Brief Exposure to Damaging Light Causes Focal Recruitment of Macrophages, and Long-Term Destabilization of Photoreceptors in the Albino Rat Retina

REFERENCES

• Noell WK, Walker VS, Kang BS, Berman S. Retinal damage by light in rats. Invest Ophthalmol 1966;5:450–473.
   PubMedGoogle Scholar
• Abler AS, Chang CJ, Ful J, Tso MO, Lam TT. Photic injury triggers apoptosis of photoreceptor cells. Res Commun Mol Pathol Pharmacol 1996;92:177–189.
   PubMedGoogle Scholar
• Bowers F, Valter K, Chan S, et al. Effects of oxygen and bFGF on the vulnerability of photoreceptors to light damage. Invest Ophthalmol Vis Sci 2001;42:804–815.
   PubMed Web of Science ®Google Scholar
• Demontis GC, Longoni B, Marchiafava PL. Molecular steps involved in light-induced oxidative damage to retinal rods. Invest Ophthalmol Vis Sci 2002;43:2421–2427.
   PubMed Web of Science ®Google Scholar
• Wiegand RD, Giusto NM, Rapp LM, Anderson RE. Evidence for rod outer segment lipid peroxidation following constant illumination of the rat retina. Invest Ophthalmol Vis Sci 1983;24:1433–1435.
   PubMed Web of Science ®Google Scholar
• Chader GJ. Animal models in research on retinal degenerations: past progress and future hope. Vision Res 2002;42:393–399.
   PubMed Web of Science ®Google Scholar
• Noell WK. Possible mechanisms of photoreceptor damage by light in mammalian eyes. Vision Res 1980;20:1163–1171.
   PubMed Web of Science ®Google Scholar
• Rapp LM, Tolman BL, Koutz CA, Thum LA. Predisposing factors to light-induced photoreceptor cell damage: retinal changes in maturing rats. Exp Eye Res 1990;51:177–184.
   PubMed Web of Science ®Google Scholar
• Rapp LM, Smith SC. Morphologic comparisons between rhodopsin-mediated and short-wavelength classes of retinal light damage. Invest Ophthalmol Vis Sci 1992;33:3367–3377.
   PubMedGoogle Scholar
• Tanito M, Kaidzu S, Ohira A, Anderson RE. Topography of retinal damage in light-exposed albino rats. Exp Eye Res 2008;87:292–295.
   PubMed Web of Science ®Google Scholar
• Marco-Gomariz MA, Hurtado-Montalbán N, Vidal-Sanz M, Lund RD, Villegas-Pérez MP. Phototoxic-induced photoreceptor degeneration causes retinal ganglion cell degeneration in pigmented rats. J Comp Neurol 2006;498:163–179.
   PubMedGoogle Scholar
• Battelle BA, LaVail MM. Rhodopsin content and rod outer segment length in albino rat eyes: modification by dark adaptation. Exp Eye Res 1978;26:487–497.
   PubMed Web of Science ®Google Scholar
• Penn JS, Williams TP. Photostasis: regulation of daily photon-catch by rat retinas in response to various cyclic illuminances. Exp Eye Res 1986;43:915–928.
   PubMed Web of Science ®Google Scholar
• Rapp L, Naash M, Wiegand R, et al. Morphological and biochemical comparisons between retinal regions having differing susceptibility to photoreceptor degeneration. In: LaVail MM, Hollyfield JG, Anderson RE (eds), Retinal Degeneration: Experimental and Clinical Studies: Liss Alan R Inc, 1985, pp. 421–437.
   Google Scholar
• Fukuda Y. A three-group classification of rat retinal ganglion cells: histological and physiological studies. Brain Res 1977;327–344.
   PubMedGoogle Scholar
• Carpenter P, Sefton AJ, Dreher B, Lim WL. Role of target tissue in regulating the development of retinal ganglion cells in the albino rat: effects of kainate lesions in the superior colliculus. J Comp Neurol 1986;251:240–259.
   PubMedGoogle Scholar
• Kuwabara T. Retinal recovery from exposure to light. Am J Ophthalmol 1970;70:187–198.
   PubMed Web of Science ®Google Scholar
• Kuwabara T, Funahashi M. Light damage in the developing rat retina. Arch Ophthalmol 1976;94:1369–1374.
   PubMedGoogle Scholar
• Oraedu AC, Voaden MJ, Marshall J. Photochemical damage in the albino rat retina: morphological changes and endogenous amino acids. J Neurochem 1980;35:1361–1369.
   PubMedGoogle Scholar
• Hansson HR. A histochemical study of cellular reactions in the rat retina transiently damaged by visible light. Exp Eye Res 1971;12:270–274.
   PubMed Web of Science ®Google Scholar
• van Best JA, Putting BJ, Oosterhuis JA, Zweypfenning RC, Vrensen GF. Function and morphology of the retinal pigment epithelium after light-induced damage. Microsc Res Tech 1997;36:77–88.
   PubMedGoogle Scholar
• Maslim J, Valter K, Egensperger R, Holländer H, Stone J. Tissue oxygen during a critical developmental period controls the death and survival of photoreceptors. Invest Ophthalmol Vis Sci 1997;38:1667–1677.
   PubMed Web of Science ®Google Scholar
• Bringmann A, Pannicke T, Grosche J, et al. Mü,ller cells in the healthy and diseased retina. Prog Retin Eye Res 2006;25:397–424.
   PubMed Web of Science ®Google Scholar
• Chen L, Yang P, Kijlstra A. Distribution, markers, and functions of retinal microglia. Ocul Immunol Inflamm 2002;10:27–39.
   PubMed Web of Science ®Google Scholar
• Moriya M, Baker BN, Williams TP. Progression and reversibility of early light-induced alterations in rat retinal rods. Cell Tissue Res 1986;246:607–621.
   PubMed Web of Science ®Google Scholar
• Jozwick C, Valter K, Stone J. Reversal of functional loss in the P23H-3 rat retina by management of ambient light. Exp Eye Res 2006;83:1074–1080.
   PubMedGoogle Scholar
• Chrysostomou V, Stone J, Stowe S, Barnett NL, Valter K. The status of cones in the rhodopsin mutant P23H-3 retina: light-regulated damage and repair in parallel with rods. Invest Ophthalmol Vis Sci 2008;49:1116–1125.
   PubMedGoogle Scholar
• Rapp LM, Williams TP. Rhodopsin content and electroretinographic sensitivity in light-damaged rat retina. Nature 1977;267:835–836.
   PubMedGoogle Scholar
• Grimm C, Wenzel A, Hafezi F, et al. Protection of Rpe65-deficient mice identifies rhodopsin as a mediator of light-induced retinal degeneration. Nat Genet 2000;25:63–66.
   PubMed Web of Science ®Google Scholar
• Gordon WC, Casey DM, Lukiw WJ, Bazan NG. DNA damage and repair in light-induced photoreceptor degeneration. Invest Ophthalmol Vis Sci 2002;43:3511–3521.
   PubMedGoogle Scholar
• Ni YQ, Xu GZ, Hu WZ, et al. Neuroprotective effects of naloxone against light-induced photoreceptor degeneration through inhibiting retinal microglial activation. Invest Ophthalmol Vis Sci 2008;49:2589–2598.
   PubMed Web of Science ®Google Scholar
• Zhang C, Shen JK, Lam TT, et al. Activation of microglia and chemokines in light-induced retinal degeneration. Mol Vis 2005;11:887–895.
   PubMed Web of Science ®Google Scholar
• Zeng HY, Zhu XA, Zhang C, et al. Identification of sequential events and factors associated with microglial activation, migration, and cytotoxicity in retinal degeneration in rd mice. Invest Ophthalmol Vis Sci 2005;46:2992–2999.
   PubMed Web of Science ®Google Scholar
• Joly S, Francke M, Ulbricht E, et al. Cooperative phagocytes: resident microglia and bone marrow immigrants remove dead photoreceptors in retinal lesions. Am J Pathol 2009;174:2310–2323.
   PubMed Web of Science ®Google Scholar
• Roque RS, Rosales AA, Jingjing L, Agarwal N, Al-Ubaidi MR. Retina-derived microglial cells induce photoreceptor cell death in vitro. Brain Res 1999;836:110–119.
   PubMed Web of Science ®Google Scholar
• Marc RE, Jones BW, Watt CB, et al. Extreme retinal remodeling triggered by light damage: implications for age related macular degeneration. Mol Vis 2008;14:782–806.
   PubMed Web of Science ®Google Scholar
• Rowe MH, Dreher B. Functional morphology of beta cells in the area centralis of the cat’s retina: a model for the evolution of central retinal specializations. Brain Behav Evol 1982;21:1–23.
   PubMedGoogle Scholar
• Penfold PL, Madigan MC, Gillies MC, Provis JM. Immuno-logical and aetiological aspects of macular degeneration. Prog Retin Eye Res 2001;20:385–414.
   PubMed Web of Science ®Google Scholar
• Provis JM, Penfold PL, Cornish EE, Sandercoe TM, Madigan MC. Anatomy and development of the macula: specialisation and the vulnerability to macular degeneration. Clin Exp Optom 2005;88:269–281.
   PubMedGoogle Scholar
• Sarks JP, Sarks SH, Killingsworth MC. Evolution of geographic atrophy of the retinal pigment epithelium. Eye (Lond) 1988;2 (Pt 5):552–577.
   PubMedGoogle Scholar
• Penfold P, Killingsworth M, Sarks S. An ultrastructural study of the role of leucocytes and fibroblasts in the breakdown of Bruch’s membrane. Aust J Ophthalmol 1984;12:23–31.
   PubMedGoogle Scholar
• Penfold PL, Killingsworth MC, Sarks SH. Senile macular degeneration. The involvement of giant cells in atrophy of the retinal pigment epithelium. Invest Ophthalmol Vis Sci 1986;27:364–371.
   PubMed Web of Science ®Google Scholar
• Green WR. Histopathology of age-related macular degeneration. Mol Vis 1999;5:27.
   PubMed Web of Science ®Google Scholar
• Green WR, Enger C. Age-related macular degeneration histopathologic studies. The 1992 Lorenz E. Zimmerman Lecture. Ophthalmology 1993;100:1519–1535.
   PubMed Web of Science ®Google Scholar
• Wu KH, Madigan MC, Billson FA, Penfold PL. Differential expression of GFAP in early v late AMD: a quantitative analysis. Br J Ophthalmol 2003;87:1159–1166.
   PubMed Web of Science ®Google Scholar
• Grunwald JE, Hariprasad SM, DuPont J, et al. Foveolar choroidal blood flow in age-related macular degeneration. Invest Ophthalmol Vis Sci 1998;39:385–390.
   PubMed Web of Science ®Google Scholar
• Grunwald JE, Metelitsina TI, Dupont JC, Ying GS, Maguire MG. Reduced foveolar choroidal blood flow in eyes with increasing AMD severity. Invest Ophthalmol Vis Sci 2005;46: 1033–1038.
   PubMed Web of Science ®Google Scholar
• Ramrattan RS, van der Schaft TL, Mooy CM, et al. Morphometric analysis of Bruch’s membrane, the choriocapillaris, and the choroid in aging. Invest Ophthalmol Vis Sci 1994;35:2857–2864.
   PubMed Web of Science ®Google Scholar
• Sarks SH. Changes in the region of the choriocapillaries in aging and degeneration. Presented at the 23rd Concilium Ophthalmologicum, Kyoto, Japan. Excerpta Medica Amsterdam 1978;228–238.
   Google Scholar
• Sullivan R, Penfold P, Pow DV. Neuronal migration and glial remodeling in degenerating retinas of aged rats and in nonneovascular AMD. Invest Ophthalmol Vis Sci 2003;44:856–865.
   PubMed Web of Science ®Google Scholar
• Wong J, Madigan M, Billson F, Penfold P. Quantification of leukocyte common antigen (CD45) expression in macular degeneration. Invest Ophthalmol Vis Sci 2001;42:S227.
   Google Scholar
• Cousins SW, Espinosa-Heidmann DG, Csaky KG. Monocyte activation in patients with age-related macular degeneration: a biomarker of risk for choroidal neovascularization? Arch Ophthalmol 2004;122:1013–1018.
   PubMedGoogle Scholar
• Ezzat MK, Hann CR, Vuk-Pavlovic S, Pulido JS. Immune cells in the human choroid. Br J Ophthalmol 2008;92:976–980.
   PubMed Web of Science ®Google Scholar
• Cherepanoff S, McMenamin PG, Gillies MC, Kettle E, Sarks SH. Bruch’s membrane and choroidal macrophages in early and advanced age-related macular degeneration. Br J Ophthalmol.2009.
   PubMedGoogle Scholar
• Espinosa-Heidmann DG, Suner IJ, Hernandez EP, et al. Macrophage depletion diminishes lesion size and severity in experimental choroidal neovascularization. Invest Ophthalmol Vis Sci 2003;44:3586–3592.
   PubMed Web of Science ®Google Scholar
• Sakurai E, Anand A, Ambati BK, van Rooijen N, Ambati J. Macrophage depletion inhibits experimental choroidal neovascularization. Invest Ophthalmol Vis Sci 2003;44:3578–3585.
   PubMed Web of Science ®Google Scholar
• Combadière C, Feumi C, Raoul W, et al. CX3CR1-dependent subretinal microglia cell accumulation is associated with cardinal features of age-related macular degeneration. J Clin Invest 2007;117:2920–2928.
   PubMed Web of Science ®Google Scholar
• Dunaief JL, Dentchev T, Ying GS, Milam AH. The role of apoptosis in age-related macular degeneration. Arch Ophthalmol 2002;120:1435–1442.
   PubMedGoogle Scholar
• Sunness JS, Gonzalez-Baron J, Applegate CA, et al. Enlargement of atrophy and visual acuity loss in the geographic atrophy form of age-related macular degeneration. Ophthalmology 1999;106:1768–1779.
   PubMed Web of Science ®Google Scholar
• Shelley EJ, Madigan MC, Natoli R, Penfold PL, Provis JM. Cone degeneration in aging and age-related macular degeneration. Arch Ophthalmol 2009;127:483–492.
   PubMedGoogle Scholar
• Rex TS, Fariss RN, Lewis GP, et al. A survey of molecular expression by photoreceptors after experimental retinal detachment. Invest Ophthalmol Vis Sci 2002;43:1234–1247.
   PubMedGoogle Scholar
• Bonilha VL, Hollyfield JG, Grover S, Fishman GA. Abnormal distribution of red/green cone opsins in a patient with an autosomal dominant cone dystrophy. Ophthalmic Genet 2005;26:69–76.
   PubMedGoogle Scholar
• John SK, Smith JE, Aguirre GD, Milam AH. Loss of cone molecular markers in rhodopsin-mutant human retinas with retinitis pigmentosa. Mol Vis 2000;6:204–215.
   PubMed Web of Science ®Google Scholar
• Hageman GS, Luthert PJ, Victor Chong NH, et al. An integrated hypothesis that considers drusen as biomarkers of immune-mediated processes at the RPE-Bruch’s membrane interface in aging and age-related macular degeneration. Prog Retin Eye Res 2001;20:705–732.
   PubMed Web of Science ®Google Scholar
• Anderson DH, Mullins RF, Hageman GS, Johnson LV. A role for local inflammation in the formation of drusen in the aging eye. Am J Ophthalmol 2002;134:411–431.
   PubMed Web of Science ®Google Scholar
• Nozaki M, Raisler BJ, Sakurai E, et al. Drusen complement components C3a and C5a promote choroidal neovascularization. Proc Natl Acad Sci USA 2006;103:2328–2333.
   PubMed Web of Science ®Google Scholar
• Taylor HR, Muñoz B, West S, et al. Visible light and risk of age-related macular degeneration. Trans Am Ophthalmol Soc 1990;88:163–73; discussion 173.
   PubMedGoogle Scholar
• Taylor HR, West S, Muñoz B, et al. The long-term effects of visible light on the eye. Arch Ophthalmol 1992;110:99–104.
   PubMed Web of Science ®Google Scholar
• Fletcher AE, Bentham GC, Agnew M, et al. Sunlight exposure, antioxidants, and age-related macular degeneration. Arch Ophthalmol 2008;126:1396–1403.
   PubMedGoogle Scholar
• Cruickshanks KJ, Klein R, Klein BE, Nondahl DM. Sunlight and the 5-year incidence of early age-related maculopathy: the beaver dam eye study. Arch Ophthalmol 2001;119:246–250.
   PubMedGoogle Scholar
• Tomany SC, Cruickshanks KJ, Klein R, Klein BE, Knudtson MD. Sunlight and the 10-year incidence of age-related maculopathy: the Beaver Dam Eye Study. Arch Ophthalmol 2004;122:750–757.
   PubMed Web of Science ®Google Scholar
• Mitchell P, Smith W, Wang JJ. Iris color, skin sun sensitivity, and age-related maculopathy. The Blue Mountains Eye Study. Ophthalmology 1998;105:1359–1363.
   PubMed Web of Science ®Google Scholar
• Young RW. Solar radiation and age-related macular degeneration. Surv Ophthalmol 1988;32:252–269.
   PubMed Web of Science ®Google Scholar
• Delcourt C, Carrière I, Ponton-Sanchez A, et al. POLA Study Group. Light exposure and the risk of age-related macular degeneration: the Pathologies Oculaires Liées à l’Age (POLA) study. Arch Ophthalmol 2001;119:1463–1468.
   PubMedGoogle Scholar
• Khan JC, Shahid H, Thurlby DA, et al. Genetic Factors in AMD Study. Age related macular degeneration and sun exposure, iris colour, and skin sensitivity to sunlight. Br J Ophthalmol 2006;90:29–32.
   PubMed Web of Science ®Google Scholar
• West SK, Rosenthal FS, Bressler NM, et al. Exposure to sunlight and other risk factors for age-related macular degeneration. Arch Ophthalmol 1989;107:875–879.
   PubMed Web of Science ®Google Scholar
• Hirakawa M, Tanaka M, Tanaka Y, et al. Age-related maculopathy and sunlight exposure evaluated by objective measurement. Br J Ophthalmol 2008;92:630–634.
   PubMedGoogle Scholar
• Klein R. Epidemiology of Age-related macular degeneration. In: Penfold P, Provis J (eds), Macular Degeneration. Berlin: Springer-Verlag, 2005.
   Google Scholar
• Organisciak DT, Darrow RM, Jiang YL, Blanks JC. Retinal light damage in rats with altered levels of rod outer segment docosahexaenoate. Invest Ophthalmol Vis Sci 1996;37:2243–2257.
   PubMed Web of Science ®Google Scholar
• Beatty S, Koh H, Phil M, Henson D, Boulton M. The role of oxidative stress in the pathogenesis of age-related macular degeneration. Surv Ophthalmol 2000;45:115–134.
   PubMed Web of Science ®Google Scholar
• Winkler BS, Boulton ME, Gottsch JD, Sternberg P. Oxidative damage and age-related macular degeneration. Mol Vis 1999;5:32.
   PubMed Web of Science ®Google Scholar
• Crabb JW, Miyagi M, Gu X, et al. Drusen proteome analysis: an approach to the etiology of age-related macular degeneration. Proc Natl Acad Sci USA 2002;99:14682–14687.
   PubMed Web of Science ®Google Scholar
• Gu X, Meer SG, Miyagi M, et al. Carboxyethylpyrrole protein adducts and autoantibodies, biomarkers for age-related macular degeneration. J Biol Chem 2003;278:42027–42035.
   PubMed Web of Science ®Google Scholar
• Gu J, Pauer GJ, Yue X, et al. Clinical Genomic and Proteomic AMD Study Group. Assessing susceptibility to age-related macular degeneration with proteomic and genomic biomarkers. Mol Cell Proteomics 2009;8:1338–1349.
   PubMed Web of Science ®Google Scholar
• Hollyfield JG, Bonilha VL, Rayborn ME, et al. Oxidative damage-induced inflammation initiates age-related macular degeneration. Nat Med 2008;14:194–198.
   PubMed Web of Science ®Google Scholar