S-opsin protein is incompletely modified during N-glycan processing in Rpe65-/- mice

Experimental Eye Research

Volumn 91, Issue 1, 2010, Pages 54-62

  Sato, Kota ^a,b   Nakazawa, Mitsuru ^b   Takeuchi, Kimio ^b   Mizukoshi, Sayuri ^a   Ishiguro, Sei ichi ^a  

^a HIROSAKI UNIVERSITY   (Japan)

^b HIROSAKI UNIVERSITY   (Japan)

Author keywords

11 cis retinal; Degradation; N glycosylation; RPE65; S opsin

Indexed keywords

GLYCAN; GLYCOPEPTIDASE; M OPSIN; MESSENGER RNA; OPSIN; PIGMENT EPITHELIUM DERIVED FACTOR; PIGMENT EPITHELIUM SPECIFIC PROTEIN 65; S OPSIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCATION; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN PROCESSING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE; WESTERN BLOTTING; WILD TYPE;

ANIMALS; BLOTTING, WESTERN; CARRIER PROTEINS; CHOROID; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EYE PROTEINS; GLYCOSYLATION; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; PROTEIN PROCESSING, POST-TRANSLATIONAL; RETINA; RETINAL DEGENERATION; RETINAL PIGMENT EPITHELIUM; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHODOPSIN; RNA, MESSENGER; ROD OPSINS;

EID: 77953356504     PISSN: 00144835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exer.2010.03.020     Document Type: Article

References (46)

1. Ablonczy Z., Crouch R.K., Goletz P.W., Redmond T.M., Knapp D.R., Ma J.X., Rohrer B. 11-cis-retinal reduces constitutive opsin phosphorylation and improves quantum catch in retinoid-deficient mouse rod photoreceptors. J. Biol. Chem. 2002, 277:40491-40498.
2. Applebury M.L., Antoch M.P., Baxter L.C., Chun L.L., Falk J.D., Farhangfar F., Kage K., Krzystolik 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.
3. 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.
4. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
5. Colley N.J., Baker E.K., Stamnes M.A., Zuker C.S. The cyclophilin homolog ninaA is required in the secretory pathway. Cell 1991, 67:255-263.
6. -/- mouse model of Leber's congenital amaurosis during progression of the disease. FASEB J. 2006, 20:2036-2049.
7. Crouch R.K., Chader G.J., Wiggert B., Pepperberg D.R. Retinoids and the visual process. Photochem. Photobiol. 1996, 64:613-621.
8. -/- mice: comparable models of Leber congenital amaurosis. Invest. Ophthalmol. Vis. Sci. 2008, 49:2384-2389.
9. Feathers K.L., Lyubarsky A.L., Khan N.W., Teofilo K., Swaroop A., Williams D.S., Pugh E.N., Thompson D.A. Nrl-knockout mice deficient in Rpe65 fail to synthesize 11-cis retinal and cone outer segments. Invest. Ophthalmol. Vis. Sci. 2008, 49:1126-1135.
10. Gu S.M., Thompson D.A., Srikumari C.R., Lorenz B., Finckh U., Nicoletti A., Murthy K.R., Rathmann M., Kumaramanickavel G., Denton M.J., Gal A. Mutations in RPE65 cause autosomal recessive childhood-onset severe retinal dystrophy. Nat. Genet. 1997, 17:194-197.
11. Harris E.W. Leber's congenital amaurosis and RPE65. Int. Ophthalmol. Clin. 2001, 41:73-82.
12. Heyman R.A., Mangelsdorf D.J., Dyck J.A., Stein R.B., Eichele G., Evans R.M., Thaller C. 9-cis retinoic acid is a high affinity ligand for the retinoid X receptor. Cell 1992, 68:397-406.
13. Huber A., Wolfrum U., Paulsen R. Opsin maturation and targeting to rhabdomeral photoreceptor membranes requires the retinal chromophore. Eur. J. Cell Biol. 1994, 63:219-229.
14. Jacobson S.G., Aleman T.S., Cideciyan A.V., Heon E., Golczak M., Beltran W.A., Sumaroka A., Schwartz S.B., Roman A.J., Windsor E.A., Wilson J.M., Aguirre G.D., Stone E.M., Palczewski K. Human cone photoreceptor dependence on RPE65 isomerase. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:15123-15128.
15. 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.
16. Lorenz B., Gyurus P., Preising M., Bremser D., Gu S., Andrassi M., Gerth C., Gal A. Early-onset severe rod-cone dystrophy in young children with RPE65 mutations. Invest. Ophthalmol. Vis. Sci. 2000, 41:2735-2742.
17. 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.
18. Marlhens F., Griffoin J.M., Bareil C., Arnaud B., Claustres M., Hamel C.P. Autosomal recessive retinal dystrophy associated with two novel mutations in the RPE65 gene. Eur. J. Hum. Genet. 1998, 6:527-531.
19. Moiseyev G., Crouch R.K., Goletz P., Oatis J., Redmond T.M., Ma J.X. Retinyl esters are the substrate for isomerohydrolase. Biochemistry 2003, 42:2229-2238.
20. 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.
21. Morimura H., Fishman G.A., Grover S.A., Fulton A.B., Berson E.L., Dryja T.P. Mutations in the RPE65 gene in patients with autosomal recessive retinitis pigmentosa or Leber congenital amaurosis. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:3088-3093.
22. Ozaki K., Nagatani H., Ozaki M., Tokunaga F. Maturation of major Drosophila rhodopsin, ninaE, requires chromophore 3-hydroxyretinal. Neuron 1993, 10:1113-1119.
23. Palczewski K. G protein-coupled receptor rhodopsin. Annu. Rev. Biochem. 2006, 75:743-767.
24. Phelan J.K., Bok D. A brief review of retinitis pigmentosa and the identified retinitis pigmentosa genes. Mol. Vis. 2000, 6:116-124.
25. Rando R.R. Molecular mechanisms in visual pigment regeneration. Photochem. Photobiol. 1992, 56:1145-1156.
26. Rando R.R. The biochemistry of the visual cycle. Chem. Rev. 2001, 101:1881-1896.
27. 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.
28. 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.
29. Roberts M.R., Hendrickson A., McGuire C.R., Reh T.A. Retinoid X receptor (gamma) is necessary to establish the S-opsin gradient in cone photoreceptors of the developing mouse retina. Invest. Ophthalmol. Vis. Sci. 2005, 46:2897-2904.
30. Rohlich P., van Veen T., Szel A. Two different visual pigments in one retinal cone cell. Neuron 1994, 13:1159-1166.
31. -/- mice: a defect that can be corrected by 11-cis retinal. Invest. Ophthalmol. Vis. Sci. 2005, 46:3876-3882.
32. Seeliger M.W., Grimm C., Stahlberg F., Friedburg C., Jaissle G., Zrenner E., Guo H., Reme C.E., Humphries P., Hofmann F., Biel M., Fariss R.N., Redmond T.M., Wenzel A. New views on RPE65 deficiency: the rod system is the source of vision in a mouse model of Leber congenital amaurosis. Nat. Genet. 2001, 29:70-74.
33. Simpson D.A., Feeney S., Boyle C., Stitt A.W. Retinal VEGF mRNA measured by SYBR green I fluorescence: a versatile approach to quantitative PCR. Mol. Vis. 2000, 6:178-183.
34. St Jules R.S., Wallingford J.C., Smith S.B., O'Brien P.J. Addition of the chromophore to rat rhodopsin is an early post-translational event. Exp. Eye Res. 1989, 48:653-665.
35. Stephenson R.S., O'Tousa J., Scavarda N.J., Randall L.L., Pak W.L. Drosophila mutants with reduced rhodopsin content. Symp. Soc. Exp. Biol. 1983, 36:477-501.
36. Thompson D.A., Gyurus P., Fleischer L.L., Bingham E.L., McHenry C.L., Apfelstedt-Sylla E., Zrenner E., Lorenz B., Richards J.E., Jacobson S.G., Sieving P.A., Gal A. Genetics and phenotypes of RPE65 mutations in inherited retinal degeneration. Invest. Ophthalmol. Vis. Sci. 2000, 41:4293-4299.
37. Thompson D.A., Li Y., McHenry C.L., Carlson T.J., Ding X., Sieving P.A., Apfelstedt-Sylla E., Gal A. Mutations in the gene encoding lecithin retinol acyltransferase are associated with early-onset severe retinal dystrophy. Nat. Genet. 2001, 28:123-124.
38. Thompson D.A., Gal A. Genetic defects in vitamin A metabolism of the retinal pigment epithelium. Dev. Ophthalmol. 2003, 37:141-154.
39. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. U.S.A. 1979, 76:4350-4354.
40. de Urquiza A.M., Liu S., Sjoberg M., Zetterstrom R.H., Griffiths W., Sjovall J., Perlmann T. Docosahexaenoic acid, a ligand for the retinoid X receptor in mouse brain. Science 2000, 290:2140-2144.
41. Van Hooser J.P., Liang Y., Maeda T., Kuksa V., Jang G.F., He Y.G., Rieke F., Fong H.K., Detwiler P.B., Palczewski K. Recovery of visual functions in a mouse model of Leber congenital amaurosis. J. Biol. Chem. 2002, 277:19173-19182.
42. Wald G. The molecular basis of visual excitation. Nature 1968, 219:800-807.
43. +/- retinas are protected against light damage-mediated stress. Invest. Ophthalmol. Vis. Sci. 2007, 48:2877-2886.
44. 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.
45. Znoiko S.L., Crouch R.K., Moiseyev G., Ma J.X. Identification of the RPE65 protein in mammalian cone photoreceptors. Invest. Ophthalmol. Vis. Sci. 2002, 43:1604-1609.
46. -/- mouse at early ages. Invest. Ophthalmol. Vis. Sci. 2005, 46:1473-1479.