejo-Isidro, J. McGinty, I. Munro, D. S. Elson, N. P. Galletly, M. J. Lever, M. A. A. Neil, G. W. Stamp, P. M. French, P. A. Kellett, J. D. Hares, and A. K. Dymoke-Bradshaw, “High-speed wide-field time-gated endoscopic fluorescence-lifetime imaging,” Opt. Lett. 29(19), 2249–2251 (2004). [CrossRef] [PubMed]
- R. El-Gazzar, M. Macluskey, and G. R. Ogden, “Evidence for a field change effect based on angiogenesis in the oral mucosa? A brief report,” Oral Oncol. 41(1), 25–30 (2005). [CrossRef]
- D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004). [CrossRef] [PubMed]
- I. Munro, J. McGinty, N. Galletly, J. Requejo-Isidro, P. M. P. Lanigan, D. S. Elson, C. Dunsby, M. A. Neil, M. J. Lever, G. W. Stamp, and P. M. French, “Toward the clinical application of time-domain fluorescence lifetime imaging,” J. Biomed. Opt. 10(5), 051403 (2005). [CrossRef] [PubMed]
- J. Requejo-Isidro, J. McGinty, I. Munro, D. S. Elson, N. P. Galletly, M. J. Lever, M. A. A. Neil, G. W. Stamp, P. M. French, P. A. Kellett, J. D. Hares, and A. K. Dymoke-Bradshaw, “High-speed wide-field time-gated endoscopic fluorescence-lifetime imaging,” Opt. Lett. 29(19), 2249–2251 (2004). [CrossRef] [PubMed]
- G. J. Babcock, M. Farzan, and J. Sodroski, “Ligand-independent dimerization of CXCR4, a principal HIV-1 coreceptor,” J. Biol. Chem. 278(5), 3378–3385 (2003). [CrossRef]
- F. Festy, S. M. Ameer-Beg, T. Ng, and K. Suhling, “Imaging proteins in vivo using fluorescence lifetime microscopy,” Mol. Biosyst. 3(6), 381–391 (2007). [CrossRef] [PubMed]
- C. C. Fjeld, W. T. Birdsong, and R. H. Goodman, “Differential binding of NAD+ and NADH allows the transcriptional corepressor carboxyl-terminal binding protein to serve as a metabolic sensor,” Proc. Natl. Acad. Sci. U.S.A. 100(16), 9202–9207 (2003). [CrossRef] [PubMed]
- T. Förster, “Intermolecular energy migration and fluorescence,” Ann. Phys. 2, 55 (1948). [CrossRef]
- E. M. Merzlyak, J. Goedhart, D. Shcherbo, M. E. Bulina, A. S. Shcheglov, A. F. Fradkov, A. Gaintzeva, K. A. Lukyanov, S. Lukyanov, T. W. Gadella, and D. M. Chudakov, “Bright monomeric red fluorescent protein with an extended fluorescence lifetime,” Nat. Methods 4(7), 555–557 (2007). [CrossRef] [PubMed]
- D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004). [CrossRef] [PubMed]
- S. Kumar, C. Dunsby, P. A. A. De Beule, D. M. Owen, U. Anand, P. M. P. Lanigan, R. K. P. Benninger, D. M. Davis, M. A. Neil, P. Anand, C. Benham, A. Naylor, and P. M. French, “Multifocal multiphoton excitation and time correlated single photon counting detection for 3-D fluorescence lifetime imaging,” Opt. Express 15(20), 12548–12561 (2007). [CrossRef] [PubMed]
- I. Munro, J. McGinty, N. Galletly, J. Requejo-Isidro, P. M. P. Lanigan, D. S. Elson, C. Dunsby, M. A. Neil, M. J. Lever, G. W. Stamp, and P. M. French, “Toward the clinical application of time-domain fluorescence lifetime imaging,” J. Biomed. Opt. 10(5), 051403 (2005). [CrossRef] [PubMed]
- K. Suhling, P. M. French, and D. Phillips, “Time-resolved fluorescence microscopy,” Photochem. Photobiol. Sci. 4(1), 13–22 (2005). [CrossRef]
- J. Requejo-Isidro, J. McGinty, I. Munro, D. S. Elson, N. P. Galletly, M. J. Lever, M. A. A. Neil, G. W. Stamp, P. M. French, P. A. Kellett, J. D. Hares, and A. K. Dymoke-Bradshaw, “High-speed wide-field time-gated endoscopic fluorescence-lifetime imaging,” Opt. Lett. 29(19), 2249–2251 (2004). [CrossRef] [PubMed]
- E. M. Merzlyak, J. Goedhart, D. Shcherbo, M. E. Bulina, A. S. Shcheglov, A. F. Fradkov, A. Gaintzeva, K. A. Lukyanov, S. Lukyanov, T. W. Gadella, and D. M. Chudakov, “Bright monomeric red fluorescent protein with an extended fluorescence lifetime,” Nat. Methods 4(7), 555–557 (2007). [CrossRef] [PubMed]
- T. W. J. Gadella, T. M. Jovin, and R. M. Clegg, “Fluorescence lifetime imaging microscopy (FLIM): Spatial resolution of microstructures on the nanosecond time scale,” Biophys. Chem. 48(2), 221–239 (1993). [CrossRef]
- E. M. Merzlyak, J. Goedhart, D. Shcherbo, M. E. Bulina, A. S. Shcheglov, A. F. Fradkov, A. Gaintzeva, K. A. Lukyanov, S. Lukyanov, T. W. Gadella, and D. M. Chudakov, “Bright monomeric red fluorescent protein with an extended fluorescence lifetime,” Nat. Methods 4(7), 555–557 (2007). [CrossRef] [PubMed]
- I. Munro, J. McGinty, N. Galletly, J. Requejo-Isidro, P. M. P. Lanigan, D. S. Elson, C. Dunsby, M. A. Neil, M. J. Lever, G. W. Stamp, and P. M. French, “Toward the clinical application of time-domain fluorescence lifetime imaging,” J. Biomed. Opt. 10(5), 051403 (2005). [CrossRef] [PubMed]
- J. Requejo-Isidro, J. McGinty, I. Munro, D. S. Elson, N. P. Galletly, M. J. Lever, M. A. A. Neil, G. W. Stamp, P. M. French, P. A. Kellett, J. D. Hares, and A. K. Dymoke-Bradshaw, “High-speed wide-field time-gated endoscopic fluorescence-lifetime imaging,” Opt. Lett. 29(19), 2249–2251 (2004). [CrossRef] [PubMed]
- P. R. Barber, S. M. Ameer-Beg, J. Gilbey, L. M. Carlin, M. Keppler, T. Ng, and B. Vojnovic, “Multiphoton time-domain fluorescence lifetime imaging microscopy: practical application to protein–protein interactions using global analysis,” J. R. Soc. Interface 6(0), 93–105 (2009). [CrossRef]
- G. McConnell, J. M. Girkin, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, T. Ng, A. Banerjee, T. F. Watson, and R. J. Cook, “Time-correlated single-photon counting fluorescence lifetime confocal imaging of decayed and sound dental structures with a white-light supercontinuum source,” J. Microsc. 225(2), 126–136 (2007). [CrossRef] [PubMed]
- E. M. Merzlyak, J. Goedhart, D. Shcherbo, M. E. Bulina, A. S. Shcheglov, A. F. Fradkov, A. Gaintzeva, K. A. Lukyanov, S. Lukyanov, T. W. Gadella, and D. M. Chudakov, “Bright monomeric red fluorescent protein with an extended fluorescence lifetime,” Nat. Methods 4(7), 555–557 (2007). [CrossRef] [PubMed]
- C. C. Fjeld, W. T. Birdsong, and R. H. Goodman, “Differential binding of NAD+ and NADH allows the transcriptional corepressor carboxyl-terminal binding protein to serve as a metabolic sensor,” Proc. Natl. Acad. Sci. U.S.A. 100(16), 9202–9207 (2003). [CrossRef] [PubMed]
- T. Ng, D. Shima, A. Squire, P. I. H. Bastiaens, S. Gschmeissner, M. J. Humphries, and P. J. Parker, “PKCalpha regulates beta1 integrin-dependent cell motility through association and control of integrin traffic,” EMBO J. 18, 3909–3923 (1999). [CrossRef] [PubMed]
- T. Ng, A. Squire, G. Hansra, F. Bornancin, C. Prevostel, A. Hanby, W. Harris, D. Barnes, S. Schmidt, H. Mellor, P. I. Bastiaens, and P. J. Parker, “Imaging protein kinase Calpha activation in cells,” Science 283(5410), 2085–2089 (1999). [CrossRef] [PubMed]
- T. Ng, A. Squire, G. Hansra, F. Bornancin, C. Prevostel, A. Hanby, W. Harris, D. Barnes, S. Schmidt, H. Mellor, P. I. Bastiaens, and P. J. Parker, “Imaging protein kinase Calpha activation in cells,” Science 283(5410), 2085–2089 (1999). [CrossRef] [PubMed]
- J. Requejo-Isidro, J. McGinty, I. Munro, D. S. Elson, N. P. Galletly, M. J. Lever, M. A. A. Neil, G. W. Stamp, P. M. French, P. A. Kellett, J. D. Hares, and A. K. Dymoke-Bradshaw, “High-speed wide-field time-gated endoscopic fluorescence-lifetime imaging,” Opt. Lett. 29(19), 2249–2251 (2004). [CrossRef] [PubMed]
- T. Ng, A. Squire, G. Hansra, F. Bornancin, C. Prevostel, A. Hanby, W. Harris, D. Barnes, S. Schmidt, H. Mellor, P. I. Bastiaens, and P. J. Parker, “Imaging protein kinase Calpha activation in cells,” Science 283(5410), 2085–2089 (1999). [CrossRef] [PubMed]
- W. Becker, H. Hickl, C. Zander, K. H. Drexhage, M. Sauer, S. Siebert, and J. Wolfrum, “Time-resolved detection and identification of single analyte molecules in microcapillaries by time-correlated single photon counting,” Rev. Sci. Instrum. 70(3), 1835–1841 (1999). [CrossRef]
- R. Maeda-Mamiya, E. Noiri, H. Isobe, W. Nakanishi, K. Okamoto, K. Doi, T. Sugaya, T. Izumi, T. Homma, and E. Nakamura, “In vivo gene delivery by cationic tetraamino fullerene,” Procs. Nat. Acad. Sci. 107(12), 5339–5344 (2010). [CrossRef]
- M. Peter, S. M. Ameer-Beg, M. K. Y. Hughes, M. D. Keppler, S. Prag, M. Marsh, B. Vojnovic, and T. Ng, “Multiphoton-FLIM quantification of the EGFP-mRFP1 FRET pair for localization of membrane receptor-kinase interactions,” Biophys. J. 88(2), 1224–1237 (2005). [CrossRef]
- T. Ng, D. Shima, A. Squire, P. I. H. Bastiaens, S. Gschmeissner, M. J. Humphries, and P. J. Parker, “PKCalpha regulates beta1 integrin-dependent cell motility through association and control of integrin traffic,” EMBO J. 18, 3909–3923 (1999). [CrossRef] [PubMed]
- S. Prag, M. Parsons, M. D. Keppler, S. M. Ameer-Beg, P. Barber, J. Hunt, A. J. Beavil, R. Calvert, M. Arpin, B. Vojnovic, and T. Ng, “Activated ezrin promotes cell migration through recruitment of the GEF Dbl to lipid rafts and preferential downstream activation of Cdc42,” Mol. Biol. Cell 18(8), 2935–2948 (2007). [CrossRef] [PubMed]
- R. Maeda-Mamiya, E. Noiri, H. Isobe, W. Nakanishi, K. Okamoto, K. Doi, T. Sugaya, T. Izumi, T. Homma, and E. Nakamura, “In vivo gene delivery by cationic tetraamino fullerene,” Procs. Nat. Acad. Sci. 107(12), 5339–5344 (2010). [CrossRef]
- R. Maeda-Mamiya, E. Noiri, H. Isobe, W. Nakanishi, K. Okamoto, K. Doi, T. Sugaya, T. Izumi, T. Homma, and E. Nakamura, “In vivo gene delivery by cationic tetraamino fullerene,” Procs. Nat. Acad. Sci. 107(12), 5339–5344 (2010). [CrossRef]
- E. A. Jares-Erijman and T. M. Jovin, “FRET imaging,” Nat. Biotechnol. 21(11), 1387–1395 (2003). [CrossRef] [PubMed]
- H. Morise, O. Shimomura, F. H. Johnson, and J. Winant, “Intermolecular energy transfer in the bioluminescent system of Aequorea,” Biochemistry 13(12), 2656–2662 (1974). [CrossRef] [PubMed]
- E. A. Jares-Erijman and T. M. Jovin, “FRET imaging,” Nat. Biotechnol. 21(11), 1387–1395 (2003). [CrossRef] [PubMed]
- T. W. J. Gadella, T. M. Jovin, and R. M. Clegg, “Fluorescence lifetime imaging microscopy (FLIM): Spatial resolution of microstructures on the nanosecond time scale,” Biophys. Chem. 48(2), 221–239 (1993). [CrossRef]
- C. Buranachai, D. Kamiyama, A. Chiba, B. D. Williams, and R. M. Clegg, “Rapid frequency-domain FLIM spinning disk confocal microscope: lifetime resolution, image improvement and wavelet analysis,” J. Fluoresc. 18(5), 929–942 (2008). [CrossRef] [PubMed]
- J. Requejo-Isidro, J. McGinty, I. Munro, D. S. Elson, N. P. Galletly, M. J. Lever, M. A. A. Neil, G. W. Stamp, P. M. French, P. A. Kellett, J. D. Hares, and A. K. Dymoke-Bradshaw, “High-speed wide-field time-gated endoscopic fluorescence-lifetime imaging,” Opt. Lett. 29(19), 2249–2251 (2004). [CrossRef] [PubMed]
- P. R. Barber, S. M. Ameer-Beg, J. Gilbey, L. M. Carlin, M. Keppler, T. Ng, and B. Vojnovic, “Multiphoton time-domain fluorescence lifetime imaging microscopy: practical application to protein–protein interactions using global analysis,” J. R. Soc. Interface 6(0), 93–105 (2009). [CrossRef]
- K. Makrogianneli, L. M. Carlin, M. D. Keppler, D. R. Matthews, E. Ofo, A. Coolen, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, and T. Ng, “Integrating receptor signal inputs that influence small Rho GTPase activation dynamics at the immunological synapse,” Mol. Cell. Biol. 29(11), 2997–3006 (2009). [CrossRef] [PubMed]
- S. Prag, M. Parsons, M. D. Keppler, S. M. Ameer-Beg, P. Barber, J. Hunt, A. J. Beavil, R. Calvert, M. Arpin, B. Vojnovic, and T. Ng, “Activated ezrin promotes cell migration through recruitment of the GEF Dbl to lipid rafts and preferential downstream activation of Cdc42,” Mol. Biol. Cell 18(8), 2935–2948 (2007). [CrossRef] [PubMed]
- M. Peter, S. M. Ameer-Beg, M. K. Y. Hughes, M. D. Keppler, S. Prag, M. Marsh, B. Vojnovic, and T. Ng, “Multiphoton-FLIM quantification of the EGFP-mRFP1 FRET pair for localization of membrane receptor-kinase interactions,” Biophys. J. 88(2), 1224–1237 (2005). [CrossRef]
- M. Parsons, J. Monypenny, S. M. Ameer-Beg, T. H. Millard, L. M. Machesky, M. Peter, M. D. Keppler, G. Schiavo, R. Watson, J. Chernoff, D. Zicha, B. Vojnovic, and T. Ng, “Spatially distinct binding of Cdc42 to PAK1 and N-WASP in breast carcinoma cells,” Mol. Cell. Biol. 25(5), 1680–1695 (2005). [CrossRef] [PubMed]
- S. Kumar, C. Dunsby, P. A. A. De Beule, D. M. Owen, U. Anand, P. M. P. Lanigan, R. K. P. Benninger, D. M. Davis, M. A. Neil, P. Anand, C. Benham, A. Naylor, and P. M. French, “Multifocal multiphoton excitation and time correlated single photon counting detection for 3-D fluorescence lifetime imaging,” Opt. Express 15(20), 12548–12561 (2007). [CrossRef] [PubMed]
- T. Y. Lee, C. T. Lin, S. Y. Kuo, D. K. Chang, and H. C. Wu, “Peptide-mediated targeting to tumor blood vessels of lung cancer for drug delivery,” Cancer Res. 67(22), 10958–10965 (2007). [CrossRef] [PubMed]
- D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004). [CrossRef] [PubMed]
- S. Kumar, C. Dunsby, P. A. A. De Beule, D. M. Owen, U. Anand, P. M. P. Lanigan, R. K. P. Benninger, D. M. Davis, M. A. Neil, P. Anand, C. Benham, A. Naylor, and P. M. French, “Multifocal multiphoton excitation and time correlated single photon counting detection for 3-D fluorescence lifetime imaging,” Opt. Express 15(20), 12548–12561 (2007). [CrossRef] [PubMed]
- I. Munro, J. McGinty, N. Galletly, J. Requejo-Isidro, P. M. P. Lanigan, D. S. Elson, C. Dunsby, M. A. Neil, M. J. Lever, G. W. Stamp, and P. M. French, “Toward the clinical application of time-domain fluorescence lifetime imaging,” J. Biomed. Opt. 10(5), 051403 (2005). [CrossRef] [PubMed]
- V. Calleja, S. M. Ameer-Beg, B. Vojnovic, R. Woscholski, J. Downward, and B. Larijani, “Monitoring conformational changes of proteins in cells by fluorescence lifetime imaging microscopy,” Biochem. J. 372(1), 33–40 (2003). [CrossRef] [PubMed]
- T. Y. Lee, C. T. Lin, S. Y. Kuo, D. K. Chang, and H. C. Wu, “Peptide-mediated targeting to tumor blood vessels of lung cancer for drug delivery,” Cancer Res. 67(22), 10958–10965 (2007). [CrossRef] [PubMed]
- D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004). [CrossRef] [PubMed]
- I. Munro, J. McGinty, N. Galletly, J. Requejo-Isidro, P. M. P. Lanigan, D. S. Elson, C. Dunsby, M. A. Neil, M. J. Lever, G. W. Stamp, and P. M. French, “Toward the clinical application of time-domain fluorescence lifetime imaging,” J. Biomed. Opt. 10(5), 051403 (2005). [CrossRef] [PubMed]
- J. Requejo-Isidro, J. McGinty, I. Munro, D. S. Elson, N. P. Galletly, M. J. Lever, M. A. A. Neil, G. W. Stamp, P. M. French, P. A. Kellett, J. D. Hares, and A. K. Dymoke-Bradshaw, “High-speed wide-field time-gated endoscopic fluorescence-lifetime imaging,” Opt. Lett. 29(19), 2249–2251 (2004). [CrossRef] [PubMed]
- H. Lomas, M. Massignani, K. A. Abdullah, I. Canton, C. Lo Presti, S. MacNeil, J. Du, A. Blanazs, J. Madsen, S. P. Armes, A. L. Lewis, and G. Battaglia, “Non-cytotoxic polymer vesicles for rapid and efficient intracellular delivery,” Faraday Discuss. 139, 143–159, discussion 213–228, 419–420 (2008). [CrossRef] [PubMed]
- T. Y. Lee, C. T. Lin, S. Y. Kuo, D. K. Chang, and H. C. Wu, “Peptide-mediated targeting to tumor blood vessels of lung cancer for drug delivery,” Cancer Res. 67(22), 10958–10965 (2007). [CrossRef] [PubMed]
- H. Lomas, M. Massignani, K. A. Abdullah, I. Canton, C. Lo Presti, S. MacNeil, J. Du, A. Blanazs, J. Madsen, S. P. Armes, A. L. Lewis, and G. Battaglia, “Non-cytotoxic polymer vesicles for rapid and efficient intracellular delivery,” Faraday Discuss. 139, 143–159, discussion 213–228, 419–420 (2008). [CrossRef] [PubMed]
- C. LoPresti, H. Lomas, M. Massignani, T. Smart, and G. Battaglia, “Polymersomes: nature inspired nanometer sized compartments,” J. Mater. Chem. 19(22), 3576–3590 (2009). [CrossRef]
- H. Lomas, M. Massignani, K. A. Abdullah, I. Canton, C. Lo Presti, S. MacNeil, J. Du, A. Blanazs, J. Madsen, S. P. Armes, A. L. Lewis, and G. Battaglia, “Non-cytotoxic polymer vesicles for rapid and efficient intracellular delivery,” Faraday Discuss. 139, 143–159, discussion 213–228, 419–420 (2008). [CrossRef] [PubMed]
- C. LoPresti, H. Lomas, M. Massignani, T. Smart, and G. Battaglia, “Polymersomes: nature inspired nanometer sized compartments,” J. Mater. Chem. 19(22), 3576–3590 (2009). [CrossRef]
- E. M. Merzlyak, J. Goedhart, D. Shcherbo, M. E. Bulina, A. S. Shcheglov, A. F. Fradkov, A. Gaintzeva, K. A. Lukyanov, S. Lukyanov, T. W. Gadella, and D. M. Chudakov, “Bright monomeric red fluorescent protein with an extended fluorescence lifetime,” Nat. Methods 4(7), 555–557 (2007). [CrossRef] [PubMed]
- E. M. Merzlyak, J. Goedhart, D. Shcherbo, M. E. Bulina, A. S. Shcheglov, A. F. Fradkov, A. Gaintzeva, K. A. Lukyanov, S. Lukyanov, T. W. Gadella, and D. M. Chudakov, “Bright monomeric red fluorescent protein with an extended fluorescence lifetime,” Nat. Methods 4(7), 555–557 (2007). [CrossRef] [PubMed]
- M. Parsons, J. Monypenny, S. M. Ameer-Beg, T. H. Millard, L. M. Machesky, M. Peter, M. D. Keppler, G. Schiavo, R. Watson, J. Chernoff, D. Zicha, B. Vojnovic, and T. Ng, “Spatially distinct binding of Cdc42 to PAK1 and N-WASP in breast carcinoma cells,” Mol. Cell. Biol. 25(5), 1680–1695 (2005). [CrossRef] [PubMed]
- R. El-Gazzar, M. Macluskey, and G. R. Ogden, “Evidence for a field change effect based on angiogenesis in the oral mucosa? A brief report,” Oral Oncol. 41(1), 25–30 (2005). [CrossRef]
- H. Lomas, M. Massignani, K. A. Abdullah, I. Canton, C. Lo Presti, S. MacNeil, J. Du, A. Blanazs, J. Madsen, S. P. Armes, A. L. Lewis, and G. Battaglia, “Non-cytotoxic polymer vesicles for rapid and efficient intracellular delivery,” Faraday Discuss. 139, 143–159, discussion 213–228, 419–420 (2008). [CrossRef] [PubMed]
- H. Lomas, M. Massignani, K. A. Abdullah, I. Canton, C. Lo Presti, S. MacNeil, J. Du, A. Blanazs, J. Madsen, S. P. Armes, A. L. Lewis, and G. Battaglia, “Non-cytotoxic polymer vesicles for rapid and efficient intracellular delivery,” Faraday Discuss. 139, 143–159, discussion 213–228, 419–420 (2008). [CrossRef] [PubMed]
- R. Maeda-Mamiya, E. Noiri, H. Isobe, W. Nakanishi, K. Okamoto, K. Doi, T. Sugaya, T. Izumi, T. Homma, and E. Nakamura, “In vivo gene delivery by cationic tetraamino fullerene,” Procs. Nat. Acad. Sci. 107(12), 5339–5344 (2010). [CrossRef]
- K. Makrogianneli, L. M. Carlin, M. D. Keppler, D. R. Matthews, E. Ofo, A. Coolen, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, and T. Ng, “Integrating receptor signal inputs that influence small Rho GTPase activation dynamics at the immunological synapse,” Mol. Cell. Biol. 29(11), 2997–3006 (2009). [CrossRef] [PubMed]
- A. Cobos-Correa, J. B. Trojanek, S. Diemer, M. A. Mall, and C. Schultz, “Membrane-bound FRET probe visualizes MMP12 activity in pulmonary inflammation,” Nat. Chem. Biol. 5(9), 628–630 (2009). [CrossRef] [PubMed]
- M. Peter, S. M. Ameer-Beg, M. K. Y. Hughes, M. D. Keppler, S. Prag, M. Marsh, B. Vojnovic, and T. Ng, “Multiphoton-FLIM quantification of the EGFP-mRFP1 FRET pair for localization of membrane receptor-kinase interactions,” Biophys. J. 88(2), 1224–1237 (2005). [CrossRef]
- A. J. Vila-Coro, J. M. Rodríguez-Frade, A. Martín De Ana, M. C. Moreno-Ortíz, C. Martínez-A, and M. Mellado, “The chemokine SDF-1alpha triggers CXCR4 receptor dimerization and activates the JAK/STAT pathway,” FASEB J. 13(13), 1699–1710 (1999). [PubMed]
- A. J. Vila-Coro, J. M. Rodríguez-Frade, A. Martín De Ana, M. C. Moreno-Ortíz, C. Martínez-A, and M. Mellado, “The chemokine SDF-1alpha triggers CXCR4 receptor dimerization and activates the JAK/STAT pathway,” FASEB J. 13(13), 1699–1710 (1999). [PubMed]
- C. LoPresti, H. Lomas, M. Massignani, T. Smart, and G. Battaglia, “Polymersomes: nature inspired nanometer sized compartments,” J. Mater. Chem. 19(22), 3576–3590 (2009). [CrossRef]
- H. Lomas, M. Massignani, K. A. Abdullah, I. Canton, C. Lo Presti, S. MacNeil, J. Du, A. Blanazs, J. Madsen, S. P. Armes, A. L. Lewis, and G. Battaglia, “Non-cytotoxic polymer vesicles for rapid and efficient intracellular delivery,” Faraday Discuss. 139, 143–159, discussion 213–228, 419–420 (2008). [CrossRef] [PubMed]
- K. Makrogianneli, L. M. Carlin, M. D. Keppler, D. R. Matthews, E. Ofo, A. Coolen, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, and T. Ng, “Integrating receptor signal inputs that influence small Rho GTPase activation dynamics at the immunological synapse,” Mol. Cell. Biol. 29(11), 2997–3006 (2009). [CrossRef] [PubMed]
- G. McConnell, J. M. Girkin, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, T. Ng, A. Banerjee, T. F. Watson, and R. J. Cook, “Time-correlated single-photon counting fluorescence lifetime confocal imaging of decayed and sound dental structures with a white-light supercontinuum source,” J. Microsc. 225(2), 126–136 (2007). [CrossRef] [PubMed]
- I. Munro, J. McGinty, N. Galletly, J. Requejo-Isidro, P. M. P. Lanigan, D. S. Elson, C. Dunsby, M. A. Neil, M. J. Lever, G. W. Stamp, and P. M. French, “Toward the clinical application of time-domain fluorescence lifetime imaging,” J. Biomed. Opt. 10(5), 051403 (2005). [CrossRef] [PubMed]
- D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004). [CrossRef] [PubMed]
- J. Requejo-Isidro, J. McGinty, I. Munro, D. S. Elson, N. P. Galletly, M. J. Lever, M. A. A. Neil, G. W. Stamp, P. M. French, P. A. Kellett, J. D. Hares, and A. K. Dymoke-Bradshaw, “High-speed wide-field time-gated endoscopic fluorescence-lifetime imaging,” Opt. Lett. 29(19), 2249–2251 (2004). [CrossRef] [PubMed]
- A. J. Vila-Coro, J. M. Rodríguez-Frade, A. Martín De Ana, M. C. Moreno-Ortíz, C. Martínez-A, and M. Mellado, “The chemokine SDF-1alpha triggers CXCR4 receptor dimerization and activates the JAK/STAT pathway,” FASEB J. 13(13), 1699–1710 (1999). [PubMed]
- T. Ng, A. Squire, G. Hansra, F. Bornancin, C. Prevostel, A. Hanby, W. Harris, D. Barnes, S. Schmidt, H. Mellor, P. I. Bastiaens, and P. J. Parker, “Imaging protein kinase Calpha activation in cells,” Science 283(5410), 2085–2089 (1999). [CrossRef] [PubMed]
- E. M. Merzlyak, J. Goedhart, D. Shcherbo, M. E. Bulina, A. S. Shcheglov, A. F. Fradkov, A. Gaintzeva, K. A. Lukyanov, S. Lukyanov, T. W. Gadella, and D. M. Chudakov, “Bright monomeric red fluorescent protein with an extended fluorescence lifetime,” Nat. Methods 4(7), 555–557 (2007). [CrossRef] [PubMed]
- M. Parsons, J. Monypenny, S. M. Ameer-Beg, T. H. Millard, L. M. Machesky, M. Peter, M. D. Keppler, G. Schiavo, R. Watson, J. Chernoff, D. Zicha, B. Vojnovic, and T. Ng, “Spatially distinct binding of Cdc42 to PAK1 and N-WASP in breast carcinoma cells,” Mol. Cell. Biol. 25(5), 1680–1695 (2005). [CrossRef] [PubMed]
- M. Parsons, J. Monypenny, S. M. Ameer-Beg, T. H. Millard, L. M. Machesky, M. Peter, M. D. Keppler, G. Schiavo, R. Watson, J. Chernoff, D. Zicha, B. Vojnovic, and T. Ng, “Spatially distinct binding of Cdc42 to PAK1 and N-WASP in breast carcinoma cells,” Mol. Cell. Biol. 25(5), 1680–1695 (2005). [CrossRef] [PubMed]
- A. J. Vila-Coro, J. M. Rodríguez-Frade, A. Martín De Ana, M. C. Moreno-Ortíz, C. Martínez-A, and M. Mellado, “The chemokine SDF-1alpha triggers CXCR4 receptor dimerization and activates the JAK/STAT pathway,” FASEB J. 13(13), 1699–1710 (1999). [PubMed]
- H. Morise, O. Shimomura, F. H. Johnson, and J. Winant, “Intermolecular energy transfer in the bioluminescent system of Aequorea,” Biochemistry 13(12), 2656–2662 (1974). [CrossRef] [PubMed]
- I. Munro, J. McGinty, N. Galletly, J. Requejo-Isidro, P. M. P. Lanigan, D. S. Elson, C. Dunsby, M. A. Neil, M. J. Lever, G. W. Stamp, and P. M. French, “Toward the clinical application of time-domain fluorescence lifetime imaging,” J. Biomed. Opt. 10(5), 051403 (2005). [CrossRef] [PubMed]
- J. Requejo-Isidro, J. McGinty, I. Munro, D. S. Elson, N. P. Galletly, M. J. Lever, M. A. A. Neil, G. W. Stamp, P. M. French, P. A. Kellett, J. D. Hares, and A. K. Dymoke-Bradshaw, “High-speed wide-field time-gated endoscopic fluorescence-lifetime imaging,” Opt. Lett. 29(19), 2249–2251 (2004). [CrossRef] [PubMed]
- D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004). [CrossRef] [PubMed]
- R. Maeda-Mamiya, E. Noiri, H. Isobe, W. Nakanishi, K. Okamoto, K. Doi, T. Sugaya, T. Izumi, T. Homma, and E. Nakamura, “In vivo gene delivery by cationic tetraamino fullerene,” Procs. Nat. Acad. Sci. 107(12), 5339–5344 (2010). [CrossRef]
- R. Maeda-Mamiya, E. Noiri, H. Isobe, W. Nakanishi, K. Okamoto, K. Doi, T. Sugaya, T. Izumi, T. Homma, and E. Nakamura, “In vivo gene delivery by cationic tetraamino fullerene,” Procs. Nat. Acad. Sci. 107(12), 5339–5344 (2010). [CrossRef]
- S. Kumar, C. Dunsby, P. A. A. De Beule, D. M. Owen, U. Anand, P. M. P. Lanigan, R. K. P. Benninger, D. M. Davis, M. A. Neil, P. Anand, C. Benham, A. Naylor, and P. M. French, “Multifocal multiphoton excitation and time correlated single photon counting detection for 3-D fluorescence lifetime imaging,” Opt. Express 15(20), 12548–12561 (2007). [CrossRef] [PubMed]
- D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004). [CrossRef] [PubMed]
- S. Kumar, C. Dunsby, P. A. A. De Beule, D. M. Owen, U. Anand, P. M. P. Lanigan, R. K. P. Benninger, D. M. Davis, M. A. Neil, P. Anand, C. Benham, A. Naylor, and P. M. French, “Multifocal multiphoton excitation and time correlated single photon counting detection for 3-D fluorescence lifetime imaging,” Opt. Express 15(20), 12548–12561 (2007). [CrossRef] [PubMed]
- I. Munro, J. McGinty, N. Galletly, J. Requejo-Isidro, P. M. P. Lanigan, D. S. Elson, C. Dunsby, M. A. Neil, M. J. Lever, G. W. Stamp, and P. M. French, “Toward the clinical application of time-domain fluorescence lifetime imaging,” J. Biomed. Opt. 10(5), 051403 (2005). [CrossRef] [PubMed]
- J. Requejo-Isidro, J. McGinty, I. Munro, D. S. Elson, N. P. Galletly, M. J. Lever, M. A. A. Neil, G. W. Stamp, P. M. French, P. A. Kellett, J. D. Hares, and A. K. Dymoke-Bradshaw, “High-speed wide-field time-gated endoscopic fluorescence-lifetime imaging,” Opt. Lett. 29(19), 2249–2251 (2004). [CrossRef] [PubMed]
- K. Makrogianneli, L. M. Carlin, M. D. Keppler, D. R. Matthews, E. Ofo, A. Coolen, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, and T. Ng, “Integrating receptor signal inputs that influence small Rho GTPase activation dynamics at the immunological synapse,” Mol. Cell. Biol. 29(11), 2997–3006 (2009). [CrossRef] [PubMed]
- P. R. Barber, S. M. Ameer-Beg, J. Gilbey, L. M. Carlin, M. Keppler, T. Ng, and B. Vojnovic, “Multiphoton time-domain fluorescence lifetime imaging microscopy: practical application to protein–protein interactions using global analysis,” J. R. Soc. Interface 6(0), 93–105 (2009). [CrossRef]
- S. Prag, M. Parsons, M. D. Keppler, S. M. Ameer-Beg, P. Barber, J. Hunt, A. J. Beavil, R. Calvert, M. Arpin, B. Vojnovic, and T. Ng, “Activated ezrin promotes cell migration through recruitment of the GEF Dbl to lipid rafts and preferential downstream activation of Cdc42,” Mol. Biol. Cell 18(8), 2935–2948 (2007). [CrossRef] [PubMed]
- F. Festy, S. M. Ameer-Beg, T. Ng, and K. Suhling, “Imaging proteins in vivo using fluorescence lifetime microscopy,” Mol. Biosyst. 3(6), 381–391 (2007). [CrossRef] [PubMed]
- G. McConnell, J. M. Girkin, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, T. Ng, A. Banerjee, T. F. Watson, and R. J. Cook, “Time-correlated single-photon counting fluorescence lifetime confocal imaging of decayed and sound dental structures with a white-light supercontinuum source,” J. Microsc. 225(2), 126–136 (2007). [CrossRef] [PubMed]
- M. Parsons, J. Monypenny, S. M. Ameer-Beg, T. H. Millard, L. M. Machesky, M. Peter, M. D. Keppler, G. Schiavo, R. Watson, J. Chernoff, D. Zicha, B. Vojnovic, and T. Ng, “Spatially distinct binding of Cdc42 to PAK1 and N-WASP in breast carcinoma cells,” Mol. Cell. Biol. 25(5), 1680–1695 (2005). [CrossRef] [PubMed]
- M. Peter, S. M. Ameer-Beg, M. K. Y. Hughes, M. D. Keppler, S. Prag, M. Marsh, B. Vojnovic, and T. Ng, “Multiphoton-FLIM quantification of the EGFP-mRFP1 FRET pair for localization of membrane receptor-kinase interactions,” Biophys. J. 88(2), 1224–1237 (2005). [CrossRef]
- T. Ng, D. Shima, A. Squire, P. I. H. Bastiaens, S. Gschmeissner, M. J. Humphries, and P. J. Parker, “PKCalpha regulates beta1 integrin-dependent cell motility through association and control of integrin traffic,” EMBO J. 18, 3909–3923 (1999). [CrossRef] [PubMed]
- T. Ng, A. Squire, G. Hansra, F. Bornancin, C. Prevostel, A. Hanby, W. Harris, D. Barnes, S. Schmidt, H. Mellor, P. I. Bastiaens, and P. J. Parker, “Imaging protein kinase Calpha activation in cells,” Science 283(5410), 2085–2089 (1999). [CrossRef] [PubMed]
- R. Maeda-Mamiya, E. Noiri, H. Isobe, W. Nakanishi, K. Okamoto, K. Doi, T. Sugaya, T. Izumi, T. Homma, and E. Nakamura, “In vivo gene delivery by cationic tetraamino fullerene,” Procs. Nat. Acad. Sci. 107(12), 5339–5344 (2010). [CrossRef]
- K. Makrogianneli, L. M. Carlin, M. D. Keppler, D. R. Matthews, E. Ofo, A. Coolen, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, and T. Ng, “Integrating receptor signal inputs that influence small Rho GTPase activation dynamics at the immunological synapse,” Mol. Cell. Biol. 29(11), 2997–3006 (2009). [CrossRef] [PubMed]
- R. El-Gazzar, M. Macluskey, and G. R. Ogden, “Evidence for a field change effect based on angiogenesis in the oral mucosa? A brief report,” Oral Oncol. 41(1), 25–30 (2005). [CrossRef]
- R. Maeda-Mamiya, E. Noiri, H. Isobe, W. Nakanishi, K. Okamoto, K. Doi, T. Sugaya, T. Izumi, T. Homma, and E. Nakamura, “In vivo gene delivery by cationic tetraamino fullerene,” Procs. Nat. Acad. Sci. 107(12), 5339–5344 (2010). [CrossRef]
- S. Kumar, C. Dunsby, P. A. A. De Beule, D. M. Owen, U. Anand, P. M. P. Lanigan, R. K. P. Benninger, D. M. Davis, M. A. Neil, P. Anand, C. Benham, A. Naylor, and P. M. French, “Multifocal multiphoton excitation and time correlated single photon counting detection for 3-D fluorescence lifetime imaging,” Opt. Express 15(20), 12548–12561 (2007). [CrossRef] [PubMed]
- Z. Papagatsia, A. Tappuni, T. F. Watson, and R. J. Cook, “Single wavelength micro-endoscopy in non-surgical vascular lesion diagnosis & characterization,” J. Microsc. 230(2), 203–211 (2008). [CrossRef] [PubMed]
- T. Ng, A. Squire, G. Hansra, F. Bornancin, C. Prevostel, A. Hanby, W. Harris, D. Barnes, S. Schmidt, H. Mellor, P. I. Bastiaens, and P. J. Parker, “Imaging protein kinase Calpha activation in cells,” Science 283(5410), 2085–2089 (1999). [CrossRef] [PubMed]
- T. Ng, D. Shima, A. Squire, P. I. H. Bastiaens, S. Gschmeissner, M. J. Humphries, and P. J. Parker, “PKCalpha regulates beta1 integrin-dependent cell motility through association and control of integrin traffic,” EMBO J. 18, 3909–3923 (1999). [CrossRef] [PubMed]
- S. Prag, M. Parsons, M. D. Keppler, S. M. Ameer-Beg, P. Barber, J. Hunt, A. J. Beavil, R. Calvert, M. Arpin, B. Vojnovic, and T. Ng, “Activated ezrin promotes cell migration through recruitment of the GEF Dbl to lipid rafts and preferential downstream activation of Cdc42,” Mol. Biol. Cell 18(8), 2935–2948 (2007). [CrossRef] [PubMed]
- M. Parsons, J. Monypenny, S. M. Ameer-Beg, T. H. Millard, L. M. Machesky, M. Peter, M. D. Keppler, G. Schiavo, R. Watson, J. Chernoff, D. Zicha, B. Vojnovic, and T. Ng, “Spatially distinct binding of Cdc42 to PAK1 and N-WASP in breast carcinoma cells,” Mol. Cell. Biol. 25(5), 1680–1695 (2005). [CrossRef] [PubMed]
- S. Pelet, M. J. R. Previte, and P. T. So, “Comparing the quantification of Forster resonance energy transfer measurement accuracies based on intensity, spectral, and lifetime imaging,” J. Biomed. Opt. 11(3), 034017 (2006). [CrossRef]
- M. Peter, S. M. Ameer-Beg, M. K. Y. Hughes, M. D. Keppler, S. Prag, M. Marsh, B. Vojnovic, and T. Ng, “Multiphoton-FLIM quantification of the EGFP-mRFP1 FRET pair for localization of membrane receptor-kinase interactions,” Biophys. J. 88(2), 1224–1237 (2005). [CrossRef]
- M. Parsons, J. Monypenny, S. M. Ameer-Beg, T. H. Millard, L. M. Machesky, M. Peter, M. D. Keppler, G. Schiavo, R. Watson, J. Chernoff, D. Zicha, B. Vojnovic, and T. Ng, “Spatially distinct binding of Cdc42 to PAK1 and N-WASP in breast carcinoma cells,” Mol. Cell. Biol. 25(5), 1680–1695 (2005). [CrossRef] [PubMed]
- M. Peter and S. M. Ameer-Beg, “Imaging molecular interactions by multiphoton FLIM,” Biol. Cell 96(3), 231–236 (2004). [CrossRef] [PubMed]
- K. Suhling, P. M. French, and D. Phillips, “Time-resolved fluorescence microscopy,” Photochem. Photobiol. Sci. 4(1), 13–22 (2005). [CrossRef]
- D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004). [CrossRef] [PubMed]
- S. Prag, M. Parsons, M. D. Keppler, S. M. Ameer-Beg, P. Barber, J. Hunt, A. J. Beavil, R. Calvert, M. Arpin, B. Vojnovic, and T. Ng, “Activated ezrin promotes cell migration through recruitment of the GEF Dbl to lipid rafts and preferential downstream activation of Cdc42,” Mol. Biol. Cell 18(8), 2935–2948 (2007). [CrossRef] [PubMed]
- M. Peter, S. M. Ameer-Beg, M. K. Y. Hughes, M. D. Keppler, S. Prag, M. Marsh, B. Vojnovic, and T. Ng, “Multiphoton-FLIM quantification of the EGFP-mRFP1 FRET pair for localization of membrane receptor-kinase interactions,” Biophys. J. 88(2), 1224–1237 (2005). [CrossRef]
- S. Pelet, M. J. R. Previte, and P. T. So, “Comparing the quantification of Forster resonance energy transfer measurement accuracies based on intensity, spectral, and lifetime imaging,” J. Biomed. Opt. 11(3), 034017 (2006). [CrossRef]
- T. Ng, A. Squire, G. Hansra, F. Bornancin, C. Prevostel, A. Hanby, W. Harris, D. Barnes, S. Schmidt, H. Mellor, P. I. Bastiaens, and P. J. Parker, “Imaging protein kinase Calpha activation in cells,” Science 283(5410), 2085–2089 (1999). [CrossRef] [PubMed]
- D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004). [CrossRef] [PubMed]
- I. Munro, J. McGinty, N. Galletly, J. Requejo-Isidro, P. M. P. Lanigan, D. S. Elson, C. Dunsby, M. A. Neil, M. J. Lever, G. W. Stamp, and P. M. French, “Toward the clinical application of time-domain fluorescence lifetime imaging,” J. Biomed. Opt. 10(5), 051403 (2005). [CrossRef] [PubMed]
- D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004). [CrossRef] [PubMed]
- J. Requejo-Isidro, J. McGinty, I. Munro, D. S. Elson, N. P. Galletly, M. J. Lever, M. A. A. Neil, G. W. Stamp, P. M. French, P. A. Kellett, J. D. Hares, and A. K. Dymoke-Bradshaw, “High-speed wide-field time-gated endoscopic fluorescence-lifetime imaging,” Opt. Lett. 29(19), 2249–2251 (2004). [CrossRef] [PubMed]
- A. J. Vila-Coro, J. M. Rodríguez-Frade, A. Martín De Ana, M. C. Moreno-Ortíz, C. Martínez-A, and M. Mellado, “The chemokine SDF-1alpha triggers CXCR4 receptor dimerization and activates the JAK/STAT pathway,” FASEB J. 13(13), 1699–1710 (1999). [PubMed]
- D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004). [CrossRef] [PubMed]
- W. Becker, H. Hickl, C. Zander, K. H. Drexhage, M. Sauer, S. Siebert, and J. Wolfrum, “Time-resolved detection and identification of single analyte molecules in microcapillaries by time-correlated single photon counting,” Rev. Sci. Instrum. 70(3), 1835–1841 (1999). [CrossRef]
- M. Parsons, J. Monypenny, S. M. Ameer-Beg, T. H. Millard, L. M. Machesky, M. Peter, M. D. Keppler, G. Schiavo, R. Watson, J. Chernoff, D. Zicha, B. Vojnovic, and T. Ng, “Spatially distinct binding of Cdc42 to PAK1 and N-WASP in breast carcinoma cells,” Mol. Cell. Biol. 25(5), 1680–1695 (2005). [CrossRef] [PubMed]
- T. Ng, A. Squire, G. Hansra, F. Bornancin, C. Prevostel, A. Hanby, W. Harris, D. Barnes, S. Schmidt, H. Mellor, P. I. Bastiaens, and P. J. Parker, “Imaging protein kinase Calpha activation in cells,” Science 283(5410), 2085–2089 (1999). [CrossRef] [PubMed]
- A. Cobos-Correa, J. B. Trojanek, S. Diemer, M. A. Mall, and C. Schultz, “Membrane-bound FRET probe visualizes MMP12 activity in pulmonary inflammation,” Nat. Chem. Biol. 5(9), 628–630 (2009). [CrossRef] [PubMed]
- E. M. Merzlyak, J. Goedhart, D. Shcherbo, M. E. Bulina, A. S. Shcheglov, A. F. Fradkov, A. Gaintzeva, K. A. Lukyanov, S. Lukyanov, T. W. Gadella, and D. M. Chudakov, “Bright monomeric red fluorescent protein with an extended fluorescence lifetime,” Nat. Methods 4(7), 555–557 (2007). [CrossRef] [PubMed]
- E. M. Merzlyak, J. Goedhart, D. Shcherbo, M. E. Bulina, A. S. Shcheglov, A. F. Fradkov, A. Gaintzeva, K. A. Lukyanov, S. Lukyanov, T. W. Gadella, and D. M. Chudakov, “Bright monomeric red fluorescent protein with an extended fluorescence lifetime,” Nat. Methods 4(7), 555–557 (2007). [CrossRef] [PubMed]
- T. Ng, D. Shima, A. Squire, P. I. H. Bastiaens, S. Gschmeissner, M. J. Humphries, and P. J. Parker, “PKCalpha regulates beta1 integrin-dependent cell motility through association and control of integrin traffic,” EMBO J. 18, 3909–3923 (1999). [CrossRef] [PubMed]
- H. Morise, O. Shimomura, F. H. Johnson, and J. Winant, “Intermolecular energy transfer in the bioluminescent system of Aequorea,” Biochemistry 13(12), 2656–2662 (1974). [CrossRef] [PubMed]
- R. R. Duncan, A. Bergmann, M. A. Cousin, D. K. Apps, and M. J. Shipston, “Multi-dimensional time-correlated single photon counting (TCSPC) fluorescence lifetime imaging microscopy (FLIM) to detect FRET in cells,” J. Microsc. 215(1), 1–12 (2004). [CrossRef] [PubMed]
- W. Becker, H. Hickl, C. Zander, K. H. Drexhage, M. Sauer, S. Siebert, and J. Wolfrum, “Time-resolved detection and identification of single analyte molecules in microcapillaries by time-correlated single photon counting,” Rev. Sci. Instrum. 70(3), 1835–1841 (1999). [CrossRef]
- D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004). [CrossRef] [PubMed]
- C. LoPresti, H. Lomas, M. Massignani, T. Smart, and G. Battaglia, “Polymersomes: nature inspired nanometer sized compartments,” J. Mater. Chem. 19(22), 3576–3590 (2009). [CrossRef]
- S. Pelet, M. J. R. Previte, and P. T. So, “Comparing the quantification of Forster resonance energy transfer measurement accuracies based on intensity, spectral, and lifetime imaging,” J. Biomed. Opt. 11(3), 034017 (2006). [CrossRef]
- G. J. Babcock, M. Farzan, and J. Sodroski, “Ligand-independent dimerization of CXCR4, a principal HIV-1 coreceptor,” J. Biol. Chem. 278(5), 3378–3385 (2003). [CrossRef]
- T. Ng, D. Shima, A. Squire, P. I. H. Bastiaens, S. Gschmeissner, M. J. Humphries, and P. J. Parker, “PKCalpha regulates beta1 integrin-dependent cell motility through association and control of integrin traffic,” EMBO J. 18, 3909–3923 (1999). [CrossRef] [PubMed]
- T. Ng, A. Squire, G. Hansra, F. Bornancin, C. Prevostel, A. Hanby, W. Harris, D. Barnes, S. Schmidt, H. Mellor, P. I. Bastiaens, and P. J. Parker, “Imaging protein kinase Calpha activation in cells,” Science 283(5410), 2085–2089 (1999). [CrossRef] [PubMed]
- D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004). [CrossRef] [PubMed]
- I. Munro, J. McGinty, N. Galletly, J. Requejo-Isidro, P. M. P. Lanigan, D. S. Elson, C. Dunsby, M. A. Neil, M. J. Lever, G. W. Stamp, and P. M. French, “Toward the clinical application of time-domain fluorescence lifetime imaging,” J. Biomed. Opt. 10(5), 051403 (2005). [CrossRef] [PubMed]
- J. Requejo-Isidro, J. McGinty, I. Munro, D. S. Elson, N. P. Galletly, M. J. Lever, M. A. A. Neil, G. W. Stamp, P. M. French, P. A. Kellett, J. D. Hares, and A. K. Dymoke-Bradshaw, “High-speed wide-field time-gated endoscopic fluorescence-lifetime imaging,” Opt. Lett. 29(19), 2249–2251 (2004). [CrossRef] [PubMed]
- L. Stryer, “Fluorescence energy transfer as a spectroscopic ruler,” Annu. Rev. Biochem. 47(1), 819–846 (1978). [CrossRef] [PubMed]
- R. Maeda-Mamiya, E. Noiri, H. Isobe, W. Nakanishi, K. Okamoto, K. Doi, T. Sugaya, T. Izumi, T. Homma, and E. Nakamura, “In vivo gene delivery by cationic tetraamino fullerene,” Procs. Nat. Acad. Sci. 107(12), 5339–5344 (2010). [CrossRef]
- F. Festy, S. M. Ameer-Beg, T. Ng, and K. Suhling, “Imaging proteins in vivo using fluorescence lifetime microscopy,” Mol. Biosyst. 3(6), 381–391 (2007). [CrossRef] [PubMed]
- K. Suhling, P. M. French, and D. Phillips, “Time-resolved fluorescence microscopy,” Photochem. Photobiol. Sci. 4(1), 13–22 (2005). [CrossRef]
- D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004). [CrossRef] [PubMed]
- D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004). [CrossRef] [PubMed]
- D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004). [CrossRef] [PubMed]
- Z. Papagatsia, A. Tappuni, T. F. Watson, and R. J. Cook, “Single wavelength micro-endoscopy in non-surgical vascular lesion diagnosis & characterization,” J. Microsc. 230(2), 203–211 (2008). [CrossRef] [PubMed]
- D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004). [CrossRef] [PubMed]
- A. Cobos-Correa, J. B. Trojanek, S. Diemer, M. A. Mall, and C. Schultz, “Membrane-bound FRET probe visualizes MMP12 activity in pulmonary inflammation,” Nat. Chem. Biol. 5(9), 628–630 (2009). [CrossRef] [PubMed]
- F. S. Wouters, P. J. Verveer, and P. I. Bastiaens, “Imaging biochemistry inside cells,” Trends Cell Biol. 11(5), 203–211 (2001). [CrossRef] [PubMed]
- A. J. Vila-Coro, J. M. Rodríguez-Frade, A. Martín De Ana, M. C. Moreno-Ortíz, C. Martínez-A, and M. Mellado, “The chemokine SDF-1alpha triggers CXCR4 receptor dimerization and activates the JAK/STAT pathway,” FASEB J. 13(13), 1699–1710 (1999). [PubMed]
- P. R. Barber, S. M. Ameer-Beg, J. Gilbey, L. M. Carlin, M. Keppler, T. Ng, and B. Vojnovic, “Multiphoton time-domain fluorescence lifetime imaging microscopy: practical application to protein–protein interactions using global analysis,” J. R. Soc. Interface 6(0), 93–105 (2009). [CrossRef]
- K. Makrogianneli, L. M. Carlin, M. D. Keppler, D. R. Matthews, E. Ofo, A. Coolen, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, and T. Ng, “Integrating receptor signal inputs that influence small Rho GTPase activation dynamics at the immunological synapse,” Mol. Cell. Biol. 29(11), 2997–3006 (2009). [CrossRef] [PubMed]
- S. Prag, M. Parsons, M. D. Keppler, S. M. Ameer-Beg, P. Barber, J. Hunt, A. J. Beavil, R. Calvert, M. Arpin, B. Vojnovic, and T. Ng, “Activated ezrin promotes cell migration through recruitment of the GEF Dbl to lipid rafts and preferential downstream activation of Cdc42,” Mol. Biol. Cell 18(8), 2935–2948 (2007). [CrossRef] [PubMed]
- G. McConnell, J. M. Girkin, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, T. Ng, A. Banerjee, T. F. Watson, and R. J. Cook, “Time-correlated single-photon counting fluorescence lifetime confocal imaging of decayed and sound dental structures with a white-light supercontinuum source,” J. Microsc. 225(2), 126–136 (2007). [CrossRef] [PubMed]
- M. Peter, S. M. Ameer-Beg, M. K. Y. Hughes, M. D. Keppler, S. Prag, M. Marsh, B. Vojnovic, and T. Ng, “Multiphoton-FLIM quantification of the EGFP-mRFP1 FRET pair for localization of membrane receptor-kinase interactions,” Biophys. J. 88(2), 1224–1237 (2005). [CrossRef]
- M. Parsons, J. Monypenny, S. M. Ameer-Beg, T. H. Millard, L. M. Machesky, M. Peter, M. D. Keppler, G. Schiavo, R. Watson, J. Chernoff, D. Zicha, B. Vojnovic, and T. Ng, “Spatially distinct binding of Cdc42 to PAK1 and N-WASP in breast carcinoma cells,” Mol. Cell. Biol. 25(5), 1680–1695 (2005). [CrossRef] [PubMed]
- V. Calleja, S. M. Ameer-Beg, B. Vojnovic, R. Woscholski, J. Downward, and B. Larijani, “Monitoring conformational changes of proteins in cells by fluorescence lifetime imaging microscopy,” Biochem. J. 372(1), 33–40 (2003). [CrossRef] [PubMed]
- D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004). [CrossRef] [PubMed]
- M. Parsons, J. Monypenny, S. M. Ameer-Beg, T. H. Millard, L. M. Machesky, M. Peter, M. D. Keppler, G. Schiavo, R. Watson, J. Chernoff, D. Zicha, B. Vojnovic, and T. Ng, “Spatially distinct binding of Cdc42 to PAK1 and N-WASP in breast carcinoma cells,” Mol. Cell. Biol. 25(5), 1680–1695 (2005). [CrossRef] [PubMed]
- Z. Papagatsia, A. Tappuni, T. F. Watson, and R. J. Cook, “Single wavelength micro-endoscopy in non-surgical vascular lesion diagnosis & characterization,” J. Microsc. 230(2), 203–211 (2008). [CrossRef] [PubMed]
- G. McConnell, J. M. Girkin, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, T. Ng, A. Banerjee, T. F. Watson, and R. J. Cook, “Time-correlated single-photon counting fluorescence lifetime confocal imaging of decayed and sound dental structures with a white-light supercontinuum source,” J. Microsc. 225(2), 126–136 (2007). [CrossRef] [PubMed]
- D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004). [CrossRef] [PubMed]
- C. Buranachai, D. Kamiyama, A. Chiba, B. D. Williams, and R. M. Clegg, “Rapid frequency-domain FLIM spinning disk confocal microscope: lifetime resolution, image improvement and wavelet analysis,” J. Fluoresc. 18(5), 929–942 (2008). [CrossRef] [PubMed]
- H. Morise, O. Shimomura, F. H. Johnson, and J. Winant, “Intermolecular energy transfer in the bioluminescent system of Aequorea,” Biochemistry 13(12), 2656–2662 (1974). [CrossRef] [PubMed]
- W. Becker, H. Hickl, C. Zander, K. H. Drexhage, M. Sauer, S. Siebert, and J. Wolfrum, “Time-resolved detection and identification of single analyte molecules in microcapillaries by time-correlated single photon counting,” Rev. Sci. Instrum. 70(3), 1835–1841 (1999). [CrossRef]
- V. Calleja, S. M. Ameer-Beg, B. Vojnovic, R. Woscholski, J. Downward, and B. Larijani, “Monitoring conformational changes of proteins in cells by fluorescence lifetime imaging microscopy,” Biochem. J. 372(1), 33–40 (2003). [CrossRef] [PubMed]
- F. S. Wouters, P. J. Verveer, and P. I. Bastiaens, “Imaging biochemistry inside cells,” Trends Cell Biol. 11(5), 203–211 (2001). [CrossRef] [PubMed]
- F. S. Wouters and P. I. Bastiaens, “Fluorescence lifetime imaging of receptor tyrosine kinase activity in cells,” Curr. Biol. 9(19), 1127–1130 (1999). [CrossRef] [PubMed]
- T. Y. Lee, C. T. Lin, S. Y. Kuo, D. K. Chang, and H. C. Wu, “Peptide-mediated targeting to tumor blood vessels of lung cancer for drug delivery,” Cancer Res. 67(22), 10958–10965 (2007). [CrossRef] [PubMed]
- H. Bar, I. Yacoby, and I. Benhar, “Killing cancer cells by targeted drug-carrying phage nanomedicines,” BMC Biotechnol. 8(1), 37 (2008). [CrossRef] [PubMed]
- W. Becker, H. Hickl, C. Zander, K. H. Drexhage, M. Sauer, S. Siebert, and J. Wolfrum, “Time-resolved detection and identification of single analyte molecules in microcapillaries by time-correlated single photon counting,” Rev. Sci. Instrum. 70(3), 1835–1841 (1999). [CrossRef]
- M. Parsons, J. Monypenny, S. M. Ameer-Beg, T. H. Millard, L. M. Machesky, M. Peter, M. D. Keppler, G. Schiavo, R. Watson, J. Chernoff, D. Zicha, B. Vojnovic, and T. Ng, “Spatially distinct binding of Cdc42 to PAK1 and N-WASP in breast carcinoma cells,” Mol. Cell. Biol. 25(5), 1680–1695 (2005). [CrossRef] [PubMed]
Ann. Phys.
- T. Förster, “Intermolecular energy migration and fluorescence,” Ann. Phys. 2, 55 (1948). [CrossRef]
Annu. Rev. Biochem.
- L. Stryer, “Fluorescence energy transfer as a spectroscopic ruler,” Annu. Rev. Biochem. 47(1), 819–846 (1978). [CrossRef] [PubMed]
Appl. Opt.
- A. Schönle, M. Glatz, and S. W. Hell, “Four-dimensional multiphoton microscopy with time-correlated single-photon counting,” Appl. Opt. 39(34), 6306–6311 (2000). [CrossRef]
Biochem. J.
- V. Calleja, S. M. Ameer-Beg, B. Vojnovic, R. Woscholski, J. Downward, and B. Larijani, “Monitoring conformational changes of proteins in cells by fluorescence lifetime imaging microscopy,” Biochem. J. 372(1), 33–40 (2003). [CrossRef] [PubMed]
Biochemistry
- H. Morise, O. Shimomura, F. H. Johnson, and J. Winant, “Intermolecular energy transfer in the bioluminescent system of Aequorea,” Biochemistry 13(12), 2656–2662 (1974). [CrossRef] [PubMed]
Biol. Cell
- M. Peter and S. M. Ameer-Beg, “Imaging molecular interactions by multiphoton FLIM,” Biol. Cell 96(3), 231–236 (2004). [CrossRef] [PubMed]
Biophys. Chem.
- T. W. J. Gadella, T. M. Jovin, and R. M. Clegg, “Fluorescence lifetime imaging microscopy (FLIM): Spatial resolution of microstructures on the nanosecond time scale,” Biophys. Chem. 48(2), 221–239 (1993). [CrossRef]
Biophys. J.
- M. Peter, S. M. Ameer-Beg, M. K. Y. Hughes, M. D. Keppler, S. Prag, M. Marsh, B. Vojnovic, and T. Ng, “Multiphoton-FLIM quantification of the EGFP-mRFP1 FRET pair for localization of membrane receptor-kinase interactions,” Biophys. J. 88(2), 1224–1237 (2005). [CrossRef]
BMC Biotechnol.
- H. Bar, I. Yacoby, and I. Benhar, “Killing cancer cells by targeted drug-carrying phage nanomedicines,” BMC Biotechnol. 8(1), 37 (2008). [CrossRef] [PubMed]
Cancer Res.
- T. Y. Lee, C. T. Lin, S. Y. Kuo, D. K. Chang, and H. C. Wu, “Peptide-mediated targeting to tumor blood vessels of lung cancer for drug delivery,” Cancer Res. 67(22), 10958–10965 (2007). [CrossRef] [PubMed]
Curr. Biol.
- F. S. Wouters and P. I. Bastiaens, “Fluorescence lifetime imaging of receptor tyrosine kinase activity in cells,” Curr. Biol. 9(19), 1127–1130 (1999). [CrossRef] [PubMed]
EMBO J.
- T. Ng, D. Shima, A. Squire, P. I. H. Bastiaens, S. Gschmeissner, M. J. Humphries, and P. J. Parker, “PKCalpha regulates beta1 integrin-dependent cell motility through association and control of integrin traffic,” EMBO J. 18, 3909–3923 (1999). [CrossRef] [PubMed]
Faraday Discuss.
- H. Lomas, M. Massignani, K. A. Abdullah, I. Canton, C. Lo Presti, S. MacNeil, J. Du, A. Blanazs, J. Madsen, S. P. Armes, A. L. Lewis, and G. Battaglia, “Non-cytotoxic polymer vesicles for rapid and efficient intracellular delivery,” Faraday Discuss. 139, 143–159, discussion 213–228, 419–420 (2008). [CrossRef] [PubMed]
FASEB J.
- A. J. Vila-Coro, J. M. Rodríguez-Frade, A. Martín De Ana, M. C. Moreno-Ortíz, C. Martínez-A, and M. Mellado, “The chemokine SDF-1alpha triggers CXCR4 receptor dimerization and activates the JAK/STAT pathway,” FASEB J. 13(13), 1699–1710 (1999). [PubMed]
J. Biol. Chem.
- G. J. Babcock, M. Farzan, and J. Sodroski, “Ligand-independent dimerization of CXCR4, a principal HIV-1 coreceptor,” J. Biol. Chem. 278(5), 3378–3385 (2003). [CrossRef]
J. Biomed. Opt.
- I. Munro, J. McGinty, N. Galletly, J. Requejo-Isidro, P. M. P. Lanigan, D. S. Elson, C. Dunsby, M. A. Neil, M. J. Lever, G. W. Stamp, and P. M. French, “Toward the clinical application of time-domain fluorescence lifetime imaging,” J. Biomed. Opt. 10(5), 051403 (2005). [CrossRef] [PubMed]
- S. Pelet, M. J. R. Previte, and P. T. So, “Comparing the quantification of Forster resonance energy transfer measurement accuracies based on intensity, spectral, and lifetime imaging,” J. Biomed. Opt. 11(3), 034017 (2006). [CrossRef]
J. Fluoresc.
- C. Buranachai, D. Kamiyama, A. Chiba, B. D. Williams, and R. M. Clegg, “Rapid frequency-domain FLIM spinning disk confocal microscope: lifetime resolution, image improvement and wavelet analysis,” J. Fluoresc. 18(5), 929–942 (2008). [CrossRef] [PubMed]
J. Mater. Chem.
- C. LoPresti, H. Lomas, M. Massignani, T. Smart, and G. Battaglia, “Polymersomes: nature inspired nanometer sized compartments,” J. Mater. Chem. 19(22), 3576–3590 (2009). [CrossRef]
J. Microsc.
- R. R. Duncan, A. Bergmann, M. A. Cousin, D. K. Apps, and M. J. Shipston, “Multi-dimensional time-correlated single photon counting (TCSPC) fluorescence lifetime imaging microscopy (FLIM) to detect FRET in cells,” J. Microsc. 215(1), 1–12 (2004). [CrossRef] [PubMed]
- G. McConnell, J. M. Girkin, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, T. Ng, A. Banerjee, T. F. Watson, and R. J. Cook, “Time-correlated single-photon counting fluorescence lifetime confocal imaging of decayed and sound dental structures with a white-light supercontinuum source,” J. Microsc. 225(2), 126–136 (2007). [CrossRef] [PubMed]
- Z. Papagatsia, A. Tappuni, T. F. Watson, and R. J. Cook, “Single wavelength micro-endoscopy in non-surgical vascular lesion diagnosis & characterization,” J. Microsc. 230(2), 203–211 (2008). [CrossRef] [PubMed]
J. R. Soc. Interface
- P. R. Barber, S. M. Ameer-Beg, J. Gilbey, L. M. Carlin, M. Keppler, T. Ng, and B. Vojnovic, “Multiphoton time-domain fluorescence lifetime imaging microscopy: practical application to protein–protein interactions using global analysis,” J. R. Soc. Interface 6(0), 93–105 (2009). [CrossRef]
Mol. Biol. Cell
- S. Prag, M. Parsons, M. D. Keppler, S. M. Ameer-Beg, P. Barber, J. Hunt, A. J. Beavil, R. Calvert, M. Arpin, B. Vojnovic, and T. Ng, “Activated ezrin promotes cell migration through recruitment of the GEF Dbl to lipid rafts and preferential downstream activation of Cdc42,” Mol. Biol. Cell 18(8), 2935–2948 (2007). [CrossRef] [PubMed]
Mol. Biosyst.
- F. Festy, S. M. Ameer-Beg, T. Ng, and K. Suhling, “Imaging proteins in vivo using fluorescence lifetime microscopy,” Mol. Biosyst. 3(6), 381–391 (2007). [CrossRef] [PubMed]
Mol. Cell. Biol.
- M. Parsons, J. Monypenny, S. M. Ameer-Beg, T. H. Millard, L. M. Machesky, M. Peter, M. D. Keppler, G. Schiavo, R. Watson, J. Chernoff, D. Zicha, B. Vojnovic, and T. Ng, “Spatially distinct binding of Cdc42 to PAK1 and N-WASP in breast carcinoma cells,” Mol. Cell. Biol. 25(5), 1680–1695 (2005). [CrossRef] [PubMed]
- K. Makrogianneli, L. M. Carlin, M. D. Keppler, D. R. Matthews, E. Ofo, A. Coolen, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, and T. Ng, “Integrating receptor signal inputs that influence small Rho GTPase activation dynamics at the immunological synapse,” Mol. Cell. Biol. 29(11), 2997–3006 (2009). [CrossRef] [PubMed]
Nat. Biotechnol.
- E. A. Jares-Erijman and T. M. Jovin, “FRET imaging,” Nat. Biotechnol. 21(11), 1387–1395 (2003). [CrossRef] [PubMed]
Nat. Chem. Biol.
- A. Cobos-Correa, J. B. Trojanek, S. Diemer, M. A. Mall, and C. Schultz, “Membrane-bound FRET probe visualizes MMP12 activity in pulmonary inflammation,” Nat. Chem. Biol. 5(9), 628–630 (2009). [CrossRef] [PubMed]
Nat. Methods
- E. M. Merzlyak, J. Goedhart, D. Shcherbo, M. E. Bulina, A. S. Shcheglov, A. F. Fradkov, A. Gaintzeva, K. A. Lukyanov, S. Lukyanov, T. W. Gadella, and D. M. Chudakov, “Bright monomeric red fluorescent protein with an extended fluorescence lifetime,” Nat. Methods 4(7), 555–557 (2007). [CrossRef] [PubMed]
Opt. Express
- S. Kumar, C. Dunsby, P. A. A. De Beule, D. M. Owen, U. Anand, P. M. P. Lanigan, R. K. P. Benninger, D. M. Davis, M. A. Neil, P. Anand, C. Benham, A. Naylor, and P. M. French, “Multifocal multiphoton excitation and time correlated single photon counting detection for 3-D fluorescence lifetime imaging,” Opt. Express 15(20), 12548–12561 (2007). [CrossRef] [PubMed]
Opt. Lett.
- J. Requejo-Isidro, J. McGinty, I. Munro, D. S. Elson, N. P. Galletly, M. J. Lever, M. A. A. Neil, G. W. Stamp, P. M. French, P. A. Kellett, J. D. Hares, and A. K. Dymoke-Bradshaw, “High-speed wide-field time-gated endoscopic fluorescence-lifetime imaging,” Opt. Lett. 29(19), 2249–2251 (2004). [CrossRef] [PubMed]
Oral Oncol.
- R. El-Gazzar, M. Macluskey, and G. R. Ogden, “Evidence for a field change effect based on angiogenesis in the oral mucosa? A brief report,” Oral Oncol. 41(1), 25–30 (2005). [CrossRef]
Photochem. Photobiol. Sci.
- K. Suhling, P. M. French, and D. Phillips, “Time-resolved fluorescence microscopy,” Photochem. Photobiol. Sci. 4(1), 13–22 (2005). [CrossRef]
- D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004). [CrossRef] [PubMed]
Proc. Natl. Acad. Sci. U.S.A.
- C. C. Fjeld, W. T. Birdsong, and R. H. Goodman, “Differential binding of NAD+ and NADH allows the transcriptional corepressor carboxyl-terminal binding protein to serve as a metabolic sensor,” Proc. Natl. Acad. Sci. U.S.A. 100(16), 9202–9207 (2003). [CrossRef] [PubMed]
Procs. Nat. Acad. Sci.
- R. Maeda-Mamiya, E. Noiri, H. Isobe, W. Nakanishi, K. Okamoto, K. Doi, T. Sugaya, T. Izumi, T. Homma, and E. Nakamura, “In vivo gene delivery by cationic tetraamino fullerene,” Procs. Nat. Acad. Sci. 107(12), 5339–5344 (2010). [CrossRef]
Rev. Sci. Instrum.
- W. Becker, H. Hickl, C. Zander, K. H. Drexhage, M. Sauer, S. Siebert, and J. Wolfrum, “Time-resolved detection and identification of single analyte molecules in microcapillaries by time-correlated single photon counting,” Rev. Sci. Instrum. 70(3), 1835–1841 (1999). [CrossRef]
Science
- T. Ng, A. Squire, G. Hansra, F. Bornancin, C. Prevostel, A. Hanby, W. Harris, D. Barnes, S. Schmidt, H. Mellor, P. I. Bastiaens, and P. J. Parker, “Imaging protein kinase Calpha activation in cells,” Science 283(5410), 2085–2089 (1999). [CrossRef] [PubMed]
Trends Cell Biol.
- F. S. Wouters, P. J. Verveer, and P. I. Bastiaens, “Imaging biochemistry inside cells,” Trends Cell Biol. 11(5), 203–211 (2001). [CrossRef] [PubMed]
Other
- P. Cotton, and C. Williams, Practical gastrointestinal endoscopy (Blackwell Science, 2003).
2010, Maeda-Mamiya, Procs. Nat. Acad. Sci.
- R. Maeda-Mamiya, E. Noiri, H. Isobe, W. Nakanishi, K. Okamoto, K. Doi, T. Sugaya, T. Izumi, T. Homma, and E. Nakamura, “In vivo gene delivery by cationic tetraamino fullerene,” Procs. Nat. Acad. Sci. 107(12), 5339–5344 (2010). [CrossRef]
- C. LoPresti, H. Lomas, M. Massignani, T. Smart, and G. Battaglia, “Polymersomes: nature inspired nanometer sized compartments,” J. Mater. Chem. 19(22), 3576–3590 (2009). [CrossRef]
- P. R. Barber, S. M. Ameer-Beg, J. Gilbey, L. M. Carlin, M. Keppler, T. Ng, and B. Vojnovic, “Multiphoton time-domain fluorescence lifetime imaging microscopy: practical application to protein–protein interactions using global analysis,” J. R. Soc. Interface 6(0), 93–105 (2009). [CrossRef]
- K. Makrogianneli, L. M. Carlin, M. D. Keppler, D. R. Matthews, E. Ofo, A. Coolen, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, and T. Ng, “Integrating receptor signal inputs that influence small Rho GTPase activation dynamics at the immunological synapse,” Mol. Cell. Biol. 29(11), 2997–3006 (2009). [CrossRef] [PubMed]
- A. Cobos-Correa, J. B. Trojanek, S. Diemer, M. A. Mall, and C. Schultz, “Membrane-bound FRET probe visualizes MMP12 activity in pulmonary inflammation,” Nat. Chem. Biol. 5(9), 628–630 (2009). [CrossRef] [PubMed]
- H. Lomas, M. Massignani, K. A. Abdullah, I. Canton, C. Lo Presti, S. MacNeil, J. Du, A. Blanazs, J. Madsen, S. P. Armes, A. L. Lewis, and G. Battaglia, “Non-cytotoxic polymer vesicles for rapid and efficient intracellular delivery,” Faraday Discuss. 139, 143–159, discussion 213–228, 419–420 (2008). [CrossRef] [PubMed]
- H. Bar, I. Yacoby, and I. Benhar, “Killing cancer cells by targeted drug-carrying phage nanomedicines,” BMC Biotechnol. 8(1), 37 (2008). [CrossRef] [PubMed]
- Z. Papagatsia, A. Tappuni, T. F. Watson, and R. J. Cook, “Single wavelength micro-endoscopy in non-surgical vascular lesion diagnosis & characterization,” J. Microsc. 230(2), 203–211 (2008). [CrossRef] [PubMed]
- C. Buranachai, D. Kamiyama, A. Chiba, B. D. Williams, and R. M. Clegg, “Rapid frequency-domain FLIM spinning disk confocal microscope: lifetime resolution, image improvement and wavelet analysis,” J. Fluoresc. 18(5), 929–942 (2008). [CrossRef] [PubMed]
- F. Festy, S. M. Ameer-Beg, T. Ng, and K. Suhling, “Imaging proteins in vivo using fluorescence lifetime microscopy,” Mol. Biosyst. 3(6), 381–391 (2007). [CrossRef] [PubMed]
- G. McConnell, J. M. Girkin, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, T. Ng, A. Banerjee, T. F. Watson, and R. J. Cook, “Time-correlated single-photon counting fluorescence lifetime confocal imaging of decayed and sound dental structures with a white-light supercontinuum source,” J. Microsc. 225(2), 126–136 (2007). [CrossRef] [PubMed]
- T. Y. Lee, C. T. Lin, S. Y. Kuo, D. K. Chang, and H. C. Wu, “Peptide-mediated targeting to tumor blood vessels of lung cancer for drug delivery,” Cancer Res. 67(22), 10958–10965 (2007). [CrossRef] [PubMed]
- E. M. Merzlyak, J. Goedhart, D. Shcherbo, M. E. Bulina, A. S. Shcheglov, A. F. Fradkov, A. Gaintzeva, K. A. Lukyanov, S. Lukyanov, T. W. Gadella, and D. M. Chudakov, “Bright monomeric red fluorescent protein with an extended fluorescence lifetime,” Nat. Methods 4(7), 555–557 (2007). [CrossRef] [PubMed]
- S. Prag, M. Parsons, M. D. Keppler, S. M. Ameer-Beg, P. Barber, J. Hunt, A. J. Beavil, R. Calvert, M. Arpin, B. Vojnovic, and T. Ng, “Activated ezrin promotes cell migration through recruitment of the GEF Dbl to lipid rafts and preferential downstream activation of Cdc42,” Mol. Biol. Cell 18(8), 2935–2948 (2007). [CrossRef] [PubMed]
- S. Kumar, C. Dunsby, P. A. A. De Beule, D. M. Owen, U. Anand, P. M. P. Lanigan, R. K. P. Benninger, D. M. Davis, M. A. Neil, P. Anand, C. Benham, A. Naylor, and P. M. French, “Multifocal multiphoton excitation and time correlated single photon counting detection for 3-D fluorescence lifetime imaging,” Opt. Express 15(20), 12548–12561 (2007). [CrossRef] [PubMed]
- S. Pelet, M. J. R. Previte, and P. T. So, “Comparing the quantification of Forster resonance energy transfer measurement accuracies based on intensity, spectral, and lifetime imaging,” J. Biomed. Opt. 11(3), 034017 (2006). [CrossRef]
- M. Parsons, J. Monypenny, S. M. Ameer-Beg, T. H. Millard, L. M. Machesky, M. Peter, M. D. Keppler, G. Schiavo, R. Watson, J. Chernoff, D. Zicha, B. Vojnovic, and T. Ng, “Spatially distinct binding of Cdc42 to PAK1 and N-WASP in breast carcinoma cells,” Mol. Cell. Biol. 25(5), 1680–1695 (2005). [CrossRef] [PubMed]
- M. Peter, S. M. Ameer-Beg, M. K. Y. Hughes, M. D. Keppler, S. Prag, M. Marsh, B. Vojnovic, and T. Ng, “Multiphoton-FLIM quantification of the EGFP-mRFP1 FRET pair for localization of membrane receptor-kinase interactions,” Biophys. J. 88(2), 1224–1237 (2005). [CrossRef]
- K. Suhling, P. M. French, and D. Phillips, “Time-resolved fluorescence microscopy,” Photochem. Photobiol. Sci. 4(1), 13–22 (2005). [CrossRef]
- R. El-Gazzar, M. Macluskey, and G. R. Ogden, “Evidence for a field change effect based on angiogenesis in the oral mucosa? A brief report,” Oral Oncol. 41(1), 25–30 (2005). [CrossRef]
- I. Munro, J. McGinty, N. Galletly, J. Requejo-Isidro, P. M. P. Lanigan, D. S. Elson, C. Dunsby, M. A. Neil, M. J. Lever, G. W. Stamp, and P. M. French, “Toward the clinical application of time-domain fluorescence lifetime imaging,” J. Biomed. Opt. 10(5), 051403 (2005). [CrossRef] [PubMed]
- R. R. Duncan, A. Bergmann, M. A. Cousin, D. K. Apps, and M. J. Shipston, “Multi-dimensional time-correlated single photon counting (TCSPC) fluorescence lifetime imaging microscopy (FLIM) to detect FRET in cells,” J. Microsc. 215(1), 1–12 (2004). [CrossRef] [PubMed]
- J. Requejo-Isidro, J. McGinty, I. Munro, D. S. Elson, N. P. Galletly, M. J. Lever, M. A. A. Neil, G. W. Stamp, P. M. French, P. A. Kellett, J. D. Hares, and A. K. Dymoke-Bradshaw, “High-speed wide-field time-gated endoscopic fluorescence-lifetime imaging,” Opt. Lett. 29(19), 2249–2251 (2004). [CrossRef] [PubMed]
- D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004). [CrossRef] [PubMed]
- M. Peter and S. M. Ameer-Beg, “Imaging molecular interactions by multiphoton FLIM,” Biol. Cell 96(3), 231–236 (2004). [CrossRef] [PubMed]
- E. A. Jares-Erijman and T. M. Jovin, “FRET imaging,” Nat. Biotechnol. 21(11), 1387–1395 (2003). [CrossRef] [PubMed]
- V. Calleja, S. M. Ameer-Beg, B. Vojnovic, R. Woscholski, J. Downward, and B. Larijani, “Monitoring conformational changes of proteins in cells by fluorescence lifetime imaging microscopy,” Biochem. J. 372(1), 33–40 (2003). [CrossRef] [PubMed]
- C. C. Fjeld, W. T. Birdsong, and R. H. Goodman, “Differential binding of NAD+ and NADH allows the transcriptional corepressor carboxyl-terminal binding protein to serve as a metabolic sensor,” Proc. Natl. Acad. Sci. U.S.A. 100(16), 9202–9207 (2003). [CrossRef] [PubMed]
- G. J. Babcock, M. Farzan, and J. Sodroski, “Ligand-independent dimerization of CXCR4, a principal HIV-1 coreceptor,” J. Biol. Chem. 278(5), 3378–3385 (2003). [CrossRef]
- F. S. Wouters, P. J. Verveer, and P. I. Bastiaens, “Imaging biochemistry inside cells,” Trends Cell Biol. 11(5), 203–211 (2001). [CrossRef] [PubMed]
- T. Ng, A. Squire, G. Hansra, F. Bornancin, C. Prevostel, A. Hanby, W. Harris, D. Barnes, S. Schmidt, H. Mellor, P. I. Bastiaens, and P. J. Parker, “Imaging protein kinase Calpha activation in cells,” Science 283(5410), 2085–2089 (1999). [CrossRef] [PubMed]
- T. Ng, D. Shima, A. Squire, P. I. H. Bastiaens, S. Gschmeissner, M. J. Humphries, and P. J. Parker, “PKCalpha regulates beta1 integrin-dependent cell motility through association and control of integrin traffic,” EMBO J. 18, 3909–3923 (1999). [CrossRef] [PubMed]
- F. S. Wouters and P. I. Bastiaens, “Fluorescence lifetime imaging of receptor tyrosine kinase activity in cells,” Curr. Biol. 9(19), 1127–1130 (1999). [CrossRef] [PubMed]
- W. Becker, H. Hickl, C. Zander, K. H. Drexhage, M. Sauer, S. Siebert, and J. Wolfrum, “Time-resolved detection and identification of single analyte molecules in microcapillaries by time-correlated single photon counting,” Rev. Sci. Instrum. 70(3), 1835–1841 (1999). [CrossRef]
- A. J. Vila-Coro, J. M. Rodríguez-Frade, A. Martín De Ana, M. C. Moreno-Ortíz, C. Martínez-A, and M. Mellado, “The chemokine SDF-1alpha triggers CXCR4 receptor dimerization and activates the JAK/STAT pathway,” FASEB J. 13(13), 1699–1710 (1999). [PubMed]
- T. W. J. Gadella, T. M. Jovin, and R. M. Clegg, “Fluorescence lifetime imaging microscopy (FLIM): Spatial resolution of microstructures on the nanosecond time scale,” Biophys. Chem. 48(2), 221–239 (1993). [CrossRef]
- L. Stryer, “Fluorescence energy transfer as a spectroscopic ruler,” Annu. Rev. Biochem. 47(1), 819–846 (1978). [CrossRef] [PubMed]
- H. Morise, O. Shimomura, F. H. Johnson, and J. Winant, “Intermolecular energy transfer in the bioluminescent system of Aequorea,” Biochemistry 13(12), 2656–2662 (1974). [CrossRef] [PubMed]
- T. Förster, “Intermolecular energy migration and fluorescence,” Ann. Phys. 2, 55 (1948). [CrossRef]
Cited By |
 Alert me when this paper is cited |
OSA is able to provide readers links to articles that cite this paper by participating in CrossRef's Cited-By Linking service. CrossRef includes content from more than 3000 publishers and societies. In addition to listing OSA journal articles that cite this paper, citing articles from other participating publishers will also be listed.
Related Journal Articles 
- Slit-Scanning Confocal Microendoscope for High-Resolution In Vivo Imaging (AO)
- Multiphoton endoscopy (OL)
- Enhancing early bladder cancer detection with fluorescence-guided endoscopic optical coherent tomography (OL)
- In vivo fluorescence microscopy of neuronal activity in three dimensions by use of voltage-sensitive dyes (OL)
- Design and Demonstration of a Miniature Catheter for a Confocal Microendoscope (AO)
Related Conference Papers
- Fluorescence endoscopic imaging of the pancreas
- In vivo Fluorescence Endoscopic Cellular Imaging of Internal Organs in Mice
- In vivo Fluorescence Cellular Imaging by Side-view Endomicroscopy
- Spectrally Encoded Fluorescence Imaging Based on a Wavelength-Swept Source
- A Side-View Confocal Microendoscope for In Vivo Sagittal Imaging of the Mouse Brain
« Previous Article | Next Article »
OSA is a member of 
For optimal display we recommend the following web browsers:
- Firefox 11+
- Google Chrome 17+
- Internet Explorer 9+
- Safari 5+