Table of Contents Author Guidelines Submit a Manuscript
Journal of Ophthalmology
Volume 2012, Article ID 279037, 6 pages
http://dx.doi.org/10.1155/2012/279037
Review Article

Leukocyte Adhesion Molecules in Diabetic Retinopathy

1Laboratory of Ocular Cell Biology and Visual Science, Hokkaido University Graduate School of Medicine, N-15, W-7, Kita-ku, Sapporo 060-8638, Japan
2Department of Ophthalmology, Hokkaido University Graduate School of Medicine, N-15, W-7, Kita-ku, Sapporo 060-8638, Japan
3Department of Ophthalmology, Graduate School of Medical Sciences, Kyushu University, Fukuoka 812-8582, Japan

Received 13 August 2011; Accepted 24 September 2011

Academic Editor: Ofra Benny

Copyright © 2012 Kousuke Noda et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. H. Xu, M. Chen, and J. V. Forrester, “Para-inflammation in the aging retina,” Progress in Retinal and Eye Research, vol. 28, no. 5, pp. 348–368, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  2. D. A. Antonetti, A. J. Barber, S. K. Bronson et al., “Diabetic retinopathy: seeing beyond glucose-induced microvascular disease,” Diabetes, vol. 55, no. 9, pp. 2401–2411, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  3. T. W. Gardner, D. A. Antonetti, A. J. Barber, K. F. LaNoue, and S. W. Levison, “Diabetic retinopathy: more than meets the eye,” Survey of Ophthalmology, vol. 47, supplement 2, pp. S253–S262, 2002. View at Publisher · View at Google Scholar · View at Scopus
  4. A. P. Adamis and A. J. Berman, “Immunological mechanisms in the pathogenesis of diabetic retinopathy,” Seminars in Immunopathology, vol. 30, no. 2, pp. 65–84, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  5. D. S. McLeod, D. J. Lefer, C. Merges, and G. A. Lutty, “Enhanced expression of intracellular adhesion molecule-1 and P-selectin in the diabetic human retina and choroid,” American Journal of Pathology, vol. 147, no. 3, pp. 642–653, 1995. View at Google Scholar · View at Scopus
  6. G. A. Lutty, J. Cao, and D. S. McLeod, “Relationship of polymorphonuclear leukocytes to capillary dropout in the human diabetic choroid,” American Journal of Pathology, vol. 151, no. 3, pp. 707–714, 1997. View at Google Scholar · View at Scopus
  7. A. W. Stitt, T. A. Gardiner, and D. B. Archer, “Histological and ultrastructural investigation of retinal microaneurysm development in diabetic patients,” British Journal of Ophthalmology, vol. 79, no. 4, pp. 362–367, 1995. View at Google Scholar · View at Scopus
  8. S. Y. Kim, M. A. Johnson, D. S. McLeod, T. Alexander, B. C. Hansen, and G. A. Lutty, “Neutrophils are associated with capillary closure in spontaneously diabetic monkey retinas,” Diabetes, vol. 54, no. 5, pp. 1534–1542, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. A. M. Joussen, V. Poulaki, N. Mitsiades et al., “Suppression of Fas-FasL-induced endothelial cell apoptosis prevents diabetic blood-retinal barrier breakdown in a model of streptozotocin-induced diabetes,” The FASEB Journal, vol. 17, no. 1, pp. 76–78, 2003. View at Google Scholar · View at Scopus
  10. K. Miyamoto, S. Khosrof, S. E. Bursell et al., “Prevention of leukostasis and vascular leakage in streptozotocin-induced diabetic retinopathy via intercellular adhesion molecule-1 inhibition,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 19, pp. 10836–10841, 1999. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Yanoff and B. S. Fine, Ocular Pathology, Mosby-Wolfe, London, UK, 1996.
  12. S. Tang and K. C. Le-Ruppert, “Activated T lymphocytes in epiretinal membranes from eyes of patients with proliferative diabetic retinopathy,” Graefe's Archive for Clinical and Experimental Ophthalmology, vol. 233, no. 1, pp. 21–25, 1995. View at Google Scholar · View at Scopus
  13. S. Kase, W. Saito, S. Ohno, and S. Ishida, “Proliferative diabetic retinopathy with lymphocyte-rich epiretinal membrane associated with poor visual prognosis,” Investigative Ophthalmology & Visual Science, vol. 50, no. 12, pp. 5909–5912, 2009. View at Google Scholar · View at Scopus
  14. K. Ley, “Functions of selectins,” Results and Problems in Cell Differentiation, vol. 33, pp. 177–200, 2001. View at Google Scholar
  15. R. P. McEver, “Selectins: lectins that initiate cell adhesion under flow,” Current Opinion in Cell Biology, vol. 14, no. 5, pp. 581–586, 2002. View at Publisher · View at Google Scholar · View at Scopus
  16. C. W. Wyble, K. L. Hynes, J. Kuchibhotla, B. C. Marcus, D. Hallahan, and B. L. Gewertz, “TNF-α and IL-1 upregulate membrane-bound and soluble E-selectin through a common pathway,” Journal of Surgical Research, vol. 73, no. 2, pp. 107–112, 1997. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  17. N. A. Essani, M. A. Fisher, C. A. Simmons, J. L. Hoover, A. Farhood, and H. Jaeschke, “Increased P-selectin gene expression in the liver vasculature and its role in the pathophysiology of neutrophil-induced liver injury in murine endotoxin shock,” Journal of Leukocyte Biology, vol. 63, no. 3, pp. 288–296, 1998. View at Google Scholar · View at Scopus
  18. A. Weller, S. Isenmann, and D. Vestweber, “Cloning of the mouse endothelial selectins. Expression of both E- and P-selectin is inducible by tumor necrosis factor α,” Journal of Biological Chemistry, vol. 267, no. 21, pp. 15176–15183, 1992. View at Google Scholar · View at Scopus
  19. N. C. Kaneider, A. J. Leger, and A. Kuliopulos, “Therapeutic targeting of molecules involved in leukocyte-endothelial cell interactions,” FEBS Journal, vol. 273, no. 19, pp. 4416–4424, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  20. H. Ulbrich, E. E. Eriksson, and L. Lindbom, “Leukocyte and endothelial cell adhesion molecules as targets for therapeutic interventions in inflammatory disease,” Trends in Pharmacological Sciences, vol. 24, no. 12, pp. 640–647, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. N. Hogg, I. Patzak, and F. Willenbrock, “The insider's guide to leukocyte integrin signalling and function,” Nature Reviews Immunology, vol. 11, no. 6, pp. 416–426, 2011. View at Publisher · View at Google Scholar · View at PubMed
  22. M. Salmi and S. Jalkanen, “A 90-kilodalton endothelial cell molecule mediating lymphocyte binding in humans,” Science, vol. 257, no. 5075, pp. 1407–1409, 1992. View at Google Scholar · View at Scopus
  23. E. Akin, J. Aversa, and A. C. Steere, “Expression of adhesion molecules in synovia of patients with treatment-resistant lyme arthritis,” Infection and Immunity, vol. 69, no. 3, pp. 1774–1780, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  24. K. Jaakkola, S. Jalkanen, K. Kaunismäki et al., “Vascular adhesion protein-1, intercellular adhesion molecule-1 and P-selectin mediate leukocyte binding to ischemic heart in humans,” Journal of the American College of Cardiology, vol. 36, no. 1, pp. 122–129, 2000. View at Publisher · View at Google Scholar
  25. M. Salmi, K. Kalimo, and S. Jalkanen, “Induction and function of vascular adhesion protein-1 at sites of inflammation,” Journal of Experimental Medicine, vol. 178, no. 6, pp. 2255–2260, 1993. View at Publisher · View at Google Scholar · View at Scopus
  26. B. Singh, T. Tschernig, M. Van Griensven, A. Fieguth, and R. Pabst, “Expression of vascular adhesion protein-1 in normal and inflamed mice lungs and normal human lungs,” Virchows Archiv, vol. 442, no. 5, pp. 491–495, 2003. View at Google Scholar · View at Scopus
  27. L. Almulki, K. Noda, S. Nakao, T. Hisatomi, K. L. Thomas, and A. Hafezi-Moghadam, “Localization of vascular adhesion protein-1 (VAP-1) in the human eye,” Experimental Eye Research, vol. 90, no. 1, pp. 26–32, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  28. K. Noda, S. Miyahara, T. Nakazawa et al., “Inhibition of vascular adhesion protein-1 suppresses endotoxin-induced uveitis,” The FASEB Journal, vol. 22, no. 4, pp. 1094–1103, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  29. K. Noda, H. She, T. Nakazawa et al., “Vascular adhesion protein-1 blockade suppresses choroidal neovascularization,” The FASEB Journal, vol. 22, no. 8, pp. 2928–2935, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  30. K. Mastej and R. Adamiec, “Neutrophil surface expression of CD11b and CD62L in diabetic microangiopathy,” Acta Diabetologica, vol. 45, no. 3, pp. 183–190, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  31. D. M. Smalley and K. Ley, “L-selectin: mechanisms and physiological significance of ectodomain cleavage,” Journal of Cellular and Molecular Medicine, vol. 9, no. 2, pp. 255–266, 2005. View at Google Scholar · View at Scopus
  32. K. Matsumoto, Y. Sera, Y. Ueki, G. Inukai, E. Niiro, and S. Miyake, “Comparison of serum concentrations of soluble adhesion molecules in diabetic microangiopathy and macroangiopathy,” Diabetic Medicine, vol. 19, no. 10, pp. 822–826, 2002. View at Publisher · View at Google Scholar · View at Scopus
  33. S. S. Soedamah-Muthu, N. Chaturvedi, C. G. Schalkwijk, C. D. Stehouwer, P. Ebeling, and J. H. Fuller, “Soluble vascular cell adhesion molecule-1 and soluble E-selectin are associated with micro- and macrovascular complications in Type 1 diabetic patients,” Journal of Diabetes and its Complications, vol. 20, no. 3, pp. 188–195, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  34. M. Nowak, T. Wielkoszyński, B. Marek et al., “Blood serum levels of vascular cell adhesion molecule (sVCAM-1), intercellular adhesion molecule (sICAM-1) and endothelial leucocyte adhesion molecule-1 (ELAM-1) in diabetic retinopathy,” Clinical and Experimental Medicine, vol. 8, no. 3, pp. 159–164, 2008. View at Publisher · View at Google Scholar · View at PubMed
  35. A. M. Spijkerman, M. A. Gall, L. Tarnow et al., “Endothelial dysfunction and low-grade inflammation and the progression of retinopathy in Type 2 diabetes,” Diabetic Medicine, vol. 24, no. 9, pp. 969–976, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  36. C. Gustavsson, E. Agardh, B. Bengtsson, and C. D. Agardh, “TNF-α is an independent serum marker for proliferative retinopathy in type 1 diabetic patients,” Journal of Diabetes and its Complications, vol. 22, no. 5, pp. 309–316, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  37. V. H. Guaiquil, S. Swendeman, W. Zhou et al., “ADAM8 is a negative regulator of retinal neovascularization and of the growth of heterotopically injected tumor cells in mice,” Journal of Molecular Medicine, vol. 88, no. 5, pp. 497–505, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  38. A. Chalaris, N. Adam, C. Sina et al., “Critical role of the disintegrin metalloprotease ADAM17 for intestinal inflammation and regeneration in mice,” Journal of Experimental Medicine, vol. 207, no. 8, pp. 1617–1624, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  39. J. Scheller, A. Chalaris, C. Garbers, and S. Rose-John, “ADAM17: a molecular switch to control inflammation and tissue regeneration,” Trends in Immunology, vol. 32, no. 8, pp. 380–387, 2011. View at Publisher · View at Google Scholar · View at PubMed
  40. J. Adamiec-Mroczek, J. Oficjalska-Młyńczak, and M. Misiuk-Hojło, “Proliferative diabetic retinopathy-The influence of diabetes control on the activation of the intraocular molecule system,” Diabetes Research and Clinical Practice, vol. 84, no. 1, pp. 46–50, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  41. G. A. Limb, J. Hickman-Casey, R. D. Hollifield, and A. H. Chignell, “Vascular adhesion molecules in vitreous from eyes with proliferative diabetic retinopathy,” Investigative Ophthalmology and Visual Science, vol. 40, no. 10, pp. 2453–2457, 1999. View at Google Scholar · View at Scopus
  42. J. A. Olson, C. M. Whitelaw, K. C. McHardy, D. W. Pearson, and J. V. Forrester, “Soluble leucocyte adhesion molecules in diabetic retinopathy stimulate retinal capillary endothelial cell migration,” Diabetologia, vol. 40, no. 10, pp. 1166–1171, 1997. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  43. A. E. Koch, M. M. Halloran, C. J. Haskell, M. R. Shah, and P. J. Polverini, “Angiogenesis mediated by soluble forms of E-selectin and vascular cell adhesion molecule-1,” Nature, vol. 376, no. 6540, pp. 517–519, 1995. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  44. H. P. Heidenkummer and A. Kampik, “Intercellular adhesion molecule-1 (ICAM-1) and leukocyte function-associated antigen-1 (LFA-1) expression in human epiretinal membranes,” Graefe's Archive for Clinical and Experimental Ophthalmology, vol. 230, no. 5, pp. 483–487, 1992. View at Google Scholar · View at Scopus
  45. H. Song, L. Wang, and Y. Hui, “Expression of CD18 on the neutrophils of patients with diabetic retinopathy,” Graefe's Archive for Clinical and Experimental Ophthalmology, vol. 245, no. 1, pp. 24–31, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  46. A. Kretowski, J. Myśliwiec, and I. Kinalska, “The alterations of CD11A expression on peripheral blood lymphocytes/monocytes and CD62L expression on peripheral blood lymphocytes in Graves' disease and type 1 diabetes,” Roczniki Akademii Medycznej w Bialymstoku (1995), vol. 44, pp. 151–159, 1999. View at Google Scholar · View at Scopus
  47. N. Kociok, S. Radetzky, T. U. Krohne et al., “ICAM-1 depletion does not alter retinal vascular development in a model of oxygen-mediated neovascularization,” Experimental Eye Research, vol. 89, no. 4, pp. 503–510, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  48. J. L. Wautier and M. P. Wautier, “Blood cells and vascular cell interactions in diabetes,” Clinical Hemorheology and Microcirculation, vol. 25, no. 2, pp. 49–53, 2001. View at Google Scholar · View at Scopus
  49. C. Gustavsson, C. D. Agardh, A. V. Zetterqvist, J. Nilsson, E. Agardh, and M. F. Gomez, “Vascular cellular adhesion molecule-1 (VCAM-1) expression in mice retinal vessels is affected by both hyperglycemia and hyperlipidemia,” PLoS One, vol. 5, no. 9, Article ID e12699, pp. 1–12, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  50. E. Iliaki, V. Poulaki, N. Mitsiades, C. S. Mitsiades, J. W. Miller, and E. S. Gragoudas, “Role of α4 integrin (CD49d) in the pathogenesis of diabetic retinopathy,” Investigative Ophthalmology and Visual Science, vol. 50, no. 10, pp. 4898–4904, 2009. View at Publisher · View at Google Scholar · View at PubMed
  51. K. Noda, S. Nakao, S. Zandi, V. Engelstädter, Y. Mashima, and A. Hafezi-Moghadam, “Vascular adhesion protein-1 regulates leukocyte transmigration rate in the retina during diabetes,” Experimental Eye Research, vol. 89, no. 5, pp. 774–781, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  52. S. Tazzyman, C. E. Lewis, and C. Murdoch, “Neutrophils: key mediators of tumour angiogenesis,” International Journal of Experimental Pathology, vol. 90, no. 3, pp. 222–231, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  53. A. M. Joussen, T. Murata, A. Tsujikawa, B. Kirchhof, S. E. Bursell, and A. P. Adamis, “Leukocyte-mediated endothelial cell injury and death in the diabetic retina,” American Journal of Pathology, vol. 158, no. 1, pp. 147–152, 2001. View at Google Scholar · View at Scopus
  54. H. Garpenstrand, J. Ekblom, L. B. Bäcklund, L. Oreland, and U. Rosenqvist, “Elevated plasma semicarbazide-sensitive amine oxidase (SSAO) activity in Type 2 diabetes mellitus complicated by retinopathy,” Diabetic Medicine, vol. 16, no. 6, pp. 514–521, 1999. View at Publisher · View at Google Scholar
  55. J. L. Grönvall-Nordquist, L. B. Bäcklund, H. Garpenstrand et al., “Follow-up of plasma semicarbazide-sensitive amine oxidase activity and retinopathy in Type 2 diabetes mellitus,” Journal of Diabetes and its Complications, vol. 15, no. 5, pp. 250–256, 2001. View at Publisher · View at Google Scholar · View at Scopus
  56. D. J. Smith and P. J. Vainio, “Targeting vascular adhesion protein-1 to treat autoimmune and inflammatory diseases,” Annals of the New York Academy of Sciences, vol. 1110, pp. 382–388, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  57. M. Bourajjaj, C. D. Stehouwer, V. W. Van Hinsbergh, and C. G. Schalkwijk, “Role of methylglyoxal adducts in the development of vascular complications in diabetes mellitus,” Biochemical Society Transactions, vol. 31, no. 6, pp. 1400–1402, 2003. View at Google Scholar · View at Scopus
  58. E. A. Ellis, D. L. Guberski, M. Somogyi-Mann, and M. B. Grant, “Increased H2O2, vascular endothelial growth factor and receptors in the retina of the BBZ/WOR diabetic rat,” Free Radical Biology and Medicine, vol. 28, no. 1, pp. 91–101, 2000. View at Publisher · View at Google Scholar · View at Scopus