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International Journal of Inflammation
Volume 2013, Article ID 503725, 12 pages
http://dx.doi.org/10.1155/2013/503725
Research Article

Infiltration of Proinflammatory M1 Macrophages into the Outer Retina Precedes Damage in a Mouse Model of Age-Related Macular Degeneration

1Department of Ophthalmology, Bascom Palmer Eye Institute, University of Miami Miller School of Medicine, Miami, FL 33136, USA
2Department of Microbiology and Immunology, University of Miami Miller School of Medicine, Miami, FL 33136, USA
3Department of Chemistry, Case Western Reserve University, Cleveland, OH 44106, USA
4Department of Ophthalmology and Visual Sciences, Washington University School of Medicine, St. Louis, MO 63110, USA
5Department of Ophthalmology, Cole Eye Institute, Cleveland Clinic Lerner College of Medicine, Cleveland, OH 44195, USA
6Ophthalmology, Immunology & Microbiology, University of Miami Miller School of Medicine, Bascom Palmer Eye Institute, Miami, FL 33136, USA

Received 17 October 2012; Revised 20 December 2012; Accepted 24 January 2013

Academic Editor: Robert B. Nussenblatt

Copyright © 2013 Fernando Cruz-Guilloty 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. C. A. Augood, J. R. Vingerling, P. T. V. M. De Jong et al., “Prevalence of age-related maculopathy in older Europeans: the European Eye Study (EUREYE),” Archives of Ophthalmology, vol. 124, no. 4, pp. 529–535, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. J. C. Javitt, Z. Zhou, M. G. Maguire, S. L. Fine, and R. J. Willke, “Incidence of exudative age-related macular degeneration among elderly Americans,” Ophthalmology, vol. 110, no. 8, pp. 1534–1539, 2003. View at Publisher · View at Google Scholar · View at Scopus
  3. S. B. Bressler, M. G. Maguire, N. M. Bressler, and S. L. Fine, “Relationship of drusen and abnormalities of the retinal pigment epithelium to the prognosis of neovascular macular degeneration,” Archives of Ophthalmology, vol. 108, no. 10, pp. 1442–1447, 1990. View at Google Scholar · View at Scopus
  4. S. H. Sarks, D. Van Driel, L. Maxwell, and M. Killingsworth, “Softening of drusen and subretinal neovascularization,” Transactions of the Ophthalmological Societies of the United Kingdom, vol. 100, no. 3, pp. 414–422, 1980. View at Google Scholar · View at Scopus
  5. F. G. Holz, C. Bellman, S. Staudt, F. Schütt, and H. E. Völcker, “Fundus autofluorescence and development of geographic atrophy in age-related macular degeneration,” Investigative Ophthalmology and Visual Science, vol. 42, no. 5, pp. 1051–1056, 2001. View at Google Scholar · View at Scopus
  6. Y. Imamura, S. Noda, K. Hashizume et al., “Drusen, choroidal neovascularization, and retinal pigment epithelium dysfunction in SOD1-deficient mice: a model of age-related macular degeneration,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 30, pp. 11282–11287, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. J. W. Crabb, M. Miyagi, X. Gu et al., “Drusen proteome analysis: an approach to the etiology of age-related macular degeneration,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 23, pp. 14682–14687, 2002. View at Publisher · View at Google Scholar · View at Scopus
  8. A. O. Edwards, R. Ritter, K. J. Abel, A. Manning, C. Panhuysen, and L. A. Farrer, “Complement factor H polymorphism and age-related macular degeneration,” Science, vol. 308, no. 5720, pp. 421–424, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. B. Gold, J. E. Merriam, J. Zernant et al., “Variation in factor B (BF) and complement component 2 (C2) genes is associated with age-related macular degeneration,” Nature Genetics, vol. 38, no. 4, pp. 458–462, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. G. S. Hageman, D. H. Anderson, L. V. Johnson et al., “A common haplotype in the complement regulatory gene factor H (HF1/CFH) predisposes individuals to age-related macular degeneration,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 20, pp. 7227–7232, 2005. View at Publisher · View at Google Scholar · View at Scopus
  11. J. L. Haines, M. A. Hauser, S. Schmidt et al., “Complement factor H variant increases the risk of age-related macular degeneration,” Science, vol. 308, no. 5720, pp. 419–421, 2005. View at Publisher · View at Google Scholar · View at Scopus
  12. R. J. Klein, C. Zeiss, E. Y. Chew et al., “Complement factor H polymorphism in age-related macular degeneration,” Science, vol. 308, no. 5720, pp. 385–389, 2005. View at Publisher · View at Google Scholar · View at Scopus
  13. J. R. W. Yates, T. Sepp, B. K. Matharu et al., “Complement C3 variant and the risk of age-related macular degeneration,” New England Journal of Medicine, vol. 357, no. 6, pp. 553–561, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. D. H. Anderson, R. F. Mullins, G. S. Hageman, and L. V. Johnson, “A role for local inflammation in the formation of drusen in the aging eye,” American Journal of Ophthalmology, vol. 134, no. 3, pp. 411–431, 2002. View at Publisher · View at Google Scholar · View at Scopus
  15. R. B. Nussenblatt and F. Ferris III, “Age-related macular degeneration and the immune response: implications for therapy,” American Journal of Ophthalmology, vol. 144, no. 4, pp. 618–626, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. D. Weismann, K. Hartvigsen, N. Lauer et al., “Complement factor H binds malondialdehyde epitopes and protects from oxidative stress,” Nature, vol. 478, no. 7367, pp. 76–81, 2011. View at Publisher · View at Google Scholar
  17. D. S. Friedman, B. J. O'Colmain, S. C. Tomany et al., “Prevalence of age-related macular degeneration in the United States,” Archives of Ophthalmology, vol. 122, no. 4, pp. 564–572, 2004. View at Publisher · View at Google Scholar
  18. P. J. Rosenfeld, D. M. Brown, J. S. Heier et al., “Ranibizumab for neovascular age-related macular degeneration,” New England Journal of Medicine, vol. 355, no. 14, pp. 1419–1431, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. X. Gu, S. G. Meer, M. Miyagi et al., “Carboxyethylpyrrole protein adducts and autoantibodies, biomarkers for age-related macular degeneration,” Journal of Biological Chemistry, vol. 278, no. 43, pp. 42027–42035, 2003. View at Publisher · View at Google Scholar · View at Scopus
  20. J. Gu, G. J. T. Pauer, X. Yue et al., “Proteomic and genomic biomarkers for age-related macular degeneration,” Advances in Experimental Medicine and Biology, vol. 664, pp. 411–417, 2010. View at Publisher · View at Google Scholar
  21. R. E. Anderson, “Lipids of ocular tissues. IV. A comparison of the phospholipids from the retina of six mammalian species,” Experimental Eye Research, vol. 10, no. 2, pp. 339–344, 1970. View at Google Scholar · View at Scopus
  22. J. G. Hollyfield, V. L. Bonilha, M. E. Rayborn et al., “Oxidative damage-induced inflammation initiates age-related macular degeneration,” Nature Medicine, vol. 14, no. 2, pp. 194–198, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. J. G. Hollyfield, V. L. Perez, and R. G. Salomon, “A hapten generated from an oxidation fragment of docosahexaenoic acid is sufficient to initiate age-related macular degeneration,” Molecular Neurobiology, vol. 41, no. 2-3, pp. 290–298, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. R. B. Nussenblatt, B. Iu, and Z. Li, “Age-related macular degeneration: an immunologically driven disease,” Current Opinion in Investigational Drugs, vol. 10, no. 5, pp. 434–442, 2009. View at Google Scholar · View at Scopus
  25. P. S. Mettu, A. R. Wielgus, S. S. Ong, and S. W. Cousins, “Retinal pigment epithelium response to oxidant injury in the pathogenesis of early age-related macular degeneration,” Molecular Aspects of Medicine, vol. 33, no. 4, pp. 376–398, 2012. View at Publisher · View at Google Scholar
  26. S. K. Biswas and A. Mantovani, “Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm,” Nature Immunology, vol. 11, no. 10, pp. 889–896, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Sica and A. Mantovani, “Macrophage plasticity and polarization: in vivo veritas,” Journal of Clinical Investigation, vol. 122, no. 3, pp. 787–795, 2012. View at Publisher · View at Google Scholar
  28. Y. Wang, M. Burnier, B. Detrick, and J. J. Hooks, “Genetic predisposition to coronavirus-induced retinal disease,” Investigative Ophthalmology and Visual Science, vol. 37, no. 1, pp. 250–254, 1996. View at Google Scholar · View at Scopus
  29. J. Ambati, A. Anand, S. Fernandez et al., “An animal model of age-related macular degeneration in senescent Ccl-2- or Ccr-2-deficient mice,” Nature Medicine, vol. 9, no. 11, pp. 1390–1397, 2003. View at Publisher · View at Google Scholar · View at Scopus
  30. S. Y. Schmidt and R. D. Peisch, “Melanin concentration in normal human retinal pigment epithelium. Regional variation and age-related reduction,” Investigative Ophthalmology and Visual Science, vol. 27, no. 7, pp. 1063–1067, 1986. View at Google Scholar · View at Scopus
  31. T. F. Ng and J. W. Streilein, “Light-induced migration of retinal microglia into the subretinal space,” Investigative Ophthalmology and Visual Science, vol. 42, no. 13, pp. 3301–3310, 2001. View at Google Scholar · View at Scopus
  32. U. F. O. Luhmann, S. Robbie, P. M. G. Munro et al., “The drusenlike phenotype in aging Ccl2-knockout mice is caused by an accelerated accumulation of swollen autofluorescent subretinal macrophages,” Investigative Ophthalmology and Visual Science, vol. 50, no. 12, pp. 5934–5943, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. J. Kelly, A. A. Khan, J. Yin, T. A. Ferguson, and R. S. Apte, “Senescence regulates macrophage activation and angiogenic fate at sites of tissue injury in mice,” Journal of Clinical Investigation, vol. 117, no. 11, pp. 3421–3426, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. C. A. Lange, S. Robbie, P. M. G. Munro et al., “Differential modulation of retinal degeneration by Ccl2 and Cx3cr1 chemokine signalling,” PLoS ONE, vol. 7, no. 4, Article ID e35551, 2012. View at Publisher · View at Google Scholar
  35. M. J. Mattapallil, E. F. Wawrousek, C. C. Chan et al., “The Rd8 mutation of the Crb1 gene is present in vendor lines of C57BL/6N mice and embryonic stem cells, and confounds ocular induced mutant phenotypes,” Investigative Ophthalmology & Visual Science, vol. 53, no. 6, pp. 2921–2927, 2012. View at Google Scholar
  36. W. Ma, L. Zhao, A. M. Fontainhas, R. N. Fariss, and W. T. Wong, “Microglia in the mouse retina alter the structure and function of retinal pigmented epithelial cells: a potential cellular interaction relevant to AMD,” PLoS ONE, vol. 4, no. 11, Article ID e7945, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. S. L. Doyle, M. Campbell, E. Ozaki et al., “NLRP3 has a protective role in age-related macular degeneration through the induction of IL-18 by drusen components,” Nature Medicine, vol. 18, no. 5, pp. 791–798, 2012. View at Publisher · View at Google Scholar
  38. A. London, E. Itskovich, I. Benhar et al., “Neuroprotection and progenitor cell renewal in the injured adult murine retina requires healing monocyte-derived macrophages,” Journal of Experimental Medicine, vol. 208, no. 1, pp. 23–39, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. X. Cao, D. Shen, M. M. Patel et al., “Macrophage polarization in the maculae of age-related macular degeneration: a pilot study,” Pathology International, vol. 61, no. 9, pp. 528–535, 2011. View at Publisher · View at Google Scholar
  40. L. Lu, X. Gu, L. Hong et al., “Synthesis and structural characterization of carboxyethylpyrrole-modified proteins: mediators of age-related macular degeneration,” Bioorganic and Medicinal Chemistry, vol. 17, no. 21, pp. 7548–7561, 2009. View at Publisher · View at Google Scholar · View at Scopus