New insights into retinoid metabolism and cycling within the retina

Progress in Retinal and Eye Research

Volumn 32, Issue 1, 2013, Pages 48-63

  Tang, Peter H ^a   Kono, Masahiro ^a   Koutalos, Yiannis ^a   Ablonczy, Zsolt ^a   Crouch, Rosalie K ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Opsin; Photoreceptors; Retinal; Retinoid; Visual cycle; Visual pigment

Indexed keywords

11 CIS RETINAL; G PROTEIN COUPLED RECEPTOR; LIPOFUSCIN; PROTEIN RPE65; RETINAL; RETINOID; UNCLASSIFIED DRUG; VISUAL PIGMENT;

CHROMATOPHORE; HUMAN; MOUSE; NONHUMAN; PHOTORECEPTOR CELL; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN METABOLISM; PROTEIN PROCESSING; RETINA; RETINA CONE; RETINA ROD; REVIEW; VISION;

ANIMALS; EYE PROTEINS; HUMANS; RETINA; RETINAL CONE PHOTORECEPTOR CELLS; RETINAL PIGMENTS; RETINOIDS;

EID: 84871377137     PISSN: 13509462     EISSN: 18731635     Source Type: Journal    
DOI: 10.1016/j.preteyeres.2012.09.002     Document Type: Review

References (177)

1. Ablonczy Z., Gutierrez D.B., Grey A.C., Schey K.L., Crouch R.K. Molecule-specific imaging and quantitation of A2E in the RPE. Adv. Exp. Med. Biol. 2012, 723:75-81.
2. Ablonczy Z., Higbee D., Hanneken A.M., Schey K.L., Koutalos Y., Crouch R.K. Linking retinoids to clinical patterns of AMD. Invest. Ophthalmol. Vis. Sci. 2012, ARVO E-Abstract 6477.
3. Ablonczy Z., Kono M., Knapp D.R., Crouch R.K. Palmitylation of cone opsins. Vis. Res. 2006, 46:4493-4501.
4. Acland G.M., Aguirre G.D., Ray J., Zhang Q., Aleman T.S., Cideciyan A.V., Pearce-Kelling S.E., Anand V., Zeng Y., Maguire A.M., Jacobson S.G., Hauswirth W.W., Bennett J. Gene therapy restores vision in a canine model of childhood blindness. Nat. Genet. 2001, 28:92-95.
5. Acland G.M., Aquirre G.D., Bennett J., Aleman T.S., Cideciyan A.V., Bennicelli J., Dejneka N.S., Pearce-Kelling S.E., Maguire A.M., Palczewski K., Hauswirth W.W., Jacobson S.G. Long-term restoration of rod and cone vision by single dose rAAV-mediated gene transfer to the retina in a canine model of childhood blindness. Mol. Ther. 2005, 12:1072-1082.
6. Ala-Laurila P., Cornwall M.C., Crouch R.K., Kono M. The action of 11-cis retinol on cone opsins and intact cone photoreceptors. J. Biol. Chem. 2009, 284:16492-16500.
7. Ala-Laurila P., Kolesnikov A.V., Crouch R.K., Tsina E., Shukolyukov S.A., Govardovskii V.I., Koutalos Y., Wiggert B., Estevez M.E., Cornwall M.C. Visual cycle: dependence of retinol production and removal on photoproduct decay and cell morphology. J. Gen. Physiol. 2006, 128:153-169.
8. Amemiya T. Electron microscopic and cytochemical study on paraboloid glycogen of the accessory cone of the chick retina. Histochemistry 1975, 43:185-192.
9. Anderson D.H., Fisher S.K., Steinberg R.H. Mammalian cones: disc shedding, phagocytosis, and renewal. Invest. Ophthalmol. Vis. Sci. 1978, 17:117-133.
10. Applebury M.L., Antoch M.P., Baxter L.C., Chun L.L., Falk J.D., Farhangfar F., Kage K., Kryzstolik M.G., Lyass L.A., Robbins J.T. The murine cone photoreceptor: a single cone type expresses both S and M opsins with retinal spatial patterning. Neuron 2000, 27:513-523.
11. Archer S.N., Lythgoe J.N. The visual pigment basis for cone polymorphism in the guppy, Poecilia reticulata. Vis. Res. 1990, 30:225-233.
12. Arikawa K., Molday L.L., Molday R.S., Williams D.S. Localization of peripherin/rds in the disk membranes of cone and rod photoreceptors - relationship to disk membrane morphogenesis and retinal degeneration. J. Cell. Biol. 1992, 116:659-667.
13. Bainbridge J.W., Smith A.J., Barker S.S., Robbie S., Henderson R., Balaggan K., Viswanathan A., Holder G.E., Stockman A., Tyler N., Petersen-Jones S., Bhattacharya S.S., Thrasher A.J., Fitzke F.W., Carter B.J., Rubin G.S., Moore A.T., Ali R.R. Effect of gene therapy on visual function in Leber's congenital amaurosis. N. Engl. J. Med. 2008, 358:2231-2239.
14. Batten M.L., Imanishi Y., Maeda T., Tu D.C., Moise A.R., Bronson D., Possin D., Van-Gelder R.N., Baehr W., Palczewski K. Lecithin-retinol acyltransferase is essential for accumulation of all-trans-retinyl esters in the eye and in the liver. J. Biol. Chem. 2004, 279:10422-10432.
15. Baylor D.A., Lamb T.D., Yau K.W. The membrane current of single rod outer segments. J. Physiol. 1979, 288:589-611.
16. Baylor D.A., Nunn B.J., Schnapf J.L. The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca fascicularis. J. Physiol. 1984, 357:575-607.
17. Ben-Shabat S., Itagaki Y., Jockusch S., Sparrow J.R., Turro N.J., Nakanishi K. Formation of a nonaoxirane from A2E, a lipofuscin fluorophore related to macular degeneration, and evidence of singlet oxygen involvement. Angew. Chem. Int. Engl. 2002, 41:814-817.
18. Ben-Shabat S., Parish C.A., Vollmer H.R., Itagaki Y., Fishkin N., Nakanishi K., Sparrow J.R. Biosynthetic studies of A2E, a major fluorophore of retinal pigment epithelial lipofuscin. J. Biol. Chem. 2002, 277:7183-7190.
19. Bhosale P., Serban B., Bernstein P.S. Retinal carotenoids can attenuate formation of A2E in the retinal pigment epithelium. Arch. Biochem. Biophys. 2009, 483:175-181.
20. Birnbach C.D., Järveläinen M., Possin D.E., Milam A.H. Histopathology and immunocytochemistry of the neurosensory retina in fundus flavimaculatus. Ophthalmology 1994, 101:1211-1219.
21. Blakeley L.R., Chen C., Chen C.K., Chen J., Crouch R.K., Travis G.H., Koutalos Y. Rod outer segment retinol formation is independent of Abca4, arrestin, rhodopsin kinase, and rhodopsin palmitylation. Invest. Ophthalmol. Vis. Sci. 2011, 52:3483-3491.
22. Boyer N.P., Highbee D., Currin M.B., Blakeley L.R., Chen C., Ablonczy Z., Crouch R.K., Koutalos Y. Lipofuscin and N-retinylidene-N-retinylethanolamine (A2E) accumulate in the retinal pigment epithelium in the absence of light exposure: their origin is 11-cis retinal. J. Biol. Chem. 2012, 287:22276-22286.
23. Boyer, N.P., Tang, P.H., Higbee, D., Ablonczy, Z., Crouch, R.K., Koutalos, Y. Lipofuscin and A2E accumulate with age in the retinal pigment epithelium of Nrl-/- mice. Photochem. Photobiol., in press.
24. Braekevelt C.R. Retinal photoreceptor fine structure in the mallard duck (Anas platyrhynchos). Histol. Histopathol. 1990, 5:123-131.
25. Bunt-Milam A.H., Saari J.C. Immunocytochemical localization of two retinoid-binding proteins in vertebrate retina. J. Cell. Biol. 1983, 97:703-712.
26. Carter-Dawson L., Burroughs M. Interphotoreceptor retinoid-binding protein in the cone matrix sheath. Electron microscopic immunocytochemical localization. Invest. Ophthalmol. Vis. Sci. 1992, 33:1584-1588.
27. Carter-Dawson L., Burroughs M. Interphotoreceptor retinoid-binding protein in the golgi apparatus of monkey foveal cones. Electron microscopic immunocytochemical localization. Invest. Ophthalmol. Vis. Sci. 1992, 33:1589-1594.
28. Carter-Dawson L.D., LaVail M.M. Rods and cones in the mouse retina. I. Structural analysis using light and electron microscopy. J. Comp. Neurol. 1979, 188:245-262.
29. Chen C., Blakeley L.R., Koutalos Y. Formation of all-trans retinol after visual pigment bleaching in mouse photoreceptors. Invest. Ophthalmol. Vis. Sci. 2009, 50:3589-3595.
30. Chen C., Thompson D.A., Koutalos Y. Reduction of all-trans retinal in vertebrate rod photoreceptors requires the combined action of RDH8 and RDH12. J. Biol. Chem. 2012, 287:24662-24670.
31. Chen C., Tsina E., Cornwall M.C., Crouch R.K., Vijayaraghavan S., Koutalos Y. Reduction of all-trans retinal to all-trans retinol in the outer segments of frog and mouse rod photoreceptors. Biophys. J. 2005, 88:2278-2287.
32. Chen M.H., Kuemmel C., Birge R.R., Knox B.E. Rapid retinal release from a cone visual pigment following photoactivation. Biochemistry 2012, 51:4117-4126.
33. Chrispell J.D., Feathers K.L., Kane M.A., Kim C.Y., Brooks M., Khanna R., Kurth I., Hübner C.A., Gal A., Mears A.J., Swaroop A., Napoli J.L., Sparrow J.R., Thompson D.A. Rdh12 activity and effects on retinoid processing in the murine retina. J. Biol. Chem. 2009, 284:21468-21477.
34. Collery R., McLoughlin S., Vendrell V., Finneagan J., Crabb J.W., Saari J.C., Kennedy B.N. Duplication and divergence of zebrafish CRALBP genes uncovers novel role for RPE- and Muller-CRALBP in cone vision. Invest. Ophthalmol. Vis. Sci. 2008, 49:3812-3820.
35. Corson D.W., Kefalov V.J., Cornwall M.C., Crouch R.K. Effect of 11-cis 13-demethylretinal on phototransduction in bleach-adapted rod and cone photoreceptors. J. Gen. Physiol. 2000, 116:283-297.
36. Crescitelli F. The gecko visual pigment: the dark exchange of chromophore. Vis. Res. 1984, 24:1551-1553.
37. Crouch R.K., Hazard E.S., Lind T., Wiggert B., Chader G., Corson D.W. Interphotoreceptor retinoid-binding protein and alpha-tocopherol preserve the isomeric and oxidation state of retinol. Photochem. Photobiol. 1992, 56:251-255.
38. Das J., Crouch R.K., Ma J.X., Oprian D.D., Kono M. Role of the 9-methyl group of retinal in cone visual pigments. Biochemistry 2004, 43:5532-5538.
39. Das S.R., Bhardwaj N., Kjeldbye H., Gouras P. Muller cells of chicken retina synthesize 11-cis-retinol. Biochem. J. 1992, 285:907-913.
40. Delmelle M. Retinal sensitized photodynamic damage to liposomes. Photochem. Photobiol. 1978, 28:357-360.
41. Delori F.C., Staurenghi G., Arend O., Dorey C.K., Goger D.G., Weiter J.J. In vivo measurement of lipofuscin in Stargardt's disease - fundus flavimaculatus. Invest. Ophthalmol. Vis. Sci. 1995, 36:2327-2331.
42. Dowling J.E. Nutritional and inherited blindness in the rat. Exp. Eye Res. 1964, 3:348-356.
43. Ebrey T., Koutalos Y. Vertebrate photoreceptors. Prog. Retin. Eye Res. 2001, 20:49-94.
44. Edwards R.B., Adler A.J. Exchange of retinol between IRBP and CRBP. Exp. Eye Res. 1994, 59:161-170.
45. Edwards R.B., Adler A.J. IRBP enhances removal of 11-cis retinaldehyde from isolated RPE membranes. Exp. Eye Res. 2000, 70:235-245.
46. Eisenfeld A.J., Bunt-Milam A.H., Saari J.C. Localization of retinoid-binding proteins in developing rat retina. Exp. Eye Res. 1985, 41:299-304.
47. Eldred G.E., Lasky M.R. Retinal age pigments generated by self-assembling lysosomotropic detergents. Nature 1993, 361:724-726.
48. Estevez M.E., Ala-Laurila P., Crouch R.K., Cornwall M.C. Turning cones off: the role of the 9-methyl group of retinal in red cones. J. Gen. Physiol. 2006, 128:671-685.
49. Estevez M.E., Kolesnikov A.V., Ala-Laurila P., Crouch R.K., Govardovskii V.I., Cornwall M.C. The 9-methyl group of retinal is essential for rapid meta II decay and phototransduction quenching in red cones. J. Gen. Physiol. 2009, 134:137-150.
50. Fan J., Crouch R.K., Kono M. Light prevents exogenous 11-cis retinal from maintaining cone photoreceptors in chromophore-deficient mice. Invest. Ophthalmol. Vis. Sci. 2011, 52:2412-2416.
51. Fan J., Rohrer B., Frederick J.M., Baehr W., Crouch R.K. RPE65-/- and LRAT-/- mice: comparable models of Leber congenital amaurosis. Invest. Ophthalmol. Vis. Sci. 2008, 49:2384-2389.
52. Feeney L. Lipofuscin and melanin of human retinal pigment epithelium. Fluorescence, enzyme cytochemical, and ultrastructural studies. Invest. Ophthalmol. Vis. Sci. 1978, 17:583-600.
53. Fleisch V.C., Schonthaler H.B., von-Lintig J., Neuhauss S.C. Subfunctionalization of a retinoid-binding protein provides evidence for two parallel visual cycles in the cone-dominant zebrafish retina. J. Neurosci. 2008, 28:8208-8216.
54. Fliesler S.J., Anderson R.E. Chemistry and metabolism of lipids in the vertebrate retina. Prog. Lipid Res. 1983, 22:79-131.
55. Fu Y., Yau K.W. Phototransduction in mouse rods and cones. Pflugers Arch. 2007, 454:805-819.
56. Fukada Y., Okano T., Shichida Y., Yoshizawa T., Trehan A., Mead D., Denny M., Asato A.E., Liu R.S. Comparative study on the chromophore binding sites of rod and red-sensitive cone visual pigments by use of synthetic retinal isomers and analogues. Biochemistry 1990, 29:3133-3140.
57. Futterman S., Hendrickson A., Bishop P.E., Rollins M.H., Vacano E. Metabolism of glucose and reduction of retinaldehyde in retinal photoreceptors. J. Neurochem. 1970, 17:149-156.
58. Golczak M., Maeda A., Bereta G., Maeda T., Kiser P.D., Hunzelmann S., von-Lintig J., Blaner W.S., Palczewski K. Metabolic basis of visual cycle inhibition by retinoid and nonretinoid compounds in the vertebrate retina. J. Biol. Chem. 2008, 283:9543-9554.
59. Goldstein E.B. Visual pigments and the early receptor potential of the isolated frog retina. Vis. Res. 1968, 8:953-963.
60. Gonzalez-Fernandez F. Interphotoreceptor retinoid-binding protein - an old gene for new eyes. Vis. Res. 2003, 43:3021-3036.
61. Grey A.C., Crouch R.K., Koutalos Y., Schey K.L., Ablonczy Z. Spatial localization of A2E in the retinal pigment epithelium. Invest. Ophthalmol. Vis. Sci. 2011, 52:3926-3933.
62. Hamel C.P., Tsilou E., Pfeffer B.A., Hooks J.J., Detrick B., Redmond T.M. Molecular cloning and expression of RPE65, a novel retinal pigment epithelium-specific microsomal protein that is post-transcriptionally regulated in vitro. J. Biol. Chem. 1993, 268:15751-15757.
63. Harris E.W. Leber's congenital amaurosis and RPE65. Int. Ophthalmol. Clin. 2001, 41:73-82.
64. Hemati N., Feathers K.L., Chrispell J.D., Reed D.M., Carlson T.J., Thompson D.A. RPE65 surface epitopes, protein interactions, and expression in rod- and cone-dominant species. Mol. Vis. 2005, 11:1151-1165.
65. Hicks D., Sahel J. The implications of rod-dependent cone survival for basic clinical research. Invest. Ophthalmol. Vis. Sci. 1999, 40:3071-3074.
66. Hinterhuber G., Cauza K., Brugger K., Dingelmaier-Hovorka R., Horvat R., Wolff K., Foedinger D. RPE65 of retinal pigment epithelium, a putative receptor molecule for plasma retinol-binding protein, is expressed in human keratinocytes. J. Invest. Dermatol. 2004, 122:406-413.
67. Hinterhuber G., Cauza K., Dingelmaier-Hovorka R., Diem E., Horvat R., Wolff K., Foedinger D. Expression of RPE65, a putative receptor for plasma retinol-binding protein, in nonmelanocytic skin tumours. Br. J. Dermatol. 2005, 153:785-789.
68. Holz F.G., Bellman C., Staudt S., Schütt F., Völcker H.E. Fundus autofluorescence and development of geographic atrophy in age-related macular degeneration. Invest. Ophthalmol. Vis. Sci. 2001, 42:1051-1056.
69. Hood D.C., Hock P.A. Recovery of cone receptor activity in the frog's isolated retina. Vis. Res. 1973, 13:1943-1951.
70. Hunt D.M., Carvalho L.S., Cowing J.A., Davies W.L. Evolution and spectral tuning of visual pigments in birds and mammals. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2009, 364:2941-2955.
71. Isayama T., Chen Y., Kono M., Degrip W.J., Ma J.X., Crouch R.K., Makino C.L. Differences in the pharmacological activation of visual opsins. Vis. Neurosci. 2006, 23:899-908.
72. Jin J., Crouch R.K., Corson D.W., Katz B.M., MacNichol E.F., Cornwall M.C. Noncovalent occupancy of the retinal-binding pocket of opsin diminishes bleaching adaptation of retinal cones. Neuron 1993, 11:513-522.
73. Jin J., Jones G.J., Cornwall M.C. Movement of retinal along cone and rod photoreceptors. Vis. Neurosci. 1994, 11:389-399.
74. Jin M., Li S., Moghrabi W.N., Sun H., Travis G.H. Rpe65 is the retinoid isomerase in bovine retinal pigment epithelium. Cell 2005, 122:449-459.
75. Jin M., Li S., Nusinowitz S., Lloyd M., Hu J., Radu R.A., Bok D., Travis G.H. The role of interphotoreceptor retinoid-binding protein on the translocation of visual retinoids and function of cone photoreceptors. J. Neurosci. 2009, 29:1486-1495.
76. John S.K., Smith J.E., Aguirre G.D., Milam A.H. Loss of cone molecular markers in rhodopsin-mutant human retinas with retinitis pigmentosa. Mol. Vis. 2000, 6:204-215.
77. Jones G.J., Crouch R.K., Wiggert B., Cornwall M.C., Chader G.J. Retinoid requirements for recovery of sensitivity after visual-pigment bleaching in isolated photoreceptors. Proc. Natl. Acad. Sci. U. S. A. 1989, 86:9606-9610.
78. Kanan Y., Kasus-Jacobi A., Moiseyev G., Sawyer K., Ma J.X., al-Ubaidi M.R. Retinoid processing in cone and Müller cell lines. Exp. Eye Res. 2008, 86:344-354.
79. Katz M.L., Eldred G.E., Robison W.G. Lipofuscin autofluorescence: evidence for vitamin A involvement in the retina. Mech. Ageing Dev. 1987, 39:81-90.
80. Katz M.L., Redmond T.M. Effect of Rpe65 knockout on accumulation of lipofuscin fluorophores in the retinal pigment epithelium. Invest. Ophthalmol. Vis. Sci. 2001, 42:3023-3030.
81. Katz M.L., Robinson W.G. What is lipofuscin? Defining characteristics and differentiation from other autofluorescent lysosomal storage bodies. Arch. Gerontol. Geriatr. 2002, 34:169-184.
82. Kawaguchi R., Yu J., Honda J., Hu J., Whitelegge J., Ping P., Wiita P., Bok D., Sun H. A membrane receptor for retinol binding protein mediates cellular uptake of vitamin A. Science 2007, 315:820-825.
83. Kaylor, J.J., Yuan, Q., Cook, J., Sarfare, S., Makshanoff, J., Miu, A., Kim, A., Kim, P., Habib, S., Roybal, C.N., Xu, T., Nusinowitz, S., Travis, G.H. Identification of DES1 as a vitamin A isomerase in Müller glia cells of the retina. Nat. Chem. Biol., in press.
84. Kefalov V.J., Cornwall M.C., Crouch R.K. Occupancy of the chromophore binding site of opsin activates visual transduction in rod photoreceptors. J. Gen. Physiol. 1999, 113:491-503.
85. Kefalov V.J., Estevez M.E., Kono M., Goletz P.W., Crouch R.K., Cornwall M.C., Yau K.W. Breaking the covalent bond - a pigment property that contributes to desensitization in cones. Neuron 2005, 46:879-890.
86. Kefalov V.J., Fu Y., Marsh-Armstrong N., Yau K.W. Role of visual pigment properties in rod and cone phototransduction. Nature 2003, 425:526-531.
87. Kim S.R., Jang Y.P., Jockusch S., Fishkin N.E., Turro N.J., Sparrow J.R. The all-trans-retinal dimer series of lipofuscin pigments in retinal pigment epithelial cells in a recessive Stargardt disease model. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:19273-19278.
88. Kim S.R., Jockusch S., Itagaki Y., Turro N.J., Sparrow J.R. Mechanisms involved in A2E oxidation. Exp. Eye Res. 2008, 86:975-982.
89. Kiser P.D., Golczak M., Lodowski D.T., Chance M.R., Palczewski K. Crystal structure of native RPE65, the retinoid isomerase of the visual cycle. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:17325-17330.
90. Kociok N., Heppekausen H., Schraermeyer U., Esser P., Thumann G., Grisanti S., Heimann K. The mRNA expression of cytokines and their receptors in cultured iris pigment epithelial cells: a comparison with retinal pigment epithelial cells. Exp. Eye Res. 1998, 67:237-250.
91. Kolesnikov A.V., Ala-Laurila P., Shukolyukov S.A., Crouch R.K., Wiggert B., Estevez M.E., Govardovskii V.I., Cornwall M.C. Visual cycle and its metabolic support in gecko photoreceptors. Vis. Res. 2007, 47:363-374.
92. Kono M., Crouch R.K. In vitro assays of rod and cone opsin activity: retinoid analogs as agonists and inverse agonists. Methods Mol. Biol. 2010, 652:85-94.
93. Kono M., Crouch R.K. Probing human red cone opsin activity with retinal analogues. J. Nat. Prod. 2011, 74:391-394.
94. Kono M., Goletz P.W., Crouch R.K. 11-cis and all-trans retinols can activate rod opsin: rational design of the visual cycle. Biochemistry 2008, 47:7567-7571.
95. Krasnovsky A.A., Kagan V.E. Photosensitization and quenching of singlet oxygen by pigments and lipids of photoreceptor cells of the retina. FEBS Lett. 1979, 108:152-154.
96. Liou G.I., Peachey N.S., Matragoon S., Wei S., Blaner W.S., Wang Y., Liu C., Gottesman M.E., Ripps H. Early onset photoreceptor abnormalities induced by targeted disruption of the interphotoreceptor retinoid-binding protein gene. J. Neurosci. 1998, 18:4511-4520.
97. Liu J., Itagaki Y., Ben-Shabat S., Nakanishi K., Sparrow J.R. The biosynthesis of A2E, a fluorophore of aging retina, involves the formation of the precursor, A2-PE, in the photoreceptor outer segment membrane. J. Biol. Chem. 2000, 275:29354-29360.
98. Lukáts A., Szabó A., Röhlich P., Vigh B., Szél A. Photopigment coexpression in mammals: comparative and developmental aspects. Histol. Histopathol. 2005, 20:551-574.
99. Ma J., Znoiko S., Othersen K.L., Ryan J.C., Das J., Isayama T., Kono M., Oprian D.D., Corson D.W., Cornwall M.C., Cameron D.A., Harosi F.I., Makino C.L., Crouch R.K. A visual pigment expressed in both rod and cone photoreceptors. Neuron 2001, 32:451-461.
100. Ma J.X., Xu L., Othersen D.K., Redmond T.M., Crouch R.K. Cloning and localization of RPE65 mRNA in salamander cone photoreceptor cells. Biochim. Biophys. Acta 1998, 1443:255-261.
101. Ma J.X., Zhang D., Laser M., Brownlee N.A., Re G.G., Hazen-Martin D.J., Redmond T.M., Crouch R.K. Identification of RPE65 in transformed kidney cells. FEBS Lett. 1999, 452:199-204.
102. Maeda A., Golczak M., Chen Y., Okano K., Kohno H., Shiose S., Ishikawa K., Harte W., Palczewski G., Maeda T., Palczewski K. Primary amines protect against retinal degeneration in mouse models of retinopathies. Nat. Chem. Biol. 2011, 8:170-178.
103. Maeda A., Maeda T., Golczak M., Chou S., Desai A., Hoppel C.L., Matsuyama S., Palczewski K. Involvement of all-trans-retinal in acute light-induced retinopathy of mice. J. Biol. Chem. 2009, 284:15173-15183.
104. Maeda A., Maeda T., Imanishi Y., Kuksa V., Alekseev A., Bronson J.D., Zhang H., Zhu L., Sun W., Saperstein D.A., Rieke F., Baehr W., Palczewski K. Role of photoreceptor-specific retinol dehydrogenase in the retinoid cycle in vivo. J. Biol. Chem. 2005, 280:18822-18832.
105. Maeda A., Okano K., Park P.S., Lem J., Crouch R.K., Maeda T., Palczewski K. Palmitoylation stabilizes unliganded rod opsin. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:8428-8433.
106. Maeda T., Cideciyan A.V., Maeda A., Golczak M., Aleman T.S., Jacobson S.G., Palczewski K. Loss of cone photoreceptors caused by chromophore depletion is partially prevented by the artificial chromophore pro-drug, 9-cis-retinyl acetate. Hum. Mol. Genet. 2009, 18:2277-2287.
107. Maguire A., Simonelli F., Pierce E.A., Pugh E.N., Mingozzi F., Bennicelli J., Banfi S., Marshall K.A., Testa F., Surace E.M., Rossi S., Lyubarsky A., Arruda V.R., Konkle B., Stone E., Sun J., Jacobs J., Dell'Osso L., Hertle R., Ma J.X., Redmond T.M., Zhu X., Hauck B., Zelenaia O., Shindler K.S., Maguire M.G., Wright J.F., Volpe N.J., McDonnell J.W., Auricchio A., High K.A., Bennett J. Safety and efficacy of gene transfer for Leber's congenital amaurosis. N. Engl. J. Med. 2008, 358:2240-2248.
108. Maguire A.M., High K.A., Auricchio A., Wright J.F., Pierce E.A., Testa F., Mingozzi F., Bennicelli J.L., Ying G.S., Rossi S., Fulton A., Marshall K.A., Banfi S., Chung D.C., Morgan J.I., Hauck B., Zelenaia O., Zhu X., Raffini L., Coppieters F., De-Baere E., Shindler K.S., Volpe N.J., Surace E.M., Acerra C., Lyubarsky A., Redmond T.M., Stone E., Sun J., McDonnell J.W., Leroy B.P., Simonelli F., Bennett J. Age-dependent effects of RPE65 gene therapy for Leber's congenital amaurosis: a phase 1 dose-escalation trial. Lancet 2009, 374:1597-1605.
109. Maiti P., Kong J., Kim S.R., Allikmets R., Rando R.R. Small molecule RPE65 antagonists limit the visual cycle and prevent lipofuscin formation. Biochemistry 2006, 45:852-860.
110. Makaretz M., Levine R.L. A light microscopic study of the bifoveate retina in the lizard Anolis carolinensis: general observations and convergence ratios. Vis. Res. 1980, 20:679-686.
111. Makino C.L., Dodd R.L. Multiple visual pigments in a photoreceptor of the salamander retina. J. Gen. Physiol. 1996, 108:27-34.
112. Marlhens F., Bareil C., Griffoin J.M., Zrenner E., Amalric P., Eliaou C., Liu S.Y., Harris E., Redmond T.M., Arnaud B., Claustres M., Hamel C.P. Mutations in RPE65 cause Leber's congenital amaurosis. Nat. Genet. 1997, 17:139-141.
113. Mata N.L., Weng J., Travis G.H. Biosynthesis of a major lipofuscin fluorophore in mice and humans with ABCR-mediated retinal and macular degeneration. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:7154-7159.
114. Matsumoto H., Tokunaga F., Yoshizawa T. Accessibility of the iodopsin chromophore. Biochim. Biophys. Acta 1975, 404:300-308.
115. Matsumoto H., Yoshizawa T. Existence of a beta-ionone ring-binding site in the rhodopsin molecule. Nature 1975, 258:523-526.
116. McBee J.K., Kuksa V., Alvarez R., de-Lera A.R., Prezhdo O., Haeseleer F., Sokal I., Palczewski K. Isomerization of all-trans-retinol to cis-retinoids in bovine retinal pigment epithelial cells: dependence on the specificity of retinoid-binding proteins. Biochemistry 2000, 39:11370-11380.
117. Mears A.J., Kondo M., Swain P.K., Takada Y., Bush R.A., Saunders T.L., Sieving P.A., Swaroop A. Nrl is required for rod photoreceptor development. Nat. Genet. 2001, 29:447-452.
118. Miyazono S., Shimauchi-Matsukawa Y., Tachibanaki S., Kawamura S. Highly efficient retinal metabolism in cones. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:16051-16056.
119. Moiseyev G., Chen Y., Takahashi Y., Wu B.X., Ma J.X. RPE65 is the isomerohydrolase in the retinoid visual cycle. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:12413-12418.
120. Moiseyev G., Crouch R.K., Goletz P., Oatis J.J., Redmond T.M., Ma J.X. Retinyl esters are the substrate for isomerohydrolase. Biochemistry 2003, 42:2229-2238.
121. Muniz A., Betts B.S., Trevino A.R., Buddavarapu K., Roman R., Ma J.X., Tsin A.T. Evidence for two retinoid cycles in the cone-dominant chicken eye. Biochemistry 2009, 48:6854-6863.
122. Muniz A., Villazana-Espinoza E.T., Hatch A.L., Trevino S.G., Allen D.M., Tsin A.T. A novel cone visual cycle in the cone-dominant retina. Exp. Eye Res. 2007, 85:175-184.
123. Mustafi D., Engel A.H., Palczewski K. Structure of cone photoreceptors. Prog. Retin. Eye Res. 2009, 28:289-302.
124. Nelson R., deRiel J.K., Kropf A. 13-Desmethyl rhodopsin and 13-desmethyl isorhodopsin: visual pigment analogues. Proc. Natl. Acad. Sci. U. S. A. 1970, 66:531-538.
125. Ng K.P., Gugiu B., Renganathan K., Davies M.W., Gu X., Crabb J.S., Kim S.R., Rozanowska M.B., Bonilha V.L., Rayborn M.E., Salomon R.G., Sparrow J.R., Boulton M.E., Hollyfield J.G., Crabb J.W. Retinal pigment epithelium lipofuscin proteomics. Mol. Cell. Proteomics 2008, 7:1397-1405.
126. Palczewski K. Retinoids for treatment of retinal diseases. Trends Pharmacol. Sci. 2010, 31:284-295.
127. Palczewski K., Van-Hooser J.P., Garwin G.G., Chen J., Liou G.I., Saari J.C. Kinetics of visual pigment regeneration in excised mouse eyes and in mice with a targeted disruption of the gene encoding interphotoreceptor retinoid-binding protein or arrestin. Biochemistry 1999, 38:12012-12019.
128. Pang J.J., Chang B., Kumar A., Nusinowitz S., Noorwez S.M., Li J., Rani A., Foster T.C., Chiodo V.A., Doyle T., Li H., Malhotra R., Teusner J.T., McDowell J.H., Min S.H., Li Q., Kaushal S., Hauswirth W.W. Gene therapy restores vision-dependent behavior as well as retinal structure and function in a mouse model of RPE65 Leber congenital amaurosis. Mol. Ther. 2006, 13:565-572.
129. Parish C.A., Hashimoto M., Nakanishi K., Dillon J., Sparrow J.R. 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.
130. Parker R.O., Fan J., Nickerson J.M., Liou G.I., Crouch R.K. Normal cone function requires the interphotoreceptor retinoid binding protein. J. Neurosci. 2009, 29:4616-4621.
131. Parker R.O., Wang J.S., Kefalov V.J., Crouch R.K. Interphotoreceptor retinoid-binding protein as the physiologically relevant carrier of 11-cis-retinol in the cone visual cycle. J. Neurosci. 2011, 31:4714-4719.
132. Pepperberg D.R., Okajima T.L., Wiggert B., Ripps H., Crouch R.K., Chader G.J. Interphotoreceptor retinoid-binding protein (IRBP): molecular biology and physiological role in the visual cycle of rhodopsin. Mol. Neurobiol. 1993, 6:61-85.
133. Perry R.J., McNaughton P.A. Response properties of cones from the retina of the tiger salamander. J. Physiol. 1991, 433:561-587.
134. Redmond T.M., Gentleman S., Duncan T., Yu S., Wiggert B., Grantt F.X.C. Identification, expression, and substrate specificity of a mammalian beta-carotene 15,15'-dioxygenase. J. Biol. Chem. 2001, 276:6560-6565.
135. Redmond T.M., Hamel C.P. Genetic analysis of RPE65: from human disease to mouse model. Methods Enzymol. 2000, 316:705-724.
136. Redmond T.M., Poliakov E., Kuo S., Chander P., Gentleman S. RPE65, visual cycle retinol isomerase, is not inherently 11-cis-specific: support for a carbocation mechanism of retinol isomerization. J. Biol. Chem. 2010, 285:1919-1927.
137. Redmond T.M., Poliakov E., Yu S., Tsai J.Y., Lu Z., Gentleman S. Mutation of key residues of Rpe65 abolishes its enzymatic role as isomerohydrolase in the visual cycle. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:13658-13663.
138. Redmond T.M., Yu S., Lee E., Bok D., Hamasaki D., Chen N., Goletz P., Ma J.X., Crouch R.K., Pfeifer K. RPE65 is necessary for production of 11-cis-vitamin A in the retinal visual cycle. Nat. Genet. 1998, 20:344-351.
139. Rigtrup K.M., Ong D.E. A retinyl ester hydrolase activity intrinsic to the brush border membrane of rat small intestine. Biochemistry 1992, 31:2920-2926.
140. Ripps H., Peachey N.S., Xu X., Nozell S.E., Smith S.B., Liou G.I. The rhodopsin cycle is preserved in IRBP " knockout" mice despite abnormalities in retinal structure and function. Vis. Neurosci. 2000, 17:97-105.
141. Roberts J.E., Kukielczak B.M., Hu D.N., Miller D.S., Bilski P., Sik R.H., Motten A.G., Chignell C.F. The role of A2E in prevention or enhancement of light damage in human retinal pigment epithelial cells. Photochem. Photobiol. 2002, 75:184-190.
142. Rohrer B., Lohr H.R., Humphries P., Redmond T.M., Seeliger M.W., Crouch R.K. Cone opsin mislocalization in Rpe65-/- mice: a defect that can be corrected by 11-cis retinal. Invest. Ophthalmol. Vis. Sci. 2005, 46:3876-3882.
143. Rozanowska M., Sarna T. Light-induced damage to the retina: role of rhodopsin chromophore revisited. Photochem. Photobiol. 2005, 81:1305-1330.
144. Saari J.C., Teller D.C., Crabb J.W., Bredberg L. Properties of an interphotoreceptor retinoid-binding protein from bovine retina. J. Biol. Chem. 1985, 260:195-201.
145. Sakai T., Furukawa T., Iwanari H., Oka C., Nakano T., Kawaichi M., Honjo T. Loss of immunostaining of the RBP-J kappa transcription factor F9 cell differentiation induced by retinoic acid. J. Biochem. 1995, 118:621-628.
146. Sarantis M., Mobbs P. The spatial relationship between Müller cell processes and the photoreceptor output synapse. Brain Res. 1992, 584:299-304.
147. Schnapf J.L., Nunn B.J., Meister M., Baylor D.A. Visual transduction in cones of the monkey Macaca fascicularis. J. Physiol. 1990, 427:681-713.
148. Shichida Y., Imai H. Visual pigment: G-protein-coupled receptor for light signals. Cell. Mol. Life Sci. 1998, 54:1299-1315.
149. Sparrow J.R., Gregory-Roberts E., Yamamoto K., Blonska A., Ghosh S.K., Ueda K., Zhou J. The bisretinoids of retinal pigment epithelium. Prog. Retin. Eye Res. 2012, 31:121-135.
150. Sparrow J.R., Wu Y., Kim C.Y., Zhou J. Phospholipid meets all-trans retinal: the making of RPE bisretinoids. J. Lipid Res. 2010, 51:247-261.
151. Sun H. Membrane receptors and transporters involved in the function and transport of vitamin A and its derivatives. Biochim. Biophys. Acta 2012, 1821:99-112.
152. Takahashi Y., Moiseyev G., Chen Y., Ma J.X. The roles of three palmitoylation sites of RPE65 in its membrane association and isomerohydrolase activity. Invest. Ophthalmol. Vis. Sci. 2006, 47:5191-5196.
153. Tan E., Ding X.Q., Saadi A., Agarwal N., Naash M.I., Al-Ubaidi M.R. Expression of cone-photoreceptor-specific antigens in a cell line derived from retinal tumors in transgenic mice. Invest. Ophthalmol. Vis. Sci. 2004, 45:764-768.
154. Tang P.H., Buhusi M.C., Ma J.X., Crouch R.K. RPE65 is present in human green/red cones and promotes photopigment regeneration in an in vitro cone cell model. J. Neurosci. 2011, 31:18618-18626.
155. Tang P.H., Fan J., Goletz P.W., Wheless L., Crouch R.K. Effective and sustained delivery of hydrophobic retinoids to photoreceptors. Invest. Ophthalmol. Vis. Sci. 2010, 51:5958-5964.
156. Tang P.H., Wheless L., Crouch R.K. Regeneration of photopigment is enhanced in mouse cone photoreceptors expressing RPE65 protein. J. Neurosci. 2011, 31:10403-10411.
157. Travis G.H., Golczak M., Moise A.R., Palczewski K. Diseases caused by defects in the visual cycle: retinoids as potential therapeutic agents. Annu. Rev. Pharmocol. Toxicol. 2007, 47:1-44.
158. Trehan A., Cañada F.J., Rando R.R. Inhibitors of retinyl ester formation also prevent the biosynthesis of 11-cis retinol. Biochemistry 1990, 29:309-312.
159. Tsilou E., Hamel C.P., Yu S., Redmond T.M. RPE65, the major retinal pigment epithelium microsomal membrane protein, associates with phospholipid liposomes. Arch. Biochem. Biophys. 1997, 346:21-27.
160. Tsina E., Chen C., Koutalos Y., Ala-Laurila P., Tsacopoulos M., Wiggert B., Crouch R.K., Cornwall M.C. Physiological and microfluorometric studies of reduction and clearance of retinal in bleached rod photoreceptors. J. Gen. Physiol. 2004, 124:429-443.
161. Uehara F., Matthes M.T., Yasumura D., LaVail M.M. Light-evoked changes in the interphotoreceptor matrix. Science 1990, 248:1633-1636.
162. von-Lintig J., Vogt K. Filling the gap in vitamin A research. Molecular identification of an enzyme cleaving beta-carotene to retinal. J. Biol. Chem. 2000, 275:11915-11920.
163. Wald G. Carotenoids and the visual cycle. J. Gen. Physiol. 1935, 19:351-371.
164. Wald G. The chemistry of rod vision. Science 1951, 113:287-291.
165. Wald G., Brown P.K., Smith P.H. Iodopsin. J. Gen. Physiol. 1955, 38:623-681.
166. Wang J.S., Estevez M.E., Cornwall M.C., Kefalov V.J. Intra-retinal visual cycle required for rapid and complete cone dark adaptation. Nat. Neurosci. 2009, 12:295-302.
167. Wang J.S., Kefalov V.J. The cone-specific visual cycle. Prog. Retin. Eye Res. 2011, 30:115-128.
168. Wang Z., Keller L.M., Dillon J., Gaillard E.R. Oxidation of A2E results in the formation of highly reactive aldehydes and ketones. Photochem. Photobiol. 2006, 82:1251-1257.
169. Wang Z., Wen X.H., Ablonczy Z., Crouch R.K., Makino C.L., Lem J. Enhanced shutoff of phototransduction in transgenic mice expressing palmitoylation-deficient rhodopsin. J. Biol. Chem. 2005, 280:24293-24300.
170. Wenzel A., von-Lintig J., Oberhauser V., Tanimoto N., Grimm C., Seeliger M.W. RPE65 is essential for the function of cone photoreceptors in NRL-deficient mice. Invest. Ophthalmol. Vis. Sci. 2007, 48:534-542.
171. Wing G.L., Blanchard G.C., Weiter J.J. The topography and age relationship of lipofuscin concentration in the retinal pigment epithelium. Invest. Ophthalmol. Vis. Sci. 1978, 17:601-607.
172. Wolf G. The visual cycle of the cone photoreceptors of the retina. Nutr. Rev. 2004, 62:283-286.
173. Wu Q., Blakeley L.R., Cornwall M.C., Crouch R.K., Wiggert B.N., Koutalos Y. Interphotoreceptor retinoid-binding protein is the physiologically relevant carrier that removes retinol from rod photoreceptor outer segments. Biochemistry 2007, 46:8669-8679.
174. Yokoyama S. Molecular evolution of vertebrate visual pigments. Prog. Retin. Eye Res. 2000, 19:385-419.
175. Young R.W. The renewal of photoreceptor cell outer segments. J. Cell. Biol. 1967, 33:61-72.
176. Zhang H., Fan J., Li S., Karan S., Rohrer B., Palczewski K., Frederick J.M., Crouch R.K., Baehr W. Trafficking of membrane-associated proteins to cone photoreceptor outer segments requires the chromophore 11-cis-retinal. J. Neurosci. 2008, 28:4008-4014.
177. Znoiko S.L., Rohrer B., Lu K., Lohr H.R., Crouch R.K., Ma J.X. Downregulation of cone-specific gene expression and degeneration of cone photoreceptors in the Rpe65-/- mouse at early ages. Invest. Ophthalmol. Vis. Sci. 2005, 46:1473-1479.