ABCA4 is an N-retinylidene-phosphatidylethanolamine and phosphatidylethanolamine importer

Nature Communications

Volumn 3, Issue , 2012, Pages

  Quazi, Faraz ^a   Lenevich, Stepan ^a   Molday, Robert S ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ABCA4 PROTEIN; N RETINYLIDENE PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLETHANOLAMINE; REACTIVE OXYGEN METABOLITE; RETINOID; UNCLASSIFIED DRUG; ABCA4 PROTEIN, MOUSE; LIPOSOME; N-RETINYLIDENE-PHOSPHATIDYLETHANOLAMINE;

ARTICLE; BIOCHEMISTRY; GENE MUTATION; HUMAN; HUMAN CELL; ISOTOPE LABELING; LIPID VESICLE; NUCLEAR IMPORT; PHOTORECEPTOR; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PURIFICATION; PROTEIN TRANSPORT; STARGARDT DISEASE; ANIMAL; GENETICS; METABOLISM; MOUSE; MOUSE MUTANT; PHOTORECEPTOR CELL;

EUKARYOTA; MAMMALIA; PROKARYOTA;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; LIPOSOMES; MICE; MICE, KNOCKOUT; PHOSPHATIDYLETHANOLAMINES; PHOTORECEPTOR CELLS, VERTEBRATE; RETINOIDS;

EID: 84863304501     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms1927     Document Type: Article

References (60)

1. Hollenstein, K., Dawson, R. J. & Locher, K. P. Structure and mechanism of ABC transporter proteins. Curr. Opin. Struct. Biol. 17, 412-418 (2007). (Pubitemid 47451766)
2. Yazaki, K., Shitan, N., Sugiyama, A. & Takanashi, K. Cell and molecular biology of ATP-binding cassette proteins in plants. Int. Rev. Cell. Mol. Biol. 276, 263-299 (2009).
3. Davidson, A. L., Dassa, E., Orelle, C. & Chen, J. Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol. Mol. Biol. Rev. 72, 317-364 (2008). (Pubitemid 351822295)
4. Borst, P. & Elferink, R. O. Mammalian ABC transporters in health and disease. Annu. Rev. Biochem. 71, 537-592 (2002). (Pubitemid 34800230)
5. Dawson, R. J., Hollenstein, K. & Locher, K. P. Uptake or extrusion: crystal structures of full ABC transporters suggest a common mechanism. Mol. Microbiol. 65, 250-257 (2007). (Pubitemid 47052721)
6. Jones, P. M., O'Mara, M. L. & George, A. M. ABC transporters: a riddle wrapped in a mystery inside an enigma. Trends Biochem. Sci. 34, 520-531 (2009).
7. Rees, D. C., Johnson, E. & Lewinson, O. ABC transporters: the power to change. Nat. Rev. Mol. Cell. Biol. 10, 218-227 (2009).
8. Dean, M., Rzhetsky, A. & Allikmets, R. The human ATP-binding cassette (ABC) transporter superfamily. Genome Res. 11, 1156-1166 (2001). (Pubitemid 32677289)
9. Kaminski, W. E., Piehler, A. & Wenzel, J. J. ABC A-subfamily transporters: structure, function and disease. Biochim. Biophys. Acta. 1762, 510-524 (2006).
10. Rust, S. et al. Tangier disease is caused by mutations in the gene encoding ATP-binding cassette transporter 1. Nat. Genet. 22, 352-355 (1999). (Pubitemid 29369525)
11. Shulenin, S. et al. ABCA3 gene mutations in newborns with fatal surfactant deficiency. N. Engl. J. Med. 350, 1296-1303 (2004). (Pubitemid 38375364)
12. Lefevre, C. et al. Mutations in the transporter ABCA12 are associated with lamellar ichthyosis type 2. Hum. Mol. Genet. 12, 2369-2378 (2003). (Pubitemid 37160881)
13. Allikmets, R. et al. A photoreceptor cell-specific ATP-binding transporter gene (ABCR) is mutated in recessive Stargardt macular dystrophy. Nat. Genet. 15, 236-246 (1997). (Pubitemid 27098715)
14. Fishman, G. A., Farbman, J. S. & Alexander, K. R. Delayed rod dark adaptation in patients with Stargardt's disease. Ophthalmology 98, 957-962 (1991).
15. Weleber, R. G. Stargardt's macular dystrophy. Arch. Ophthalmol. 112, 752-754 (1994). (Pubitemid 24180508)
16. Cremers, F. P. et al. 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 (1998). (Pubitemid 28120622)
17. Allikmets, R. et al. Mutation of the Stargardt disease gene (ABCR) in age-related macular degeneration. Science 277, 1805-1807 (1997). (Pubitemid 27449189)
18. Illing, M., Molday, L. L. & Molday, R. S. The 220-kDa rim protein of retinal rod outer segments is a member of the ABC transporter superfamily. J. Biol. Chem. 272, 10303-10310 (1997). (Pubitemid 27171713)
19. Bungert, S., Molday, L. L. & Molday, R. S. 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 (2001).
20. Molday, L. L., Rabin, A. R. & Molday, R. S. ABCR expression in foveal cone photoreceptors and its role in stargardt macular dystrophy. Am. J. Ophthalmol. 130, 689 (2000).
21. Sun, H. & Nathans, J. Stargardt's ABCR is localized to the disc membrane of retinal rod outer segments. Nat. Genet. 17, 15-16 (1997).
22. Ahn, J., Wong, J. T. & Molday, R. S. 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 (2000). (Pubitemid 30457616)
23. Sun, H., Molday, R. S. & Nathans, J. 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 (1999).
24. Beharry, S., Zhong, M. & Molday, R. S. N-retinylidene- phosphatidylethanolamine is the preferred retinoid substrate for the photoreceptor-specific ABC transporter ABCA4 (ABCR). J. Biol. Chem. 279, 53972-53979 (2004). (Pubitemid 40053128)
25. Weng, J. et al. 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 (1999). (Pubitemid 29331192)
26. Mata, N. L., Weng, J. & Travis, G. H. 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 (2000). (Pubitemid 30431433)
27. Molday, R. S., Zhong, M. & Quazi, F. The role of the photoreceptor ABC transporter ABCA4 in lipid transport and Stargardt macular degeneration. Biochim. Biophys. Acta. 1791, 573-583 (2009).
28. Noy, N. & Xu, Z. J. Kinetic parameters of the interactions of retinol with lipid bilayers. Biochemistry 29, 3883-3888 (1990). (Pubitemid 20151300)
29. Rando, R. R. & Bangerter, F. W. The rapid intermembraneous transfer of retinoids. Biochem. Biophys. Res. Commun. 104, 430-436 (1982). (Pubitemid 12151495)
30. Zhong, M., Molday, L. L. & Molday, R. S. Role of the C terminus of the photoreceptor ABCA4 transporter in protein folding, function, and retinal degenerative diseases. J. Biol. Chem. 284, 3640-3649 (2009).
31. Smith, H. G. Jr., Stubbs, G. W. & Litman, B. J. The isolation and purification of osmotically intact discs from retinal rod outer segments. Exp. Eye Res. 20, 211-217 (1975).
32. Clark, S. P. & Molday, R. S. Orientation of membrane glycoproteins in sealed rod outer segment disks. Biochemistry 18, 5868-5873 (1979).
33. Romsicki, Y. & Sharom, F. J. Phospholipid flippase activity of the reconstituted P-glycoprotein multidrug transporter. Biochemistry 40, 6937-6947 (2001). (Pubitemid 32538241)
34. Coleman, J. A., Kwok, M. C. & Molday, R. S. Localization, purification, and functional reconstitution of the P4-ATPase Atp8a2, a phosphatidylserine flippase in photoreceptor disc membranes. J. Biol. Chem. 284, 32670-32679 (2009).
35. McIntyre, J. C. & Sleight, R. G. Fluorescence assay for phospholipid membrane asymmetry. Biochemistry 30, 11819-11827 (1991).
36. Borst, P., Zelcer, N. & van Helvoort, A. ABC transporters in lipid transport. Biochim. Biophys. Acta. 1486, 128-144 (2000). (Pubitemid 30336797)
37. Sun, H., Smallwood, P. M. & Nathans, J. Biochemical defects in ABCR protein variants associated with human retinopathies. Nat. Genet. 26, 242-246 (2000).
38. Ahn, J. & Molday, R. S. Purification and characterization of ABCR from bovine rod outer segments. Methods Enzymol. 315, 864-879 (2000). (Pubitemid 30123335)
39. Janvilisri, T. et al. Sterol transport by the human breast cancer resistance protein (ABCG2) expressed in Lactococcus lactis. J. Biol. Chem. 278, 20645-20651 (2003). (Pubitemid 36806364)
40. Kobayashi, A. et al. Efflux of sphingomyelin, cholesterol, and phosphatidylcholine by ABCG1. J. Lipid. Res. 47, 1791-1802 (2006). (Pubitemid 44222830)
41. Vaughan, A. M. & Oram, J. F. ABCA1 and ABCG1 or ABCG4 act sequentially to remove cellular cholesterol and generate cholesterol-rich HDL. J. Lipid. Res. 47, 2433-2443 (2006). (Pubitemid 44936105)
42. Abele, R. & Tampe, R. The TAP translocation machinery in adaptive immunity and viral escape mechanisms. Essays Biochem. 50, 249-264 (2011).
43. Shitan, N. et al. Involvement of CjMDR1, a plant multidrug-resistance- type ATP-binding cassette protein, in alkaloid transport in Coptis japonica. Proc. Natl Acad. Sci. USA 100, 751-756 (2003). (Pubitemid 36126124)
44. Attie, A. D. ABCA1: at the nexus of cholesterol, HDL and atherosclerosis. Trends. Biochem. Sci. 32, 172-179 (2007). (Pubitemid 46603277)
45. Linsel-Nitschke, P. et al. Potential role of ABCA7 in cellular lipid efflux to apoA-I. J. Lipid Res. 46, 86-92 (2005). (Pubitemid 40066674)
46. Oram, J. F. & Vaughan, A. M. ATP-Binding cassette cholesterol transporters and cardiovascular disease. Circ. Res. 99, 1031-1043 (2006). (Pubitemid 44729927)
47. Hollenstein, K., Frei, D. C. & Locher, K. P. Structure of an ABC transporter in complex with its binding protein. Nature 446, 213-216 (2007). (Pubitemid 46398672)
48. Aller, S. G. et al. Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science 323, 1718-1722 (2009).
49. Dawson, R. J. & Locher, K. P. Structure of a bacterial multidrug ABC transporter. Nature 443, 180-185 (2006). (Pubitemid 44387602)
50. Linton, K. J. Structure and function of ABC transporters. Physiology 22, 122-130 (2007).
51. Heck, M. et al. Signaling states of rhodopsin. Formation of the storage form, metarhodopsin III, from active metarhodopsin II. J. Biol. Chem. 278, 3162-3169 (2003). (Pubitemid 36801226)
52. Chen, C., Blakeley, L. R. & Koutalos, Y. Formation of all-trans retinol after visual pigment bleaching in mouse photoreceptors. Invest. Ophthalmol. Vis. Sci. 50, 3589-3595 (2009).
53. Ishiguro, S., Suzuki, Y., Tamai, M. & Mizuno, K. Purification of retinol dehydrogenase from bovine retinal rod outer segments. J. Biol. Chem. 266, 15520-15524 (1991). (Pubitemid 21907679)
54. Rattner, A., Smallwood, P. M. & 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. 275, 11034-11043 (2000). (Pubitemid 30212743)
55. Biswas-Fiss, E. E., Kurpad, D. S., Joshi, K. & Biswas, S. B. Interaction of extracellular domain 2 of the human retina-specific ATP-binding cassette transporter (ABCA4) with all-trans-retinal. J. Biol. Chem. 285, 19372-19383 (2010).
56. Wu, G. & Hubbell, W. L. Phospholipid asymmetry and transmembrane diffusion in photoreceptor disc membranes. Biochemistry 32, 879-888 (1993). (Pubitemid 23059370)
57. Miljanich, G. P., Nemes, P. P., White, D. L. & Dratz, E. A. The asymmetric transmembrane distribution of phosphatidylethanolamine, phosphatidylserine, and fatty acids of the bovine retinal rod outer segment disk membrane. J. Membr. Biol. 60, 249-255 (1981). (Pubitemid 11041319)
58. Menon, I. et al. Opsin is a phospholipid flippase. Curr. Biol. 21, 149-153 (2011).
59. Hessel, E., Muller, P., Herrmann, A. & Hofmann, K. P. Light-induced reorganization of phospholipids in rod disc membranes. J. Biol. Chem. 276, 2538-2543 (2001).
60. Kim, S. R. et al. Rpe65 Leu450Met variant is associated with reduced levels of the retinal pigment epithelium lipofuscin fluorophores A2E and iso-A2E. Proc. Natl Acad. Sci. USA 101, 11668-11672 (2004). (Pubitemid 39095354)