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Quantitative tomographic imaging of intermolecular FRET in small animalsVivek Venugopal, Jin Chen, Margarida Barroso, and Xavier Intes »View Author Affiliations
Vivek Venugopal,1,3
Jin Chen,1
Margarida Barroso,2
and Xavier Intes1,*
1Department of Biomedical Engineering, Rensselaer Polytechnic Institute, 110 8th Street, Troy, New York. 12180, USA 2Center for Cardiovascular Sciences, Albany Medical College, 43 New Scotland Avenue, Albany, New York, 12208, USA 3Currently with the Center for Molecular Imaging, Beth Israel Deaconess Medical Center, 330 Brookline Avenue, Boston, Massachusetts 02215, USA *Corresponding author: intesx@rpi.edu |
Biomedical Optics Express, Vol. 3, Issue 12, pp. 3161-3175 (2012)
http://dx.doi.org/10.1364/BOE.3.003161
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Abstract
Forster resonance energy transfer (FRET) is a nonradiative transfer of energy between two fluorescent molecules (a donor and an acceptor) in nanometer range proximity. FRET imaging methods have been applied to proteomic studies and drug discovery applications based on intermolecular FRET efficiency measurements and stoichiometric measurements of FRET interaction as quantitative parameters of interest. Importantly, FRET provides information about biomolecular interactions at a molecular level, well beyond the diffraction limits of standard microscopy techniques. The application of FRET to small animal imaging will allow biomedical researchers to investigate physiological processes occurring at nanometer range in vivo as well as in situ. In this work a new method for the quantitative reconstruction of FRET measurements in small animals, incorporating a full-field tomographic acquisition system with a Monte Carlo based hierarchical reconstruction scheme, is described and validated in murine models. Our main objective is to estimate the relative concentration of two forms of donor species, i.e., a donor molecule involved in FRETing to an acceptor close by and a nonFRETing donor molecule.
© 2012 OSA
OCIS Codes
(170.3650) Medical optics and biotechnology : Lifetime-based sensing
(170.6920) Medical optics and biotechnology : Time-resolved imaging
(110.6955) Imaging systems : Tomographic imaging
ToC Category:
Image Reconstruction and Inverse Problems
History
Original Manuscript: August 2, 2012
Revised Manuscript: October 15, 2012
Manuscript Accepted: October 15, 2012
Published: November 8, 2012
Citation
Vivek Venugopal, Jin Chen, Margarida Barroso, and Xavier Intes, "Quantitative tomographic imaging of intermolecular FRET in small
animals," Biomed. Opt. Express 3, 3161-3175 (2012)
http://www.opticsinfobase.org/boe/abstract.cfm?URI=boe-3-12-3161
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- H. Wallrabe and A. Periasamy, “Imaging protein molecules using FRET and FLIM microscopy,” Curr. Opin. Biotechnol.16(1), 19–27 (2005). [CrossRef] [PubMed]
- V. Ntziachristos, J. Ripoll, L. V. Wang, and R. Weissleder, “Looking and listening to light: the evolution of whole-body photonic imaging,” Nat. Biotechnol.23(3), 313–320 (2005). [CrossRef] [PubMed]
- S. Kumar, D. Alibhai, A. Margineanu, R. Laine, G. Kennedy, J. McGinty, S. Warren, D. Kelly, Y. Alexandrov, I. Munro, C. Talbot, D. W. Stuckey, C. Kimberly, B. Viellerobe, F. Lacombe, E. W.-F. Lam, H. Taylor, M. J. Dallman, G. Stamp, E. J. Murray, F. Stuhmeier, A. Sardini, M. Katan, D. S. Elson, M. A. A. Neil, C. Dunsby, and P. M. W. French, “FLIM FRET technology for drug discovery: automated multiwell-plate high-content analysis, multiplexed readouts and application in situ,” ChemPhysChem12(3), 609–626 (2011). [CrossRef] [PubMed]
- V. Gaind, S. Kularatne, P. S. Low, and K. J. Webb, “Deep-tissue imaging of intramolecular fluorescence resonance energy-transfer parameters,” Opt. Lett.35(9), 1314–1316 (2010). [CrossRef] [PubMed]
- V. Gaind, K. J. Webb, S. Kularatne, and C. A. Bouman, “Towards in vivo imaging of intramolecular fluorescence resonance energy transfer parameters,” J. Opt. Soc. Am. A26(8), 1805–1813 (2009). [CrossRef] [PubMed]
- M. J. Niedre, R. H. de Kleine, E. Aikawa, D. G. Kirsch, R. Weissleder, and V. Ntziachristos, “Early photon tomography allows fluorescence detection of lung carcinomas and disease progression in mice in vivo,” Proc. Natl. Acad. Sci. U.S.A.105(49), 19126–19131 (2008). [CrossRef] [PubMed]
- V. Ntziachristos, J. Ripoll, L. V. Wang, and R. Weissleder, “Looking and listening to light: the evolution of whole-body photonic imaging,” Nat. Biotechnol.23(3), 313–320 (2005). [CrossRef] [PubMed]
- V. Ntziachristos and R. Weissleder, “Experimental three-dimensional fluorescence reconstruction of diffuse media by use of a normalized Born approximation,” Opt. Lett.26(12), 893–895 (2001). [CrossRef] [PubMed]
- N. Mochizuki, S. Yamashita, K. Kurokawa, Y. Ohba, T. Nagai, A. Miyawaki, and M. Matsuda, “Spatio-temporal images of growth-factor-induced activation of Ras and Rap1,” Nature411(6841), 1065–1068 (2001). [CrossRef] [PubMed]
- K. M. Yoo, F. Liu, and R. R. Alfano, “When does the diffusion approximation fail to describe photon transport in random media?” Phys. Rev. Lett.64(22), 2647–2650 (1990). [CrossRef] [PubMed]
- T. Nishioka, K. Aoki, K. Hikake, H. Yoshizaki, E. Kiyokawa, and M. Matsuda, “Rapid turnover rate of phosphoinositides at the front of migrating MDCK cells,” Mol. Biol. Cell19(10), 4213–4223 (2008). [CrossRef] [PubMed]
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Annu. Rev. Biochem.
- B. Huang, M. Bates, and X. Zhuang, “Super-resolution fluorescence microscopy,” Annu. Rev. Biochem.78(1), 993–1016 (2009). [CrossRef] [PubMed]
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Appl. Opt.
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Biochim. Biophys. Acta
- A. Nezu, A. Tanimura, T. Morita, A. Shitara, and Y. Tojyo, “A novel fluorescent method employing the FRET-based biosensor “LIBRA” for the identification of ligands of the inositol 1,4,5-trisphosphate receptors,” Biochim. Biophys. Acta1760(8), 1274–1280 (2006). [CrossRef] [PubMed]
Biomed. Opt. Express
- J. Chen, V. Venugopal, and X. Intes, “Monte Carlo based method for fluorescence tomographic imaging with lifetime multiplexing using time gates,” Biomed. Opt. Express2(4), 871–886 (2011). [CrossRef] [PubMed]
Biomed. Opt. Express
- V. Venugopal, J. Chen, and X. Intes, “Development of an optical imaging platform for functional imaging of small animals using wide-field excitation,” Biomed. Opt. Express1(1), 143–156 (2010). [CrossRef] [PubMed]
- J. McGinty, D. W. Stuckey, V. Y. Soloviev, R. Laine, M. Wylezinska-Arridge, D. J. Wells, S. R. Arridge, P. M. W. French, J. V. Hajnal, and A. Sardini, “In vivo fluorescence lifetime tomography of a FRET probe expressed in mouse,” Biomed. Opt. Express2(7), 1907–1917 (2011). [CrossRef] [PubMed]
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Biophys. J.
- M. Mank, D. F. Reiff, N. Heim, M. W. Friedrich, A. Borst, and O. Griesbeck, “A FRET-based calcium biosensor with fast signal kinetics and high fluorescence change,” Biophys. J.90(5), 1790–1796 (2006). [CrossRef] [PubMed]
- S. Padilla-Parra, N. Audugé, M. Coppey-Moisan, and M. Tramier, “Quantitative FRET analysis by fast acquisition time domain FLIM at high spatial resolution in living cells,” Biophys. J.95(6), 2976–2988 (2008). [CrossRef] [PubMed]
- P. J. Verveer, A. Squire, and P. I. Bastiaens, “Global analysis of fluorescence lifetime imaging microscopy data,” Biophys. J.78(4), 2127–2137 (2000). [CrossRef] [PubMed]
- M. Y. Berezin, K. Guo, W. Akers, R. E. Northdurft, J. P. Culver, B. Teng, O. Vasalatiy, K. Barbacow, A. Gandjbakhche, G. L. Griffiths, and S. Achilefu, “Near-infrared fluorescence lifetime pH-sensitive probes,” Biophys. J.100(8), 2063–2072 (2011). [CrossRef] [PubMed]
Biotechnol. Lett.
- I. T. Li, E. Pham, and K. Truong, “Protein biosensors based on the principle of fluorescence resonance energy transfer for monitoring cellular dynamics,” Biotechnol. Lett.28(24), 1971–1982 (2006). [CrossRef] [PubMed]
ChemPhysChem
- S. Kumar, D. Alibhai, A. Margineanu, R. Laine, G. Kennedy, J. McGinty, S. Warren, D. Kelly, Y. Alexandrov, I. Munro, C. Talbot, D. W. Stuckey, C. Kimberly, B. Viellerobe, F. Lacombe, E. W.-F. Lam, H. Taylor, M. J. Dallman, G. Stamp, E. J. Murray, F. Stuhmeier, A. Sardini, M. Katan, D. S. Elson, M. A. A. Neil, C. Dunsby, and P. M. W. French, “FLIM FRET technology for drug discovery: automated multiwell-plate high-content analysis, multiplexed readouts and application in situ,” ChemPhysChem12(3), 609–626 (2011). [CrossRef] [PubMed]
Curr. Opin. Biotechnol.
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Curr. Opin. Chem. Biol.
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IEEE Trans. Med. Imaging
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J. Biol. Chem.
- N. Gaborit, C. Larbouret, J. Vallaghe, F. Peyrusson, C. Bascoul-Mollevi, E. Crapez, D. Azria, T. Chardès, M.-A. Poul, G. Mathis, H. Bazin, and A. Pèlegrin, “Time-resolved fluorescence resonance energy transfer (TR-FRET) to analyze the disruption of EGFR/HER2 dimers: a new method to evaluate the efficiency of targeted therapy using monoclonal antibodies,” J. Biol. Chem.286(13), 11337–11345 (2011). [CrossRef] [PubMed]
J. Clin. Invest.
- B. Breart, F. Lemaître, S. Celli, and P. Bousso, “Two-photon imaging of intratumoral CD8+ T cell cytotoxic activity during adoptive T cell therapy in mice,” J. Clin. Invest.118(4), 1390–1397 (2008). [CrossRef] [PubMed]
J. Am. Chem. Soc.
- H. Ueyama, M. Takagi, and S. Takenaka, “A novel potassium sensing in aqueous media with a synthetic oligonucleotide derivative. Fluorescence resonance energy transfer associated with Guanine quartet-potassium ion complex formation,” J. Am. Chem. Soc.124(48), 14286–14287 (2002). [CrossRef] [PubMed]
J. Biomed. Opt.
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J. Biomed. Opt.
- S. Bélanger, M. Abran, X. Intes, C. Casanova, and F. Lesage, “Real-time diffuse optical tomography based on structured illumination,” J. Biomed. Opt.15(1), 016006 (2010). [CrossRef] [PubMed]
- J. Chen and X. Intes, “Mesh-based Monte Carlo method in time-domain widefield fluorescence molecular tomography,” J. Biomed. Opt.17(10), 106009 (2012). [CrossRef]
- J. R. Lakowicz and B. R. Masters, “Principles of fluorescence spectroscopy, third edition,” J. Biomed. Opt.13(2), 029901 (2008). [CrossRef]
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- N. A. Rahim, S. Pelet, R. D. Kamm, and P. T. C. So, “Methodological considerations for global analysis of cellular FLIM/FRET measurements,” J. Biomed. Opt.17(2), 026013 (2012). [CrossRef] [PubMed]
J. Cell Biol.
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J. Opt. Soc. Am. A
- V. Gaind, K. J. Webb, S. Kularatne, and C. A. Bouman, “Towards in vivo imaging of intramolecular fluorescence resonance energy transfer parameters,” J. Opt. Soc. Am. A26(8), 1805–1813 (2009). [CrossRef] [PubMed]
Med. Phys.
- J. Chen and X. Intes, “Comparison of Monte Carlo methods for fluorescence molecular tomography-computational efficiency,” Med. Phys.38(10), 5788–5798 (2011). [CrossRef] [PubMed]
Med. Res. Rev.
- H. Li and Z. M. Qian, “Transferrin/transferrin receptor-mediated drug delivery,” Med. Res. Rev.22(3), 225–250 (2002). [CrossRef] [PubMed]
Microsc. Res. Tech.
- H. Wallrabe, Y. Chen, A. Periasamy, and M. Barroso, “Issues in confocal microscopy for quantitative FRET analysis,” Microsc. Res. Tech.69(3), 196–206 (2006). [CrossRef] [PubMed]
Mol. Biol. Cell
- T. Nishioka, K. Aoki, K. Hikake, H. Yoshizaki, E. Kiyokawa, and M. Matsuda, “Rapid turnover rate of phosphoinositides at the front of migrating MDCK cells,” Mol. Biol. Cell19(10), 4213–4223 (2008). [CrossRef] [PubMed]
Nat. Biotechnol.
- V. Ntziachristos, J. Ripoll, L. V. Wang, and R. Weissleder, “Looking and listening to light: the evolution of whole-body photonic imaging,” Nat. Biotechnol.23(3), 313–320 (2005). [CrossRef] [PubMed]
Nat. Methods
- C. Vinegoni, C. Pitsouli, D. Razansky, N. Perrimon, and V. Ntziachristos, “In vivo imaging of Drosophila melanogaster pupae with mesoscopic fluorescence tomography,” Nat. Methods5(1), 45–47 (2008). [CrossRef] [PubMed]
Nature
- N. Mochizuki, S. Yamashita, K. Kurokawa, Y. Ohba, T. Nagai, A. Miyawaki, and M. Matsuda, “Spatio-temporal images of growth-factor-induced activation of Ras and Rap1,” Nature411(6841), 1065–1068 (2001). [CrossRef] [PubMed]
- A. Miyawaki, J. Llopis, R. Heim, J. M. McCaffery, J. A. Adams, M. Ikura, and R. Y. Tsien, “Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin,” Nature388(6645), 882–887 (1997). [CrossRef] [PubMed]
Neuron
- T. Kuner and G. J. Augustine, “A genetically encoded ratiometric indicator for chloride: capturing chloride transients in cultured hippocampal neurons,” Neuron27(3), 447–459 (2000). [CrossRef] [PubMed]
Opt. Lett.
- J. Chen, V. Venugopal, F. Lesage, and X. Intes, “Time-resolved diffuse optical tomography with patterned-light illumination and detection,” Opt. Lett.35(13), 2121–2123 (2010). [CrossRef] [PubMed]
Opt. Express
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Opt. Lett.
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- V. Gaind, S. Kularatne, P. S. Low, and K. J. Webb, “Deep-tissue imaging of intramolecular fluorescence resonance energy-transfer parameters,” Opt. Lett.35(9), 1314–1316 (2010). [CrossRef] [PubMed]
Phys. Med. Biol.
- A. H. Hielscher, R. E. Alcouffe, and R. L. Barbour, “Comparison of finite-difference transport and diffusion calculations for photon migration in homogeneous and heterogeneous tissues,” Phys. Med. Biol.43(5), 1285–1302 (1998). [CrossRef] [PubMed]
Phys. Rev. Lett.
- K. M. Yoo, F. Liu, and R. R. Alfano, “When does the diffusion approximation fail to describe photon transport in random media?” Phys. Rev. Lett.64(22), 2647–2650 (1990). [CrossRef] [PubMed]
Proc. Natl. Acad. Sci. U.S.A.
- M. J. Niedre, R. H. de Kleine, E. Aikawa, D. G. Kirsch, R. Weissleder, and V. Ntziachristos, “Early photon tomography allows fluorescence detection of lung carcinomas and disease progression in mice in vivo,” Proc. Natl. Acad. Sci. U.S.A.105(49), 19126–19131 (2008). [CrossRef] [PubMed]
Other
- C. Chang and M. Mycek, "Improving precision in time-gated FLIM for low-light live-cell imaging," in Molecular Imaging II, K. Licha and C. Lin, eds., Vol. 7370 of Proceedings of SPIE-OSA Biomedical Optics (Optical Society of America, 2009), paper 7370_09.
- A. Periasamy, H. Wallrabe, Y. Chen, and M. Barroso, “Quantitation of protein–protein interactions: confocal FRET microscopy,” in Biophysical Tools for Biologists, Volume Two, Vol. 89 of Methods in Cell Biology (Academic, 2008), pp. 569–598.
2012, Chen, J. Biomed. Opt.
- J. Chen and X. Intes, “Mesh-based Monte Carlo method in time-domain widefield fluorescence molecular tomography,” J. Biomed. Opt.17(10), 106009 (2012). [CrossRef]
- N. A. Rahim, S. Pelet, R. D. Kamm, and P. T. C. So, “Methodological considerations for global analysis of cellular FLIM/FRET measurements,” J. Biomed. Opt.17(2), 026013 (2012). [CrossRef] [PubMed]
- J. Chen and X. Intes, “Comparison of Monte Carlo methods for fluorescence molecular tomography-computational efficiency,” Med. Phys.38(10), 5788–5798 (2011). [CrossRef] [PubMed]
- M. Y. Berezin, K. Guo, W. Akers, R. E. Northdurft, J. P. Culver, B. Teng, O. Vasalatiy, K. Barbacow, A. Gandjbakhche, G. L. Griffiths, and S. Achilefu, “Near-infrared fluorescence lifetime pH-sensitive probes,” Biophys. J.100(8), 2063–2072 (2011). [CrossRef] [PubMed]
- N. Gaborit, C. Larbouret, J. Vallaghe, F. Peyrusson, C. Bascoul-Mollevi, E. Crapez, D. Azria, T. Chardès, M.-A. Poul, G. Mathis, H. Bazin, and A. Pèlegrin, “Time-resolved fluorescence resonance energy transfer (TR-FRET) to analyze the disruption of EGFR/HER2 dimers: a new method to evaluate the efficiency of targeted therapy using monoclonal antibodies,” J. Biol. Chem.286(13), 11337–11345 (2011). [CrossRef] [PubMed]
- J. Chen, V. Venugopal, and X. Intes, “Monte Carlo based method for fluorescence tomographic imaging with lifetime multiplexing using time gates,” Biomed. Opt. Express2(4), 871–886 (2011). [CrossRef] [PubMed]
- S. Kumar, D. Alibhai, A. Margineanu, R. Laine, G. Kennedy, J. McGinty, S. Warren, D. Kelly, Y. Alexandrov, I. Munro, C. Talbot, D. W. Stuckey, C. Kimberly, B. Viellerobe, F. Lacombe, E. W.-F. Lam, H. Taylor, M. J. Dallman, G. Stamp, E. J. Murray, F. Stuhmeier, A. Sardini, M. Katan, D. S. Elson, M. A. A. Neil, C. Dunsby, and P. M. W. French, “FLIM FRET technology for drug discovery: automated multiwell-plate high-content analysis, multiplexed readouts and application in situ,” ChemPhysChem12(3), 609–626 (2011). [CrossRef] [PubMed]
- S. Bélanger, M. Abran, X. Intes, C. Casanova, and F. Lesage, “Real-time diffuse optical tomography based on structured illumination,” J. Biomed. Opt.15(1), 016006 (2010). [CrossRef] [PubMed]
- J. Chen, V. Venugopal, F. Lesage, and X. Intes, “Time-resolved diffuse optical tomography with patterned-light illumination and detection,” Opt. Lett.35(13), 2121–2123 (2010). [CrossRef] [PubMed]
- N. Valim, J. Brock, and M. Niedre, “Experimental measurement of time-dependent photon scatter for diffuse optical tomography,” J. Biomed. Opt.15(6), 065006 (2010). [CrossRef] [PubMed]
- S. B. Raymond, D. A. Boas, B. J. Bacskai, and A. T. N. Kumar, “Lifetime-based tomographic multiplexing,” J. Biomed. Opt.15(4), 046011 (2010). [CrossRef] [PubMed]
- V. Gaind, K. J. Webb, S. Kularatne, and C. A. Bouman, “Towards in vivo imaging of intramolecular fluorescence resonance energy transfer parameters,” J. Opt. Soc. Am. A26(8), 1805–1813 (2009). [CrossRef] [PubMed]
- B. Huang, M. Bates, and X. Zhuang, “Super-resolution fluorescence microscopy,” Annu. Rev. Biochem.78(1), 993–1016 (2009). [CrossRef] [PubMed]
- B. Breart, F. Lemaître, S. Celli, and P. Bousso, “Two-photon imaging of intratumoral CD8+ T cell cytotoxic activity during adoptive T cell therapy in mice,” J. Clin. Invest.118(4), 1390–1397 (2008). [CrossRef] [PubMed]
- C. Vinegoni, C. Pitsouli, D. Razansky, N. Perrimon, and V. Ntziachristos, “In vivo imaging of Drosophila melanogaster pupae with mesoscopic fluorescence tomography,” Nat. Methods5(1), 45–47 (2008). [CrossRef] [PubMed]
- J. R. Lakowicz and B. R. Masters, “Principles of fluorescence spectroscopy, third edition,” J. Biomed. Opt.13(2), 029901 (2008). [CrossRef]
- T. Nishioka, K. Aoki, K. Hikake, H. Yoshizaki, E. Kiyokawa, and M. Matsuda, “Rapid turnover rate of phosphoinositides at the front of migrating MDCK cells,” Mol. Biol. Cell19(10), 4213–4223 (2008). [CrossRef] [PubMed]
- S. Padilla-Parra, N. Audugé, M. Coppey-Moisan, and M. Tramier, “Quantitative FRET analysis by fast acquisition time domain FLIM at high spatial resolution in living cells,” Biophys. J.95(6), 2976–2988 (2008). [CrossRef] [PubMed]
- M. J. Niedre, R. H. de Kleine, E. Aikawa, D. G. Kirsch, R. Weissleder, and V. Ntziachristos, “Early photon tomography allows fluorescence detection of lung carcinomas and disease progression in mice in vivo,” Proc. Natl. Acad. Sci. U.S.A.105(49), 19126–19131 (2008). [CrossRef] [PubMed]
- H. Wallrabe, Y. Chen, A. Periasamy, and M. Barroso, “Issues in confocal microscopy for quantitative FRET analysis,” Microsc. Res. Tech.69(3), 196–206 (2006). [CrossRef] [PubMed]
- I. T. Li, E. Pham, and K. Truong, “Protein biosensors based on the principle of fluorescence resonance energy transfer for monitoring cellular dynamics,” Biotechnol. Lett.28(24), 1971–1982 (2006). [CrossRef] [PubMed]
- E. A. Jares-Erijman and T. M. Jovin, “Imaging molecular interactions in living cells by FRET microscopy,” Curr. Opin. Chem. Biol.10(5), 409–416 (2006). [CrossRef] [PubMed]
- M. Mank, D. F. Reiff, N. Heim, M. W. Friedrich, A. Borst, and O. Griesbeck, “A FRET-based calcium biosensor with fast signal kinetics and high fluorescence change,” Biophys. J.90(5), 1790–1796 (2006). [CrossRef] [PubMed]
- A. Nezu, A. Tanimura, T. Morita, A. Shitara, and Y. Tojyo, “A novel fluorescent method employing the FRET-based biosensor “LIBRA” for the identification of ligands of the inositol 1,4,5-trisphosphate receptors,” Biochim. Biophys. Acta1760(8), 1274–1280 (2006). [CrossRef] [PubMed]
- H. Wallrabe and A. Periasamy, “Imaging protein molecules using FRET and FLIM microscopy,” Curr. Opin. Biotechnol.16(1), 19–27 (2005). [CrossRef] [PubMed]
- V. Ntziachristos, J. Ripoll, L. V. Wang, and R. Weissleder, “Looking and listening to light: the evolution of whole-body photonic imaging,” Nat. Biotechnol.23(3), 313–320 (2005). [CrossRef] [PubMed]
- A. Soubret, J. Ripoll, and V. Ntziachristos, “Accuracy of fluorescent tomography in the presence of heterogeneities: study of the normalized Born ratio,” IEEE Trans. Med. Imaging24(10), 1377–1386 (2005). [CrossRef] [PubMed]
- H. Ueyama, M. Takagi, and S. Takenaka, “A novel potassium sensing in aqueous media with a synthetic oligonucleotide derivative. Fluorescence resonance energy transfer associated with Guanine quartet-potassium ion complex formation,” J. Am. Chem. Soc.124(48), 14286–14287 (2002). [CrossRef] [PubMed]
- H. Li and Z. M. Qian, “Transferrin/transferrin receptor-mediated drug delivery,” Med. Res. Rev.22(3), 225–250 (2002). [CrossRef] [PubMed]
- N. Mochizuki, S. Yamashita, K. Kurokawa, Y. Ohba, T. Nagai, A. Miyawaki, and M. Matsuda, “Spatio-temporal images of growth-factor-induced activation of Ras and Rap1,” Nature411(6841), 1065–1068 (2001). [CrossRef] [PubMed]
- P. J. Verveer, A. Squire, and P. I. Bastiaens, “Global analysis of fluorescence lifetime imaging microscopy data,” Biophys. J.78(4), 2127–2137 (2000). [CrossRef] [PubMed]
- T. Kuner and G. J. Augustine, “A genetically encoded ratiometric indicator for chloride: capturing chloride transients in cultured hippocampal neurons,” Neuron27(3), 447–459 (2000). [CrossRef] [PubMed]
- A. H. Hielscher, R. E. Alcouffe, and R. L. Barbour, “Comparison of finite-difference transport and diffusion calculations for photon migration in homogeneous and heterogeneous tissues,” Phys. Med. Biol.43(5), 1285–1302 (1998). [CrossRef] [PubMed]
- A. K. Kenworthy and M. Edidin, “Distribution of a glycosylphosphatidylinositol-anchored protein at the apical surface of MDCK cells examined at a resolution of <100 A using imaging fluorescence resonance energy transfer,” J. Cell Biol.142(1), 69–84 (1998). [CrossRef] [PubMed]
- A. Miyawaki, J. Llopis, R. Heim, J. M. McCaffery, J. A. Adams, M. Ikura, and R. Y. Tsien, “Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin,” Nature388(6645), 882–887 (1997). [CrossRef] [PubMed]
- K. M. Yoo, F. Liu, and R. R. Alfano, “When does the diffusion approximation fail to describe photon transport in random media?” Phys. Rev. Lett.64(22), 2647–2650 (1990). [CrossRef] [PubMed]
- L. Stryer, “Fluorescence energy transfer as a spectroscopic ruler,” Annu. Rev. Biochem.47(1), 819–846 (1978). [CrossRef] [PubMed]
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