A2E accumulation influences retinal microglial activation and complement regulation

Neurobiology of Aging

Volumn 34, Issue 3, 2013, Pages 943-960

  Ma, Wenxin ^a   Coon, Steven ^b   Zhao, Lian ^a   Fariss, Robert N ^a   Wong, Wai T ^a  

^a NATIONAL EYE INSTITUTE   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

A2E; Activation; Age related macular degeneration; Aging; Chemokine; Complement; Lipofuscin; Microglia; Neuroprotection; Photoreceptors; Retina

Indexed keywords

A2E; ALTERNATIVE COMPLEMENT PATHWAY C3 C5 CONVERTASE; CHEMOKINE RECEPTOR; COMPLEMENT FACTOR H; LIPOFUSCIN; RETINOID DERIVATIVE; UNCLASSIFIED DRUG;

ADULT; AGE; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL ACTIVATION; CELL CYCLE REGULATION; CELL MIGRATION; CHEMOTAXIS; COMPLEMENT ACTIVATION; COMPLEMENT DEPOSITION; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MICROGLIA; MOUSE; NEUROPROTECTION; NONHUMAN; PATHOGENESIS; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA MACULA AGE RELATED DEGENERATION; RETINA NERVE CELL;

AGED; AGED, 80 AND OVER; AGING; ANIMALS; CELL MIGRATION INHIBITION; CELLS, CULTURED; COMPLEMENT ACTIVATION; COMPLEMENT FACTOR B; COMPLEMENT FACTOR H; HUMANS; LIPOFUSCIN; MACULAR DEGENERATION; MICE; MICE, TRANSGENIC; MICROGLIA; MIDDLE AGED; PYRIDINIUM COMPOUNDS; RECEPTORS, CHEMOKINE; RETINA; RETINOIDS;

EID: 84870515243     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2012.06.010     Document Type: Article

References (79)

1. Anderson D.H., Mullins R.F., Hageman G.S., Johnson L.V. A role for local inflammation in the formation of drusen in the aging eye. Am. J. Ophthalmol 2002, 134:411-431.
2. Augustin A.J., Kirchhof J. Inflammation and the pathogenesis of age-related macular degeneration. Expert Opin. Ther. Targets 2009, 13:641-651.
3. Biber K., Vinet J., Boddeke H.W. Neuron-microglia signaling: chemokines as versatile messengers. J. Neuroimmunol 2008, 198:69-74.
4. Boehm M.R., Oellers P., Thanos S. Inflammation and immunology of the vitreoretinal compartment. Inflamm. Allergy Drug Targets 2011, 10:283-309.
5. Cao X., Shen D., Patel M.M., Tuo J., Johnson T.M., Olsen T.W., Chan C.C. Macrophage polarization in the maculae of age-related macular degeneration: a pilot study. Pathol. Int 2011, 61:528-535.
6. Chen L., Yang P., Kijlstra A. Distribution, markers, and functions of retinal microglia. Ocul. Immunol. Inflamm 2002, 10:27-39.
7. Chen M., Forrester J.V., Xu H. Synthesis of complement factor H by retinal pigment epithelial cells is down-regulated by oxidized photoreceptor outer segments. Exp. Eye Res 2007, 84:635-645.
8. Chen M., Muckersie E., Robertson M., Forrester J.V., Xu H. Up-regulation of complement factor B in retinal pigment epithelial cells is accompanied by complement activation in the aged retina. Exp. Eye Res 2008, 87:543-550.
9. Collier R.J., Wang Y., Smith S.S., Martin E., Ornberg R., Rhoades K., Romano C. Complement deposition and microglial activation in the outer retina in light-induced retinopathy: inhibition by a 5-HT1A agonist. Invest. Ophthalmol. Vis. Sci 2011, 52:8108-8116.
10. Colton C.A., Wilcock D.M. Assessing activation states in microglia. CNS Neurol. Disord. Drug Targets 2010, 9:174-191.
11. Combadière C., Feumi C., Raoul W., Keller N., Rodéro M., Pézard A., Lavalette S., Houssier M., Jonet L., Picard E., Debré P., Sirinyan M., Deterre P., Ferroukhi T., Cohen S.Y., Chauvaud D., Jeanny J.C., Chemtob S., Behar-Cohen F., Sennlaub F. CX3CR1-dependent subretinal microglia cell accumulation is associated with cardinal features of age-related macular degeneration. J. Clin. Invest 2007, 117:2920-2928.
12. Congdon N., O'Colmain B., Klaver C.C., Klein R., Muñoz B., Friedman D.S., Kempen J., Taylor H.R., Mitchell P. Causes and prevalence of visual impairment among adults in the United States. Arch. Ophthalmol 2004, 122:477-485. Eye Diseases Prevalence Research Group.
13. Czeh M., Gressens P., Kaindl A.M. The yin and yang of microglia. Dev. Neurosci 2011, 33:199-209.
14. Damani M.R., Zhao L., Fontainhas A.M., Amaral J., Fariss R.N., Wong W.T. Age-related alterations in the dynamic behavior of microglia. Aging Cell 2011, 10:263-276.
15. Ding X., Patel M., Shen D., Herzlich A.A., Cao X., Villasmil R., Klupsch K., Tuo J., Downward J., Chan C.C. Enhanced HtrA2/Omi expression in oxidative injury to retinal pigment epithelial cells and murine models of neurodegeneration. Invest. Ophthalmol. Vis. Sci 2009, 50:4957-4966.
16. Donoso L.A., Kim D., Frost A., Callahan A., Hageman G. The role of inflammation in the pathogenesis of age-related macular degeneration. Surv. Ophthalmol 2006, 51:137-152.
17. Donoso L.A., Vrabec T., Kuivaniemi H. The role of complement Factor H in age-related macular degeneration: a review. Surv. Ophthalmol 2010, 55:227-246.
18. Eldred G.E., Lasky M.R. Retinal age pigments generated by self-assembling lysosomotropic detergents. Nature 1993, 361:724-726.
19. Friedman D.S., O'Colmain B.J., Muñoz B., Tomany S.C., McCarty C., de Jong P.T., Nemesure B., Mitchell P., Kempen J. Prevalence of age-related macular degeneration in the United States. Arch. Ophthalmol 2004, 122:564-572. Eye Diseases Prevalence Research Group.
20. Gehrs K.M., Jackson J.R., Brown E.N., Allikmets R., Hageman G.S. Complement, age-related macular degeneration and a vision of the future. Arch. Ophthalmol 2010, 128:349-358.
21. Geiss G.K., Bumgarner R.E., Birditt B., Dahl T., Dowidar N., Dunaway D.L., Fell H.P., Ferree S., George R.D., Grogan T., James J.J., Maysuria M., Mitton J.D., Oliveri P., Osborn J.L., Peng T., Ratcliffe A.L., Webster P.J., Davidson E.H., Hood L., Dimitrov K. Direct multiplexed measurement of gene expression with color-coded probe pairs. Nat. Biotechnol 2008, 26:317-325.
22. Gupta N., Brown K.E., Milam A.H. Activated microglia in human retinitis pigmentosa, late-onset retinal degeneration, and age-related macular degeneration. Exp. Eye Res 2003, 76:463-471.
23. Harada T., Harada C., Kohsaka S., Wada E., Yoshida K., Ohno S., Mamada H., Tanaka K., Parada L.F., Wada K. Microglia-Müller glia cell interactions control neurotrophic factor production during light-induced retinal degeneration. J. Neurosci 2002, 22:9228-9236.
24. Holz F.G., Schütt F., Kopitz J., Eldred G.E., Kruse F.E., Völcker H.E., Cantz M. Inhibition of lysosomal degradative functions in RPE cells by a retinoid component of lipofuscin. Invest. Ophthalmol. Vis. Sci 1999, 40:737-743.
25. Hyman L., Neborsky R. Risk factors for age-related macular degeneration: an update. Curr. Opin. Ophthalmol 2002, 13:171-175.
26. Jager R.D., Mieler W.F., Miller J.W. Age-related macular degeneration. N Engl J. Med 2008, 358:2606-2617.
27. Johnson L.V., Forest D.L., Banna C.D., Radeke C.M., Maloney M.A., Hu J., Spencer C.N., Walker A.M., Tsie M.S., Bok D., Radeke M.J., Anderson D.H. Cell culture model that mimics drusen formation and triggers complement activation associated with age-related macular degeneration. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:18277-18282.
28. Johnson L.V., Leitner W.P., Staples M.K., Anderson D.H. Complement activation and inflammatory processes in Drusen formation and age related macular degeneration. Exp. Eye Res 2001, 73:887-896.
29. Jung S., Aliberti J., Graemmel P., Sunshine M.J., Kreutzberg G.W., Sher A., Littman D.R. Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol. Cell. Biol 2000, 20:4106-4114.
30. Kanda A., Abecasis G., Swaroop A. Inflammation in the pathogenesis of age-related macular degeneration. Br. J. Ophthalmol 2008, 92:448-450.
31. Karlstetter M., Ebert S., Langmann T. Microglia in the healthy and degenerating retina: insights from novel mouse models. Immunobiology 2010, 215:685-691.
32. Lamb L.E., Simon J.D. A2E: a component of ocular lipofuscin. Photochem. Photobiol 2004, 79:127-136.
33. Lei L., Tzekov R., Tang S., Kaushal S. Accumulation and autofluorescence of phagocytized rod outer segment material in macrophages and microglial cells. Mol. Vis 2012, 18:103-113.
34. Luhmann U.F., Robbie S., Munro P.M., Barker S.E., Duran Y., Luong V., Fitzke F.W., Bainbridge J.W., Ali R.R., MacLaren R.E. The drusenlike phenotype in aging Ccl2-knockout mice is caused by an accelerated accumulation of swollen autofluorescent subretinal macrophages. Invest. Ophthalmol. Vis. Sci 2009, 50:5934-5943.
35. Luo C., Chen M., Xu H. Complement gene expression and regulation in mouse retina and retinal pigment epithelium/choroid. Mol. Vis 2011, 17:1588-1597.
36. Ma K.N., Cashman S.M., Sweigard J.H., Kumar-Singh R. Decay accelerating factor (CD55)-mediated attenuation of complement: therapeutic implications for age-related macular degeneration. Invest. Ophthalmol. Vis. Sci 2010, 51:6776-6783.
37. Ma W., Zhao L., Fontainhas A.M., Fariss R.N., Wong W.T. Microglia in the mouse retina alter the structure and function of retinal pigmented epithelial cells: a potential cellular interaction relevant to AMD. PLoS One 2009, 4:e7945.
38. Madinier A., Bertrand N., Mossiat C., Prigent-Tessier A., Beley A., Marie C., Garnier P. Microglial involvement in neuroplastic changes following focal brain ischemia in rats. PLoS One 2009, 4:e8101.
39. Mantovani A., Sica A., Sozzani S., Allavena P., Vecchi A., Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 2004, 25:677-686.
40. Ng T.F., Streilein J.W. Light-induced migration of retinal microglia into the subretinal space. Invest. Ophthalmol. Vis. Sci 2001, 42:3301-3310.
41. Olah M., Biber K., Vinet J., Boddeke H.W. Microglia phenotype diversity. CNS Neurol. Disord. Drug Targets 2011, 10:108-118.
42. Omri S., Behar-Cohen F., de Kozak Y., Sennlaub F., Verissimo L.M., Jonet L., Savoldelli M., Omri B., Crisanti P. Microglia/macrophages migrate through retinal epithelium barrier by a transcellular route in diabetic retinopathy: role of PKCζ in the Goto Kakizaki rat model. Am. J. Pathol 2011, 179:942-953.
43. Parish C.A., Hashimoto M., Nakanishi K., Dillon J., Sparrow J. Isolation and one-step preparation of A2E and iso-A2E, fluorophores from human retinal pigment epithelium. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:14609-14613.
44. Park L.C., Zhang H., Gibson G.E. Co-culture with astrocytes or microglia protects metabolically impaired neurons. Mech. Ageing Dev 2001, 123:21-27.
45. Penfold P.L., Madigan M.C., Gillies M.C., Provis J.M. Immunological and aetiological aspects of macular degeneration. Prog. Retin. Eye Res 2001, 20:385-414.
46. Pumariega N.M., Smith R.T., Sohrab M.A., Letien V., Souied E.H. A prospective study of reticular macular disease. Ophthalmology 2011, 118:1619-1625.
47. Radu R.A., Hu J., Yuan Q., Welch D.L., Makshanoff J., Lloyd M., McMullen S., Travis G.H., Bok D. Complement system dysregulation and inflammation in the retinal pigment epithelium of a mouse model for Stargardt macular degeneration. J. Biol. Chem 2011, 286:18593-18601.
48. Ramo K., Cashman S.M., Kumar-Singh R. Evaluation of adenovirus-delivered human CD59 as a potential therapy for AMD in a model of human membrane attack complex formation on murine RPE. Invest. Ophthalmol. Vis. Sci 2008, 49:4126-4136.
49. Ransohoff R.M., Liu L., Cardona A.E. Chemokines and chemokine receptors: multipurpose players in neuroinflammation. Int. Rev. Neurobiol 2007, 82:187-204.
50. Raoul W., Auvynet C., Camelo S., Guillonneau X., Feumi C., Combadière C., Sennlaub F. CCL2/CCR2 and CX3CL1/CX3CR1 chemokine axes and their possible involvement in age-related macular degeneration. J. Neuroinflammation 2010, 7:87.
51. Raoul W., Keller N., Rodéro M., Behar-Cohen F., Sennlaub F., Combadière C. Role of the chemokine receptor CX3CR1 in the mobilization of phagocytic retinal microglial cells. J. Neuroimmunol 2008, 198:56-61.
52. Rudolf M., Malek G., Messinger J.D., Clark M.E., Wang L., Curcio C.A. Sub-retinal drusenoid deposits in human retina: organization and composition. Exp. Eye Res 2008, 87:402-408.
53. Rutar M., Natoli R., Kozulin P., Valter K., Gatenby P., Provis J.M. Analysis of complement expression in light-induced retinal degeneration: synthesis and deposition of C3 by microglia/macrophages is associated with focal photoreceptor degeneration. Invest. Ophthalmol. Vis. Sci 2011, 52:5347-5358.
54. Santos A.M., Calvente R., Tassi M., Carrasco M.C., Martín-Oliva D., Marín-Teva J.L., Navascués J., Cuadros M.A. Embryonic and postnatal development of microglial cells in the mouse retina. J. Comp. Neurol 2008, 506:224-239.
55. Schmitz-Valckenberg S., Alten F., Steinberg J.S., Jaffe G.J., Fleckenstein M., Mukesh B.N., Hohman T.C., Holz F.G. Reticular drusen associated with geographic atrophy in age-related macular degeneration. Invest. Ophthalmol. Vis. Sci 2011, 52:5009-5015. Geographic Atrophy Progression (G.A.P.) Study Group.
56. Scholl H.P., Charbel Issa P., Walier M., Janzer S., Pollok-Kopp B., Börncke F., Fritsche L.G., Chong N.V., Fimmers R., Wienker T., Holz F.G., Weber B.H., Oppermann M. Systemic complement activation in age-related macular degeneration. PLoS One 2008, 3:e2593.
57. Schütt F., Davies S., Kopitz J., Holz F.G., Boulton M.E. Photodamage to human RPE cells by A2-E, a retinoid component of lipofuscin. Invest. Ophthalmol. Vis. Sci 2000, 41:2303-2308.
58. Shamsi F.A., Boulton M. Inhibition of RPE lysosomal and antioxidant activity by the age pigment lipofuscin. Invest. Ophthalmol. Vis. Sci 2001, 42:3041-3046.
59. Sparrow J.R., Boulton M. RPE lipofuscin and its role in retinal pathobiology. Exp. Eye Res 2005, 80:595-606.
60. Sparrow J.R., Cai B. Blue light-induced apoptosis of A2E-containing RPE: involvement of caspase-3 and protection by Bcl-2. Invest. Ophthalmol. Vis. Sci 2001, 42:1356-1362.
61. Sparrow J.R., Nakanishi K., Parish C.A. The lipofuscin fluorophore A2E mediates blue light-induced damage to retinal pigmented epithelial cells. Invest. Ophthalmol. Vis. Sci 2000, 41:1981-1989.
62. Sparrow J.R., Parish C.A., Hashimoto M., Nakanishi K. A2E, a lipofuscin fluorophore, in human retinal pigmented epithelial cells in culture. Invest. Ophthalmol. Vis. Sci 1999, 40:2988-2995.
63. Sparrow J.R., Wu Y., Nagasaki T., Yoon K.D., Yamamoto K., Zhou J. Fundus autofluorescence and the bisretinoids of retina. Photochem. Photobiol. Sci 2010, 9:1480-1489.
64. Sparrow J.R., Zhou J., Ben-Shabat S., Vollmer H., Itagaki Y., Nakanishi K. Involvement of oxidative mechanisms in blue-light-induced damage to A2E-laden RPE. Invest. Ophthalmol. Vis. Sci 2002, 43:1222-1227.
65. Swaroop A., Chew E.Y., Rickman C.B., Abecasis G.R. Unraveling a multifactorial late-onset disease: from genetic susceptibility to disease mechanisms for age-related macular degeneration. Annu. Rev. Genomics Hum. Genet 2009, 10:19-43.
66. Toku K., Tanaka J., Yano H., Desaki J., Zhang B., Yang L., Ishihara K., Sakanaka M., Maeda N. Microglial cells prevent nitric oxide-induced neuronal apoptosis in vitro. J. Neurosci. Res 1998, 53:415-425.
67. Tuo J., Bojanowski C.M., Zhou M., Shen D., Ross R.J., Rosenberg K.I., Cameron D.J., Yin C., Kowalak J.A., Zhuang Z., Zhang K., Chan C.C. Murine ccl2/cx3cr1 deficiency results in retinal lesions mimicking human age-related macular degeneration. Invest. Ophthalmol. Vis. Sci 2007, 48:3827-3836.
68. Tuohy G., Millington-Ward S., Kenna P.F., Humphries P., Farrar G.J. Sensitivity of photoreceptor-derived cell line (661W) to baculoviral p35, Z-VADFMK, and Fas-associated death domain. Invest. Ophthalmol. Vis. Sci 2002, 43:3583-3589.
69. Vinet J., Weering H.R., Heinrich A., Kälin R.E., Wegner A., Brouwer N., Heppner F.L., Rooijen N.v., Boddeke H.W., Biber K. Neuroprotective function for ramified microglia in hippocampal excitotoxicity. J. Neuroinflammation 2012, 9:27.
70. von Bernhardi R., Tichauer J.E., Eugenín J. Aging-dependent changes of microglial cells and their relevance for neurodegenerative disorders. J. Neurochem 2010, 112:1099-1114.
71. Wang J., Ohno-Matsui K., Yoshida T., Shimada N., Ichinose S., Sato T., Mochizuki M., Morita I. Amyloid-beta up-regulates complement factor B in retinal pigment epithelial cells through cytokines released from recruited macrophages/microglia: another mechanism of complement activation in age-related macular degeneration. J. Cell. Physiol 2009, 220:119-128.
72. Wu Z., Lauer T.W., Sick A., Hackett S.F., Campochiaro P.A. Oxidative stress modulates complement factor H expression in retinal pigmented epithelial cells by acetylation of FOXO3. J. Biol. Chem 2007, 282:22414-22425.
73. Xu H., Chen M., Forrester J.V. Para-inflammation in the aging retina. Prog. Retin. Eye Res 2009, 28:348-368.
74. Xu H., Chen M., Manivannan A., Lois N., Forrester J.V. Age-dependent accumulation of lipofuscin in perivascular and subretinal microglia in experimental mice. Aging Cell 2008, 7:58-68.
75. Zarbin M.A., Rosenfeld P.J. Pathway-based therapies for age-related macular degeneration: an integrated survey of emerging treatment alternatives. Retina 2010, 30:1350-1367.
76. Zhao L., Wang Z., Liu Y., Song Y., Li Y., Laties A.M., Wen R. Translocation of the retinal pigment epithelium and formation of sub-retinal pigment epithelium deposit induced by subretinal deposit. Mol. Vis 2007, 13:873-880.
77. Zhou J., Jang Y.P., Kim S.R., Sparrow J.R. Complement activation by photooxidation products of A2E, a lipofuscin constituent of the retinal pigment epithelium. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:16182-16187.
78. Zhou J., Kim S.R., Westlund B.S., Sparrow J.R. Complement activation by bisretinoid constituents of RPE lipofuscin. Invest. Ophthalmol. Vis. Sci 2009, 50:1392-1399.
79. Zweifel S.A., Spaide R.F., Curcio C.A., Malek G., Imamura Y. Reticular pseudodrusen are subretinal drusenoid deposits. Ophthalmology 2010, 117:303-312. e301.