Retinoid uptake, processing, and secretion in human iPSRPE support the visual cycle

Investigative Ophthalmology and Visual Science

Volumn 55, Issue 1, 2014, Pages 198-209

  Muñiz, Alberto ^a   Greene, Whitney A ^a   Plamper, Mark L ^a   Choi, Jae Hyek ^a   Johnson, Anthony J ^a   Tsin, Andrew T ^b   Wang, Heuy Ching ^a  

^a US ARMY INSTITUTE OF SURGICAL RESEARCH   (United States)

^b UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

Author keywords

Induced pluripotent stem cell; Retinal pigment epithelium; Visual cycle

Indexed keywords

EID: 84892593045     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.13-11740     Document Type: Article

References (68)

1. La Cour M, Tezel T. The retinal pigment epithelium. Adv Organ Biol. 2006;10:253-273.
2. Dowling JE. Chemistry of visual adaptation in the rat. Nature. 1960;188:114-118.
3. McBee JK, Palczewski K, Baehr W, Pepperberg DR. Confronting complexity: the interlink of phototransduction and retinoid metabolism in the vertebrate retina. Prog Retin Eye Res. 2001;20:469-529.
4. Zimmerman WF. The distribution and proportions of vitamin A compounds during the visual cycle in the rat. Vision Res. 1974;14:795-802.
5. Saari JC, Bredberg DL. Lecithin: retinol acyltransferase in retinal pigment epithelial microsomes. J Biol Chem. 1989;264: 8636-8640.
6. Saari JC, Bredberg DL. CoA-and non-CoA-dependent retinol esterification in retinal pigment epithelium. J Biol Chem. 1988;263:8084-8090.
7. Saari JC, Bredberg DL, Farrell DF. Retinol esterification in bovine retinal pigment epithelium: reversibility of lecithin: retinol acyltransferase. Biochem J. 1993;291(pt 3):697-700.
8. Ruiz A, Winston A, Lim YH, Gilbert BA, Rando RR, Bok D. Molecular and biochemical characterization of lecithin retinol acyltransferase. J Biol Chem. 1999;274:3834-3841.
9. Mondal MS, Ruiz A, Bok D, Rando RR. Lecithin retinol acyltransferase contains cysteine residues essential for catalysis. Biochemistry. 2000;39:5215-5220.
10. 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;102:12413-12418.
11. Jin M, Li S, Moghrabi WN, Sun H, Travis GH. Rpe65 is the retinoid isomerase in bovine retinal pigment epithelium. Cell. 2005;122:449-459.
12. 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;102:13658-13663.
13. Lion F, Rotmans JP, Daemen FJ, Bonting SL. Biochemical aspects of the visual process. XXVII. Stereospecificity of ocular retinol dehydrogenases and the visual cycle. Biochim Biophys Acta. 1975;384:283-292.
14. Zimmerman WF, Lion F, Daemen FJ, Bonting SL. Biochemical aspects of the visual process. XXX. Distribution of stereospecific retinol dehydrogenase activities in subcellular fractions of bovine retina and pigment epithelium. Exp Eye Res. 1975;21: 325-332.
15. Rattner A, Smallwood PM, Nathans J. 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. 2000; 275:11034-11043.
16. Suzuki Y, Ishiguro S, Tamai M. Identification and immunohistochemistry of retinol dehydrogenase from bovine retinal pigment epithelium. Biochim Biophys Acta. 1993;1163:201-208.
17. Gamble MV, Mata NL, Tsin AT, Mertz JR, Blaner WS. Substrate specificities and 13-cis-retinoic acid inhibition of human, mouse and bovine cis-retinol dehydrogenases. Biochim Biophys Acta. 2000;1476:3-8.
18. Jang GF, McBee JK, Alekseev AM, Haeseleer F, Palczewski K. Stereoisomeric specificity of the retinoid cycle in the vertebrate retina. J Biol Chem. 2000;275:28128-28138.
19. 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;85:175-184.
20. Pepperberg DR, Clack JW. Rhodopsin photoproducts and the visual response of vertebrate rods. Vision Res. 1984;24:1481-1486.
21. Bok D. Retinal photoreceptor-pigment epithelium interactions. Friedenwald lecture. Invest Ophthalmol Vis Sci. 1985; 26:1659-1694.
22. Congdon N, O'Colmain B, Klaver CC, et al. Causes and prevalence of visual impairment among adults in the United States. Arch Ophthalmol. 2004;122:477-485.
23. Coleman HR, Chan CC, Ferris FL III, Chew EY. Age-related macular degeneration. Lancet. 2008;372:1835-1845.
24. Cremers FP, van den Hurk JA, den Hollander AI. Molecular genetics of Leber congenital amaurosis. Hum Mol Genet. 2002;11:1169-1176.
25. Dev Borman A, Ocaka LA, Mackay DS, et al. Early onset retinal dystrophy due to mutations in LRAT-molecular analysis and detailed phenotypic study. Invest Ophthalmol Vis Sci. 2012; 53:3927-3938.
26. Wang HC, Brown J, Alayon H, Stuck BE. Transplantation of quantum dot-labelled bone marrow-derived stem cells into the vitreous of mice with laser-induced retinal injury: survival, integration and differentiation. Vision Res. 2010;50:665-673.
27. Organisciak DT, Vaughan DK. Retinal light damage: mechanisms and protection. Prog Retin Eye Res. 2010;29:113-134.
28. Youssef PN, Sheibani N, Albert DM. Retinal light toxicity. Eye (Lond). 2011;25:1-14.
29. Blanch RJ, Ahmed Z, Berry M, Scott RA, Logan A. Animal models of retinal injury. Invest Ophthalmol Vis Sci. 2012;53: 2913-2920.
30. Yu J, Vodyanik MA, Smuga-Otto K, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science. 2007;318:1917-1920.
31. Takahashi K, Tanabe K, Ohnuki M, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 2007;131:861-872.
32. Klimanskaya I, Hipp J, Rezai KA, West M, Atala A, Lanza R. Derivation and comparative assessment of retinal pigment epithelium from human embryonic stem cells using transcriptomics. Cloning Stem Cells. 2004;6:217-245.
33. Hirami Y, Osakada F, Takahashi K, et al. Generation of retinal cells from mouse and human induced pluripotent stem cells. Neurosci Lett. 2009;458:126-131.
34. Buchholz DE, Hikita ST, Rowland TJ, et al. Derivation of functional retinal pigmented epithelium from induced pluripotent stem cells. Stem Cells. 2009;27:2427-2434.
35. Carr AJ, Vugler AA, Hikita ST, et al. Protective effects of human iPS-derived retinal pigment epithelium cell transplantation in the retinal dystrophic rat. PLoS One. 2009;4:e8152.
36. Schwartz SD, Hubschman JP, Heilwell G, et al. Embryonic stem cell trials for macular degeneration: a preliminary report. Lancet. 2012;379:713-720.
37. Siqueira RC, Messias A, Voltarelli JC, Scott IU, Jorge R. Intravitreal injection of autologous bone marrow-derived mononuclear cells for hereditary retinal dystrophy: a phase I trial. Retina. 2011;31:1207-1214.
38. Siqueira RC. Stem cell therapy for retinal diseases: update. Stem Cell Res Ther. 2011;2:50.
39. Maminishkis A, Chen S, Jalickee S, et al. Confluent monolayers of cultured human fetal retinal pigment epithelium exhibit morphology and physiology of native tissue. Invest Ophthalmol Vis Sci. 2006;47:3612-3624.
40. Noll GN. High-performance liquid chromatographic analysis of retinal and retinol isomers. J Chromatogr A. 1996;721:247-259.
41. Garwin GG, Saari JC. High-performance liquid chromatography analysis of visual cycle retinoids. Methods Enzymol. 2000; 316:313-324.
42. Stecher H, Palczewski K. Multienzyme analysis of visual cycle. Methods Enzymol. 2000;316:330-344.
43. MacDonald PN, Ong DE. Assay of lecithin-retinol acyltransferase. Methods Enzymol. 1990;189:450-459.
44. Aronson JF. Human retinal pigment cell culture. In Vitro. 1983;19:642-650.
45. Klaassen I, Brakenhoff RH, Smeets SJ, Snow GB, Braakhuis BJ. Considerations for in vitro retinoid experiments: importance of protein interaction. Biochim Biophys Acta. 1999;1427: 265-275.
46. Belatik A, Hotchandani S, Bariyanga J, Tajmir-Riahi HA. Binding sites of retinol and retinoic acid with serum albumins. Eur J Med Chem. 2012;48:114-123.
47. 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;82:111-121.
48. Mata NL, Radu RA, Clemmons RC, Travis GH. Isomerization and oxidation of vitamin a in cone-dominant retinas: a novel pathway for visual-pigment regeneration in daylight. Neuron. 2002;36:69-80.
49. Honig B, Ebrey TG. The structure and spectra of the chromophore of the visual pigments. Annu Rev Biophys Bioeng. 1974;3:151-177.
50. Sperling W, Rafferty CN. Relationship between absorption spectrum and molecular conformations of 11-cis-retinal. Nature. 1969;224:590-594.
51. Langer H. Chapter title. In: Langer H, ed. Biochemistry and Physiology of Visual Pigments. New York, NY: SpringerVerlag; 1973:19-28.
52. Vaajasaari H, Ilmarinen T, Juuti-Uusitalo K, et al. Toward the defined and xeno-free differentiation of functional human pluripotent stem cell-derived retinal pigment epithelial cells. Mol Vis. 2011;17:558-575.
53. Flood MT, Bridges CD, Alvarez RA, Blaner WS, Gouras P. Vitamin A utilization in human retinal pigment epithelial cells in vitro. Invest Ophthalmol Vis Sci. 1983;24:1227-1235.
54. Hamel CP, Tsilou E, Harris E, et al. A developmentally regulated microsomal protein specific for the pigment epithelium of the vertebrate retina. J Neurosci Res. 1993;34: 414-425.
55. Redmond MT, Hamel CP. Genetic analysis of RPE65: from human disease to mouse model. Methods Enzymol. 2000;316: 705-724.
56. Hamel CP, Tsilou E, Pfeffer BA, Hooks JJ, Detrick B, Redmond TM. 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.
57. Blomhoff R, Rasmussen M, Nilsson A, et al. Hepatic retinol metabolism: distribution of retinoids, enzymes, and binding proteins in isolated rat liver cells. J Biol Chem. 1985;260: 13560-13565.
58. Helgerud P, Petersen LB, Norum KR. Acyl CoA: retinol acyltransferase in rat small intestine: its activity and some properties of the enzymic reaction. J Lipid Res. 1982;23:609-618.
59. Randolph RK, Winkler KE, Ross AC. Fatty acyl CoA-dependent and-independent retinol esterification by rat liver and lactating mammary gland microsomes. Arch Biochem Biophys. 1991;288:500-508.
60. Torma H, Vahlquist A. Retinol esterification by mouse epidermal microsomes: evidence for acyl-CoA: retinol acyltransferase activity. J Invest Dermatol. 1987;88:398-402.
61. Gollapalli DR, Rando RR. All-trans-retinyl esters are the substrates for isomerization in the vertebrate visual cycle. Biochemistry. 2003;42:5809-5818.
62. Bridges CD, Alvarez RA, Fong SL. Vitamin A in human eyes: amount, distribution, and composition. Invest Ophthalmol Vis Sci. 1982;22:706-714.
63. Saari JC, Bredberg DL. Acyl-CoA: retinol acyltransferase and lecithin: retinol acyltransferase activities of bovine retinal pigment epithelial microsomes. Methods Enzymol. 1990;190: 156-163.
64. MacDonald PN, Ong DE. A lecithin: retinol acyltransferase activity in human and rat liver. Biochem Biophys Res Commun. 1988;156:157-163.
65. MacDonald PN, Ong DE. Evidence for a lecithin-retinol acyltransferase activity in the rat small intestine. J Biol Chem. 1988;263:12478-12482.
66. Muniz A, Villazana-Espinoza ET, Thackeray B, Tsin AT. 11-cis-Acyl-CoA: retinol O-acyltransferase activity in the primary culture of chicken Muller cells. Biochemistry. 2006;45:12265-12273.
67. Hu J, Bok D. Culture of highly differentiated human retinal pigment epithelium for analysis of the polarized uptake, processing, and secretion of retinoids. Methods Mol Biol. 2010;652:55-73.
68. Flannery JG, O'Day W, Pfeffer BA, Horwitz J, Bok D. Uptake, processing and release of retinoids by cultured human retinal pigment epithelium. Exp Eye Res. 1990;51:717-728.