The ATP-binding cassette transporter ABCA4: Structural and functional properties and role in retinal disease

Advances in Experimental Medicine and Biology

Volumn 703, Issue , 2010, Pages 105-125

  Tsybovsky, Yaroslav ^a   Molday, Robert S ^b   Palczewski, Krzysztof ^b  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER A4; PHOSPHATIDYLETHANOLAMINE; RETINYLIDENE PHOSPHATIDYLETHANOLAMINE; UNCLASSIFIED DRUG; ABCA4 PROTEIN, HUMAN; ABCA4 PROTEIN, MOUSE; N RETINYLIDENE PHOSPHATIDYLETHANOLAMINE; N-RETINYLIDENE-PHOSPHATIDYLETHANOLAMINE; RETINOID;

ARTICLE; HUMAN; MUTATION; NONHUMAN; PATHOGENESIS; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; PROTEIN UNFOLDING; RETINA DISEASE; RETINA MACULA DEGENERATION; STARGARDT DISEASE; VISION; ACROCALLOSAL SYNDROME; ANIMAL; BIOLOGICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; DISEASE MODEL; GENETICS; METABOLISM; MOUSE; MOUSE MUTANT; MULTIPLE MALFORMATION SYNDROME; PROTEIN MOTIF; PROTEIN TERTIARY STRUCTURE; RECESSIVE GENE; RETINA ROD OUTER SEGMENT; REVIEW;

ANIMALIA; VERTEBRATA;

ABNORMALITIES, MULTIPLE; ACROCALLOSAL SYNDROME; AMINO ACID MOTIFS; ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; DISEASE MODELS, ANIMAL; GENES, RECESSIVE; HUMANS; MACULAR DEGENERATION; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MUTATION; PHOSPHATIDYLETHANOLAMINES; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; RETINAL DISEASES; RETINOIDS; ROD CELL OUTER SEGMENT;

EID: 79952198470     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4419-5635-4_8     Document Type: Article

References (85)

1. Ahn J, Molday RS (2000) Purification and characterization of ABCR from bovine rod outer segments. Methods Enzymol 315:864-879 (Pubitemid 30123335)
2. 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 (Pubitemid 30457616)
3. 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 anon-exchangeable ADP in the first nucleotide binding domain. J Biol Chem 278:39600-39608 (Pubitemid 37248519)
4. 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 (Pubitemid 40979716)
5. Allikmets R (2000) Simple and complex ABCR: genetic predisposition to retinal disease. Am J Hum Genet 67:793-799
6. 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 (1997a) Mutation of the Stargardt disease gene (ABCR) in age-related macular degeneration. Science 277:1805-1807 (Pubitemid 27449189)
7. 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 (1997b) A photoreceptor cell-specific ATP-binding transporter gene (ABCR) is mutated in recessive Stargardt macular dystrophy. Nat Genet 15:236-246 (Pubitemid 27098715)
8. 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 (Pubitemid 27273886)
9. 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 (Pubitemid 40053128)
10. 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 (Pubitemid 40344316)
11. Biswas EE (2001) Nucleotide binding domain 1 of the human retinal ABC transporter functions as a general ribonucleotidase. Biochemistry 40:8181-8187 (Pubitemid 32661877)
12. 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 (Pubitemid 32038249)
13. Biswas-Fiss EE (2003) Functional analysis of genetic mutations in nucleotide binding domain 2 of the human retina specific ABC transporter. Biochemistry 42:10683-10696 (Pubitemid 37102108)
14. Biswas-Fiss EE (2006) Interaction of the nucleotide binding domains and regulation of the ATPase activity of the human retina specific ABC transporter, ABCR. Biochemistry 45:3813-3823
15. Bungert S, Molday LL, Molday RS (2001) Membrane topology of the ATP binding cassette transporter ABCR and its relationship to ABC1 and related ABCA transporters: identification of N-linked glycosylation sites. J Biol Chem 276:23539-23546
16. Cideciyan AV, Swider M, Aleman TS, Tsybovsky Y, Schwartz SB, Windsor EA, Roman AJ, Sumaroka A, Steinberg JD, Jacobson SG, Stone EM, Palczewski K (2009) ABCA4 disease progression and a proposed strategy for gene therapy. Hum Mol Genet 18:931-941
17. Davidson AL, Chen J (2004) ATP-binding cassette transporters in bacteria. Annu Rev Biochem 73:241-268 (Pubitemid 39050369)
18. Dawson RJ, Hollenstein K, Locher KP (2007) Uptake or extrusion: crystal structures of full ABC transporters suggest a common mechanism. Mol Microbiol 65:250-257 (Pubitemid 47052721)
19. Eldred GE, Lasky MR (1993) Retinal age pigments generated by self-assembling lysosomotropic detergents. Nature 361:724-726 (Pubitemid 23070479)
20. Fitzgerald ML, Morris AL, Rhee JS, Andersson LP, Mendez AJ, Freeman MW (2002) Naturally occurring mutations in the largest extracellular loops of ABCA1 can disrupt its direct interaction with apolipoprotein A-I. J Biol Chem 277:33178-33187 (Pubitemid 34984836)
21. Gerber S, Comellas-Bigler M, Goetz BA, Locher KP (2008) Structural basis of trans-inhibition in a molybdate/tungstate ABC transporter. Science 321:246-250 (Pubitemid 351989095)
22. Hamel CP (2007) Cone rod dystrophies. Orphanet J Rare Dis 2:7
23. Harpaz Y, Gerstein M, Chothia C (1994) Volume changes on protein folding. Structure 2:641-649
24. Higgins CF (1992) ABC transporters: from microorganisms to man. Annu Rev Cell Biol 8:67-113 (Pubitemid 23000992)
25. Ho MT, Massey JB, Pownall HJ, Anderson RE, Hollyfield JG (1989) Mechanism of vitamin A movement between rod outer segments, interphotoreceptor retinoid-binding protein, and liposomes. J Biol Chem 264:928-935 (Pubitemid 19038074)
26. 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 (Pubitemid 29109453)
27. 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 (Pubitemid 27171713)
28. 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 (Pubitemid 41779106)
29. Kashiwagi K, Endo H, Kobayashi H, Takio K, Igarashi K (1995) Spermidine-preferential uptake system in Escherichia coli. ATP hydrolysis by PotA protein and its association with membrane. J Biol Chem 270:25377-25382
30. Kiefer F, Arnold K, Kunzli M, Bordoli L, Schwede T (2009) The SWISS-MODEL Repository and associated resources. Nucleic Acids Res 37:D387-D392
31. Kim WS, Weickert CS, Garner B (2008) Role of ATP-binding cassette transporters in brain lipid transport and neurological disease. J Neurochem 104:1145-1166 (Pubitemid 351293350)
32. Kolling R, Losko S (1997) The linker region of the ABC-transporter Ste6 mediates ubiquitination and fast turnover of the protein. EMBO J 16:2251-2261 (Pubitemid 27258628)
33. Kos V, Ford RC (2009) The ATP-binding cassette family: a structural perspective. Cell Mol Life Sci 66:3111-3126
34. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948 (Pubitemid 350162903)
35. 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 (Pubitemid 129500525)
36. Linton KJ, Higgins CF (2007) Structure and function of ABC transporters: the ATP switch provides flexible control. Pflugers Arch 453:555-567 (Pubitemid 46192529)
37. Maeda A, Maeda T, Sun W, Zhang H, Baehr W, Palczewski K (2007) Redundant and unique roles of retinol dehydrogenases in the mouse retina. Proc Natl Acad Sci USA 104:19565-19570
38. Maeda A, Maeda T, Golczak M, Palczewski K (2008) Retinopathy in mice induced by disrupted all-trans-retinal clearance. J Biol Chem 283:26684-26693
39. Maeda A, Golczak M, Maeda T, Palczewski K (2009a) Limited roles of Rdh8, Rdh12 and Abca4 on all-trans-retinal clearance in mouse retina. Invest Ophthalmol Vis Sci 50(11):5435-5443
40. Maeda A, Maeda T, Golczak M, Chou S, Desai A, Hoppel CL, Matsuyama S, Palczewski K (2009b) Involvement of all-trans-retinal in acute light-induced retinopathy of mice. J Biol Chem 284:15173-15183
41. Maeda T, Maeda A, Matosky M, Okano K, Roos S, Tang J, Palczewski K (2009c) Evaluation of potential therapies for a mouse model of human age-related macular degeneration caused by delayed all-trans-retinal clearance. Invest Ophthalmol Vis Sci 50:4917-4925
42. Martinez LO, Agerholm-Larsen B, Wang N, Chen W, Tall AR (2003) Phosphorylation of a pest sequence in ABCA1 promotes calpain degradation and is reversed by ApoA-I. J Biol Chem 278:37368-37374 (Pubitemid 37175255)
43. 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
44. Mata NL, Weng J, Travis GH (2000) Biosynthesis of a major lipofuscin fluorophore in mice and humans with ABCR-mediated retinal and macular degeneration. Proc Natl Acad Sci USA 97:7154-7159 (Pubitemid 30431433)
45. 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 (Pubitemid 32652338)
46. Molday RS (2007) ATP-binding cassette transporter ABCA4: molecular properties and role in vision and macular degeneration. J Bioenerg Biomembr 39:507-517
47. Molday RS, Molday LL (1979) Identification and characterization of multiple forms of rhodopsin and minor proteins in frog and bovine rod outer segment disc membranes. Electrophoresis, lectin labeling, and proteolysis studies. J Biol Chem 254:4653-4660 (Pubitemid 9203495)
48. 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 (Pubitemid 30437308)
49. Molday RS, Zhong M, Quazi F (2009) The role of the photoreceptor ABC transporter ABCA4 inlipid transport and Stargardt macular degeneration. Biochim Biophys Acta 1791:573-583
50. Mourez M, Hofnung M, Dassa E (1997) Subunit interactions in ABC transporters: a conserved sequence in hydrophobic membrane proteins of periplasmic permeases defines an important site of interaction with the ATPase subunits. EMBO J 16:3066-3077 (Pubitemid 27234946)
51. Mustafi D, Engel AH, Palczewski K (2009) Structure of cone photoreceptors. Prog Retin Eye Res 28:289-302
52. Nickell S, Park PS, Baumeister W, Palczewski K (2007) Three-dimensional architecture of murine rod outer segments determined by cryoelectron tomography. J Cell Biol 177:917-925 (Pubitemid 46873096)
53. Noe J, Hagenbuch B, Meier PJ, St-Pierre MV (2001) Characterization of the mouse bile salt export pump overexpressed in the baculovirus system. Hepatology 33:1223-1231 (Pubitemid 32378223)
54. Palczewski K, Jager S, Buczylko J, Crouch RK, Bredberg DL, Hofmann KP, Asson-Batres MA, Saari JC (1994) Rod outer segment retinol dehydrogenase: substrate specificity and role in phototransduction. Biochemistry 33:13741-13750 (Pubitemid 24381937)
55. Papermaster DS, Schneider BG, Zorn MA, Kraehenbuhl JP (1978) Immunocytochemical localization of a large intrinsic membrane protein to the incisures and margins of frog rod outer segment disks. J Cell Biol 78:415-425 (Pubitemid 8403882)
56. 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 frog retinas. Vision Res 22:1417-1428 (Pubitemid 13177446)
57. Paskowitz DM, LaVail MM, Duncan JL (2006) Light and inherited retinal degeneration. Br J Ophthalmol 90:1060-1066 (Pubitemid 44140192)
58. Pawar AS, Qtaishat NM, Little DM, Pepperberg DR (2008) Recovery of rod photoresponses in ABCR-deficient mice. Invest Ophthalmol Vis Sci 49:2743-2755
59. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, Chipot C, Skeel RD, Kale L, Schulten K (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26:1781-1802 (Pubitemid 43078511)
60. Radu RA, Mata NL, Bagla A, Travis GH (2004) Light exposure stimulates formation of A2E oxiranes in a mouse model of Stargardt's macular degeneration. Proc Natl Acad Sci USA 101:5928-5933 (Pubitemid 38520505)
61. Rando RR, Bangerter FW (1982) The rapid intermembraneous transfer of retinoids. Biochem Biophys Res Commun 104:430-436 (Pubitemid 12151495)
62. Rees DC, Johnson E, Lewinson O (2009) ABC transporters: the power to change. Nat Rev Mol Cell Biol 10:218-227
63. Roof DJ, Heuser JE (1982) Surfaces of rod photoreceptor disk membranes: integral membrane components. J Cell Biol 95:487-500 (Pubitemid 13215864)
64. 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 (Pubitemid 28316297)
65. Schmidt S, Postel EA, Agarwal A, Allen IC Jr, Walters SN, De la Paz MA, Scott WK, Haines JL, Pericak-Vance MA, Gilbert JR (2003) Detailed analysis of allelic variation in the ABCA4 gene in age-related maculopathy. Invest Ophthalmol Vis Sci 44:2868-2875 (Pubitemid 36759746)
66. See RH, Caday-Malcolm RA, Singaraja RR, Zhou S, Silverston A, Huber MT, Moran J, James ER, Janoo R, Savill JM, Rigot V, Zhang LH, Wang M, Chimini G, Wellington CL, Tafuri SR, Hayden MR (2002) Protein kinase A site-specific phosphorylation regulates ATP-binding cassette A1 (ABCA1)-mediated phospholipid efflux. J Biol Chem 277:41835-41842 (Pubitemid 35257494)
67. 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
68. Sparrow JR, Wu Y, Kim CY, Zhou J (2009) Phospholipid meets all-trans-retinal: the making of RPE bisretinoids. J Lipid Res 51(2):247-261
69. Suarez T, Biswas SB, Biswas EE (2002) Biochemical defects in retina-specific human ATP binding cassette transporter nucleotide binding domain 1 mutants associated with macular degeneration. J Biol Chem 277:21759-21767 (Pubitemid 34952327)
70. Sullivan JM (2009) Focus on molecules: ABCA4 (ABCR) - an import-directed photoreceptor retinoid flipase. Exp Eye Res 89:602-603
71. Sun H, Nathans J (1997) Stargardt's ABCR is localized to the disc membrane of retinal rod outer segments. Nat Genet 17:15-16
72. 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
73. Sun H, Smallwood PM, Nathans J (2000) Biochemical defects in ABCR protein variants associated with human retinopathies. Nat Genet 26:242-246
74. Szuts EZ (1985) Light stimulates phosphorylation of two large membrane proteins in frog photoreceptors. Biochemistry 24:4176-4184 (Pubitemid 16239771)
75. Tachikawa M, Watanabe M, Hori S, Fukaya M, Ohtsuki S, Asashima T, Terasaki T (2005) Distinct spatio-temporal expression of ABCA and ABCG transporters in the developing and adult mouse brain. J Neurochem 95:294-304 (Pubitemid 41384447)
76. Trompier D, Alibert M, Davanture S, Hamon Y, Pierres M, Chimini G (2006) Transition from dimers to higher oligomeric forms occurs during the ATPase cycle of the ABCA1 transporter. J Biol Chem 281:20283-20290 (Pubitemid 44065803)
77. van Driel MA, Maugeri A, Klevering BJ, Hoyng CB, Cremers FP (1998) ABCR unites what ophthalmologists divide(s). Ophthalmic Genet 19:117-122 (Pubitemid 28497540)
78. Vasiliou V, Vasiliou K, Nebert DW (2009) Human ATP-binding cassette (ABC) transporter family. Hum Genomics 3:281-290
79. Walia S, Fishman GA (2009) Natural history of phenotypic changes in Stargardt macular dystrophy. Ophthalmic Genet 30:63-68
80. Warren MS, Zerangue N, Woodford K, Roberts LM, Tate EH, Feng B, Li C, Feuerstein TJ, Gibbs J, Smith B, de Morais SM, Dower WJ, Koller KJ (2009) Comparative gene expression profiles of ABC transporters in brain microvessel endothelial cells and brain in five species including human. Pharmacol Res 59:404-413
81. Weleber RG (1994) Stargardt's macular dystrophy. Arch Ophthalmol 112:752-754 (Pubitemid 24180508)
82. 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 (Pubitemid 29331192)
83. 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 (Pubitemid 41418783)
84. Zarubica A, Trompier D, Chimini G (2007) ABCA1, from pathology to membrane function. Pflugers Arch 453:569-579 (Pubitemid 46192530)
85. Zhong M, Molday LL, Molday RS (2009) Role of the C terminus of the photoreceptor ABCA4 transporter in protein folding, function, and retinal degenerative diseases. J Biol Chem 284:3640-3649