ATP-binding cassette transporter ABCA4: Molecular properties and role in vision and macular degeneration (original) (raw)
Ahn J, Wong JT, Molday RS (2000) The effect of lipid environment and retinoids on the ATPase activity of ABCR, the photoreceptor ABC transporter responsible for Stargardt macular dystrophy. J Biol Chem 275:20399–20405 ArticleCAS Google Scholar
Ahn J, Beharry S, Molday LL, Molday RS (2003) Functional interaction between the two halves of the photoreceptor-specific ATP binding cassette protein ABCR (ABCA4). Evidence for a non-exchangeable ADP in the first nucleotide binding domain. J Biol Chem 278:39600–39608 ArticleCAS Google Scholar
Akiyama M, Sugiyama-Nakagiri Y, Sakai K, McMillan JR, Goto M, Arita K, Tsuji-Abe Y, Tabata N, Matsuoka K, Sasaki R, Sawamura D, Shimizu H (2005) Mutations in lipid transporter ABCA12 in harlequin ichthyosis and functional recovery by corrective gene transfer. J Clin Invest 115:1777–1784 ArticleCAS Google Scholar
Allikmets R (2000) Simple and complex ABCR: genetic predisposition to retinal disease. Am J Hum Genet 67:793–799 ArticleCAS Google Scholar
Allikmets R, Singh N, Sun H, Shroyer NF, Hutchinson A, Chidambaram A, Gerrard B, Baird L, Stauffer D, Peiffer A, Rattner A, Smallwood P, Li Y, Anderson KL, Lewis RA, Nathans J, Leppert M, Dean M, Lupski JR (1997a) A photoreceptor cell-specific ATP-binding transporter gene (ABCR) is mutated in recessive Stargardt macular dystrophy. Nat Genet 15:236–246 ArticleCAS Google Scholar
Allikmets R, Shroyer NF, Singh N, Seddon JM, Lewis RA, Bernstein PS, Peiffer A, Zabriskie NA, Li Y, Hutchinson A, Dean M, Lupski JR, Leppert M (1997b) Mutation of the Stargardt disease gene (ABCR) in age-related macular degeneration. Science 277:1805–1807 ArticleCAS Google Scholar
Anderson RE, Maude MB (1970) Phospholipids of bovine outer segments. Biochemistry 9:3624–3628 ArticleCAS Google Scholar
Arshavsky VY, Lamb TD, Pugh EN Jr (2002) G proteins and phototransduction. Annu Rev Physiol 64:153–187 ArticleCAS Google Scholar
Azarian SM, Travis GH (1997) The photoreceptor rim protein is an ABC transporter encoded by the gene for recessive Stargardt's disease (ABCR). FEBS Lett 409:247–252 ArticleCAS Google Scholar
Ban N, Matsumura Y, Sakai H, Takanezawa Y, Sasaki M, Arai H, Inagaki N (2007) ABCA3 as a lipid transporter in pulmonary surfactant biogenesis. J Biol Chem 282:9628–9634 ArticleCAS Google Scholar
Beharry S, Zhong M, Molday RS (2004) N-retinylidene-phosphatidylethanolamine is the preferred retinoid substrate for the photoreceptor-specific ABC transporter ABCA4 (ABCR). J Biol Chem 279:53972–53979 ArticleCAS Google Scholar
Ben-Shabat S, Parish CA, Vollmer HR, Itagaki Y, Fishkin N, Nakanishi K, Sparrow JR (2002) Biosynthetic studies of A2E, a major fluorophore of retinal pigment epithelial lipofuscin. J Biol Chem 277:7183–7190 ArticleCAS Google Scholar
Bhongsatiern J, Ohtsuki S, Tachikawa M, Hori S, Terasaki T (2005) Retinal-specific ATP-binding cassette transporter (ABCR/ABCA4) is expressed at the choroid plexus in rat brain. J Neurochem 92:1277–1280 ArticleCAS Google Scholar
Biswas EE (2001) Nucleotide binding domain 1 of the human retinal ABC transporter functions as a general ribonucleotides. Biochemistry 40:8181–8187 ArticleCAS Google Scholar
Biswas EE, Biswas SB (2000) The C-terminal nucleotide binding domain of the human retinal ABCR protein is an adenosine triphosphatase. Biochemistry 39:15879–15886 ArticleCAS Google Scholar
Borst P, Elferink RO (2002) Mammalian ABC transporters in health and disease. Annu Rev Biochem 71:537–592 ArticleCAS Google Scholar
Borst P, Zelcer N, van Helvoort A (2000) ABC transporters in lipid transport. Biochim Biophys Acta 1486:128–144 CAS Google Scholar
Brooks-Wilson A, Marcil M, Clee SM, Zhang LH, Roomp K, van Dam M, Yu L, Brewer C, Collins JA, Molhuizen HO et al (1999) Mutations in ABCI in Tangier disease and familial high-density lipoprotein deficiency. Nat Genet 22:336–345 ArticleCAS Google Scholar
Buczylko J, Saari JC, Crouch RK, Palczewski K (1996) Mechanisms of opsin activation. J Biol Chem 271:20621–20630 ArticleCAS Google Scholar
Bui TV, Han Y, Radu RA, Travis GH, Mata NL (2006) Characterization of native retinal fluorophores involved in biosynthesis of A2E and lipofuscin-associated retinopathies. J Biol Chem 281:18112–18119 ArticleCAS Google Scholar
Bungert S, Molday LL, Molday RS (2001) Membrane topology of the ATP binding cassette transporter ABCR and its relationship to ABCl and related ABCA transporters: identification of N-linked glycosylations sites. J Biol Chem 276:23539–23546 ArticleCAS Google Scholar
Chroni A, Liu T, Fitzgerald ML, Freeman MW, Zannis VI (2004) Cross-linking and lipid efflux properties of apoA-I mutants suggest direct association between apoA-I helices and ABCA1. Biochemistry 43:2126–2139 ArticleCAS Google Scholar
Cremers FP, van de Pol DJ, van Driel M, den Hollander AI, van Haren FJ, Knoers NV, Tijmes N, Bergen AA, Rohrschneider K, Blankenagel A et al (1998) Autosomal recessive retinitis pigmentosa and cone-rod dystrophy caused by splice site mutations in the Stargardt’s disease gene ABCR. Hum Mol Genet 7:355–362 ArticleCAS Google Scholar
Dean M, Allikmets R (2001) Complete characterization of the human ABC gene family. J Bioenerg Biomembr 33:475–479 ArticleCAS Google Scholar
Dean M, Annilo T (2005) Evolution of the ATP-binding cassette (ABC) transporter superfamily in vertebrates. Annu Rev Genomics Hum Genet 6:123–142 ArticleCAS Google Scholar
Delori FC, Staurenghi G, Arend O, Dorey CK, Goger DG, Weiter JJ (1995) In vivo measurement of lipofuscin in Stargardt's disease–Fundus flavimaculatus. Invest Ophthalmol Vis Sci 36:2327–2331 CAS Google Scholar
Eldred GE, Lasky MR (1993) Retinal age pigments generated by self-assembling lysosomotropic detergents. Nature 361:724–726 ArticleCAS Google Scholar
Fishman GA, Farbman JS, Alexander KR (1991) Delayed rod dark adaptation in patients with Stargardt’s disease. Ophthalmology 98:957–962 CAS Google Scholar
Fitzgerald ML, Morris AL, Rhee JS, Andersson LP, Mendez AJ, Freeman MW (2002) Naturally occurring mutations in the largest extracellular loops of ABCAI can disrupt its direct interaction with apolipoprotein A-I. J Biol Chem 277:33178–33187 ArticleCAS Google Scholar
Fitzgerald ML, Okuhira K, Short GF 3rd, Manning JJ, Bell SA, Freeman MW (2004) ATP-binding cassette transporter Al contains a novel C-terminal VFVNFA motif that is required for its cholesterol efflux and ApoA-I binding activities. J Biol Chem 279:48477–48485 ArticleCAS Google Scholar
Fliesler SJ, Anderson RE (1983) Chemistry and metabolism of lipids in the vertebrate retina. Prog Lipid Res 22:79–131 ArticleCAS Google Scholar
Gelisken O, De Laey JJ (1985) A clinical review of Stargardt’s disease and/or fundus flavimaculatus with follow-up. Int Ophthalmol 8:225–235 ArticleCAS Google Scholar
Higgins CF (1992) ABC transporters: from microorganisms to man. Annu Rev Cell Biol 8:67–113 ArticleCAS Google Scholar
Higgins CF, Linton KJ (2004) The ATP switch model for ABC transporters. Nat Struct Mol Biol 11:918–926 ArticleCAS Google Scholar
Holz FG, Schutt F, Kopitz J, Eldred GE, Kruse FE, Volcker HE, Cantz M (1999) Inhibition of lysosomal degradative functions in RPE cells by a retinoid component of lipofuscin. Invest Ophthalmol Vis Sci 40:737–743 CAS Google Scholar
Illing M, Molday LL, Molday RS (1997) The 220-kDa rim protein of retinal rod outer segments is a member of the ABC transporter superfamily. J Biol Chem 272:10303–10310 ArticleCAS Google Scholar
Jang YP, Matsuda H, Itagaki Y, Nakanishi K, Sparrow JR (2005) Characterization of peroxy-A2E and furan-A2E photooxidation products and detection in human and mouse retinal pigment epithelial cell lipofuscin. J Biol Chem 280:39732–39739 ArticleCAS Google Scholar
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 ArticleCAS Google Scholar
Kaminski WE, Piehler A, Wenzel JJ (2006) ABC a-subfamily transporters: structure, function and disease. Biochim Biophys Acta 1762:510–524 CAS Google Scholar
Lamb TD, Pugh EN Jr (2004) Dark adaptation and the retinoid cycle of vision. Prog Retin Eye Res 23:307–380 ArticleCAS Google Scholar
Lamb TD, Pugh EN Jr (2006) Phototransduction, dark adaptation, and rhodopsin regeneration the proctor lecture. Invest Ophthalmol Vis Sci 47:5137–5152 Article Google Scholar
Lefevre C, Audebert S, Jobard F, Bouadjar B, Lakhdar H, Boughdene-Stambouli O, Blanchet-Bardon C, Heilig R, Foglio M, Weissenbach J et al (2003) Mutations in the transporter ABCA12 are associated with lamellar ichthyosis type2. Hum Mol Genet 12:2369–2378 ArticleCAS Google Scholar
Lewis RA, Shroyer NF, Singh N, Allikmets R, Hutchinson A, Li Y, Lupski JR, Leppert M, Dean M (1999) Genotype/Phenotype analysis of a photoreceptor-specific ATP-binding cassette transporter gene, ABCR, in Stargardt disease. Am J Hum Genet 64:422–434 ArticleCAS Google Scholar
Martinez-Mir A, Paloma E, Allikmets R, Ayuso C, del Rio T, Dean M, Vilageliu L, Gonzalez-Duarte R, Balcells S (1998) Retinitis pigmentosa caused by a homozygous mutation in the Stargardt disease gene ABCR. Nat Genet 18:11–12 ArticleCAS Google Scholar
Mata NL, Weng J, Travis GH (2000) Biosynthesis of a major lipofuscin fluorophore in mice and humans with ABCR-mediated retinal and macular deseneration. Proc Natl Acad Sci U S A 97:7154–7159 ArticleCAS Google Scholar
Mata NL, Tzekov RT, Liu X, Weng J, Birch DG, Travis GH (2001) Delayed dark-adaptation and lipofuscin accumulation in abcr+/- mice: implications for involvement of ABCR in age-related macular degeneration. Invest Ophthalmol Vis Sci 42:1685–1690 CAS Google Scholar
Maugeri A, Klevering BJ, Rohrschneider K, Blankenagel A, Brunner HG, Deutman AF, Hoyng CB, Cremers FP (2000) Mutations in the ABCA4 (ABCR) gene are the major cause of autosomal recessive cone-Rod dystrophy. Am J Hum Genet 67:960–966 ArticleCAS Google Scholar
Maugeri A, van Driel MA, van de Pol DJ, Klevering BJ, van Haren FJ, Tijmes N, Bergen AA, Rohrschneider K, Blankenagel A, Pinckers AJ et al (1999) The 2588G–>C mutation in the ABCR gene is a mild frequent founder mutation in the Western European population and allows the classification of ABCR mutations in patients with Stargardt disease. Am J Hum Genet 64:1024–1035 ArticleCAS Google Scholar
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 ArticleCAS Google Scholar
Moiseyev G, Chen Y, Takahashi Y, Wu BX, Ma JX (2005) RPE65 is the isomerohydrolase in the retinoid visual cycle. Proc Natl Acad Sci U S A 102:12413–12418 ArticleCAS Google Scholar
Molday LL, Rabin AR, Molday RS (2000) ABCR expression in foveal cone photoreceptors and its role in Stargardt macular dystrophy. Nat Genet 25:257–258 ArticleCAS Google Scholar
Nasonkin I, Illing M, Koehler MR, Schmid M, Molday RS, Weber BH (1998) Mapping of the rod photoreceptor ABC transporler (ABCR) to 1p2l -p22.1 and identification of novel mutations in Stargardt’s disease. Hum Genet 102:21–26 ArticleCAS Google Scholar
Oram JF (2002) ATP-binding cassette transporter Al and cholesterol trafficking. Curr Opin Lipidol 13:373–381 ArticleCAS Google Scholar
Oswald C, Holland IB, Schmitt L (2006) The motor domains of ABC-transporters. What can structures tell us? Naunyn Schmiedebergs Arch Pharmacol 372:385–399 ArticleCAS Google Scholar
Papermaster DS, Reilly P, Schneider BG (1982) Cone lamellae and red and green rod outer segment disks contain a large intrinsic membrane protein on their margins: an ultrastructural immunocytochemical study of fiog retinas. Vision Res 22:1417–1428 ArticleCAS Google Scholar
Papermaster DS, Schneider BG, Zorn MA, Kraehenbuhl JP (1978) lmmunocytochemical localization of a large intrinsic membrane protein to the incisures and margins of frog rod outer segment disks. J Cell Biol 78:415–425 ArticleCAS Google Scholar
Parish CA, Hashimoto M, Nakanishi K, Dillon J, Sparrow J (1998) Isolation and one-step preparation of A2E and iso-A2E, fluorophores from human retinal pigment epithelium. Proc Natl Acad Sci U S A 95:14609–14613 ArticleCAS Google Scholar
Poincelot RP, Millar PG, Kimbel RL Jr, Abrahamson EW (1969) Lipid to protein chromophore transfer in the photolysis of visual pigments. Nature 221:256–257 ArticleCAS Google Scholar
Radu RA, Mata NL, Bagla A, Travis GH (2004) Light exposure stimulates formation of A2E oxiranes in a mouse model of Starsardt’s macular deseneration. Proc Natl Acad Sci U S A 101:5928–5933 ArticleCAS Google Scholar
Radu RA, Mata NL, Nusinowitz S, Liu X, Sieving PA, Travis GH (2003) Treatment with isotretinoin inhibits lipofuscin accumulation in a mouse model of recessive Stargardt’s macular degeneration. Proc Natl Acad Sci U S A 100:4742–4747 ArticleCAS Google Scholar
Rivera A, White K, Stohr H, Steiner K, Hemmrich N, Grimm T, Jurklies B, Lorenz B, Scholl HP, Apfelstedt-Sylla E, Weber BH (2000) A comprehensive survey of sequence variation in the ABCA4 (ABCR) gene in Stargardt disease and age-related macular degeneration. Am J Hum Genet 67:800–813 ArticleCAS Google Scholar
Rozet JM, Gerber S, Souied E, Ducroq D, Perrault I, Ghazi I, Soubrane G, Coscas G, Dufier JL, Munnich A, Kaplan J (1999) The ABCR gene: a major disease gene in macular and peripheral retinal degenerations with onset from early childhood to the elderly. Mol Genet Metab 68:310–315 ArticleCAS Google Scholar
Rozet JM, Gerber S, Souied E, Perrault I, Chatelin S, Ghazi I, Leowski C, Dufier JL, Munnich A, Kaplan J (1998) Spectrum of ABCR gene mutations in autosomal recessive macular dystrophies. Eur J Hum Genet 6:291–295 ArticleCAS Google Scholar
Saari JC (2000) Biochemistry of visual pigment regeneration: the Friedenwald lecture. Invest Ophthalmol Vis Sci 41:337–348 CAS Google Scholar
Shapiro AB, Ling V (1994) ATPase activity of purified and reconstituted P-glycoprotein from Chinese hamster ovary cells. J Biol Chem 269:3745–3754 CAS Google Scholar
Shroyer NF, Lewis RA, Allikmets R, Singh N, Dean M, Leppert M, Lupski JR (1999) The rod photoreceptor ATP-binding cassette transporter gene, ABCR, and retinal disease: from monogenic to multifactorial. Vision Res 39:2537–2544 ArticleCAS Google Scholar
Shulenin S, Nogee LM, Annilo T, Wert SE, Whitsett JA, Dean M (2004) ABCA3 gene mutations in newborns with fatal surfactant deficiency. N Engl J Med 350:1296–1303 ArticleCAS Google Scholar
Sparrow JR, Boulton M (2005) RPE lipofuscin and its role in retinal pathobiology. Exp Eye Res 80:595–606 ArticleCAS Google Scholar
Sparrow JR, Nakanishi K, Parish CA (2000) The lipofuscin fluorophore A2E mediates blue light-induced damage to retinal pigmented epithelial cells. Invest Ophthalmol Vis Sci 41:1981–1989 CAS Google Scholar
Stargardt K (1909) Uber familiare, progressive degeenration under makulagegend des augen. Albrecht von Graefes Arch Ophthalmol 71:534–550 Google Scholar
Stenirri S, Battistella S, Fermo I, Manitto MP, Martina E, Brancato R, Ferrari M, Cremonesi L (2006) De novo deletion removes a conserved motif in the C-terminus of ABCA4 and results in cone-rod dystrophy. Clin Chem Lab Med 44:533–537 ArticleCAS Google Scholar
Sun H, Molday RS, Nathans J (1999) Retinal stimulates ATP hydrolysis by purified and reconstituted ABCR, the photoreceptor-specific ATP-binding cassette transporter responsible for Stargardt disease. J Biol Chem 274:8269–8281 ArticleCAS Google Scholar
Sun H, Nathans J (1997) Stargardt’s ABCR is localized to the disc membrane of retinal rod outer segments. Nat Genet 17:15–16 Article Google Scholar
Sun H, Smallwood PM, Nathans J (2000) Biochemical defects in ABCR protein variants associated with human retinopathies. Nat Genet 26:242–246 ArticleCAS Google Scholar
Surya A, Knox BE (1998) Enhancement of opsin activity by all-trans-retinal. Exp Eye Res 66:599–603 ArticleCAS Google Scholar
Takahashi K, Kimura Y, Kioka N, Matsuo M, Ueda K (2006) Purification and ATPase activity of human ABCA1. J Biol Chem 281:10760–10768 ArticleCAS Google Scholar
Wang N, Silver DL, Costet P, Tall AR (2000) Specific binding of ApoA-I, enhanced cholesterol efflux, and altered plasma membrane morphology in cells expressing ABCI. J Biol Chem 275:33053–33058 ArticleCAS Google Scholar
Wang N, Silver DL, Thiele C, Tall AR (2001) ATP-binding cassette transporter Al (ABCAI) functions as a cholesterol efflux regulatory protein. J Biol Chem 276:23742–23747 ArticleCAS Google Scholar
Webster AR, Heon E, Lotery AJ, Vandenburgh K, Casavant TL, Oh KT, Beck G, Fishman GA, Lam BL, Levin A et al (2001) An analysis of allelic variation in the ABCA4 gene. Invest Ophthalmol Vis Sci 42:1179–1189 CAS Google Scholar
Weleber RG (1994) Stargardt’s macular dystrophy. Arch Ophthalmol 112:752–754 CAS Google Scholar
Weng J, Mata NL, Azarian SM, Tzekov RT, Birch DG, Travis GH (1999) Insights into the function of rim protein in photoreceptors and etiology of Stargardt’s Disease from the phenotype in abcr knockout mice. Cell 98:13–23 ArticleCAS Google Scholar
Wiszniewski W, Zaremba CM, Yatsenko AN, Jamrich M, Wensel TG, Lewis RA, Lupski JR (2005) ABCA4 mutations causing mislocalization are found frequently in patients with severe retinal dystrophies. Hum Mol Genet 14:2769–2778 ArticleCAS Google Scholar
Yatsenko AN, Wiszniewski W, Zaremba CM, Jamrich M, Lupski JR (2005) Evolution of ABCA4 proteins in vertebrates. J Mol Evol 60:72–80 ArticleCAS Google Scholar
Zhou J, Jang YP, Kim SR, Sparrow JR (2006) Complement activation by photooxidation products of A2E, a lipofuscin constituent of the retinal pigment epithelium. Proc Natl Acad Sci U S A 103:16182–16187 ArticleCAS Google Scholar