Purified RPE65 shows isomerohydrolase activity after reassociation with a phospholipid membrane

FEBS Journal

Volumn 276, Issue 11, 2009, Pages 3020-3030

  Nikolaeva, Olga ^a   Takahashi, Yusuke ^a   Moiseyev, Gennadiy ^a   Ma, Jian Xing ^a  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

Author keywords

Isomerohydrolase; Liposome; Retina; Retinyl ester; RPE65

Indexed keywords

HYDROLASE; LIPOSOME; PROTEIN RPE 65; RETINOID DERIVATIVE; RETINOID ISOMEROHYDROLASE; RETINOL ESTER; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CELL CULTURE; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME MECHANISM; ENZYME PURIFICATION; KINETICS; PHOSPHOLIPID MEMBRANE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION;

ANIMALS; BLOTTING, WESTERN; CELL LINE; CHICKENS; CHROMATOGRAPHY, AFFINITY; CIS-TRANS-ISOMERASES; EYE PROTEINS; HUMANS; KINETICS; LIPID BILAYERS; LIPOSOMES; PHOSPHOLIPIDS; RECOMBINANT PROTEINS; VITAMIN A;

EID: 65549131951     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07021.x     Document Type: Article

References (38)

1. Baylor D (1996) How photons start vision. Proc Natl Acad Sci USA 93, 560 565. (Pubitemid 26041128)
2. McBee JK, Palczewski K, Baehr W Pepperberg DR (2001) Confronting complexity: the interlink of phototransduction and retinoid metabolism in the vertebrate retina. Prog Retin Eye Res 20, 469 529. (Pubitemid 32523896)
3. Lamb TD Pugh EN Jr. (2004) Dark adaptation and the retinoid cycle of vision. Prog Retin Eye Res 23, 307 380. (Pubitemid 38737131)
4. Saari JC (2000) Biochemistry of visual pigment regeneration: the Friedenwald lecture. Invest Ophthalmol Vis Sci 41, 337 348. (Pubitemid 30080432)
5. Rando RR (2001) The biochemistry of the visual cycle. Chem Rev 101, 1881 1896. (Pubitemid 35377790)
6. Rattner A, Smallwood PM 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. (Pubitemid 30212743)
7. Saari JC Bredberg DL (1989) Lecithin:retinol acyltransferase in retinal pigment epithelial microsomes. J Biol Chem 264, 8636 8640. (Pubitemid 19151579)
8. Rando RR (1991) Membrane phospholipids as an energy source in the operation of the visual cycle. Biochemistry 30, 595 602.
9. Deigner PS, Law WC, Canada FJ Rando RR (1989) Membranes as the energy source in the endergonic transformation of vitamin A to 11-cis-retinol. Science 244, 968 971. (Pubitemid 19152285)
10. Hamel CP, Tsilou E, Pfeffer BA, Hooks JJ, Detrick B Redmond TM (1993) Molecular cloning and expression of RPE65, a novel retinal pigment epithelium-specific microsomal protein that is post-transcriptionally regulated in vitro. J Biol Chem 268, 15751 15757. (Pubitemid 23222076)
11. Ma J, Zhang J, Othersen KL, Moiseyev G, Ablonczy Z, Redmond TM, Chen Y Crouch RK (2001) Expression, purification, and MALDI analysis of RPE65. Invest Ophthalmol Vis Sci 42, 1429 1435. (Pubitemid 32520730)
12. Takahashi Y, Moiseyev G, Ablonczy Z, Chen Y, Crouch RK Ma JX (2009) Identification of a novel palmitylation site essential for membrane association and isomerohydrolase activity of RPE65. J Biol Chem 284, 3211 3218.
13. Redmond TM, Yu S, Lee E, Bok D, Hamasaki D, Chen N, Goletz P, Ma JX, Crouch RK Pfeifer K (1998) Rpe65 is necessary for production of 11-cis-vitamin A in the retinal visual cycle. Nat Genet 20, 344 351. (Pubitemid 28541631)
14. Thompson DA Gal A (2003) Genetic defects in vitamin A metabolism of the retinal pigment epithelium. Dev Ophthalmol 37, 141 154.
15. Thompson DA, Gyurus P, Fleischer LL, Bingham EL, McHenry CL, Apfelstedt-Sylla E, Zrenner E, Lorenz B, Richards JE, Jacobson SG et al. (2000) Genetics and phenotypes of RPE65 mutations in inherited retinal degeneration. Invest Ophthalmol Vis Sci 41, 4293 4299.
16. Jin M, Li S, Moghrabi WN, Sun H Travis GH (2005) Rpe65 is the retinoid isomerase in bovine retinal pigment epithelium. Cell 122, 449 459. (Pubitemid 41127145)
17. Moiseyev G, Chen Y, Takahashi Y, Wu BX Ma JX (2005) RPE65 is the isomerohydrolase in the retinoid visual cycle. Proc Natl Acad Sci USA 102, 12413 12418. (Pubitemid 41266373)
18. Redmond TM, Poliakov E, Yu S, Tsai JY, 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, 13658 13663. (Pubitemid 41420904)
19. Xue L, Jahng WJ, Gollapalli D Rando RR (2006) Palmitoyl transferase activity of lecithin retinol acyl transferase. Biochemistry 45, 10710 10718. (Pubitemid 44320486)
20. Mata NL, Moghrabi WN, Lee JS, Bui TV, Radu RA, Horwitz J Travis GH (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. (Pubitemid 38044868)
21. Gollapalli DR, Maiti P Rando RR (2003) RPE65 operates in the vertebrate visual cycle by stereospecifically binding all-trans-retinyl esters. Biochemistry 42, 11824 11830. (Pubitemid 37243643)
22. Moiseyev G, Takahashi Y, Chen Y, Kim S Ma JX (2008) RPE65 from cone-dominant chicken is a more efficient isomerohydrolase compared with that from rod-dominant species. J Biol Chem 283, 8110 8117.
23. Yethon JA, Epand RF, Leber B, Epand RM Andrews DW (2003) Interaction with a membrane surface triggers a reversible conformational change in Bax normally associated with induction of apoptosis. J Biol Chem 278, 48935 48941.
24. Moiseyev G, Crouch RK, Goletz P, Oatis J Jr., Redmond TM Ma JX (2003) Retinyl esters are the substrate for isomerohydrolase. Biochemistry 42, 2229 2238. (Pubitemid 36258697)
25. Bernstein PS, Law WC Rando RR (1987) Isomerization of all-trans-retinoids to 11-cis-retinoids in vitro [see comments]. Proc Natl Acad Sci USA 84, 1849 1853. (Pubitemid 17054110)
26. Barry RJ, Canada FJ Rando RR (1989) Solubilization and partial purification of retinyl ester synthetase and retinoid isomerase from bovine ocular pigment epithelium. J Biol Chem 264, 9231 9238. (Pubitemid 19157558)
27. McBee JK, Kuksa V, Alvarez R, de Lera AR, Prezhdo O, Haeseleer F, Sokal I Palczewski K (2000) Isomerization of all-trans-retinol to cis-retinols in bovine retinal pigment epithelial cells: dependence on the specificity of retinoid-binding proteins. Biochemistry 39, 11370 11380.
28. Huang WC, Westlake AC, Marechal JD, Joyce MG, Moody PC Roberts GC (2007) Filling a hole in cytochrome P450 BM3 improves substrate binding and catalytic efficiency. J Mol Biol 373, 633 651. (Pubitemid 47488398)
29. Ho MT, Pownall HJ Hollyfield JG (1989) Spontaneous transfer of retinoic acid, retinyl acetate, and retinyl palmitate between single unilamellar vesicles. J Biol Chem 264, 17759 17763. (Pubitemid 19279238)
30. Imanishi Y, Batten ML, Piston DW, Baehr W Palczewski K (2004) Noninvasive two-photon imaging reveals retinyl ester storage structures in the eye. J Cell Biol 164, 373 383. (Pubitemid 38174765)
31. Tsilou E, Hamel CP, Yu S Redmond TM (1997) RPE65, the major retinal pigment epithelium microsomal membrane protein, associates with phospholipid liposomes. Arch Biochem Biophys 346, 21 27. (Pubitemid 27415291)
32. Xue L, Gollapalli DR, Maiti P, Jahng WJ Rando RR (2004) A palmitoylation switch mechanism in the regulation of the visual cycle. Cell 117, 761 771. (Pubitemid 38748892)
33. Trudel E, Beaufils S, Renault A, Breton R Salesse C (2006) Binding of RPE65 fragments to lipid monolayers and identification of its partners by glutathione S-transferase pull-down assays. Biochemistry 45, 3337 3347. (Pubitemid 43376352)
34. Jin M, Yuan Q, Li S Travis GH (2007) Role of LRAT on the retinoid isomerase activity and membrane association of Rpe65. J Biol Chem 282, 20915 20924. (Pubitemid 47099920)
35. Takahashi Y, Moiseyev G, Chen Y Ma JX (2005) Identification of conserved histidines and glutamic acid as key residues for isomerohydrolase activity of RPE65, an enzyme of the visual cycle in the retinal pigment epithelium. FEBS Lett 579, 5414 5418. (Pubitemid 41395164)
36. Bok D, Ruiz A, Yaron O, Jahng WJ, Ray A, Xue L Rando RR (2003) Purification and characterization of a transmembrane domain-deleted form of lecithin retinol acyltransferase. Biochemistry 42, 6090 6098. (Pubitemid 36608916)
37. Lindqvist A Andersson S (2002) Biochemical properties of purified recombinant human beta-carotene 15,15′-monooxygenase. J Biol Chem 277, 23942 23948.
38. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248 254.