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Mouse phenotyping with near-infrared fluorescence lymphatic imagingSunkuk Kwon and Eva M. Sevick-Muraca »View Author Affiliations
Sunkuk Kwon*
and Eva M. Sevick-Muraca
Center for Molecular Imaging, The Brown Foundation Institute of Molecular Medicine, The University of Texas Health Science Center at Houston, Houston, TX 77584, USA *Corresponding author: sunkuk.kwon@uth.tmc.edu |
Biomedical Optics Express, Vol. 2, Issue 6, pp. 1403-1411 (2011)
http://dx.doi.org/10.1364/BOE.2.001403
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Abstract
We demonstrate the ability to non-invasively and quantitatively image lymphatic architecture and contractile function using dynamic near-infrared (NIR) fluorescence imaging with injection of indocyanine green in normal and transgenic mice. Unlike normal mice, which showed well defined lymphatic drainage patterns and orthograde propagation of contraction waves, we observed tortuous and mispatterned lymphatic vessels and persistent retrograde lymph flow in mice with deficiency in Prox1, a transcription factor essential for lymphatic vascular development. NIR fluorescence imaging provides a method for quantifying lymphatic function for future studies designed to discern differences in lymphatic function in murine models of human lymphatic disease.
© 2011 OSA
OCIS Codes
(170.0110) Medical optics and biotechnology : Imaging systems
(170.0170) Medical optics and biotechnology : Medical optics and biotechnology
(170.3880) Medical optics and biotechnology : Medical and biological imaging
(170.4580) Medical optics and biotechnology : Optical diagnostics for medicine
(170.2655) Medical optics and biotechnology : Functional monitoring and imaging
ToC Category:
Functional Imaging
History
Original Manuscript: March 14, 2011
Revised Manuscript: April 20, 2011
Manuscript Accepted: April 29, 2011
Published: May 2, 2011
Virtual Issues
In vivo Microcirculation Imaging
(2011) Biomedical Optics Express
Citation
Sunkuk Kwon and Eva M. Sevick-Muraca, "Mouse phenotyping with near-infrared fluorescence lymphatic imaging," Biomed. Opt. Express 2, 1403-1411 (2011)
http://www.opticsinfobase.org/boe/abstract.cfm?URI=boe-2-6-1403
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References
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Adams, K. E.
Aldrich, M. B.
Alitalo, K.
Barry, M. A.
Benoit, J. N.
Bernas, M. J.
Blanchard, D. K.
Bonefas, E.
Boyd, K.
Brock, J. A.
Brooks, B. P.
Bueler, H.
Cameron, A.
Caulder, M. S.
Chan, W.
Cherrick, G. R.
Chiang, S. B.
Cote, G. L.
Covington, K. R.
Craandijk, A.
Crowe, M. J.
Dagenais, S. L.
Darne, C.
Davidson, C. S.
Davis, K. L.
Davis, M. J.
Dillard, M. E.
Dixon, J. B.
Eichmann, A.
Elledge, R.
Erickson, R. P.
Fan, Z.
Ferrell, R. E.
Fife, C. E.
Finegold, D. N.
Fisher, R. E.
Gashev, A. A.
Glover, T. W.
Granger, H. J.
Greiner, S. T.
Guilloid, R.
Harvey, N. L.
Hinds, W. M.
Hirschi, K.
Houston, J. P.
Hoy, S.
Jackson, D.
Jackson, D. G.
Johnson, N. C.
Joshi, A.
Jussila, L.
Karila, K. A.
Karkkainen, M. J.
Karpanen, T.
Kauppinen, R.
Ke, S.
Kettunen, M. I.
Kriederman, B. M.
Kubo, H.
Kwon, S.
Laine, G. A.
Lawrence, E. C.
Leevy, C. M.
Liang, F.
Lu, Y.
Lynch, M. T.
Mäkinen, T.
Marshall, M. V.
Maus, E. A.
Mawad, M. E.
McHale, N. G.
Meharg, M. K.
Miura, N.
Moore, J. E.
Myloyde, T. L.
Nishikawa, S.
Oliver, G.
Pajusola, K.
Pham, H. Q.
Pulkkanen, K. J.
Rasmussen, J. C.
Rennels, M.
Saaristo, A.
Sampath, L.
Schuster, R.
Sevick-Muraca, E. M.
Sharma, R.
Sleeman, M. W.
Smith, L. A.
Smith, R. O.
Srinivasan, R. S.
Stein, S. W.
Stewart, R. H.
Sutton, R.
Tammela, T.
Tan, I. C.
Tan, I.-C.
Tsopelas, C.
Van Beek, C. A.
Van Helden, D. F.
Veikkola, T.
von der Weid, P. Y.
Wang, W.
Wang, Y.
Wendt, J. A.
Wigle, J. T.
Witte, C. L.
Witte, M. H.
Yla-Herttuala, S.
Ylä-Herttuala, S.
Zawieja, D. C.
- I.-C. Tan, E. A. Maus, J. C. Rasmussen, M. V. Marshall, K. E. Adams, C. E. Fife, L. A. Smith, W. Chan, and E. M. Sevick-Muraca, “Assessment of lymphatic contractile function after manual lymphatic drainage using near-infrared fluorescence imaging,” Arch. Phys. Ment. Rehabil. 92, 756–764.e1 (2011)
- K. E. Adams, J. C. Rasmussen, C. Darne, I. C. Tan, M. B. Aldrich, M. V. Marshall, C. E. Fife, E. A. Maus, L. A. Smith, R. Guilloid, S. Hoy, and E. M. Sevick-Muraca, “Direct evidence of lymphatic function improvement after advanced pneumatic compression device treatment of lymphedema,” Biomed. Opt. Express 1(1), 114–125 (2010). [CrossRef] [PubMed]
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- K. E. Adams, S. Ke, S. Kwon, F. Liang, Z. Fan, Y. Lu, K. Hirschi, M. E. Mawad, M. A. Barry, and E. M. Sevick-Muraca, “Comparison of visible and near-infrared wavelength-excitable fluorescent dyes for molecular imaging of cancer,” J. Biomed. Opt. 12(2), 024017 (2007). [CrossRef] [PubMed]
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- T. Mäkinen, L. Jussila, T. Veikkola, T. Karpanen, M. I. Kettunen, K. J. Pulkkanen, R. Kauppinen, D. G. Jackson, H. Kubo, S. Nishikawa, S. Ylä-Herttuala, and K. Alitalo, “Inhibition of lymphangiogenesis with resulting lymphedema in transgenic mice expressing soluble VEGF receptor-3,” Nat. Med. 7(2), 199–205 (2001). [CrossRef] [PubMed]
- M. J. Karkkainen, A. Saaristo, L. Jussila, K. A. Karila, E. C. Lawrence, K. Pajusola, H. Bueler, A. Eichmann, R. Kauppinen, M. I. Kettunen, S. Yla-Herttuala, D. N. Finegold, R. E. Ferrell, and K. Alitalo, “A model for gene therapy of human hereditary lymphedema,” Proc. Natl. Acad. Sci. U.S.A. 98(22), 12677–12682 (2001). [CrossRef] [PubMed]
- K. E. Adams, S. Ke, S. Kwon, F. Liang, Z. Fan, Y. Lu, K. Hirschi, M. E. Mawad, M. A. Barry, and E. M. Sevick-Muraca, “Comparison of visible and near-infrared wavelength-excitable fluorescent dyes for molecular imaging of cancer,” J. Biomed. Opt. 12(2), 024017 (2007). [CrossRef] [PubMed]
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- E. M. Sevick-Muraca, R. Sharma, J. C. Rasmussen, M. V. Marshall, J. A. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. K. Blanchard, R. E. Fisher, S. B. Chiang, R. Elledge, and M. E. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study,” Radiology 246(3), 734–741 (2008). [CrossRef] [PubMed]
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- N. L. Harvey, R. S. Srinivasan, M. E. Dillard, N. C. Johnson, M. H. Witte, K. Boyd, M. W. Sleeman, and G. Oliver, “Lymphatic vascular defects promoted by Prox1 haploinsufficiency cause adult-onset obesity,” Nat. Genet. 37(10), 1072–1081 (2005). [CrossRef] [PubMed]
- M. J. Crowe, P. Y. von der Weid, J. A. Brock, and D. F. Van Helden, “Co-ordination of contractile activity in guinea-pig mesenteric lymphatics,” J. Physiol. 500(Pt 1), 235–244 (1997). [PubMed]
- B. M. Kriederman, T. L. Myloyde, M. H. Witte, S. L. Dagenais, C. L. Witte, M. Rennels, M. J. Bernas, M. T. Lynch, R. P. Erickson, M. S. Caulder, N. Miura, D. Jackson, B. P. Brooks, and T. W. Glover, “FOXC2 haploinsufficient mice are a model for human autosomal dominant lymphedema-distichiasis syndrome,” Hum. Mol. Genet. 12(10), 1179–1185 (2003). [CrossRef] [PubMed]
- M. J. Karkkainen, A. Saaristo, L. Jussila, K. A. Karila, E. C. Lawrence, K. Pajusola, H. Bueler, A. Eichmann, R. Kauppinen, M. I. Kettunen, S. Yla-Herttuala, D. N. Finegold, R. E. Ferrell, and K. Alitalo, “A model for gene therapy of human hereditary lymphedema,” Proc. Natl. Acad. Sci. U.S.A. 98(22), 12677–12682 (2001). [CrossRef] [PubMed]
- R. Sharma, W. Wang, J. C. Rasmussen, A. Joshi, J. P. Houston, K. E. Adams, A. Cameron, S. Ke, S. Kwon, M. E. Mawad, and E. M. Sevick-Muraca, “Quantitative imaging of lymph function,” Am. J. Physiol. Heart Circ. Physiol. 292(6), H3109–H3118 (2007). [CrossRef] [PubMed]
- B. M. Kriederman, T. L. Myloyde, M. H. Witte, S. L. Dagenais, C. L. Witte, M. Rennels, M. J. Bernas, M. T. Lynch, R. P. Erickson, M. S. Caulder, N. Miura, D. Jackson, B. P. Brooks, and T. W. Glover, “FOXC2 haploinsufficient mice are a model for human autosomal dominant lymphedema-distichiasis syndrome,” Hum. Mol. Genet. 12(10), 1179–1185 (2003). [CrossRef] [PubMed]
- I.-C. Tan, E. A. Maus, J. C. Rasmussen, M. V. Marshall, K. E. Adams, C. E. Fife, L. A. Smith, W. Chan, and E. M. Sevick-Muraca, “Assessment of lymphatic contractile function after manual lymphatic drainage using near-infrared fluorescence imaging,” Arch. Phys. Ment. Rehabil. 92, 756–764.e1 (2011)
- G. R. Cherrick, S. W. Stein, C. M. Leevy, and C. S. Davidson, “Indocyanine green: observations on its physical properties, plasma decay, and hepatic extraction,” J. Clin. Invest. 39(4), 592–600 (1960). [CrossRef] [PubMed]
- E. M. Sevick-Muraca, R. Sharma, J. C. Rasmussen, M. V. Marshall, J. A. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. K. Blanchard, R. E. Fisher, S. B. Chiang, R. Elledge, and M. E. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study,” Radiology 246(3), 734–741 (2008). [CrossRef] [PubMed]
- J. B. Dixon, S. T. Greiner, A. A. Gashev, G. L. Cote, J. E. Moore, and D. C. Zawieja, “Lymph flow, shear stress, and lymphocyte velocity in rat mesenteric prenodal lymphatics,” Microcirculation 13(7), 597–610 (2006). [CrossRef] [PubMed]
- J. C. Rasmussen, I. C. Tan, M. V. Marshall, K. E. Adams, S. Kwon, C. E. Fife, E. A. Maus, L. A. Smith, K. R. Covington, and E. M. Sevick-Muraca, “Human lymphatic architecture and dynamic transport imaged using near-infrared fluorescence,” Transl Oncol 3(6), 362–372 (2010). [PubMed]
- A. Craandijk and C. A. Van Beek, “Indocyanine green fluorescence angiography of the choroid,” Br. J. Ophthalmol. 60(5), 377–385 (1976). [CrossRef] [PubMed]
- M. J. Crowe, P. Y. von der Weid, J. A. Brock, and D. F. Van Helden, “Co-ordination of contractile activity in guinea-pig mesenteric lymphatics,” J. Physiol. 500(Pt 1), 235–244 (1997). [PubMed]
- B. M. Kriederman, T. L. Myloyde, M. H. Witte, S. L. Dagenais, C. L. Witte, M. Rennels, M. J. Bernas, M. T. Lynch, R. P. Erickson, M. S. Caulder, N. Miura, D. Jackson, B. P. Brooks, and T. W. Glover, “FOXC2 haploinsufficient mice are a model for human autosomal dominant lymphedema-distichiasis syndrome,” Hum. Mol. Genet. 12(10), 1179–1185 (2003). [CrossRef] [PubMed]
- K. E. Adams, J. C. Rasmussen, C. Darne, I. C. Tan, M. B. Aldrich, M. V. Marshall, C. E. Fife, E. A. Maus, L. A. Smith, R. Guilloid, S. Hoy, and E. M. Sevick-Muraca, “Direct evidence of lymphatic function improvement after advanced pneumatic compression device treatment of lymphedema,” Biomed. Opt. Express 1(1), 114–125 (2010). [CrossRef] [PubMed]
- G. R. Cherrick, S. W. Stein, C. M. Leevy, and C. S. Davidson, “Indocyanine green: observations on its physical properties, plasma decay, and hepatic extraction,” J. Clin. Invest. 39(4), 592–600 (1960). [CrossRef] [PubMed]
- D. C. Zawieja, K. L. Davis, R. Schuster, W. M. Hinds, and H. J. Granger, “Distribution, propagation, and coordination of contractile activity in lymphatics,” Am. J. Physiol. 264(4 Pt 2), H1283–H1291 (1993). [PubMed]
- A. A. Gashev, M. J. Davis, and D. C. Zawieja, “Inhibition of the active lymph pump by flow in rat mesenteric lymphatics and thoracic duct,” J. Physiol. 540(Pt 3), 1023–1037 (2002). [PubMed]
- N. L. Harvey, R. S. Srinivasan, M. E. Dillard, N. C. Johnson, M. H. Witte, K. Boyd, M. W. Sleeman, and G. Oliver, “Lymphatic vascular defects promoted by Prox1 haploinsufficiency cause adult-onset obesity,” Nat. Genet. 37(10), 1072–1081 (2005). [CrossRef] [PubMed]
- J. B. Dixon, S. T. Greiner, A. A. Gashev, G. L. Cote, J. E. Moore, and D. C. Zawieja, “Lymph flow, shear stress, and lymphocyte velocity in rat mesenteric prenodal lymphatics,” Microcirculation 13(7), 597–610 (2006). [CrossRef] [PubMed]
- M. J. Karkkainen, A. Saaristo, L. Jussila, K. A. Karila, E. C. Lawrence, K. Pajusola, H. Bueler, A. Eichmann, R. Kauppinen, M. I. Kettunen, S. Yla-Herttuala, D. N. Finegold, R. E. Ferrell, and K. Alitalo, “A model for gene therapy of human hereditary lymphedema,” Proc. Natl. Acad. Sci. U.S.A. 98(22), 12677–12682 (2001). [CrossRef] [PubMed]
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- T. Mäkinen, L. Jussila, T. Veikkola, T. Karpanen, M. I. Kettunen, K. J. Pulkkanen, R. Kauppinen, D. G. Jackson, H. Kubo, S. Nishikawa, S. Ylä-Herttuala, and K. Alitalo, “Inhibition of lymphangiogenesis with resulting lymphedema in transgenic mice expressing soluble VEGF receptor-3,” Nat. Med. 7(2), 199–205 (2001). [CrossRef] [PubMed]
- Y. Wang and G. Oliver, “Current views on the function of the lymphatic vasculature in health and disease,” Genes Dev. 24(19), 2115–2126 (2010). [CrossRef] [PubMed]
- N. L. Harvey, R. S. Srinivasan, M. E. Dillard, N. C. Johnson, M. H. Witte, K. Boyd, M. W. Sleeman, and G. Oliver, “Lymphatic vascular defects promoted by Prox1 haploinsufficiency cause adult-onset obesity,” Nat. Genet. 37(10), 1072–1081 (2005). [CrossRef] [PubMed]
- J. T. Wigle and G. Oliver, “Prox1 function is required for the development of the murine lymphatic system,” Cell 98(6), 769–778 (1999). [CrossRef] [PubMed]
- M. J. Karkkainen, A. Saaristo, L. Jussila, K. A. Karila, E. C. Lawrence, K. Pajusola, H. Bueler, A. Eichmann, R. Kauppinen, M. I. Kettunen, S. Yla-Herttuala, D. N. Finegold, R. E. Ferrell, and K. Alitalo, “A model for gene therapy of human hereditary lymphedema,” Proc. Natl. Acad. Sci. U.S.A. 98(22), 12677–12682 (2001). [CrossRef] [PubMed]
- E. M. Sevick-Muraca, R. Sharma, J. C. Rasmussen, M. V. Marshall, J. A. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. K. Blanchard, R. E. Fisher, S. B. Chiang, R. Elledge, and M. E. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study,” Radiology 246(3), 734–741 (2008). [CrossRef] [PubMed]
- T. Mäkinen, L. Jussila, T. Veikkola, T. Karpanen, M. I. Kettunen, K. J. Pulkkanen, R. Kauppinen, D. G. Jackson, H. Kubo, S. Nishikawa, S. Ylä-Herttuala, and K. Alitalo, “Inhibition of lymphangiogenesis with resulting lymphedema in transgenic mice expressing soluble VEGF receptor-3,” Nat. Med. 7(2), 199–205 (2001). [CrossRef] [PubMed]
- I.-C. Tan, E. A. Maus, J. C. Rasmussen, M. V. Marshall, K. E. Adams, C. E. Fife, L. A. Smith, W. Chan, and E. M. Sevick-Muraca, “Assessment of lymphatic contractile function after manual lymphatic drainage using near-infrared fluorescence imaging,” Arch. Phys. Ment. Rehabil. 92, 756–764.e1 (2011)
- J. C. Rasmussen, I. C. Tan, M. V. Marshall, K. E. Adams, S. Kwon, C. E. Fife, E. A. Maus, L. A. Smith, K. R. Covington, and E. M. Sevick-Muraca, “Human lymphatic architecture and dynamic transport imaged using near-infrared fluorescence,” Transl Oncol 3(6), 362–372 (2010). [PubMed]
- K. E. Adams, J. C. Rasmussen, C. Darne, I. C. Tan, M. B. Aldrich, M. V. Marshall, C. E. Fife, E. A. Maus, L. A. Smith, R. Guilloid, S. Hoy, and E. M. Sevick-Muraca, “Direct evidence of lymphatic function improvement after advanced pneumatic compression device treatment of lymphedema,” Biomed. Opt. Express 1(1), 114–125 (2010). [CrossRef] [PubMed]
- J. C. Rasmussen, I. C. Tan, M. V. Marshall, C. E. Fife, and E. M. Sevick-Muraca, “Lymphatic imaging in humans with near-infrared fluorescence,” Curr. Opin. Biotechnol. 20(1), 74–82 (2009). [CrossRef] [PubMed]
- E. M. Sevick-Muraca, R. Sharma, J. C. Rasmussen, M. V. Marshall, J. A. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. K. Blanchard, R. E. Fisher, S. B. Chiang, R. Elledge, and M. E. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study,” Radiology 246(3), 734–741 (2008). [CrossRef] [PubMed]
- R. Sharma, W. Wang, J. C. Rasmussen, A. Joshi, J. P. Houston, K. E. Adams, A. Cameron, S. Ke, S. Kwon, M. E. Mawad, and E. M. Sevick-Muraca, “Quantitative imaging of lymph function,” Am. J. Physiol. Heart Circ. Physiol. 292(6), H3109–H3118 (2007). [CrossRef] [PubMed]
- B. M. Kriederman, T. L. Myloyde, M. H. Witte, S. L. Dagenais, C. L. Witte, M. Rennels, M. J. Bernas, M. T. Lynch, R. P. Erickson, M. S. Caulder, N. Miura, D. Jackson, B. P. Brooks, and T. W. Glover, “FOXC2 haploinsufficient mice are a model for human autosomal dominant lymphedema-distichiasis syndrome,” Hum. Mol. Genet. 12(10), 1179–1185 (2003). [CrossRef] [PubMed]
- M. J. Karkkainen, A. Saaristo, L. Jussila, K. A. Karila, E. C. Lawrence, K. Pajusola, H. Bueler, A. Eichmann, R. Kauppinen, M. I. Kettunen, S. Yla-Herttuala, D. N. Finegold, R. E. Ferrell, and K. Alitalo, “A model for gene therapy of human hereditary lymphedema,” Proc. Natl. Acad. Sci. U.S.A. 98(22), 12677–12682 (2001). [CrossRef] [PubMed]
- E. M. Sevick-Muraca, R. Sharma, J. C. Rasmussen, M. V. Marshall, J. A. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. K. Blanchard, R. E. Fisher, S. B. Chiang, R. Elledge, and M. E. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study,” Radiology 246(3), 734–741 (2008). [CrossRef] [PubMed]
- D. C. Zawieja, K. L. Davis, R. Schuster, W. M. Hinds, and H. J. Granger, “Distribution, propagation, and coordination of contractile activity in lymphatics,” Am. J. Physiol. 264(4 Pt 2), H1283–H1291 (1993). [PubMed]
- I.-C. Tan, E. A. Maus, J. C. Rasmussen, M. V. Marshall, K. E. Adams, C. E. Fife, L. A. Smith, W. Chan, and E. M. Sevick-Muraca, “Assessment of lymphatic contractile function after manual lymphatic drainage using near-infrared fluorescence imaging,” Arch. Phys. Ment. Rehabil. 92, 756–764.e1 (2011)
- K. E. Adams, J. C. Rasmussen, C. Darne, I. C. Tan, M. B. Aldrich, M. V. Marshall, C. E. Fife, E. A. Maus, L. A. Smith, R. Guilloid, S. Hoy, and E. M. Sevick-Muraca, “Direct evidence of lymphatic function improvement after advanced pneumatic compression device treatment of lymphedema,” Biomed. Opt. Express 1(1), 114–125 (2010). [CrossRef] [PubMed]
- J. C. Rasmussen, I. C. Tan, M. V. Marshall, K. E. Adams, S. Kwon, C. E. Fife, E. A. Maus, L. A. Smith, K. R. Covington, and E. M. Sevick-Muraca, “Human lymphatic architecture and dynamic transport imaged using near-infrared fluorescence,” Transl Oncol 3(6), 362–372 (2010). [PubMed]
- S. Kwon and E. M. Sevick-Muraca, “Functional lymphatic imaging in tumor-bearing mice,” J. Immunol. Methods 360(1-2), 167–172 (2010). [CrossRef] [PubMed]
- J. C. Rasmussen, I. C. Tan, M. V. Marshall, C. E. Fife, and E. M. Sevick-Muraca, “Lymphatic imaging in humans with near-infrared fluorescence,” Curr. Opin. Biotechnol. 20(1), 74–82 (2009). [CrossRef] [PubMed]
- E. M. Sevick-Muraca, R. Sharma, J. C. Rasmussen, M. V. Marshall, J. A. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. K. Blanchard, R. E. Fisher, S. B. Chiang, R. Elledge, and M. E. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study,” Radiology 246(3), 734–741 (2008). [CrossRef] [PubMed]
- K. E. Adams, S. Ke, S. Kwon, F. Liang, Z. Fan, Y. Lu, K. Hirschi, M. E. Mawad, M. A. Barry, and E. M. Sevick-Muraca, “Comparison of visible and near-infrared wavelength-excitable fluorescent dyes for molecular imaging of cancer,” J. Biomed. Opt. 12(2), 024017 (2007). [CrossRef] [PubMed]
- R. Sharma, W. Wang, J. C. Rasmussen, A. Joshi, J. P. Houston, K. E. Adams, A. Cameron, S. Ke, S. Kwon, M. E. Mawad, and E. M. Sevick-Muraca, “Quantitative imaging of lymph function,” Am. J. Physiol. Heart Circ. Physiol. 292(6), H3109–H3118 (2007). [CrossRef] [PubMed]
- S. Kwon and E. M. Sevick-Muraca, “Noninvasive quantitative imaging of lymph function in mice,” Lymphat. Res. Biol. 5(4), 219–232 (2007). [CrossRef] [PubMed]
- E. M. Sevick-Muraca, R. Sharma, J. C. Rasmussen, M. V. Marshall, J. A. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. K. Blanchard, R. E. Fisher, S. B. Chiang, R. Elledge, and M. E. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study,” Radiology 246(3), 734–741 (2008). [CrossRef] [PubMed]
- R. Sharma, W. Wang, J. C. Rasmussen, A. Joshi, J. P. Houston, K. E. Adams, A. Cameron, S. Ke, S. Kwon, M. E. Mawad, and E. M. Sevick-Muraca, “Quantitative imaging of lymph function,” Am. J. Physiol. Heart Circ. Physiol. 292(6), H3109–H3118 (2007). [CrossRef] [PubMed]
- N. L. Harvey, R. S. Srinivasan, M. E. Dillard, N. C. Johnson, M. H. Witte, K. Boyd, M. W. Sleeman, and G. Oliver, “Lymphatic vascular defects promoted by Prox1 haploinsufficiency cause adult-onset obesity,” Nat. Genet. 37(10), 1072–1081 (2005). [CrossRef] [PubMed]
- I.-C. Tan, E. A. Maus, J. C. Rasmussen, M. V. Marshall, K. E. Adams, C. E. Fife, L. A. Smith, W. Chan, and E. M. Sevick-Muraca, “Assessment of lymphatic contractile function after manual lymphatic drainage using near-infrared fluorescence imaging,” Arch. Phys. Ment. Rehabil. 92, 756–764.e1 (2011)
- K. E. Adams, J. C. Rasmussen, C. Darne, I. C. Tan, M. B. Aldrich, M. V. Marshall, C. E. Fife, E. A. Maus, L. A. Smith, R. Guilloid, S. Hoy, and E. M. Sevick-Muraca, “Direct evidence of lymphatic function improvement after advanced pneumatic compression device treatment of lymphedema,” Biomed. Opt. Express 1(1), 114–125 (2010). [CrossRef] [PubMed]
- J. C. Rasmussen, I. C. Tan, M. V. Marshall, K. E. Adams, S. Kwon, C. E. Fife, E. A. Maus, L. A. Smith, K. R. Covington, and E. M. Sevick-Muraca, “Human lymphatic architecture and dynamic transport imaged using near-infrared fluorescence,” Transl Oncol 3(6), 362–372 (2010). [PubMed]
- R. O. Smith, “Lymphatic contractility; a possible intrinsic mechanism of lymphatic vessels for the transport of lymph,” J. Exp. Med. 90(5), 497–509 (1949). [CrossRef] [PubMed]
- N. L. Harvey, R. S. Srinivasan, M. E. Dillard, N. C. Johnson, M. H. Witte, K. Boyd, M. W. Sleeman, and G. Oliver, “Lymphatic vascular defects promoted by Prox1 haploinsufficiency cause adult-onset obesity,” Nat. Genet. 37(10), 1072–1081 (2005). [CrossRef] [PubMed]
- G. R. Cherrick, S. W. Stein, C. M. Leevy, and C. S. Davidson, “Indocyanine green: observations on its physical properties, plasma decay, and hepatic extraction,” J. Clin. Invest. 39(4), 592–600 (1960). [CrossRef] [PubMed]
- A. A. Gashev, W. Wang, G. A. Laine, R. H. Stewart, and D. C. Zawieja, “Characteristics of the active lymph pump in bovine prenodal mesenteric lymphatics,” Lymphat. Res. Biol. 5(2), 71–80 (2007). [CrossRef] [PubMed]
- C. Tsopelas and R. Sutton, “Why certain dyes are useful for localizing the sentinel lymph node,” J. Nucl. Med. 43(10), 1377–1382 (2002). [PubMed]
- T. Tammela and K. Alitalo, “Lymphangiogenesis: Molecular mechanisms and future promise,” Cell 140(4), 460–476 (2010). [CrossRef] [PubMed]
- K. E. Adams, J. C. Rasmussen, C. Darne, I. C. Tan, M. B. Aldrich, M. V. Marshall, C. E. Fife, E. A. Maus, L. A. Smith, R. Guilloid, S. Hoy, and E. M. Sevick-Muraca, “Direct evidence of lymphatic function improvement after advanced pneumatic compression device treatment of lymphedema,” Biomed. Opt. Express 1(1), 114–125 (2010). [CrossRef] [PubMed]
- J. C. Rasmussen, I. C. Tan, M. V. Marshall, K. E. Adams, S. Kwon, C. E. Fife, E. A. Maus, L. A. Smith, K. R. Covington, and E. M. Sevick-Muraca, “Human lymphatic architecture and dynamic transport imaged using near-infrared fluorescence,” Transl Oncol 3(6), 362–372 (2010). [PubMed]
- J. C. Rasmussen, I. C. Tan, M. V. Marshall, C. E. Fife, and E. M. Sevick-Muraca, “Lymphatic imaging in humans with near-infrared fluorescence,” Curr. Opin. Biotechnol. 20(1), 74–82 (2009). [CrossRef] [PubMed]
- I.-C. Tan, E. A. Maus, J. C. Rasmussen, M. V. Marshall, K. E. Adams, C. E. Fife, L. A. Smith, W. Chan, and E. M. Sevick-Muraca, “Assessment of lymphatic contractile function after manual lymphatic drainage using near-infrared fluorescence imaging,” Arch. Phys. Ment. Rehabil. 92, 756–764.e1 (2011)
- C. Tsopelas and R. Sutton, “Why certain dyes are useful for localizing the sentinel lymph node,” J. Nucl. Med. 43(10), 1377–1382 (2002). [PubMed]
- A. Craandijk and C. A. Van Beek, “Indocyanine green fluorescence angiography of the choroid,” Br. J. Ophthalmol. 60(5), 377–385 (1976). [CrossRef] [PubMed]
- M. J. Crowe, P. Y. von der Weid, J. A. Brock, and D. F. Van Helden, “Co-ordination of contractile activity in guinea-pig mesenteric lymphatics,” J. Physiol. 500(Pt 1), 235–244 (1997). [PubMed]
- T. Mäkinen, L. Jussila, T. Veikkola, T. Karpanen, M. I. Kettunen, K. J. Pulkkanen, R. Kauppinen, D. G. Jackson, H. Kubo, S. Nishikawa, S. Ylä-Herttuala, and K. Alitalo, “Inhibition of lymphangiogenesis with resulting lymphedema in transgenic mice expressing soluble VEGF receptor-3,” Nat. Med. 7(2), 199–205 (2001). [CrossRef] [PubMed]
- M. J. Crowe, P. Y. von der Weid, J. A. Brock, and D. F. Van Helden, “Co-ordination of contractile activity in guinea-pig mesenteric lymphatics,” J. Physiol. 500(Pt 1), 235–244 (1997). [PubMed]
- R. Sharma, W. Wang, J. C. Rasmussen, A. Joshi, J. P. Houston, K. E. Adams, A. Cameron, S. Ke, S. Kwon, M. E. Mawad, and E. M. Sevick-Muraca, “Quantitative imaging of lymph function,” Am. J. Physiol. Heart Circ. Physiol. 292(6), H3109–H3118 (2007). [CrossRef] [PubMed]
- A. A. Gashev, W. Wang, G. A. Laine, R. H. Stewart, and D. C. Zawieja, “Characteristics of the active lymph pump in bovine prenodal mesenteric lymphatics,” Lymphat. Res. Biol. 5(2), 71–80 (2007). [CrossRef] [PubMed]
- Y. Wang and G. Oliver, “Current views on the function of the lymphatic vasculature in health and disease,” Genes Dev. 24(19), 2115–2126 (2010). [CrossRef] [PubMed]
- E. M. Sevick-Muraca, R. Sharma, J. C. Rasmussen, M. V. Marshall, J. A. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. K. Blanchard, R. E. Fisher, S. B. Chiang, R. Elledge, and M. E. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study,” Radiology 246(3), 734–741 (2008). [CrossRef] [PubMed]
- J. T. Wigle and G. Oliver, “Prox1 function is required for the development of the murine lymphatic system,” Cell 98(6), 769–778 (1999). [CrossRef] [PubMed]
- B. M. Kriederman, T. L. Myloyde, M. H. Witte, S. L. Dagenais, C. L. Witte, M. Rennels, M. J. Bernas, M. T. Lynch, R. P. Erickson, M. S. Caulder, N. Miura, D. Jackson, B. P. Brooks, and T. W. Glover, “FOXC2 haploinsufficient mice are a model for human autosomal dominant lymphedema-distichiasis syndrome,” Hum. Mol. Genet. 12(10), 1179–1185 (2003). [CrossRef] [PubMed]
- N. L. Harvey, R. S. Srinivasan, M. E. Dillard, N. C. Johnson, M. H. Witte, K. Boyd, M. W. Sleeman, and G. Oliver, “Lymphatic vascular defects promoted by Prox1 haploinsufficiency cause adult-onset obesity,” Nat. Genet. 37(10), 1072–1081 (2005). [CrossRef] [PubMed]
- B. M. Kriederman, T. L. Myloyde, M. H. Witte, S. L. Dagenais, C. L. Witte, M. Rennels, M. J. Bernas, M. T. Lynch, R. P. Erickson, M. S. Caulder, N. Miura, D. Jackson, B. P. Brooks, and T. W. Glover, “FOXC2 haploinsufficient mice are a model for human autosomal dominant lymphedema-distichiasis syndrome,” Hum. Mol. Genet. 12(10), 1179–1185 (2003). [CrossRef] [PubMed]
- M. J. Karkkainen, A. Saaristo, L. Jussila, K. A. Karila, E. C. Lawrence, K. Pajusola, H. Bueler, A. Eichmann, R. Kauppinen, M. I. Kettunen, S. Yla-Herttuala, D. N. Finegold, R. E. Ferrell, and K. Alitalo, “A model for gene therapy of human hereditary lymphedema,” Proc. Natl. Acad. Sci. U.S.A. 98(22), 12677–12682 (2001). [CrossRef] [PubMed]
- T. Mäkinen, L. Jussila, T. Veikkola, T. Karpanen, M. I. Kettunen, K. J. Pulkkanen, R. Kauppinen, D. G. Jackson, H. Kubo, S. Nishikawa, S. Ylä-Herttuala, and K. Alitalo, “Inhibition of lymphangiogenesis with resulting lymphedema in transgenic mice expressing soluble VEGF receptor-3,” Nat. Med. 7(2), 199–205 (2001). [CrossRef] [PubMed]
- A. A. Gashev, W. Wang, G. A. Laine, R. H. Stewart, and D. C. Zawieja, “Characteristics of the active lymph pump in bovine prenodal mesenteric lymphatics,” Lymphat. Res. Biol. 5(2), 71–80 (2007). [CrossRef] [PubMed]
- J. B. Dixon, S. T. Greiner, A. A. Gashev, G. L. Cote, J. E. Moore, and D. C. Zawieja, “Lymph flow, shear stress, and lymphocyte velocity in rat mesenteric prenodal lymphatics,” Microcirculation 13(7), 597–610 (2006). [CrossRef] [PubMed]
- A. A. Gashev, M. J. Davis, and D. C. Zawieja, “Inhibition of the active lymph pump by flow in rat mesenteric lymphatics and thoracic duct,” J. Physiol. 540(Pt 3), 1023–1037 (2002). [PubMed]
- D. C. Zawieja, K. L. Davis, R. Schuster, W. M. Hinds, and H. J. Granger, “Distribution, propagation, and coordination of contractile activity in lymphatics,” Am. J. Physiol. 264(4 Pt 2), H1283–H1291 (1993). [PubMed]
Am. J. Physiol.
- D. C. Zawieja, K. L. Davis, R. Schuster, W. M. Hinds, and H. J. Granger, “Distribution, propagation, and coordination of contractile activity in lymphatics,” Am. J. Physiol. 264(4 Pt 2), H1283–H1291 (1993). [PubMed]
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Am. J. Physiol. Heart Circ. Physiol.
- R. Sharma, W. Wang, J. C. Rasmussen, A. Joshi, J. P. Houston, K. E. Adams, A. Cameron, S. Ke, S. Kwon, M. E. Mawad, and E. M. Sevick-Muraca, “Quantitative imaging of lymph function,” Am. J. Physiol. Heart Circ. Physiol. 292(6), H3109–H3118 (2007). [CrossRef] [PubMed]
Arch. Phys. Ment. Rehabil.
- I.-C. Tan, E. A. Maus, J. C. Rasmussen, M. V. Marshall, K. E. Adams, C. E. Fife, L. A. Smith, W. Chan, and E. M. Sevick-Muraca, “Assessment of lymphatic contractile function after manual lymphatic drainage using near-infrared fluorescence imaging,” Arch. Phys. Ment. Rehabil. 92, 756–764.e1 (2011)
Biomed. Opt. Express
- K. E. Adams, J. C. Rasmussen, C. Darne, I. C. Tan, M. B. Aldrich, M. V. Marshall, C. E. Fife, E. A. Maus, L. A. Smith, R. Guilloid, S. Hoy, and E. M. Sevick-Muraca, “Direct evidence of lymphatic function improvement after advanced pneumatic compression device treatment of lymphedema,” Biomed. Opt. Express 1(1), 114–125 (2010). [CrossRef] [PubMed]
Br. J. Ophthalmol.
- A. Craandijk and C. A. Van Beek, “Indocyanine green fluorescence angiography of the choroid,” Br. J. Ophthalmol. 60(5), 377–385 (1976). [CrossRef] [PubMed]
Cell
- T. Tammela and K. Alitalo, “Lymphangiogenesis: Molecular mechanisms and future promise,” Cell 140(4), 460–476 (2010). [CrossRef] [PubMed]
- J. T. Wigle and G. Oliver, “Prox1 function is required for the development of the murine lymphatic system,” Cell 98(6), 769–778 (1999). [CrossRef] [PubMed]
Curr. Opin. Biotechnol.
- J. C. Rasmussen, I. C. Tan, M. V. Marshall, C. E. Fife, and E. M. Sevick-Muraca, “Lymphatic imaging in humans with near-infrared fluorescence,” Curr. Opin. Biotechnol. 20(1), 74–82 (2009). [CrossRef] [PubMed]
Genes Dev.
- Y. Wang and G. Oliver, “Current views on the function of the lymphatic vasculature in health and disease,” Genes Dev. 24(19), 2115–2126 (2010). [CrossRef] [PubMed]
Hum. Mol. Genet.
- B. M. Kriederman, T. L. Myloyde, M. H. Witte, S. L. Dagenais, C. L. Witte, M. Rennels, M. J. Bernas, M. T. Lynch, R. P. Erickson, M. S. Caulder, N. Miura, D. Jackson, B. P. Brooks, and T. W. Glover, “FOXC2 haploinsufficient mice are a model for human autosomal dominant lymphedema-distichiasis syndrome,” Hum. Mol. Genet. 12(10), 1179–1185 (2003). [CrossRef] [PubMed]
J. Biomed. Opt.
- K. E. Adams, S. Ke, S. Kwon, F. Liang, Z. Fan, Y. Lu, K. Hirschi, M. E. Mawad, M. A. Barry, and E. M. Sevick-Muraca, “Comparison of visible and near-infrared wavelength-excitable fluorescent dyes for molecular imaging of cancer,” J. Biomed. Opt. 12(2), 024017 (2007). [CrossRef] [PubMed]
J. Clin. Invest.
- G. R. Cherrick, S. W. Stein, C. M. Leevy, and C. S. Davidson, “Indocyanine green: observations on its physical properties, plasma decay, and hepatic extraction,” J. Clin. Invest. 39(4), 592–600 (1960). [CrossRef] [PubMed]
J. Exp. Med.
- R. O. Smith, “Lymphatic contractility; a possible intrinsic mechanism of lymphatic vessels for the transport of lymph,” J. Exp. Med. 90(5), 497–509 (1949). [CrossRef] [PubMed]
J. Immunol. Methods
- S. Kwon and E. M. Sevick-Muraca, “Functional lymphatic imaging in tumor-bearing mice,” J. Immunol. Methods 360(1-2), 167–172 (2010). [CrossRef] [PubMed]
J. Nucl. Med.
- C. Tsopelas and R. Sutton, “Why certain dyes are useful for localizing the sentinel lymph node,” J. Nucl. Med. 43(10), 1377–1382 (2002). [PubMed]
J. Physiol.
- A. A. Gashev, M. J. Davis, and D. C. Zawieja, “Inhibition of the active lymph pump by flow in rat mesenteric lymphatics and thoracic duct,” J. Physiol. 540(Pt 3), 1023–1037 (2002). [PubMed]
- M. J. Crowe, P. Y. von der Weid, J. A. Brock, and D. F. Van Helden, “Co-ordination of contractile activity in guinea-pig mesenteric lymphatics,” J. Physiol. 500(Pt 1), 235–244 (1997). [PubMed]
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