Melanization and phagocytosis: Implications for age related macular degeneration

Molecular Vision

Volumn 11, Issue , 2005, Pages 482-490

  Sarangarajan, Rangaprasad ^a   Apte, Shireesh P ^b,c  

^a MASSACHUSETTS COLLEGE OF PHARMACY AND HEALTH SCIENCES   (United States)

^b Baxter IV Systems   (United States)

^c NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE A2 RECEPTOR; ANGIOGENESIS INHIBITOR; APOLIPOPROTEIN E; APOLIPOPROTEIN E4; BASIC FIBROBLAST GROWTH FACTOR; CYCLIC AMP; CYTOSKELETON PROTEIN; FIBROBLAST GROWTH FACTOR 2; INTEGRIN ANTAGONIST; ISOTRETINOIN; LIPOFUSCIN; MELANIN; NEW DRUG; NITRIC OXIDE; OXYGEN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHODIESTERASE INHIBITOR; PHOSPHODIESTERASE V INHIBITOR; PROTEIN KINASE C; UNCLASSIFIED DRUG; VACCINE; VITRONECTIN RECEPTOR ANTIBODY;

BIOACCUMULATION; CLINICAL TRIAL; DEGRADATION; DISEASE COURSE; DOWN REGULATION; HUMAN; ISOMERIZATION; LIGHT INTENSITY; METABOLISM; MICROVILLUS; MODULATION; OXYGEN CONSUMPTION; PHAGOCYTOSIS; PHOTORECEPTOR; PIGMENT EPITHELIUM; PRIORITY JOURNAL; RETINA MACULA AGE RELATED DEGENERATION; RETINA ROD OUTER SEGMENT; REVIEW; SIGNAL TRANSDUCTION; UPREGULATION; ZETA POTENTIAL;

ANIMALS; HUMANS; MACULAR DEGENERATION; MELANINS; OXYGEN CONSUMPTION; PHAGOCYTOSIS; PIGMENT EPITHELIUM OF EYE; ROD OUTER SEGMENTS; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 26244461245     PISSN: 10900535     EISSN: 10900535     Source Type: Journal    
DOI: None     Document Type: Review

References (140)

1. Boyle D, Tien LF, Cooper NG, Shepherd V, McLaughlin BJ. A mannose receptor is involved in retinal phagocytosis. Invest Ophthalmol Vis Sci 1991; 32:1464-70.
2. Ryeom SW, Sparrow JR, Silverstein RL. CD36 participates in the phagocytosis of rod outer segments by retinal pigment epithelium. J Cell Sci 1996; 109:387-95.
3. Nguyen-Legros J, Hicks D. Renewal of photoreceptor outer segments and their phagocytosis by the retinal pigment epithelium. Int Rev Cytol 2000; 196:245-313.
4. D'Cruz PM, Yasumura D, Weir J, Matthes MT, Abderrahim H, LaVail MM, Vollrath D. Mutation of the receptor tyrosine kinase gene Mertk in the retinal dystrophic RCS rat. Hum Mol Genet 2000; 9:645-51.
5. Chaitin MH, Hall MO. The distribution of actin in cultured normal and dystrophic rat pigment epithelial cells during the phagocytosis of rod outer segments. Invest Ophthalmol Vis Sci 1983; 24:821-31.
6. Chowers I, Kim Y, Farkas RH, Gunatilaka TL, Hackam AS, Campochiaro PA, Finnemann SC, Zack DJ. Changes in retinal pigment epithelial gene expression induced by rod outer segment uptake. Invest Ophthalmol Vis Sci 2004; 45:2098-106.
7. Bosch E, Horwitz J, Bok D. Phagocytosis of outer segments by retinal pigment epithelium: phagosome-lysosome interaction. J Histochem Cytochem 1993; 41:253-63.
8. Gal A, Li Y, Thompson DA, Weir J, Orth U, Jacobson SG, Apfelstedt-Sylla E, Vollrath D. Mutations in MERTK, the human orthologue of the RCS rat retinal dystrophy gene, cause retinitis pigmentosa. Nat Genet 2000; 26:270-1.
9. Vollrath D, Feng W, Duncan JL, Yasumura D, D'Cruz PM, Chappelow A, Matthes MT, Kay MA, LaVail MM. Correction of the retinal dystrophy phenotype of the RCS rat by viral gene transfer of Mertk. Proc Natl Acad Sci U S A 2001; 98:12584-9.
10. Sun H, Nathans J. The challenge of macular degeneration. Sci Am 2001; 285:68-75.
11. Finnemann SC, Leung LW, Rodriguez-Boulan E. The lipofuscin component A2E selectively inhibits phagolysosomal degradation of photoreceptor phospholipid by the retinal pigment epithelium. Proc Natl Acad Sci U S A 2002; 99:3842-7.
12. Becquet F, Goureau O, Soubrane G, Coscas G, Courtois Y, Hicks D. Superoxide inhibits proliferation and phagocytic internalization of photoreceptor outer segments by bovine retinal pigment epithelium in vitro. Exp Cell Res 1994; 212:374-82.
13. Wihlmark U, Wrigstad A, Roberg K, Brunk UT, Nilsson SE. Formation of lipofuscin in cultured retinal pigment epithelial cells exposed to pre-oxidized photoreceptor outer segments. APMIS 1996; 104:272-9.
14. Hoppe G, Marmorstein AD, Pennock EA, Hoff HF. Oxidized low density lipoprotein-induced inhibition of processing of photoreceptor outer segments by RPE. Invest Ophthalmol Vis Sci 2001; 42:2714-20.
15. Zarbin MA. Age-related macular degeneration: review of pathogenesis. Eur J Ophthalmol 1998; 8:199-206.
16. Bird A. Age-related macular disease. Br J Ophthalmol 1996; 80:2-3.
17. Curcio CA, Owsley C, Jackson GR. Spare the rods, save the cones in aging and age-related maculopathy. Invest Ophthalmol Vis Sci 2000; 41:2015-8.
18. Curcio CA, Millican CL, Allen KA, Kalina RE. Aging of the human photoreceptor mosaic: evidence for selective vulnerability of rods in central retina. Invest Ophthalmol Vis Sci 1993; 34:3278-96.
19. Wing GL, Blanchard GC, Weiter JJ. The topography and age relationship of lipofuscin concentration in the retinal pigment epithelium. Invest Ophthalmol Vis Sci 1978; 17:601-7.
20. Bird AC. What is the future of research in age-related macular disease? Arch Ophthalmol 1997; 115:1311-3.
21. Kennedy CJ, Rakoczy PE, Robertson TA, Papadimitriou JM, Constable IJ. Kinetic studies on phagocytosis and lysosomal digestion of rod outer segments by human retinal pigment epithelial cells in vitro. Exp Cell Res 1994; 210:209-14.
22. Rakoczy P, Constable IJ. Pathogenesis of macular degeneration: is there any progress? Aust N Z J Ophthalmol 1998; 26:67-70.
23. Rakoczy PE, Lai CM, Baines M, Di Grandi S, Fitton JH, Constable IJ. Modulation of cathepsin D activity in retinal pigment epithelial cells. Biochem J 1997; 324:935-40.
24. Deguchi J, Yamamoto A, Yoshimori T, Sugasawa K, Moriyama Y, Futai M, Suzuki T, Kato K, Uyama M, Tashiro Y. Acidification of phagosomes and degradation of rod outer segments in rat retinal pigment epithelium. Invest Ophthalmol Vis Sci 1994; 35:568-79.
25. Mousavi SA, Kjeken R, Berg TO, Seglen PO, Berg T, Brech A. Effects of inhibitors of the vacuolar proton pump on hepatic heterophagy and autophagy. Biochim Biophys Acta 2001; 1510:243-57.
26. Schutt F, Davies S, Kopitz J, Holz FG, Boulton ME. Photodamage to human RPE cells by A2-E, a retinoid component of lipofuscin. Invest Ophthalmol Vis Sci 2000; 41:2303-8.
27. Sundelin S, Wihlmark U, Nilsson SE, Brunk UT. Lipofuscin accumulation in cultured retinal pigment epithelial cells reduces their phagocytic capacity. Curr Eye Res 1998; 17:851-7.
28. Manga P, Orlow SJ. Inverse correlation between pink-eyed dilution protein expression and induction of melanogenesis by bafilomycin A1. Pigment Cell Res 2001; 14:362-7.
29. Ancans J, Tobin DJ, Hoogduijn MJ, Smit NP, Wakamatsu K, Thody AJ. Melanosomal pH controls rate of melanogenesis, eumelanin/phaeomelanin ratio and melanosome maturation in melanocytes and melanoma cells. Exp Cell Res 2001; 268:26-35.
30. Fuller BB, Spaulding DT, Smith DR. Regulation of the catalytic activity of preexisting tyrosinase in black and Caucasian human melanocyte cell cultures. Exp Cell Res 2001; 262:197-208.
31. Crabb JW, Miyagi M, Gu X, Shadrach K, West KA, Sakaguchi H, Kamei M, Hasan A, Yan L, Rayborn ME, Salomon RG, Hollyfield JG. Drusen proteome analysis: an approach to the etiology of age-related macular degeneration. Proc Natl Acad Sci U S A 2002; 99:14682-7.
32. Winkler BS, Boulton ME, Gottsch JD, Sternberg P. Oxidative damage and age-related macular degeneration. Mol Vis 1999; 5:32.
33. Cai J, Nelson KC, Wu M, Sternberg P Jr, Jones DP. Oxidative damage and protection of the RPE. Prog Retin Eye Res 2000; 19:205-21.
34. Liang FQ, Godley BF. Oxidative stress-induced mitochondrial DNA damage in human retinal pigment epithelial cells: a possible mechanism for RPE aging and age-related macular degeneration. Exp Eye Res 2003; 76:397-403.
35. Korytowski W, Sarna T, Zar ba M. Antioxidant action of neuromelanin: the mechanism of inhibitory effect on lipid peroxidation. Arch Biochem Biophys 1995; 319:142-8.
36. Zareba M, Bober A, Korytowski W, Zecca L, Sarna T. The effect of a synthetic neuromelanin on yield of free hydroxyl radicals generated in model systems. Biochim Biophys Acta 1995; 1271:343-8.
37. Sealy RC, Sarna T, Wanner EJ, Reszka K. Photosensitization of melanin: an electron spin resonance study of sensitized radical production and oxygen consumption. Photochem Photobiol 1984; 40:453-9.
38. Sarna T, Menon IA, Sealy RC. Photosensitization of melanins: a comparative study. Photochem Photobiol 1985; 42:529-32.
39. Sarna T, Pilas B, Land EJ, Truscott TG. Interaction of radicals from water radiolysis with melanin. Biochim Biophys Acta 1986; 883:162-7.
40. Geremia E, Corsaro C, Bonomo R, Giardinelli R, Pappalardo P, Vanella A, Sichel G. Eumelanins as free radical trap and superoxide dismutase activity in Amphibia. Comp Biochem Physiol B 1984; 79:67-9.
41. Korytowski W, Kalyanaraman B, Menon IA, Sarna T, Sealy RC. Reaction of superoxide anions with melanins: electron spin resonance and spin trapping studies. Biochim Biophys Acta 1986; 882:145-53.
42. Diment S, Eidelman M, Rodriguez GM, Orlow SJ. Lysosomal hydrolases are present in melanosomes and are elevated in melanizing cells. J Biol Chem 1995; 270:4213-5.
43. Stepien K, Wilczok A, Zajdel A, Dzierzega-Lecznar A, Wilczok T. Peroxynitrite mediated linoleic acid oxidation and tyrosine nitration in the presence of synthetic neuromelanins. Acta Biochim Pol 2000; 47:931-40.
44. Crabb JW, O'Neil J, Miyagi M, West K, Hoff HF. Hydroxynonenal inactivates cathepsin B by forming Michael adducts with active site residues. Protein Sci 2002; 11:831-40.
45. Sarna T, Rozanowska M, Zareba M, Wielgus A. Mechanisms of melanin photoprotection: inhibition of lipid peroxidation by ocular melanin. 9th Congress of the European Society for Photobiology; 2001 Sep 3-8; Lillehammer, Norway.
46. Kayatz P, Esser P, Peters S, Schraermeyer U. Ultrastructural localization of lipid peroxides in the choroid of the albino mouse. 96th Deutsche Ophthalmologische Gesellschaft Annual Meeting; 1998 Sep 19-22; Berlin, Germany.
47. Radu RA, Mata NL, Bagla A, Travis GH. Light exposure stimulates formation of A2E oxiranes in a mouse model of Stargardt's macular degeneration. Proc Natl Acad Sci U S A 2004; 101:5928-33.
48. Schutt F, Bergmann M, Kopitz J, Holz FG. [Mechanism of the inhibition of lysosomal functions in the retinal pigment epithelium by lipofuscin retinoid component A2-E]. Ophthalmologe 2001; 98:721-4.
49. Bergmann M, Schutt F, Holz FG, Kopitz J. Inhibition of the ATPdriven proton pump in RPE lysosomes by the major lipofuscin fluorophore A2-E may contribute to the pathogenesis of agerelated macular degeneration. FASEB J 2004; 18:562-4.
50. Akeo K, Hiramitsu T, Yorifuji H, Okisaka S. Membranes of retinal pigment epithelial cells in vitro are damaged in the phagocytotic process of the photoreceptor outer segment discs peroxidized by ferrous ions. Pigment Cell Res 2002; 15:341-7.
51. Hahn P, Milam AH, Dunaief JL. Maculas affected by age-related macular degeneration contain increased chelatable iron in the retinal pigment epithelium and Bruch's membrane. Arch Ophthalmol 2003; 121:1099-105.
52. Sundelin SP, Nilsson SE, Brunk UT. Lipofuscin-formation in cultured retinal pigment epithelial cells is related to their melanin content. Free Radic Biol Med 2001; 30:74-81.
53. Naash MI, Ripps H, Li S, Goto Y, Peachey NS. Polygenic disease and retinitis pigmentosa: albinism exacerbates photoreceptor degeneration induced by the expression of a mutant opsin in transgenic mice. J Neurosci 1996; 16:7853-8.
54. Dorey CK, Wu G, Ebenstein D, Garsd A, Weiter JJ. Cell loss in the aging retina. Relationship to lipofuscin accumulation and macular degeneration. Invest Ophthalmol Vis Sci 1989; 30:1691-9.
55. Rossi AG, McCutcheon JC, Roy N, Chilvers ER, Haslett C, Dransfield I. Regulation of macrophage phagocytosis of apoptotic cells by cAMP. J Immunol 1998; 160:3562-8.
56. Eckmiller MS, Burnside B. Light-induced photoreceptor shedding in teleost retina blocked by dibutyryl cyclic AMP. Invest Ophthalmol Vis Sci 1983; 24:1328-32.
57. Gregory CY, Abrams TA, Hall MO. Stimulation of A2 adenosine receptors inhibits the ingestion of photoreceptor outer segments by retinal pigment epithelium. Invest Ophthalmol Vis Sci 1994; 35:819-25.
58. Hall MO, Abrams TA, Mittag TW. ROS ingestion by RPE cells is turned off by increased protein kinase C activity and by increased calcium. Exp Eye Res 1991; 52:591-8.
59. Hu DN, McCormick SA, Orlow SJ, Rosemblat S, Lin AY. Regulation of melanogenesis by human uveal melanocytes in vitro. Exp Eye Res 1997; 64:397-404.
60. Karlsson AM, Lerner MR, Unett D, Lundstrom I, Svensson SP. Melatonin-induced organelle movement in melanophores is coupled to tyrosine phosphorylation of a high molecular weight protein. Cell Signal 2000; 12:469-74.
61. Ikemoto A, Fukuma A, Fujii Y, Okuyama H. Lysosomal enzyme activities are decreased in the retina and their circadian rhythms are different from those in the pineal gland of rats fed an alphalinolenic acid-restricted diet. J Nutr 2000; 130:3059-62.
62. Fliesler SJ, Anderson RE. Chemistry and metabolism of lipids in the vertebrate retina. Prog Lipid Res 1983; 22:79-131.
63. Baker BN, Moriya M, Maude MB, Anderson RE, Williams TP. Oil droplets of the retinal epithelium of the rat. Exp Eye Res 1986; 42:547-57.
64. Gazzah N, Gharib A, Delton I, Moliere P, Durand G, Christon R, Lagarde M, Sarda N. Effect of an n-3 fatty acid-deficient diet on the adenosine-dependent melatonin release in cultured rat pineal. J Neurochem 1993; 61:1057-63.
65. Bush RA, Malnoe A, Reme CE, Williams TP. Dietary deficiency of N-3 fatty acids alters rhodopsin content and function in the rat retina. Invest Ophthalmol Vis Sci 1994; 35:91-100.
66. Reilein AR, Tint IS, Peunova NI, Enikolopov GN, Gelfand VI. Regulation of organelle movement in melanophores by protein kinase A (PKA), protein kinase C (PKC), and protein phosphatase 2A (PP2A). J Cell Biol 1998; 142:803-13.
67. Miceli MV, Newsome DA. Effects of extracellular matrix and Bruch's membrane on retinal outer segment phagocytosis by cultured human retinal pigment epithelium. Curr Eye Res 1996; 15:17-26. Erratum in: Curr Eye Res 1996; 15:804-5.
68. Nir I, Harrison JM, Haque R, Low MJ, Grandy DK, Rubinstein M, Iuvone PM. Dysfunctional light-evoked regulation of cAMP in photoreceptors and abnormal retinal adaptation in mice lacking dopamine D4 receptors. J Neurosci 2002; 22:2063-73.
69. Edwards RB, Bakshian S. Phagocytosis of outer segments by cultured rat pigment epithelium. Reduction by cyclic AMP and phosphodiesterase inhibitors. Invest Ophthalmol Vis Sci 1980; 19:1184-8.
70. Zhao MW, Jin ML, He S, Spee C, Ryan SJ, Hinton DR. A distinct integrin-mediated phagocytic pathway for extracellular matrix remodeling by RPE cells. Invest Ophthalmol Vis Sci 1999; 40:2713-23.
71. Guo X, Ghalayini AJ, Chen H, Anderson RE. Phosphatidylinositol 3-kinase in bovine photoreceptor rod outer segments. Invest Ophthalmol Vis Sci 1997; 38:1873-82.
72. King-Smith C, Chen P, Garcia D, Rey H, Burnside B. Calciumindependent regulation of pigment granule aggregation and dispersion in teleost retinal pigment epithelial cells. J Cell Sci 1996; 109:33-43.
73. Murray RL, Dubin MW. The occurrence of actinlike filaments in association with migrating pigment granules in frog retinal pigment epithelium. J Cell Biol 1975; 64:705-10.
74. Kim IT, Choi JB. Melanosomes of retinal pigment epithelium-distribution, shape, and acid phosphatase activity. Korean J Ophthalmol 1998; 12:85-91.
75. Greenberg S, Chang P, Wang DC, Xavier R, Seed B. Clustered syk tyrosine kinase domains trigger phagocytosis. Proc Natl Acad Sci U S A 1996; 93:1103-7.
76. Cox D, Berg JS, Cammer M, Chinegwundoh JO, Dale BM, Cheney RE, Greenberg S. Myosin X is a downstream effector of PI(3)K during phagocytosis. Nat Cell Biol 2002; 4:469-77.
77. Busca R, Bertolotto C, Ortonne JP, Ballotti R. Inhibition of the phosphatidylinositol 3-kinase/p70(S6)-kinase pathway induces B16 melanoma cell differentiation. J Biol Chem 1996; 271:31824-30.
78. Tsatmali M, Ancans J, Thody AJ. Melanocyte function and its control by melanocortin peptides. J Histochem Cytochem 2002; 50:125-33.
79. Romero-Graillet C, Aberdam E, Biagoli N, Massabni W, Ortonne JP, Ballotti R. Ultraviolet B radiation acts through the nitric oxide and cGMP signal transduction pathway to stimulate melanogenesis in human melanocytes. J Biol Chem 1996; 271:28052-6.
80. Nilsson HM, Karlsson AM, Loitto VM, Svensson SP, Sundqvist T. Nitric oxide modulates intracellular translocation of pigment organelles in Xenopus laevis melanophores. Cell Motil Cytoskeleton 2000; 47:209-18.
81. Wang F, Nobes CD, Hall A, Spiegel S. Sphingosine 1-phosphate stimulates rho-mediated tyrosine phosphorylation of focal adhesion kinase and paxillin in Swiss 3T3 fibroblasts. Biochem J 1997; 324:481-8.
82. Busca R, Bertolotto C, Abbe P, Englaro W, Ishizaki T, Narumiya S, Boquet P, Ortonne JP, Ballotti R. Inhibition of Rho is required for cAMP-induced melanoma cell differentiation. Mol Biol Cell 1998; 9:1367-78.
83. Finnemann SC. Focal adhesion kinase signaling promotes phagocytosis of integrin-bound photoreceptors. EMBO J 2003; 22:4143-54.
84. Zhu N, Eves PC, Katerinaki E, Szabo M, Morandini R, Ghanem G, Lorigan P, MacNeil S, Haycock JW. Melanoma cell attachment, invasion, and integrin expression is upregulated by tumor necrosis factor alpha and suppressed by alpha melanocyte stimulating hormone. J Invest Dermatol 2002; 119:1165-71.
85. Klaver CC, Kliffen M, van Duijn CM, Hofman A, Cruts M, Grobbee DE, van Broeckhoven C, de Jong PT. Genetic association of apolipoprotein E with age-related macular degeneration. Am J Hum Genet 1998; 63:200-6. Erratum in: Am J Hum Genet 1998; 63:1252.
86. Simonelli F, Margaglione M, Testa F, Cappucci G, Manitto MP, Brancato R, Rinaldi E. Apolipoprotein E polymorphisms in agerelated macular degeneration in an Italian population. Ophthalmic Res 2001; 33:325-8.
87. Corder EH, Saunders AM, Strittmatter WJ, Schmechel DE, Gaskell PC, Small GW, Roses AD, Haines JL, Pericak-Vance MA. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 1993; 261:921-3.
88. Dithmar S, Curcio CA, Le NA, Brown S, Grossniklaus HE. Ultrastructural changes in Bruch's membrane of apolipoprotein E-deficient mice. Invest Ophthalmol Vis Sci 2000; 41:2035-42.
89. Ong JM, Zorapapel NC, Rich KA, Wagstaff RE, Lambert RW, Rosenberg SE, Moghaddas F, Pirouzmanesh A, Aoki AM, Kenney MC. Effects of cholesterol and apolipoprotein E on retinal abnormalities in ApoE-deficient mice. Invest Ophthalmol Vis Sci 2001; 42:1891-900.
90. Ohkubo N, Mitsuda N, Tamatani M, Yamaguchi A, Lee YD, Ogihara T, Vitek MP, Tohyama M. Apolipoprotein E4 stimulates cAMP response element-binding protein transcriptional activity through the extracellular signal-regulated kinase pathway. J Biol Chem 2001; 276:3046-53.
91. Nosanchuk JD, Casadevall A. Cellular charge of Cryptococcus neoformans: contributions from the capsular polysaccharide, melanin, and monoclonal antibody binding. Infect Immun 1997; 65:1836-41.
92. Casadevall A, Rosas AL, Nosanchuk JD. Melanin and virulence in Cryptococcus neoformans. Curr Opin Microbiol 2000; 3:354-8.
93. Nosanchuk JD, Cleare W, Franzot SP, Casadevall A. Amphotericin B and fluconazole affect cellular charge, macrophage phagocytosis, and cellular morphology of Cryptococcus neoformans at subinhibitory concentrations. Antimicrob Agents Chemother 1999; 43:233-9.
94. Ryeom SW, Silverstein RL, Scotto A, Sparrow JR. Binding of anionic phospholipids to retinal pigment epithelium may be mediated by the scavenger receptor CD36. J Biol Chem 1996; 271:20536-9.
95. Futter CE, Ramalho JS, Jaissle GB, Seeliger MW, Seabra MC. The role of Rab27a in the regulation of melanosome distribution within retinal pigment epithelial cells. Mol Biol Cell 2004; 15:2264-75.
96. Gollapalli DR, Rando RR. The specific binding of retinoic acid to RPE65 and approaches to the treatment of macular degeneration. Proc Natl Acad Sci U S A 2004; 101:10030-5.
97. Katz ML, Redmond TM. Effect of Rpe65 knockout on accumulation of lipofuscin fluorophores in the retinal pigment epithelium. Invest Ophthalmol Vis Sci 2001; 42:3023-30.
98. Sieving PA, Chaudhry P, Kondo M, Provenzano M, Wu D, Carlson TJ, Bush RA, Thompson DA. Inhibition of the visual cycle in vivo by 13-cis retinoic acid protects from light damage and provides a mechanism for night blindness in isotretinoin therapy. Proc Natl Acad Sci U S A 2001; 98:1835-40.
99. Radu RA, Mata NL, Nusinowitz S, Liu X, Sieving PA, Travis GH. Treatment with isotretinoin inhibits lipofuscin accumulation in a mouse model of recessive Stargardt's macular degeneration. Proc Natl Acad Sci U S A 2003; 100:4742-7.
100. Sparrow JR. Therapy for macular degeneration: insights from acne. Proc Natl Acad Sci U S A 2003; 100:4353-4.
101. Baehr W, Wu SM, Bird AC, Palczewski K. The retinoid cycle and retina disease. Vision Res 2003; 43:2957-8.
102. Imokawa G, Yada Y, Kimura M. Signalling mechanisms of endothelin-induced mitogenesis and melanogenesis in human melanocytes. Biochem J 1996; 314:305-12.
103. Manfioletti G, Brancolini C, Avanzi G, Schneider C. The protein encoded by a growth arrest-specific gene (gas6) is a new member of the vitamin K-dependent proteins related to protein S, a negative coregulator in the blood coagulation cascade. Mol Cell Biol 1993; 13:4976-85.
104. Hall MO, Prieto AL, Obin MS, Abrams TA, Burgess BL, Heeb MJ, Agnew BJ. Outer segment phagocytosis by cultured retinal pigment epithelial cells requires Gas6. Exp Eye Res 2001; 73:509-20.
105. Hall MO, Obin MS, Prieto AL, Burgess BL, Abrams TA. Gas6 binding to photoreceptor outer segments requires gammacarboxyglutamic acid (Gla) and Ca(2+) and is required for OS phagocytosis by RPE cells in vitro. Exp Eye Res 2002; 75:391-400.
106. Drager UC. Calcium binding in pigmented and albino eyes. Proc Natl Acad Sci U S A 1985; 82:6716-20.
107. Lavallee CR, Chalifoux JR, Moosally AJ, Balkema GW. Elevated free calcium levels in the subretinal space elevate the absolute dark-adapted threshold in hypopigmented mice. J Neurophysiol 2003; 90:3654-62.
108. Dorey CK, Staurenghi G, Delori FC. Lipofuscin in aged and AMD eyes. In: Hollyfield JG, Anderson RE, LaVail MM, editors. Retinal Degeneration: clinical and laboratory applications. New York: Plenum Press; 1993. pp. 3-14.
109. Weiter JJ, Delori FC, Wing GL, Fitch KA. Retinal pigment epithelial lipofuscin and melanin and choroidal melanin in human eyes. Invest Ophthalmol Vis Sci 1986; 27:145-52.
110. Feeney-Burns L, Hilderbrand ES, Eldridge S. Aging human RPE: morphometric analysis of macular, equatorial, and peripheral cells. Invest Ophthalmol Vis Sci 1984; 25:195-200.
111. Holz FG, Sheraidah G, Pauleikhoff D, Bird AC. Analysis of lipid deposits extracted from human macular and peripheral Bruch's membrane. Arch Ophthalmol 1994; 112:402-6.
112. Beatty S, Boulton M, Henson D, Koh HH, Murray IJ. Macular pigment and age related macular degeneration. Br J Ophthalmol 1999; 83:867-77.
113. Snodderly DM, Auran JD, Delori FC. The macular pigment. II. Spatial distribution in primate retinas. Invest Ophthalmol Vis Sci 1984; 25:674-85.
114. Snodderly DM, Sandstrom MM, Leung IY, Zucker CL, Neuringer M. Retinal pigment epithelial cell distribution in central retina of rhesus monkeys. Invest Ophthalmol Vis Sci 2002; 43:2815-8.
115. Robinson SR, Hendrickson A. Shifting relationships between photoreceptors and pigment epithelial cells in monkey retina: implications for the development of retinal topography. Vis Neurosci 1995; 12:767-78.
116. Anderson DH, Fisher SK, Erickson PA, Tabor GA. Rod and cone disc shedding in the rhesus monkey retina: a quantitative study. Exp Eye Res 1980; 30:559-74.
117. Curcio CA. Photoreceptor topography in ageing and age-related maculopathy. Eye 2001; 15:376-83.
118. Weiter JJ, Delori F, Dorey CK. Central sparing in annular macular degeneration. Am J Ophthalmol 1988; 106:286-92.
119. Berson EL. Retinitis pigmentosa. The Friedenwald Lecture. Invest Ophthalmol Vis Sci 1993; 34:1659-76.
120. Miceli MV, Liles MR, Newsome DA. Evaluation of oxidative processes in human pigment epithelial cells associated with retinal outer segment phagocytosis. Exp Cell Res 1994; 214:242-9.
121. Arden GB. The absence of diabetic retinopathy in patients with retinitis pigmentosa: implications for pathophysiology and possible treatment. Br J Ophthalmol 2001; 85:366-70.
122. Linsenmeier RA. Effects of light and darkness on oxygen distribution and consumption in the cat retina. J Gen Physiol 1986; 88:521-42.
123. Linsenmeier RA, Braun RD. Oxygen distribution and consumption in the cat retina during normoxia and hypoxemia. J Gen Physiol 1992; 99:177-97.
124. Braun RD, Linsenmeier RA, Goldstick TK. Oxygen consumption in the inner and outer retina of the cat. Invest Ophthalmol Vis Sci 1995; 36:542-54.
125. Pierce EA, Avery RL, Foley ED, Aiello LP, Smith LE. Vascular endothelial growth factor/vascular permeability factor expression in a mouse model of retinal neovascularization. Proc Natl Acad Sci U S A 1995; 92:905-9.
126. Aiello LP, Pierce EA, Foley ED, Takagi H, Chen H, Riddle L, Ferrara N, King GL, Smith LE. Suppression of retinal neovascularization in vivo by inhibition of vascular endothelial growth factor (VEGF) using soluble VEGF-receptor chimeric proteins. Proc Natl Acad Sci U S A 1995; 92:10457-61.
127. Duh E, Aiello LP. Vascular endothelial growth factor and diabetes: the agonist versus antagonist paradox. Diabetes 1999; 48:1899-906.
128. Pruett RC. Retinitis pigmentosa: clinical observations and correlations. Trans Am Ophthalmol Soc 1983; 81:693-735.
129. Uliss AE, Gregor ZJ, Bird AC. Retinitis pigmentosa and retinal neovascularization. Ophthalmology 1986; 93:1599-603.
130. Hayakawa M, Hotta Y, Imai Y, Fujiki K, Nakamura A, Yanashima K, Kanai A. Clinical features of autosomal dominant retinitis pigmentosa with rhodopsin gene codon 17 mutation and retinal neovascularization in a Japanese patient. Am J Ophthalmol 1993; 115:168-73.
131. Aiello LP, Avery RL, Arrigg PG, Keyt BA, Jampel HD, Shah ST, Pasquale LR, Thieme H, Iwamoto MA, Park JE, Nguyen HV, Aiello LM, Ferrara N, King GL. Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders. N Engl J Med 1994; 331:1480-7.
132. Lahdenranta J, Pasqualini R, Schlingemann RO, Hagedorn M, Stallcup WB, Bucana CD, Sidman RL, Arap W. An anti-angiogenic state in mice and humans with retinal photoreceptor cell degeneration. Proc Natl Acad Sci U S A 2001; 98:10368-73.
133. Katz ML, Drea CM, Eldred GE, Hess HH, Robison WG Jr. Influence of early photoreceptor degeneration on lipofuscin in the retinal pigment epithelium. Exp Eye Res 1986; 43:561-73.
134. Yu DY, Cringle SJ. Oxygen distribution and consumption within the retina in vascularised and avascular retinas and in animal models of retinal disease. Prog Retin Eye Res 2001; 20:175-208.
135. Hall MO, Abrams TA, Mittag TW. The phagocytosis of rod outer segments is inhibited by drugs linked to cyclic adenosine monophosphate production. Invest Ophthalmol Vis Sci 1993; 34:2392-401.
136. Kuriyama S, Hall MO, Abrams TA, Mittag TW. Isoproterenol inhibits rod outer segment phagocytosis by both cAMP-dependent and independent pathways. Invest Ophthalmol Vis Sci 1995; 36:730-6.
137. Mannerstrom M, Maenpaa H, Toimela T, Salminen L, Tahti H. The phagocytosis of rod outer segments is inhibited by selected drugs in retinal pigment epithelial cell cultures. Pharmacol Toxicol 2001; 88:27-33.
138. Doolittle DP, Davisson MT, Guidi JN, Green MC. Catalog of mutant genes and polymorphic loci. In: Lyon MF, Rastan S, Brown SDM, editors. Genetic variants and strains of the laboratory mouse. Oxford: Oxford University Press; 1996. pp. 17-854.
139. Jackson IJ. Homologous pigmentation mutations in human, mouse and other model organisms. Hum Mol Genet 1997; 6:1613-24.
140. Travis GH. Mechanisms of cell death in the inherited retinal degenerations. Am J Hum Genet 1998; 62:503-8.