Evolution and the origin of the visual retinoid cycle in vertebrates

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 364, Issue 1531, 2009, Pages 2897-2910

  Kusakabe, Takehiro G ^a,b   Takimoto, Noriko ^b   Jin, Minghao ^c   Tsuda, Motoyuki ^d  

^a KONAN UNIVERSITY   (Japan)

^b UNIVERSITY OF HYOGO   (Japan)

^c LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d TOKUSHIMA BUNRI UNIVERSITY   (Japan)

Author keywords

Ascidian; Chromophore regeneration; Opsin; Photoisomerase; RPE65; Visual cycle

Indexed keywords

AQUATIC ORGANISM; COMPARTMENTALIZATION; ENZYME; EUKARYOTE; EVOLUTION; INVERTEBRATE; LARVA; LIGHT EFFECT; PIGMENT; VERTEBRATE;

ASCIDIA; ASCIDIACEA; INVERTEBRATA; PROTOSTOMIA; VERTEBRATA;

EID: 70349670575     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2009.0043     Document Type: Review

References (119)

1. Ashida, A., Matsumoto, K., Ebrey, T. G. & Tsuda, M. 2004 A purified agonist-activated G-protein coupled receptor: truncated octopus acid metarhodopsin. Zool. Sci.. 21, 245-250. (doi:10.2108/zsj.21.245) (Pubitemid 38717931)
2. Bailey, M. J. & Cassone, V M. 2004 Opsin photoisomerases in the chick retina and pineal gland: characterization, localization, and circadian regulation. Invest. Ophthalmol. Vis. Sci. 45, 769-775. (doi:10.1167/iovs.03- 1125)
3. Bailey, M. J., Beremand, P. D., Hammer, R., Reidel, E., Thomas, T. L. & Cassone, V. M. 2004 Transcriptional profiling of circadian patterns of mRNA expression in the chick retina. J. Biol. Chem. 279, 52 247-52 254. (doi: 10.1074/jbc.M405679200) (Pubitemid 39656598)
4. Batten, M. L. et al. 2004 Lecithin-retinol acyltransferase is essential for accumulation of all-irarai-retinyl esters in the eye and in the liver. J. Biol. Chem. 279, 10 422-10 432. (doi: 10.1074/jbc.M312410200)
5. Bavik, C. O., Busch, C. & Eriksson, U. 1992 Characterization of a plasma retinol-binding protein membrane receptor expressed in the retinal pigment epithelium. J Biol. Chem. 267, 23 035-23 042.
6. Bok, D., Ong, D. E. & Chytil, F. 1984 Immunocytochemical localization of cellular retinol binding protein in the rat retina. Invest. Ophthalmol. Vis. Sci. 25, 877-883. (Pubitemid 14055884)
7. Bridges, C. D., Alvarez, R. A., Fong, S. L., Liou, G. I. & Ulshafer, R. J. 1987a Rhodopsin, vitamin A, and interstitial retinol-binding protein in the rd chicken. Invest. Ophthalmol. Vis. Sci. 28, 613-617. (Pubitemid 17054179)
8. Bridges, C. D., Foster, R. G., Landers, R. A. & Fong, S. L. 1987b Interstitial retinol-binding protein and cellular retinal-binding protein in the mammalian pineal. Vis. Res. 27, 2049-2060. (doi:10.1016/0042-6989(87)90119-2)
9. Bunt-Milam, A. H. & Saari, J. C. 1983 Immunocytochemical localization of two retinoid-binding proteins in vertebrate retina. J. Cell Biol. 97, 703-712. (doi:10. 1083/jcb.97.3.703)
10. Burstedt, M. S. I., Sandgren, O., Holmgren, G. & ForsmanSemb, K. 1999 Bothnia dystrophy caused by mutation in the cellular retinaldehyde-binding protein gene (RLBP1) on chromosome 15q26. Invest. Ophthalmol. Vis. Sci. 40, 995-1000. (Pubitemid 29153267)
11. Carlson, A. & Bok, D. 1992 Promotion of the release of 11-cis-retinal from cultured retinal pigment epithelium by interphotoreceptor retinoid-binding protein. Biochemistry 31, 9056-9062. (doi:10.1021/bi00152a049)
12. Chen, Y.& Noy, N. 1994 Retinoid specificity of interphotoreceptor retinoid-binding protein. Biochemistry 33, 10 658-10 665. (doi:10.1021/ bi00201a013)
13. Chen, P. et al. 2001a A photic visual cycle of rhodopsin regeneration is dependent on Rgr. Nat. Genet. 28, 256-260. (doi: 10.1038/90089) (Pubitemid 32626028)
14. Chen, P., Lee, T. D. & Fong, H. K. 2001b Interaction of 11-cis-retinol dehydrogenase with the chromophore of retinal G protein-coupled receptor opsin. J. Biol. Chem. 276, 21 098-21 104. (doi:10.1074/jbc.M010441200) (Pubitemid 37413095)
15. Chichili, G. R., Nohr, D., Schaffer, M., von Lintig, J. & Biesalski, H. K. 2005 β-Carotene conversion into vitamin A in human retinal pigment epithelial cells. Invest. Ophthalmol. Vis. Sci. 46, 3562-3569. (doi:10.1167/iovs.05-0089) (Pubitemid 44264657)
16. Choo, D. W., Cheung, E. & Rando, R. R. 1998 Lack of effect of RPE65 removal on the enzymatic processing of all-irarai-retinol into 11-cis-retinol in vitro. FEBS Lett. 440, 195-198. (doi:10.1016/S0014-5793(98)01459-8) (Pubitemid 28558763)
17. Collery, R., McLoughlin, S., Vendrell, V., Finnegan, J., Crabb, J. W., Saari, J. C. & Kennedy, B. N. 2008 Duplication and divergence of zebrafish CRALBP genes uncovers novel role for RPE- and Muller-CRALBP in cone vision. Invest. Ophthalmol. Vis. Sei. 49, 3812-3820. (doi:10.1167/iovs.08-1957)
18. Crouch, R. K., Hazard, E. S., Lind, T., Wiggert, B., Chader, G. & Corson, D. W 1992 Interphotoreceptor retinoid-binding protein and alphatocopherol preserve the isomeric and oxidation state of retinol. Photochem. Photobiol. 56, 251-255. (doi: 10.1111/j.1751-1097. 1992.tb02154.x)
19. Das, S. R., Bhardwaj, N., Kjeldbye, H. & Gouras, P 1992 Müller cells of chicken retina synthesize ll-cis-retinol. Biochem. J 285,907-913.
20. Deigner, P. S., Law, W C., Cañada, F. J. & Rando, R. R. 1989 Membranes as the energy source in the endergonic transformation of vitamin A to 11-cis-retinol. Science 244, 968-971. (doi:10.1126/science.2727688)
21. Delsuc, F., Brinkmann, H., Chourrout, D. & Philippe, H. 2006 Tunicates and not cephalochordates are the closest living relative of vertebrates. Nature 493, 965-968. (doi:10.1038/nature04336) (Pubitemid 43292413)
22. Deyts, C., Casane, D., Vernier, P., Bourrat, F. & Joly, S. 2006 Morphological and gene expression similarities suggest that the ascidian neural gland may be osmoregulatory and homologous to vertebrate peri-ventricular organs. Eur. J. Neurosci. 24, 2299-2308. (doi:10.1111/j. 1460-9568.2006.05073.X) (Pubitemid 44622350)
23. Driessen, C. A., Janssen, B. P., Winkens, H. J., van Vugt, A. H., de Leeuw, T.L. & Janssen, J. J. 1995 Cloning and expression of a cDNA encoding bovine retinal pigment epithelial 11 -cis retinol dehydrogenase. Invest. Ophthalmol. Vis. Sci. 36, 1988-1996.
24. Driessen, C. A. et al. 2000 Disruption of the 11-cis-retinol dehydrogenase gene leads to accumulation of «5-retinols and cis-retinyl esters. Mol. Cell. Biol. 20, 4275-4287. (doi:10.1128/MCB.20.12.4275-4287.2000)
25. Feathers, K. L., Lyubarsky, A. L., Khan, N. W., Teofilo, K., Swaroop, A., Williams, D. S., Pugh, E. N. & Thompson, D. A. 2008 Nrl-knockout mice deficient in Rpe65 fail to synthesize 11-cis RAL and cone outer segments. Invest. Ophthalmol. Vis. Sci. 49, 1126-1135. (doi:10.1167/iovs. 07-1234)
26. Fleisch, V. C., Schonthaler, H. B., von Lintig, J. & Neuhauss, S. C. 2008 Subfunctionalization of a retinoid-binding protein provides evidence for two parallel visual cycles in the cone-dominant zebrafish retina. J Neurosci. 28, 8208-8216. (doi:10.1523/JNEUROSCI. 2367-08.2008)
27. Foster, R. G. & Hankins, M. W 2002 Non-rod, non-cone photoreception in the vertebrates. Prog. Retin. Eye Res. 21, 507-527. (doi:10.1016/S1350- 9462(02)00036-8)
28. Gollapalli, D. R & Rando, R. R. 2003 Molecular logic of 11-cisretinoid biosynthesis in a cone-dominated species. Biochemistry 42, 14 921-14 929. (doi:10.1021/bi0356505)
29. Gonzalez-Fernandez, F. 2002 Evolution of the visual cycle: the role of retinoid-binding proteins. J Endocrinol. 175, 75-88. (doi:10.1677/joe.0.1750075) (Pubitemid 35276588)
30. Haeseleer, F., Jang, G. F., Imanishi, Y., Driessen, C. A., Matsumura, M., Nelson, P S. & Palczewski, K. 2002 Dual-substrate specificity short chain retinol dehydrogenases from the vertebrate retina. J. Biol. Chem. 277, 45 537-45 546. (doi:10.1074/jbc.M208882200) (Pubitemid 36159164)
31. Hamel, C. P., Tsilou, E., Pfeffer, B. A., Hooks, J. J., Detrick, B. & Redmond, T.M. 1993 Molecular cloning and expression of RPE65, a novel retinal pigment epithelium-specific microsomal protein that is posttranscriptionally regulated in vitro. J Biol. Chem. 268, 15751-15757. (Pubitemid 23222076)
32. Hao, W & Fong, H. K. W 1996 Blue and ultraviolet lightabsorbing opsin from the retinal pigment epithelium. Biochemistry 35, 6251-6256. (doi:10.1021/bi952420k) (Pubitemid 26164053)
33. Hara, T.& Hara, R. 1968 Regeneration of retinochrome. Nature 219, 450-454. (doi:10.1038/219450a0)
34. Hara, T.& Hara, R. 1973 Isomerization of retinal catalyzed by retinochrome in the light. Nature 242, 39-43.
35. Hara, T.& Hara, R. 1991 Retinal-binding protein: function in a chromophore exchange system in the squid visual cell. Prog. Retin. Eye. Res. 10, 179-206.
36. Hardie, R. C. 1986 Photoreceptor array of the dipteran retina. Trends Neurosci. 9, 419-423. (doi:10.1016/01662236(86)90136-0)
37. Hattar, S. et al. 2003 Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature 424, 76-81. (doi:10.1038/ nature01761) (Pubitemid 36834844)
38. Horie, T., Sakurai, D., Ohtsuki, S., Terakita, A., Shichida, Y., Usukura, J., Kusakabe, T.& Tsuda, M. 2008 Pigmented and nonpigmented ocelli in the brain vesicle of the ascidian larva. J. Comp. Neurol. 509, 88-102. (doi: 10.1002/cne.21733)
39. Inada, K., Horie, T., Kusakabe, T.& Tsuda, M. 2003 Targeted knockdown of an opsin gene inhibits the swimming behaviour photoresponse of ascidian larvae. Neurosci. Lett. 347, 167-170. (doi:10.1016/S03043940(03)00689-X)
40. Jahng, W J., David, C., Nesnas, N., Nakanishi, K. & Rando, R. R. 2003 A cleavable affinity biotinylating agent reveals a retinoid binding role for RPE65. Biochemistry 42, 6159-6168. (doi:10.1021/bi034002i) (Pubitemid 36605117)
41. Jin, M., Li, S., Moghrabi, W N., Sun, H. & Travis, G. H. 2005 Rpe65 is the retinoid isomerase in bovine retinal pigment epithelium. Cell 122, 449-459. (doi:10.1016/j. cell.2005.06.042) (Pubitemid 41127145)
42. Jin, M., Yuan, Q., Li, S. & Travis, G. H. 2007 Role of LRAT on the retinoid isomerase activity and membrane association of Rpe65. J Biol. Chem. 282, 20 915-20 924. (doi:10.1074/jbc.M701432200) (Pubitemid 47099920)
43. Jones, G. J., Crouch, R. K., Wiggert, B., Cornwall, M. C. & Chader, G. J. 1989 Retinoid requirements for recovery of sensitivity after visual-pigment bleaching in isolated photoreceptors. Proc. Natl Acad. Sci. USA 86, 9606-9610. (doi:10.1073/pnas.86.23.9606) (Pubitemid 20010477)
44. Kajiwara, S., Tamotsu, S., Morita, Y.& Numakunai, T.1990 Retinal isomers in the cerebral ganglion of the ascidian, Halocynthia roretzi. Invertebr. Reprod. Dev. 17, 155-158.
45. Kaschula, C. H., Jin, M., Desmond-Smith, N. S. & Travis, G. H. 2006 Acyl CoA:retinol acyltransferase (ARAT) activity is present in bovine retinal pigment epithelium. Exp. Eye Res. 82, 111-121. (doi:10.1016/j.exer.2005.05. 010) (Pubitemid 43063402)
46. Kiefer, C., Hessel, S., Lampert, J. M., Vogt, K., Lederer, M. O., Breithaupt, D. E. & von Lintig, J. 2001 Identification and characterization of a mammalian enzyme catalyzing the asymmetric oxidative cleavage of provitamin A. J Biol. Chem. 276, 14 110-14 116. (Pubitemid 37391796)
47. Kim, T.S., Maeda, A., Maeda, T., Heinlein, C., Kedishvili, N., Palczewski, K. & Nelson, P S. 2005 Delayed dark adaptation in 11-cis-retinol dehydrogenase-deficient mice: a role of RDHIl in visual processes in vivo. J Biol. Chem. 280, 8694-8704. (doi:10.1074/jbc. M413172200) (Pubitemid 40416700)
48. Kloer, D. P., Ruch, S., Al-Babili, S., Beyer, P & Schulz, G. E. 2005 The structure of a retinal-forming carotenoid oxygenase. Science 308, 267-269. (doi:10.1126/science. 1108965)
49. Kojima, D., Mano, H. & Fukada, Y.2000 Vertebrate ancient-long opsin: a green-sensitive photoreceptive molecule present in zebrafish deep brain and retinal horizontal cells. J. Neurosci. 20, 2845-2851. (Pubitemid 30220309)
50. Koyanagi, M., Terakita, A., Kubokawa, K. & Shichida, Y. 2002 Amphioxus homologs of Go-coupled rhodopsin and peropsin having 11-cis- and all-irarai-retinals as their chromophores. FEBS Lett. 531, 525-528. (doi:10.1016/ S0014-5793(02)03616-5) (Pubitemid 35336080)
51. Koyanagi, M., Kawano, E., Kinugawa, Y., Oishi, T., Shichida, Y., Tamotsu, S. & Terakita, A. 2004 Bistable UV pigment in the lamprey pineal. Proc. Natl Acad. Sci. USA 101, 6687-6691. (doi:10.1073/pnas.0400819101)
52. Koyanagi, M., Kubokawa, K., Tsukamoto, H., Shichida, Y.& Terakita, A. 2005 Cephalochordate melanopsin: evolutionary linkage between invertebrate visual cells and vertebrate photosensitive retinal ganglion cells. Curr. Biol. 15, 1065-1069. (doi:10.1016/j.cub.2005.04.063)
53. Kusakabe, T.& Tsuda, M. 2007 Photoreceptive systems in ascidians. Photochem. Photobiol. 83, 248-252.
54. Kusakabe, T., Kusakabe, R., Kawakami, L., Satou, Y., Satoh, N. & Tsuda, M. 2001 Ci-opsinl, a vertebrate-type opsin gene, expressed in the larval ocellus of the ascidian Ciona intestinalis. FEBS Lett. 506, 69-72. (doi:10.1016/ S0014-5793(01)02877-0)
55. Lamb, T.D. & Pugh Jr, E. 2004 Dark adaptation and the retinoid cycle of vision. Prog. Retin. Eye Res. 23, 307-380. (doi:10.1016/j.preteyeres.2004.03. 001)
56. Lampert, J. M., Holzschuh, J., Hessel, S., Driever, W., Vogt, K. & von Lintig, J. 2003 Provitamin A conversion to retinal via the β,β-carotene-15,15'-oxygenase (bcox) is essential for pattern formation and differentiation during zebrafish embryogenesis. Development 130, 2173-2186. (doi:10.1242/dev.00437) (Pubitemid 36656713)
57. Leuenberger, M. G., Engeloch-Jarret, C. & Woggon, W D. 2001 The reaction mechanism of the enzymecatalyzed central cleavage of β-carotene to retinal. Angew. Chem. Int. Ed. Engl. 40, 2613-2617. (doi:10.1002/ 1521-3773(20010716)40:14<2613::AID-ANIE2613>3. 0.CO;2-Z)
58. Lindqvist, A. & Andersson, S. 2002 Biochemical properties of purified recombinant human β-carotene 15,15'-monooxygenase. J Biol. Chem. 277, 23 942-23 948. (doi:10. 1074/jbc.M202756200) (Pubitemid 34952239)
59. Liou, G. I., Bridges, C. D., Fong, S. L., Alvarez, R. A. & Gonzalez-Fernandez, F. 1982 Vitamin A transport between retina and pigment epithelium-an interstitial protein carrying endogenous retinol (interstitial retinolbinding protein). Vis. Res. 22, 1457-1467. (doi:10. 1016/0042-6989(82) 90210-3)
60. Lucas, R. J., Hattar, S., Takao, M., Berson, D. M., Foster, R. G. & Yau, K. W 2003 Diminished pupillary light reflex at high irradiances in melanopsin-knockout mice. Science299, 245-247. (doi: 10.1126/science. 1077293) (Pubitemid 36125209)
61. Luo, W., Nicholas, M. A., Amir, R. & Nathans, J. 2004 An outer segment localization signal at the C terminus of the photoreceptor-specific retinol dehydrogenase. J Neurosci. 24, 2623-2632. (doi:10.1523/JNEUROSCI. 5302-03.2004) (Pubitemid 38380938)
62. Ma, J., Zhang, J., Othersen, K. L., Moiseyev, G., Ablonczy, Z., Redmond, T.M., Chen, Y.& Crouch, R. K. 2001 Expression, purification, and MALDI analysis of RPE65. Invest. Ophthalmol. Vis. Sei. 42, 1429-1435.
63. Maeda, T., Van Hooser, J. P., Driessen, C. A. G. G., Filipek, S., Janssen, J. J. M. & Palczewski, K. 2003 Evaluation of the role of the retinal G protein-coupled receptor (RGR) in the vertebrate retina in vivo. J Neurochem. 85, 944-956. (Pubitemid 36578626)
64. Maeda, A. et al. 2005 Role of photoreceptor-specific retinol dehydrogenase in the retinoid cycle in vivo. J. Biol. Chem. 280, 18 822-18 832. (doi:10.1074/jbc.M501757200)
65. Mano, H. & Fukada, Y.2007 A median third eye: pineal gland retraces evolution of vertebrate photoreceptive organs. Photochem. Photobiol. 83, 11-18. (Pubitemid 46697218)
66. Mata, N. L., Radu, R. A., Clemmons, R. C. & Travis, G. H. 2002 Isomerization and oxidation of vitamin A in conedominant retinas: a novel pathway for visual-pigment regeneration in daylight. Neuron 36, 69-80. (doi: 10. 1016/S0896-6273(02)00912-1)
67. Mata, N. L., Moghrabi, W N., Lee, J. S., Bui, T. V., Radu, R. A., Horwitz, J. & Travis, G. H. 2004 Rpe65 is a retinyl ester binding protein that presents insoluble substrate to the isomerase in retinal pigment epithelial cells. J. Biol. Chem. 279, 635-643. (doi:10.1074/jbc.M310042200) (Pubitemid 38044868)
68. Mata, N. L., Ruiz, A., Radu, R. A., Bui, T.V & Travis, G. H. 2005 Chicken retinas contain a retinoid isomerase activity that catalyzes the direct conversion of all-transretinol to 11-cis-retinol. Biochemistry 44, 11 715-11 721. (doi:10.1021/bi050942m) (Pubitemid 41262705)
69. Maw, M. A. et al. 1997 Mutation of the gene encoding cellular retinaldehyde-binding protein in autosomal recessive retinitis pigmentosa. Nat. Genet. 17, 198-200. (doi:10. 1038/ngl097-198)
70. Mears, A. J., Kondo, M., Swain, P. K., Takada, Y., Bush, R. A., Saunders, T.L., Sieving, P. A. & Swaroop, A. 2001 NrI is required for rod photoreceptor development. Nat. Genet. 29, 447-452. (doi:10.1038/ng774) (Pubitemid 34326696)
71. Miyazono, S., Shimauchi-Matsukawa, Y., Tachibanaki, S. & Kawamura, S. 2008 Highly efficient retinal metabolism in cones. Proc. Natl Acad Sci. USA 105, 16 051-16 056. (doi:10.1073/pnas.0806593105)
72. Moiseyev, G., Chen, Y., Takahashi, Y., Wu, B. X. & Ma, J. X. 2005 RPE65 is the isomerohydrolase in the retinoid visual cycle. Proc. Natl Acad Sci. USA 102, 12 413-12 418. (doi:10.1073/pnas.0503460102) (Pubitemid 41266373)
73. Morimura, H., Berson, E. L. & Dryja, T.P 1999 Recessive mutations in the RLBPgene encoding cellular retinaldehydebinding protein in a form of retinitis punctata albescens. Invest. Ophthalmol. Vis. Sci. 40, 1000-1004. (Pubitemid 29153268)
74. Muniz, A., Villazana-Espinoza, E. T., Hatch, A. L., Trevino, S. G., Allen, D. M. & Tsin, A. T.2007 A novel cone visual cycle in the cone-dominated retina. Exp. Eye Res. 85, 175-184. (doi:10.1016/j.exer.2007.05. 003) (Pubitemid 47087804)
75. Nakagawa, M., Miyamoto, T, Ohkuma, M. & Tsuda, M. 1999 Action spectrum for the Photophobie response of Ciona intestinalis (Ascidieacea, Urochordata) larvae implicates retinal protein. Photochem. Photobiol. 70, 359-362. (doi:10.1111/j.l751-1097.1999.tb08149.x) (Pubitemid 129555886)
76. Nakashima, Y, Kusakabe, T, Kusakabe, R., Terakita, A., Shichida, Y.& Tsuda, M. 2003 Origin of the vertebrate visual cycle: genes encoding retinal photoisomerase and two putative visual cycle proteins are expressed in whole brain of a primitive chordate. J Comp. Neurol. 460, 180-190. (doi:10.1002/cne.l0645)
77. Nickerson, J. M., Frey, R A., Ciavatta, V T.& Stenkamp, D. L. 2006 Interphotoreceptor retinoid-binding protein gene structure in tetrapods and teleost fish. Mol. Vis. 12, 1565-1585.
78. Ohkuma, M. & Tsuda, M. 2000 Visualization of retinal proteins in the cerebral ganglion of ascidian, Halocynthia roretzi. Zool. Sci. 17, 161-170. (doi:10. 2108/zsj.17.161)
79. Ohkuma, M., Katagiri, Y, Nakagawa, M. & Tsuda, M. 2000 Possible involvement of light regulated gonadotropinreleasing hormone neurons in biological clock for reproduction in the cerebral ganglion of the ascidian, Halocynthia roretzi. Neurosci. Lett. 293, 5-8. (doi: 10. 1016/S0304-3940(00) 01481-6)
80. Palczewski, K., Van Hooser, J. P, Garwin, G. G., Chen, J., Liou, G. I. & Saari, J. C. 1999 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 38, 12 012-12 019. (doi:10.1021/bi990504d) (Pubitemid 129515474)
81. Provencio, I., Jiang, G., De Grip, W J., Hayes, W P & Rollag, M. D. 1998 Melanopsin: an opsin in melanophores, brain, and eye. Proc. Natl Acad. Sci. USA 95, 340-345. (doi:10.1073/pnas.95.1.340) (Pubitemid 28103955)
82. Putnam, N. H. et al. 2008 The amphioxus genome and the evolution of the chordate karyotype. Nature 453, 1064-1071. (doi:10.1038/nature06967)
83. Qtaishat, N. M., Wiggert, B. & Pepperberg, D. R. 2005 Interphotoreceptor retinoid-binding protein (IRBP) promotes the release of all-irarai retinol from the isolated retina following rhodopsin bleaching illumination. Exp. Eye Res. 81, 455-463. (doi:10.1016/j.exer. 2005.03.005) (Pubitemid 41356509)
84. Rando, R. R. 2001 The biochemistry of the visual cycle. Chem. Rev. 101, 1881-1896. (doi:10.1021/cr960141c)
85. Rattner, A., Smallwood, P. M. & Nathans, J. 2000 Identification and characterization of all-trans-retinol dehydrogenase from photoreceptor outer segments, the visual cycle enzyme that reduces all-trans-retinal to all-trans-retinol. J. Biol. Chem. 275, 11034-11043. (doi:10.1074/jbc.275.15. 11034) (Pubitemid 30212743)
86. Redmond, T.M., Wiggert, B., Robey, F. A., Nguyen, N. Y, Lewis, M. S., Lee, L. & Chader, G. J. 1985 Isolation and characterization of monkey interphotoreceptor retinoid-binding protein, a unique extracellular matrix component of the retina. Biochemistry 24, 787-793. (doi:10.1021/bi00324a038) (Pubitemid 15142261)
87. Redmond, T.M. et al. 1998 Rpe65 is necessary for production of 11-CM-vitamin A in the retinal visual cycle. Nat. Genet. 20, 344-351. (doi: 10.1038/3813)
88. Redmond, T.M., Gentleman, S., Duncan, T, Yu, S., Wiggert, B., Grantt, E. & Cunningham Jr, F. X. 2001 Identification, expression, and substrate specificity of a mammalian ß-carotene 15,15'-dioxygenase. J. Biol. Chem. 276, 6560-6565. (doi:10.1074/jbc.M009030200) (Pubitemid 37373520)
89. Redmond, T.M., Poliakov, E., Yu, S., Tsai, J. Y, Lu, Z. & Gentleman, S. 2005 Mutation of key residues of RPE65 abolishes its enzymatic role as isomerohydrolase in the visual cycle. Proc. Natl Acad. Sci. USA 102, 13 658-13 663. (doi:10.1073/pnas.0504167102) (Pubitemid 41420904)
90. Ripps, H., Peachey, N. S., Xu, X., Nozell, S. E., Smith, S. B. & Liou, G. I. 2000 The rhodopsin cycle is preserved in IRBP 'knockout' mice despite abnormalities in retinal structure and function. Vis. Neurosci. 17, 97-105. (doi:10.1017/S095252380017110X)
91. Rodrigues, M. M., Hackett, J., Gaskins, R., Wiggert, B., Lee, L., Redmond, M. & Chader, G. J. 1986 Interphotoreceptor retinoid-binding protein in retinal rod cells and pineal gland. Invest. Ophthalmol. Vis. Sci. 27, 844-850. (Pubitemid 16080505)
92. Ruiz, A., Winston, A., Lim, Y.H., Gilbert, B. A., Rando, R. R. & Bok, D. 1999 Molecular and biochemical characterization of lecithin retinol acyltransferase. J. Biol. Chem. 274, 3834-3841. (doi:10.1074/jbc.274.6.3834) (Pubitemid 29077233)
93. Saari, J. C. 2000 Biochemistry of visual pigment regeneration: the Friedenwald lecture. Invest. Ophthalmol. Vis. Sci. 41, 337-348.
94. Saari, J. C., Huang, J., Possin, D. E., Fariss, R. N., Leonard, J., Garwin, G. G., Crabb, J. W & Milam, A. H. 1997 Cellular retinaldehyde- binding protein is expressed by oligodendrocytes in optic nerve and brain. Glia 21, 259-268. (doi:10.1002/(SICI)1098-1136(199711)21: 3<259::AID-GLIA1>3.0. CO;2-0) (Pubitemid 27491046)
95. Saari, J. C., Nawrot, M., Kennedy, B. N., Garwin, G. G., Hurley, J. B., Huang, J., Possin, D. E. & Crabb, J. W 2001 Visual cycle impartment in cellular retinaldehyde binding protein (CRALBP) knockout mice results in delayed dark adaptation. Neuron 29, 739-748. (doi: 10. 1016/S0896-6273(01)00248-3) (Pubitemid 32323946)
96. Schonthaler, H. B. et al. 2007 Evidence for RPE65independent vision in the cone-dominated zebrafish retina. Eur. J. Neurosci. 26, 1940-1949. (doi:10.1111/j. 1460-9568.2007.05801.X)
97. Soni, B. G., Philp, A. R., Foster, R. G. & Knox, B. E. 1998 Novel retinal photoreceptors. Nature 394, 27-28. (doi:10.1038/27794)
98. Sun, H., Gilbert, D. J., Copeland, N. G., Jenkins, N. A. & Nathans, J. 1997 Peropsin, a novel visual pigment-like protein located in the apical microvilli of the retinal pigment epithelium. Proc. Natl Acad. Sci. USA 94, 9893-9898. (doi:10.1073/pnas.94.18.9893) (Pubitemid 27408161)
99. Takahashi, Y, Moiseyev, G., Chen, Y.& Ma, X. 2006 The roles of three palmitoylation sites of RPE65 in its membrane association and isomerohydrolase activity. Invest. Ophthalmol. Vis. Sci. 47, 5191-5196. (doi:10.1167/iovs.06- 0614)
100. Takimoto, N., Kusakabe, T, Horie, T, Miyamoto, Y.& Tsuda, M. 2006 Origin of the vertebrate visual cycle: III. Distinct distribution of RPE65 and β-carotene 15,15'-monooxygenase homologues in Ciona intestinalis. Photochem. Photobiol. 83, 242-247.
101. Takimoto, N., Kusakabe, T.& Tsuda, M. 2007 Origin of the vertebrate visual cycle. Photochem. Photobiol. 83, 242-247.
102. Terakita, A., Hara, R. & Hara, T.1989 Retinal-binding protein as a shutter for retinal in the rhodopsinretinochrome system of the squid visual cells. Vis. Res. 29, 639-652. (doi: 10.1016/0042-6989(89)90026-6) (Pubitemid 19142615)
103. Travis, G. H., Golczak, M., Moise, A. R. & Palczewski, K. 2007 Diseases caused by defects in the visual cycle: retinoids as potential therapeutic agents. Annu. Rev. Pharmacol. Toxicol. 47, 469-512. (doi:10.1146/annurev. pharmtox.47.120505.105225) (Pubitemid 46272136)
104. Tsuda, M. 1987 Photoreception and phototransduction in invertebrate photoreceptors. Photochem. Photobiol. 45, 915-931. (doi:10.1111/j.1751-1097. 1987.tb07903.x)
105. Tsuda, M., Kawakami, I. & Shiraishi, S. 2003a Sensitization and habituation of the swimming behavior in ascidian larvae to light. Zool. Sci. 20,13-22. (doi:10.2108/zsj.20.13) (Pubitemid 36619063)
106. Tsuda, M., Kusakabe, T, Iwamoto, H., Horie, T, Nakashima, Y, Nakagawa, M. & Okunou, K. 2003b Origin of the vertebrate visual cycle: II. Visual cycle proteins are localized in whole brain including photoreceptor cells of a primitive chordate. Vis. Res. 43, 3045-3053. (doi:10.1016/j.visres.2003.09.012) (Pubitemid 37377616)
107. Tsutsui, H. & Oka, Y.2000 Light-sensitive voltage responses in the neurons of the cerebral ganglion of Ciona savignyi (Chordata: Ascidiacea). Biol. Bull. 198, 26-28. (doi: 10. 2307/1542800) (Pubitemid 30119047)
108. van Veen, T, Katial, A., Shinohara, T, Barrett, D. J., Wiggert, B., Chader, G. J. & Nickerson, J. M. 1986 Retinal photoreceptor neurons and pinealocytes accumulate mRNA for interphotoreceptor retinoid-binding protein (IRBP). FEBS Lett. 208, 133-137. (doi: 10.1016/00145793(86)81547-2) (Pubitemid 17191278)
109. Vigh, B., Manzano, M. J., Zadori, A., Frank, C. L., Lukats, A., Rohlich, P, Szel, A. & David, C. 2002 Non visual photoreceptors of the deep brain, pineal organs and retina. Histol. Histopathol. 17, 555-590. (Pubitemid 34413536)
110. von Lintig, J. & Vogt, K. 2000 Filling the gap in vitamin A research. Molecular identification of an enzyme cleaving beta-carotene to retinal. J. Biol. Chem. 275, 11 915-11 920. (doi:10.1074/jbc.275.16.11915) (Pubitemid 30237761)
111. Wald, G. 1935 Carotenoids and the visual cycle. J Gen. Physiol. 19, 351-371. (doi:10.1085/jgp.l9. 2.351)
112. Walker, M. T, Brown, R. L., Cronin, T.W & Robinson, P R 2008 Photochemistry of retinal chromophore in mouse melanopsin. Proc. Natl Acad. Sci. USA 105, 8861-8865. (doi: 10.1073/pnas.0711397105)
113. Wenzel, A. et al. 2005 The retinal G protein-coupled receptor (RGR) enhances isomerohydrolase activity independent of light. J Biol. Chem. 280, 29 874-29 884. (doi: 10.1074/jbc.M503603200) (Pubitemid 41177065)
114. Wenzel, A., von Lintig, J., Oberhauser, V., Tanimoto, N., Grimm, C. & Seeliger, M. W 2007 RPE65 is essential for the function of cone photoreceptors in NRL-deficient mice. Invest. Ophthalmol. Vis. Sci. 48, 534-542. (doi:10. 1167/IOVS.06-0652) (Pubitemid 351260682)
115. Wyss, A. 2004 Carotene oxygenases: a new family of double bond cleavage enzymes. J. Neutr. 134, 246-250. (Pubitemid 38057457)
116. Xue, L., Gollapalli, D. R., Maiti, P, Jahng, W & Rando, R. R. 2004 A palmitoylation switch mechanism in the regulation of the visual cycle. Cell 117, 761-771. (doi:10.1016/j.cell.2004.05.016) (Pubitemid 38748892)
117. Yan, W et al. 2001 Cloning and characterization of a human ß,ß-carotene-15,15'-dioxygenase that is highly expressed in the retinal pigment epithelium. Genomics 72, 193-202. (doi:10.1006/geno.2000.6476) (Pubitemid 32242959)
118. Zimmerman, W. F. 1974 The distribution and proportions of vitamin A compounds during the visual cycle in the rat. Vis. Res. 14, 795-802. (doi:10.1016/0042-6989(74) 90143-6)
119. Znoiko, S. L., Crouch, R. K., Moiseyev, G. & Ma, J. X. 2002 Identification of the RPE65 protein in mammalian cone photoreceptors. Invest. Ophthalmol. Vis. Sci. 43, 1604-1609. (Pubitemid 34462664)