Diacylglycerol O-acyltransferase type-1 synthesizes retinyl esters in the retina and retinal pigment epithelium

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Kaylor, Joanna J ^a   Radu, Roxana A ^a   Bischoff, Nicholas ^a   Makshanoff, Jacob ^a   Hu, Jane ^a   Lloyd, Marcia ^a   Eddington, Shannan ^a   Bianconi, Tran ^a   Bok, Dean ^a,b   Travis, Gabriel H ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIACYLGLYCEROL ACYLTRANSFERASE 1; OPSIN; PALMITOYL COENZYME A; PHOSPHATIDYLCHOLINE; RETINOL ACYLTRANSFERASE; RETINOL ESTER; VISUAL PIGMENT; ACYLTRANSFERASE; CIS TRANS ISOMERASE; DIACYLGLYCEROL ACYLTRANSFERASE; ESTER; LECITHIN-RETINOL ACYLTRANSFERASE; RETINAL; RETINOID ISOMEROHYDROLASE; RETINOL;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLEACHING; CATALYSIS; CHROMATOPHORE; CONTROLLED STUDY; ENZYME KINETICS; GLIA CELL; HOMOGENATE; MOUSE; NONHUMAN; PHOTORECEPTOR OUTER SEGMENT; PIGMENT EPITHELIUM; PROTEIN ANALYSIS; RETINA; VISION; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELL CULTURE; CYTOLOGY; GENE DELETION; GENETICS; METABOLISM; RETINAL PIGMENT EPITHELIUM; ULTRASTRUCTURE;

MUS;

ACYLTRANSFERASES; ANIMALS; CELLS, CULTURED; CIS-TRANS-ISOMERASES; DIACYLGLYCEROL O-ACYLTRANSFERASE; ESTERS; GENE DELETION; MICE, INBRED BALB C; MICE, INBRED C57BL; PALMITOYL COENZYME A; RETINA; RETINAL PIGMENT EPITHELIUM; RETINALDEHYDE; VITAMIN A;

EID: 84929340313     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0125921     Document Type: Article

References (36)

1. Mata NL, Radu RA, Clemmons R, Travis GH. Isomerization and oxidation of vitamin a in cone-dominant retinas. A novel pathway for visual-pigment regeneration in daylight. Neuron. 2002; 36(1): 69-80. PMID: 12367507
2. Wang JS, Kefalov VJ. An alternative pathway mediates the mouse and human cone visual cycle. Curr Biol. 2009; 19(19): 1665-9. doi: 10.1016/j.cub.2009.07.054 PMID: 19781940
3. Kaylor JJ, Yuan Q, Cook J, Sarfare S, Makshanoff J, Miu A, et al. Identification of DES1 as a vitamin A isomerase in Müller glial cells of the retina. Nature Chemical Biology. 2013; 9(1): 30-6. doi: 10.1038/nchembio.1114 PMID: 23143414
4. Jin M, Li S, Moghrabi WN, Sun H, Travis GH. Rpe65 is the retinoid isomerase in bovine retinal pigment epithelium. Cell. 2005; 122(3): 449-59. PMID: 16096063
5. Redmond TM, Poliakov E, Yu S, Tsai JY, 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(38): 13658-63. PMID: 16150724
6. Moiseyev G, Chen Y, Takahashi Y, Wu BX, Ma JX. RPE65 is the isomerohydrolase in the retinoid visual cycle. Proc Natl Acad Sci U S A. 2005; 102(35): 12413-8. PMID: 16116091
7. Gollapalli DR, Rando RR. All-trans-retinyl esters are the substrates for isomerization in the vertebrate visual cycle. Biochemistry. 2003; 42: 5809-18. PMID: 12741839
8. Mata NL, Moghrabi WN, Lee JS, Bui TV, Radu RA, Horwitz J, et al. Rpe65 is a retinyl ester binding protein that presents insoluble substrate to the isomerase in retinal pigment epithelial cells. J Biol Chem. 2004; 279(1): 635-43. PMID: 14532273
9. Deigner PS, Law WC, Canada FJ, Rando RR. Membranes as the energy source in the endergonic transformation of vitamin A to 11-cis-retinol. Science. 1989; 244(4907): 968-71. PMID: 2727688
10. Rodriguez KA, Tsin AT. Retinyl esters in the vertebrate neuroretina. American Journal of Physiology. 1989; 256(1 Pt 2): R255-8. PMID: 2783537
11. Barry RJ, Canada FJ, Rando RR. Solubilization and partial purification of retinyl ester synthetase and retinoid isomerase from bovine ocular pigment epithelium. Journal of Biological Chemistry. 1989; 264(16): 9231-8. PMID: 2722827
12. Saari JC, Bredberg DL. Lecithin:retinol acyltransferase in retinal pigment epithelial microsomes. Journal of Biological Chemistry. 1989; 264(15): 8636-40. PMID: 2722792
13. Kaschula CH, Jin MH, Desmond-Smith NS, Travis GH. Acyl CoA:retinol acyltransferase (ARAT) activity is present in bovine retinal pigment epithelium. Exp Eye Res. 2006; 82(1): 111-21. PMID: 16054134
14. Mata NL, Ruiz A, Radu RA, Bui TV, Travis GH. Chicken retinas contain a retinoid isomerase activity that catalyzes the direct conversion of all-trans-retinol to 11-cis-retinol. Biochemistry. 2005; 44(35): 11715-21. PMID: 16128572
15. Muniz A, Villazana-Espinoza ET, Hatch AL, Trevino SG, Allen DM, Tsin AT. A novel cone visual cycle in the cone-dominated retina. Exp Eye Res. 2007; 85(2): 175-84. PMID: 17618621
16. Kaylor JJ, Cook JD, Makshanoff J, Bischoff N, Yong J, Travis GH. Identification of the 11-cis-specific retinyl-ester synthase in retinal Muller cells as multifunctional O-acyltransferase (MFAT). Proc Natl Acad Sci U S A. 2014.
17. Yen CL, Monetti M, Burri BJ, Farese RV Jr. The triacylglycerol synthesis enzyme DGAT1 also catalyzes the synthesis of diacylglycerols, waxes, and retinyl esters. J Lipid Res. 2005; 46(7): 1502-11. PMID: 15834126
18. Wongsiriroj N, Piantedosi R, Palczewski K, Goldberg IJ, Johnston TP, Li E, et al. The molecular basis of retinoid absorption: a genetic dissection. J Biol Chem. 2008; 283(20): 13510-9. doi: 10.1074/jbc.M800777200 PMID: 18348983
19. Cases S, Smith SJ, Zheng YW, Myers HM, Lear SR, Sande E, et al. Identification of a gene encoding an acyl CoA:diacylglycerol acyltransferase, a key enzyme in triacylglycerol synthesis. Proc Natl Acad Sci U S A. 1998; 95(22): 13018-23. PMID: 9789033
20. Ruiz A, Ghyselinck NB, Mata N, Nusinowitz S, Lloyd M, Dennefeld C, et al. Somatic ablation of the LRAT gene in the mouse retinal pigment epithelium drastically reduces its retinoid storage. Invest Ophthalmol Vis Sci. 2007; 48(12): 5377-87. PMID: 18055784
21. Liu Q, Siloto RM, Lehner R, Stone SJ, Weselake RJ. Acyl-CoA:diacylglycerol acyltransferase: molecular biology, biochemistry and biotechnology. Progress in Lipid Research. 2012; 51(4): 350-77. doi: 10.1016/j.plipres.2012.06.001 PMID: 22705711
22. Leenheer APd, Lambert WE, Van Bocxlaer JF. Modern chromatographic analysis of vitamins. 3rd ed. New York: Marcel Dekker; 2000. ix, 616 p. p.
23. Das SR, Bhardwaj N, Kjeldbye H, Gouras P. Muller cells of chicken retina synthesize 11-cis-retinol. Biochemical Journal. 1992; 285(Pt 3): 907-13. PMID: 1497628
24. Smith SJ, Cases S, Jensen DR, Chen HC, Sande E, Tow B, et al. Obesity resistance and multiple mechanisms of triglyceride synthesis in mice lacking DGAT. Nat Genet. 2000; 25(1): 87-90. PMID: 10802663
25. O'Byrne SM, Wongsiriroj N, Libien J, Vogel S, Goldberg IJ, Baehr W, et al. Retinoid absorption and storage is impaired in mice lacking lecithin:retinol acyltransferase (LRAT). J Biol Chem. 2005; 280(42): 35647-57. PMID: 16115871
26. Radu RA, Yuan Q, Hu J, Peng JH, Lloyd M, Nusinowitz S, et al. Accelerated accumulation of lipofuscin pigments in the RPE of a mouse model for ABCA4-mediated retinal dystrophies following Vitamin A supplementation. Invest Ophthalmol Vis Sci. 2008; 49(9): 3821-9. doi: 10.1167/iovs.07-1470 PMID: 18515570
27. Bunt-Milam AH, Saari JC. Immunocytochemical localization of two retinoid-binding proteins in vertebrate retina. Journal of Cell Biology. 1983; 97(3): 703-12. PMID: 6350319
28. Wakakura M, Foulds WS. Immunocytochemical characteristics of Müller cells cultured from adult rabbit retina. Invest Ophthalmol Vis Sci. 1988; 29(6): 892-900. PMID: 3131264
29. Kawaguchi R, Yu J, Ter-Stepanian M, Zhong M, Cheng G, Yuan Q, et al. Receptor-mediated cellular uptake mechanism that couples to intracellular storage. ACS Chemical Biology. 2011; 6(10): 1041-51. doi: 10.1021/cb200178w PMID: 21774515
30. Radu RA, Han Y, Bui TV, Nusinowitz S, Bok D, Lichter J, et al. Reductions in serum vitamin A arrest accumulation of toxic retinal fluorophores: a potential therapy for treatment of lipofuscin-based retinal diseases. Invest Ophthalmol Vis Sci. 2005; 46(12): 4393-401. PMID: 16303925
31. Bok D, Ruiz A, Yaron O, Jahng WJ, Ray A, Xue L, et al. Purification and characterization of a transmembrane domain-deleted form of lecithin retinol acyltransferase. Biochemistry. 2003; 42(20): 6090-8. PMID: 12755610
32. Weng J, Mata NL, Azarian SM, Tzekov RT, Birch DG, Travis GH. Insights into the function of Rim protein in photoreceptors and etiology of Stargardt's disease from the phenotype in ABCR knockout mice. Cell. 1999; 98(1): 13-23. PMID: 10412977
33. Jin M, Li S, Nusinowitz S, Lloyd M, Hu J, Radu RA, et al. The role of interphotoreceptor retinoid-binding protein on the translocation of visual retinoids and function of cone photoreceptors. J Neurosci. 2009; 29(5): 1486-95. doi: 10.1523/JNEUROSCI.3882-08.2009 PMID: 19193895
34. Imanishi Y, Batten ML, Piston DW, Baehr W, Palczewski K. Noninvasive two-photon imaging reveals retinyl ester storage structures in the eye. J Cell Biol. 2004; 164(3): 373-83. PMID: 14745001
35. Tsilou E, Hamel CP, Yu S, Redmond TM. RPE65, the major retinal pigment epithelium microsomal membrane protein, associates with phospholipid liposomes. Archives of Biochemistry & Biophysics. 1997; 346(1): 21-7.
36. DeVita RJ, Pinto S. Current status of the research and development of diacylglycerol O-acyltransferase 1 (DGAT1) inhibitors. Journal of Medicinal Chemistry. 2013; 56(24): 9820-5. doi: 10.1021/jm4007033 PMID: 23919406