Differential transport function of lymphatic vessels in the rat tail model and the long-term effects of indocyanine green as assessed with near-infrared imaging

Frontiers in Physiology

Volumn 4 AUG, Issue , 2013, Pages

  Weiler, Michael ^a   Dixon, J Brandon ^a  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

ICG; Indocyanine green; Lymphatic; Lymphatic function; Lymphatic imaging; Near infrared imaging

Indexed keywords

GLYCERYL TRINITRATE; INDOCYANINE GREEN; MACROGOL; NITRIC OXIDE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL FUNCTION; CONTROLLED STUDY; FEMALE; FLUORESCENCE; FOLLOW UP; IMAGING; LYMPH NODE; LYMPH VESSEL; NEAR INFRARED IMAGING; NONHUMAN; RAT; STEADY STATE; TAIL;

EID: 84884568863     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2013.00215     Document Type: Article

References (40)

1. Abels, C., Fickweiler, S., Weiderer, P., Baumler, W., Hofstädter, F., Landthaler, M., et al. (2000). Indocyanine green (ICG) and laser irradiation induce photooxidation. Arch. Dermatol. Res. 292, 404-411. doi: 10.1007/s004030000147
2. Aldrich, M. B., Davies-Venn, C., Angermiller, B., Robinson, H., Chan, W., Kwon, S., et al. (2012). Concentration of indocyanine green does not significantly influence lymphatic function as assessed by near-infrared imaging. Lymphat. Res. Biol. 10, 20-24. doi: 10.1089/lrb.2011.0003
3. Baluk, P. (2005). Pathogenesis of persistent lymphatic vessel hyperplasia in chronic airway inflammation. J. Clin. Invest. 115, 247-257.
4. Blum, K. S., Proulx, S. T., Luciani, P., Leroux, J.-C., and Detmar, M. (2013). Dynamics of lymphatic regeneration and flow patterns after lymph node dissection. Breast Cancer Res. Treat. 139, 81-86. doi: 10.1007/s10549-013-2537-7
5. Boardman, K., and Swartz, M. A. (2003). Interstitial flow as a guide for lymphangiogenesis. Circ. Res. 92, 801-808. doi: 10.1161/01.RES.0000065621.69843.49
6. Bohlen, H. G., Gasheva, O. Y., and Zawieja, D. C. (2011). Nitric oxide formation by lymphatic bulb and valves is a major regulatory component of lymphatic pumping. Am. J. Physiol. Heart Circ. Physiol. 301, H1897-H11906. doi: 10.1152/ajpheart.00260.2011
7. Burrows, P. E., Gonzalez-Garay, M. L., Rasmussen, J. C., Aldrich, M. B., Guilliod, R., Maus, E. A., et al. (2013). Lymphatic abnormalities are associated with RASA1 gene mutations in mouse and man. Proc. Natl. Acad. Sci. U.S.A. 11, 8621-8626. doi: 10.1073/pnas.1222722110
8. Clavin, N. W., Avraham, T., Fernandez, J., Daluvoy, S. V., Soares, M. A., Chaudhry, A., et al. (2008). TGF-beta1 is a negative regulator of lymphatic regeneration during wound repair. Am. J. Physiol. Heart Circ. Physiol. 295, H2113-H2127. doi: 10.1152/ajpheart.00879.2008
9. Davies-Venn, C. A., Angermiller, B., Wilganowski, N., Ghosh, P., Harvey, B. R., Wu, G., et al. (2011). Albumin-binding domain conjugate for near-infrared fluorescence lymphatic imaging. Mol. Imaging Biol. 14, 301-314. doi: 10.1007/s11307-011-0499-x
10. Dixon, J. B. (2010). Lymphatic lipid transport: sewer or subway? Trends Endocrinol. Metab. 21, 480-487. doi: 10.1016/j.tem.2010.04.003
11. Dixon, J. B., Moore, J. E. Jr., Cote, G., Gashev, A. A., and Zawieja, D. C. (2006). Lymph flow, shear stress, and lympfyte velocity in rat mesenteric prenodal lymphatics. Microcirculation 13, 597-610. doi: 10.1080/10739680600893909
12. Dongaonkar, R. M., Laine, G. A., Stewart, R. H., and Quick, C. M. (2009). Balance point characterization of interstitial fluid volume regulation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297, R6-R16. doi: 10.1152/ajpregu.00097.2009
13. Ezaki, T., Baluk, P., Thurston, G., La Barbara, A., Woo, C., and McDonald, D. M. (2001). Time course of endothelial cell proliferation and microvascular remodeling in chronic inflammation. Am. J. Pathol. 158, 2043-2055. doi: 10.1016/S0002-9440(10)64676-7
14. Fickweiler, S., Szeimies, R. M., Baumler, W., Steinbach, P., Karrer, S., Goetz, A. E., et al. (1997). Indocyanine green: intracellular uptake and phototherapeutic effects in vitro. J. Photochem. Photobiol. B 38, 178-183. doi: 10.1016/S1011-1344(96)07453-2
15. Frangioni, J. (2003). In vivo near-infrared fluorescence imaging. Curr. Opin. Chem. Biol. 7, 626-634. doi: 10.1016/j.cbpa.2003.08.007
16. Gashev, A. A., Davis, M. J., and Zawieja, D. C. (2002). Inhibition of the active lymph pump by flow in rat mesenteric lymphatics and thoracic duct. J. Physiol. 540, 1023-1037.
17. Gashev, A. A., Nagai, T., and Bridenbaugh, E. A. (2010). Indocyanine green and lymphatic imaging: current problems. Lymphat. Res. Biol. 8, 127-130. doi: 10.1089/lrb.2010.0005
18. Goldman, J., Conley, K., Raehl, A., Bondy, D., Pytowski, B., Swartz, M. A., et al. (2007). Regulation of lymphatic capillary regeneration by interstitial flow in skin. Am. J. Physiol. Heart Circ. Physiol. 292, H2176-H2183. doi: 10.1152/ajpheart.01011.2006
19. Ikagawa, H., Yoneda, M., Iwaki, M., Isogai, Z., Tsujii, K., Yamazaki, R., et al. (2005). Chemical toxicity of indocyanine green damages retinal pigment epithelium. Invest. Ophthalmol. Vis. Sci. 46, 2531-2539. doi: 10.1167/iovs.04-1521
20. Kassis, T. (2012). Dual-channel in-situ optical imaging system for quantifying lipid uptake and lymphatic pump function. J. Biomed. Opt. 17:086005. doi: 10.1117/1.JBO.17.8.086005
21. Kwon, S., and Sevick-Muraca, E. M. (2010). Functional lymphatic imaging in tumor-bearing mice. J. Immunol. Methods 360, 167-172. doi: 10.1016/j.jim.2010.06.016
22. Leu, A., Berk, D., Yuan, F., and Jain, R. (1994). Flow velocity in the superficial lymphatic network of the mouse tail. Am. J. Physiol. 36, H1507-H1513.
23. Levick, J. R., and Michel, C. C. (2010). Microvascular fluid exchange and the revised Starling principle. Cardiovasc. Res. 87, 198-210. doi: 10.1093/cvr/cvq062
24. Liao, S., Cheng, G., Conner, D. A., Huang, Y., Kucherlapati, R. S., Munn, L. L., et al. (2011). Impaired lymphatic contraction associated with immunosuppression. Proc. Natl. Acad. Sci. U.S.A. 108, 18784-18789. doi: 10.1073/pnas.1116152108
25. Nipper, M. E., and Dixon, J. B. (2011). Engineering the lymphatic system. Cardiovasc. Eng. Technol. 2, 296-308. doi: 10.1007/s13239-011-0054-6
26. Proulx, S. T., Luciani, P., Christiansen, A., Karaman, S., Blum, K. S., Rinderknecht, M., et al. (2013). Use of a PEG-conjugated bright near-infrared dye for functional imaging of rerouting of tumor lymphatic drainage after sentinel lymph node metastasis. Biomaterials 34, 5128-5137. doi: 10.1016/j.biomaterials.2013.03.034
27. Proulx, S. T., Luciani, P., Derzsi, S., Rinderknecht, M., Mumprecht, V., Leroux, J.-C., et al. (2010). Quantitative imaging of lymphatic function with liposomal indocyanine green. Cancer Res. 70, 7053-7062. doi: 10.1158/0008-5472.CAN-10-0271
28. Rasmussen, J. C., Tan, I.-C., Marshall, M. V., Fife, C. E., and Sevick-Muraca, E. M. (2009). Lymphatic imaging in humans with near-infrared fluorescence. Curr. Opin. Biotechnol. 20, 74-82. doi: 10.1016/j.copbio.2009.01.009
29. Rockson, S. G. (2008). Diagnosis and management of lymphatic vascular disease. J. Am. Coll. Cardiol. 52, 799-806. doi: 10.1016/j.jacc.2008.06.005
30. Rutkowski, J. M., Moya, M., Johannes, J., Goldman, J., and Swartz, M. A. (2006). Secondary lymphedema in the mouse tail: lymphatic hyperplasia, VEGF-C upregulation, and the protective role of MMP-9. Microvasc. Res. 72, 161-171. doi: 10.1016/j.mvr.2006.05.009
31. Scallan, J. P., and Davis, M. J. (2013). Genetic removal of basal nitric oxide enhances contractile activity in isolated murine collecting lymphatic vessels. J. Physiol. 591, 2139-2156.
32. Sharma, R., Wendt, J. A., Rasmussen, J. C., Adams, K. E., Marshall, M. V., and Sevick-Muraca, E. M. (2008). New horizons for imaging lymphatic function. Ann. N.Y. Acad. Sci. 1131, 13-36. doi: 10.1196/annals.1413.002
33. Swartz, M. A., Hubbell, J. A., and Reddy, S. (2008). Lymphatic drainage function and its immunological implications: from dendritic cell homing to vaccine design. Semin. Immunol. 20, 147-156. doi: 10.1016/j.smim.2007.11.007
34. Tabibiazar, R., Cheung, L., Han, J., Swanson, J., Beilhack, A., An, A., et al. (2006). Inflammatory manifestations of experimental lymphatic insufficiency. PLoS Med. 3:e254. doi: 10.1371/journal.pmed.0030254
35. Tammela, T., and Alitalo, K. (2010). Lymphangiogenesis: molecular mechanisms and future promise. Cell 140, 460-476. doi: 10.1016/j.cell.2010.01.045
36. Unno, N., Inuzuka, K., Suzuki, M., Yamamoto, N., Sagara, D., Nishiyama, M., et al. (2007). Preliminary experience with a novel fluorescence lymphography using indocyanine green in patients with secondary lymphedema. J. Vasc. Surg. 45, 1016-1021. doi: 10.1016/j.jvs.2007.01.023
37. Weber, M., Hauschild, R., Schwarz, J., Moussion, C., de Vries, I., Legler, D. F., et al. (2013). Interstitial dendritic cell guidance by haptotactic chemokine gradients. Science 339, 328-332. doi: 10.1126/science.1228456
38. Weiler, M., Kassis, T., and Dixon, J. B. (2012). Sensitivity analysis of near-infrared functional lymphatic imaging. J. Biomed. Opt. 17:066019. doi: 10.1117/1.JBO.17.6.066019
39. Yoon, Y.-S., Murayama, T., Gravereaux, E., Tkebuchava, T., Silver, M., Curry, C., et al. (2003). VEGF-C gene therapy augments postnatal lymphangiogenesis and ameliorates secondary lymphedema. J. Clin. Invest. 111, 717-725.
40. Zampell, J. C., Elhadad, S., Avraham, T., Weitman, E., Aschen, S., Yan, A., et al. (2012). Toll-like receptor deficiency worsens inflammation and lymphedema after lymphatic injury. Am. J. Physiol. Cell Physiol. 302, C709-C719. doi: 10.1152/ajpcell.00284.2011