Retinoid binding properties of nucleotide binding domain 1 of the Stargardt disease-associated ATP binding cassette (ABC) transporter, ABCA4

Journal of Biological Chemistry

Volumn 287, Issue 53, 2012, Pages 44097-44107

  Biswas Fiss, Esther E ^a,b   Affet, Stephanie ^a   Ha, Malissa ^a   Biswas, Subhasis B ^b  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b UNIVERSITY OF MEDICINE AND DENTISTRY OF NEW JERSEY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SEQUENCE; ATP BINDING CASSETTE TRANSPORTERS; BINDING AFFINITIES; BINDING ANALYSIS; BINDING PROPERTIES; IN-VIVO; LUMENAL DOMAIN; MACULAR DEGENERATION; NUCLEOTIDE-BINDING DOMAIN; RECOMBINANT POLYPEPTIDES; SOLUBLE DOMAINS; STARGARDT DISEASE;

AMINO ACIDS; BINDING ENERGY;

OPHTHALMOLOGY;

11 CIS RETINAL; ABC TRANSPORTER; ABC TRANSPORTER A4; NUCLEOTIDE; POLYPEPTIDE; RETINAL; RETINOID; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANISOTROPY; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CYTOPLASM; DISEASE ASSOCIATION; FLUORESCENCE ANALYSIS; IN VIVO STUDY; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MOTIF; STARGARDT DISEASE; STRUCTURE ACTIVITY RELATION;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; ATP-BINDING CASSETTE TRANSPORTERS; HUMANS; ISOMERISM; KINETICS; MACULAR DEGENERATION; MOLECULAR SEQUENCE DATA; NUCLEOTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RETINOIDS; SEQUENCE ALIGNMENT;

EID: 84871791855     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.409623     Document Type: Article

References (70)

1. Zhang, K., Kniazeva, M., Hutchinson, A., Han, M., Dean, M., and Allikmets, R. (1999) The ABCR gene in recessive and dominant Stargardt diseases. Agenetic pathway in macular degeneration. Genomics 60, 234-237
2. Koenekoop, R. K. (2003) The gene for Stargardt disease, ABCA4, is a major retinal gene. A mini-review. Ophthalmic Genet. 24, 75-80
3. Souied, E. H., Ducroq, D., Rozet, J. M., Gerber, S., Perrault, I., Sterkers, M., Benhamou, N., Munnich, A., Coscas, G., Soubrane, G., and Kaplan, J. (1999) A novel ABCR nonsense mutation responsible for late-onset fundus flavimaculatus. Invest. Ophthalmol. Vis. Sci. 40, 2740-2744
4. Papaioannou, M., Ocaka, L., Bessant, D., Lois, N., Bird, A., Payne, A., and Bhattacharya, S. (2000) An analysis of ABCR mutations in British patients with recessive retinal dystrophies. Invest. Ophthalmol. Vis. Sci. 41, 16-19
5. Lois, N., Holder, G. E., Fitzke, F. W., Plant, C., and Bird, A. C. (1999) Intrafamilial variation of phenotype in Stargardt macular dystrophy-Fundus flavimaculatus. Invest. Ophthalmol. Vis. Sci. 40, 2668-2675
6. Klevering, B. J., Deutman, A. F., Maugeri, A., Cremers, F. P., and Hoyng, C. B. (2005) The spectrum of retinal phenotypes caused by mutations in the ABCA4 gene. Graefes Arch. Clin. Exp. Ophthalmol. 243, 90-100
7. Martínez-Mir, A., Paloma, E., Allikmets, R., Ayuso, C., del Rio, T., Dean, M., Vilageliu, L., González-Duarte, R., and Balcells, S. (1998) Retinitis pigmentosa caused by a homozygous mutation in the Stargardt disease gene ABCR. Nat. Genet. 18, 11-12
8. Klevering, B. J., Yzer, S., Rohrschneider, K., Zonneveld, M., Allikmets, R., van den Born, L. I., Maugeri, A., Hoyng, C. B., and Cremers, F. P. (2004) Microarray-based mutation analysis of the ABCA4 (ABCR) gene in autosomal recessive cone-rod dystrophy and retinitis pigmentosa. Eur. J. Hum. Genet. 12, 1024-1032
9. Klevering, B. J., van Driel, M., van de Pol, D. J., Pinckers, A. J., Cremers, F. P., and Hoyng, C. B. (1999) Phenotypic variations in a family with retinal dystrophy as result of different mutations in the ABCR gene. Br. J. Ophthalmol. 83, 914-918
10. Cremers, F. P., Maugeri, A., Klevering, B. J., Hoefsloot, L. H., and Hoyng, C. B. (2002) [From gene to disease. From the ABCA4 gene to Stargardt disease, cone-rod dystrophy and retinitis pigmentosa]. Ned. Tijdschr Geneeskd 146, 1581-1584
11. Allikmets, R. (2000) Simple and complex ABCR. Genetic predisposition to retinal disease. Am. J. Hum. Genet. 67, 793-799
12. van Driel, M. A., Maugeri, A., Klevering, B. J., Hoyng, C. B., and Cremers, F. P. (1998) ABCR unites what ophthalmologists divide(s). Ophthalmic Genet. 19, 117-122
13. Simonelli, F., Testa, F., Zernant, J., Nesti, A., Rossi, S., Rinaldi, E., and Allikmets, R. (2004) Association of a homozygous nonsense mutation in the ABCA4 (ABCR) gene with cone-rod dystrophy phenotype in an Italian family. Ophthalmic Res. 36, 82-88
14. Maugeri, A., Klevering, B. J., Rohrschneider, K., Blankenagel, A., Brunner, H. G., Deutman, A. F., Hoyng, C. B., and Cremers, F. P. (2000) Mutations in the ABCA4 (ABCR) gene are the major cause of autosomal recessive cone-rod dystrophy. Am. J. Hum. Genet. 67, 960-966
15. Klevering, B. J., Blankenagel, A., Maugeri, A., Cremers, F. P., Hoyng, C. B., and Rohrschneider, K. (2002) Phenotypic spectrum of autosomal recessive cone-rod dystrophies caused by mutations in the ABCA4 (ABCR) gene. Invest. Ophthalmol. Vis. Sci. 43, 1980-1985
16. Jaakson, K., Zernant, J., Külm, M., Hutchinson, A., Tonisson, N., Glavac, D., Ravnik-Glavac, M., Hawlina, M., Meltzer, M. R., Caruso, R. C., Testa, F., Maugeri, A., Hoyng, C. B., Gouras, P., Simonelli, F., Lewis, R. A., Lupski, J. R., Cremers, F. P., and Allikmets, R. (2003) Genotyping microarray (gene chip) for the ABCR (ABCA4) gene. Hum. Mutat. 22, 395-403
17. Birch, D. G., Peters, A. Y., Locke, K. L., Spencer, R., Megarity, C. F., and Travis, G. H. (2001) Visual function in patients with cone-rod dystrophy (CRD) associated with mutations in the ABCA4 (ABCR) gene. Exp. Eye Res. 73, 877-886
18. Yates, J. R., and Moore, A. T. (2000) Genetic susceptibility to age related macular degeneration. J. Med. Genet. 37, 83-87
19. De La Paz, M. A., Guy, V. K., Abou-Donia, S., Heinis, R., Bracken, B., Vance, J. M., Gilbert, J. R., Gass, J. D., Haines, J. L., and Pericak-Vance, M. A. (1999) Analysis of the Stargardt disease gene (ABCR) in age-related macular degeneration. Ophthalmology 106, 1531-1536
20. Zernant, J., Schubert, C., Im, K. M., Burke, T., Brown, C. M., Fishman, G. A., Tsang, S. H., Gouras, P., Dean, M., and Allikmets, R. (2011) Analysis of the ABCA4 gene by next-generation sequencing. Invest. Ophthalmol. Vis. Sci. 52, 8479-8487
21. Bennett, J., Chung, D. C., and Maguire, A. (2012) Gene delivery to the retina. From mouse to man. Methods Enzymol. 507, 255-274
22. Azarian, S. M., and Travis, G. H. (1997) The photoreceptor rim protein is an ABC transporter encoded by the gene for recessive Stargardt's disease (ABCR). FEBS Lett. 409, 247-252
23. Molday, L. L., Rabin, A. R., and Molday, R. S. (2000) ABCR expression in foveal cone photoreceptors and its role in Stargardt macular dystrophy. Am. J. Ophthalmol. 130, 689
24. Kiser, P. D., Golczak, M., Maeda, A., and Palczewski, K. (2012) Key enzymes of the retinoid (visual) cycle in vertebrate retina. Biochim. Biophys. Acta 1821, 137-151
25. Boyer, N. P., Higbee, D., Currin, M. B., Blakeley, L. R., Chen, C., Ablonczy, Z., Crouch, R. K., and Koutalos, Y. (2012) Lipofuscin and N-retinylidene-N-retinylethanolamine (A2E) accumulate in retinal pigment epithelium in absence of light exposure. Their origin is 11-cis-retinal. J. Biol. Chem. 287, 22276-22286
26. Walker, J. E., Saraste, M., Runswick, M. J., and Gay, N. J. (1982) Distantly related sequences in the α and β subunits of ATP synthase, myosin, kinases, and other ATP requiring enzymes and a common nucleotide binding fold. EMBO J. 1, 945-951
27. Mourez, M., Hofnung, M., and 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
28. Tsybovsky, Y., Molday, R. S., and Palczewski, K. (2010) The ATP-binding cassette transporter ABCA4. Structural and functional properties and role in retinal disease. Adv. Exp. Med. Biol. 703, 105-125
29. Rees, D. C., Johnson, E., and Lewinson, O. (2009) ABC transporters. The power to change. Nat. Rev. Mol. Cell Biol. 10, 218-227
30. Sun, H., Smallwood, P. M., and Nathans, J. (2000) Biochemical defects in ABCR protein variants associated with human retinopathies. Nat. Genet. 26, 242-246
31. Sun, H., Molday, R. S., and 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
32. Molday, R. S. (2007) ATP-binding cassette transporter ABCA4. Molecular properties and role in vision and macular degeneration. J. Bioenerg. Biomembr. 39, 507-517
33. Biswas-Fiss, E. E. (2003) Functional analysis of genetic mutations in nucleotide binding domain 2 of the human retina specific ABC transporter. Biochemistry 42, 10683-10696
34. Ahn, J., and Molday, R. S. (2000) Purification and characterization of ABCR from bovine rod outer segments. Methods Enzymol. 315, 864-879
35. Suárez, T., Biswas, S. B., and Biswas, E. E. (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
36. Biswas, E. E. (2001) Nucleotide binding domain 1 of the human retinal ABC transporter functions as a general ribonucleotidase. Biochemistry 40, 8181-8187
37. Vasiliou, V., Vasiliou, K., and Nebert, D. W. (2009) Human ATP-binding cassette (ABC) transporter family. Hum. Genomics 3, 281-290
38. Fukui, T., Yamamoto, S., Nakano, K., Tsujikawa, M., Morimura, H., Nishida, K., Ohguro, N., Fujikado, T., Irifune, M., Kuniyoshi, K., Okada, A. A., Hirakata, A., Miyake, Y., and Tano, Y. (2002) ABCA4 gene mutations in Japanese patients with Stargardt disease and retinitis pigmentosa. Invest. Ophthalmol. Vis. Sci. 43, 2819-2824
39. Biswas-Fiss, E. E., Kurpad, D. S., Joshi, K., and Biswas, S. B. (2010) 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
40. Biswas-Fiss, E. E., Ha, M., Kurpad, D and Biswas, S. B. (2011) Retinoid binding properties of the nucleotide binding domains of human ABCA4 protein. Invest. Ophthalmol. Vis. Sci. 52, E-Abstract 51
41. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Press, Cold Spring Harbor, NY
42. Winterfeld, S., Imhof, N., Roos, T., Bär, G., Kuhn, A., and Gerken, U. (2009) Substrate-induced conformational change of the Escherichia coli membrane insertase YidC. Biochemistry 48, 6684-6691
43. Booth, C. L., Pulaski, L., Gottesman, M. M., and Pastan, I. (2000) Analysis of the properties of the N-terminal nucleotide-binding domain of human P-glycoprotein. Biochemistry 39, 5518-5526
44. Balan, A., Ferreira, R. C., and Ferreira, L. C. (2008) Production of the refolded oligopeptide-binding protein (OppA) encoded by the citrus pathogen Xanthomonas axonopodis pv. Citri. Genet. Mol. Res. 7, 117-126
45. Brunkhorst, C., Wehmeier, U. F., Piepersberg, W., and Schneider, E. (2005) The acbH gene of Actinoplanes sp. encodes a solute receptor with binding activities for acarbose and longer homologs. Res. Microbiol. 156, 322-327
46. Mace, P. D., Cutfield, J. F., and Cutfield, S. M. (2007) Bacterial expression and purification of the ovine type II bone morphogenetic protein receptor ectodomain. Protein Expr. Purif. 52, 40-49
47. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254
48. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
49. Biswas, E. E., and Biswas, S. B. (2000) The C-terminal nucleotide binding domain of the human retinal ABCR protein is an adenosine triphosphatase. Biochemistry 39, 15879-15886
50. Saurin, W., Hofnung, M., and Dassa, E. (1999) Getting in or out. Early segregation between importers and exporters in the evolution of ATP-binding cassette (ABC) transporters. J. Mol. Evol. 48, 22-41
51. Katz, M. L., Farias, F. H., Sanders, D. N., Zeng, R., Khan, S., Johnson, G. S., and O'Brien, D. P. (2011) A missense mutation in canine CLN6 in an Australian shepherd with neuronal ceroid lipofuscinosis. J. Biomed. Biotechnol. 2011, 198042
52. Fishman, G. A., Roberts, M. F., Derlacki, D. J., Grimsby, J. L., Yamamoto, H., Sharon, D., Nishiguchi, K. M., and Dryja, T. P. (2004) Novel mutations in the cellular retinaldehyde-binding protein gene (RLBP1) associated with retinitis punctata albescens. Evidence of interfamilial genetic heterogeneity and fundus changes in heterozygotes. Arch. Ophthalmol. 122, 70-75
53. Ito, Y. A., Footz, T. K., Murphy, T. C., Courtens, W., and Walter, M. A. (2007) Analyses of a novel L130F missense mutation in FOXC1. Arch. Ophthalmol. 125, 128-135
54. Stankiewicz, P., and Lupski, J. R. (2006) The genomic basis of disease, mechanisms and assays for genomic disorders. Genome Dyn. 1, 1-16
55. Briggs, C. E., Rucinski, D., Rosenfeld, P. J., Hirose, T., Berson, E. L., and Dryja, T. P. (2001) Mutations in ABCR (ABCA4) in patients with Stargardt macular degeneration or cone-rod degeneration. Invest. Ophthalmol. Vis. Sci. 42, 2229-2236
56. Lewis, R. A., Shroyer, N. F., Singh, N., Allikmets, R., Hutchinson, A., Li, Y., Lupski, J. R., Leppert, M., and 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
57. Webster, A. R., Héon, E., Lotery, A. J., Vandenburgh, K., Casavant, T. L., Oh, K. T., Beck, G., Fishman, G. A., Lam, B. L., Levin, A., Heckenlively, J. R., Jacobson, S. G., Weleber, R. G., Sheffield, V. C., and Stone, E. M. (2001) An analysis of allelic variation in the ABCA4 gene. Invest. Ophthalmol. Vis. Sci. 42, 1179-1189
58. Fishman, G. A., Stone, E. M., Eilason, D. A., Taylor, C. M., Lindeman, M., and Derlacki, D. J. (2003) ABCA4 gene sequence variations in patients with autosomal recessive cone-rod dystrophy. Arch. Opthalmol. 121, 851-855
59. Ahn, J., Beharry, S., Molday, L. L., and Molday, R. S. (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
60. Biswas-Fiss, E. E. (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
61. Jones, P. M., and George, A. M. (2002) Mechanism of ABC transporters. A molecular dynamics simulation of a well characterized nucleotide-binding subunit. Proc. Natl. Acad. Sci. U.S.A. 99, 12639-12644
62. Wen, P. C., and Tajkhorshid, E. (2011) Conformational coupling of the nucleotide-binding and the transmembrane domains in ABC transporters. Biophys. J. 101, 680-690
63. Wang, J., Grishin, N., Kinch, L., Cohen, J. C., Hobbs, H. H., and Xie, X. S. (2011) Sequences in the nonconsensus nucleotide-binding domain of ABCG5/ABCG8 required for sterol transport. J. Biol. Chem. 286, 7308-7314
64. Boyer, N. P., Tang, P. H., Higbee, D., Ablonczy, Z., Crouch, R. K., and Koutalos, Y. (2012) Lipofuscin and A2E accumulate with age in the retinal pigment epithelium of Nrl(-/-) mice. Photochem Photobiol. 88, 1373-1377
65. - channel by ATP-driven nucleotide-binding domain dimerization. J. Physiol. 587, 2151-2161
66. Di Pietro, A., Conseil, G., Pérez-Victoria, J. M., Dayan, G., Baubichon-Cortay, H., Trompier, D., Steinfels, E., Jault, J. M., de Wet, H., Maitrejean, M., Comte, G., Boumendjel, A., Mariotte, A. M., Dumontet, C., McIntosh, D. B., Goffeau, A., Castanys, S., Gamarro, F., and Barron, D. (2002) Modulation by flavonoids of cell multidrug resistance mediated by P-glycoprotein and related ABC transporters. Cell Mol. Life Sci. 59, 307-322
67. Shimamura, T., Weyand, S., Beckstein, O., Rutherford, N. G., Hadden, J. M., Sharples, D., Sansom, M. S., Iwata, S., Henderson, P. J., and Cameron, A. D. (2010) Molecular basis of alternating access membrane transport by the sodium-hydantoin transporter Mhp1. Science 328, 470-473
68. Zou, P., and McHaourab, H. S. (2009) Alternating access of the putative substrate-binding chamber in the ABC transporter MsbA. J. Mol. Biol. 393, 574-585
69. Wang, W., and Linsdell, P. (2012) Alternating access to the transmembrane domain of the ATP-binding cassette protein cystic fibrosis transmembrane conductance regulator (ABCC7). J. Biol. Chem. 287, 10156-10165
70. Bungert, S., Molday, L. L., and Molday, R. S. (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