Common defects of ABCG2, a high-capacity urate exporter, cause gout: A function-based genetic analysis in a Japanese population

Science Translational Medicine

Volumn 1, Issue 5, 2009, Pages

  Matsuo, Hirotaka ^a   Takada, Tappei ^b   Ichida, Kimiyoshi ^c,d   Nakamura, Takahiro ^a,e   Nakayama, Akiyoshi ^a,f   Ikebuchi, Yuki ^b   Ito, Kousei ^b   Kusanagi, Yasuyoshi ^a   Chiba, Toshinori ^a   Tadokoro, Shin ^a   Takada, Yuzo ^a   Oikawa, Yuji ^g   Inoue, Hiroki ^a   Suzuki, Koji ^h   Okada, Rieko ⁱ   Nishiyama, Junichiro ^j   Domoto, Hideharu ^k   Watanabe, Satoru ^a   Fujita, Masanori ^a   Morimoto, Yuji ^a   Naito, Mariko ⁱ   Nishio, Kazuko ⁱ   Hishida, Asahi ⁱ   Wakai, Kenji ⁱ   Asai, Yatami ^l   Niwa, Kazuki ^g   Kamakura, Keiko ^a   Nonoyama, Shigeaki ^a   Sakurai, Yutaka ^a   Hosoya, Tatsuo ^d   Kanai, Yoshikatsu ^m   Suzuki, Hiroshi ^b   Hamajima, Nobuyuki ⁱ   Shinomiya, Nariyoshi ^a   more..

^a NATIONAL DEFENSE MEDICAL COLLEGE   (Japan)

^b UNIVERSITY OF TOKYO HOSPITAL   (Japan)

^c TOKYO UNIVERSITY OF PHARMACY AND LIFE SCIENCES   (Japan)

^d JIKEI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e INST OF PHYS AND CHEMICAL RESEARCH   (Japan)

^f Medical Platoon 9Th Aircraft Control and Warning Squadron Japan Air Self Defense Force   (Japan)

^g TOHO UNIVERSITY   (Japan)

^h FUJITA HEALTH UNIVERSITY   (Japan)

ⁱ NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^j JSDF Yokosuka Hospital   (Japan)

^k JMSDF Medical Service Unit Kure   (Japan)

^l Seirei Social Welfare Community   (Japan)

^m OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ABCG2 PROTEIN, HUMAN; TUMOR PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CHEMISTRY; GENETICS; GENOTYPE; GOUT; HUMAN; JAPAN; MOLECULAR GENETICS; MUTATION; POPULATION GENETICS;

AMINO ACID SEQUENCE; ATP-BINDING CASSETTE TRANSPORTERS; GENETICS, POPULATION; GENOTYPE; GOUT; HUMANS; JAPAN; MOLECULAR SEQUENCE DATA; MUTATION; NEOPLASM PROTEINS;

EID: 77952845866     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3000237     Document Type: Article

References (61)

1. I. Kippen, J. R. Klinenberg, A. Weinberger, W. R. Wilcox, Factors affecting urate solubility in vitro. Ann. Rheum. Dis. 33, 313-317 (1974).
2. D. I. Feig, D. H. Kang, R. J. Johnson, Uric acid and cardiovascular risk. N. Engl. J. Med. 359, 1811-1821 (2008).
3. A. J. Bleyer, T. C. Hart, Genetic factors associated with gout and hyperuricemia. Adv. Chronic Kidney Dis. 13, 124-130 (2006).
4. J. Ordi, P. L. Alonso, J. de Zulueta, J. Esteban, M. Velasco, E. Mas, E. Campo, P. L. Fernández, The severe gout of Holy Roman Emperor Charles V. N. Engl. J. Med. 355, 516-520 (2006).
5. C. Holden, Ruler laid low by gout. Science 313, 741 (2006).
6. R. J. Johnson, B. A. Rideout, Uric acid and diet - insights into the epidemic of cardiovascular disease. N. Engl. J. Med. 350, 1071-1073 (2004).
7. M. Hakoda, Epidemiology of hyperuricemia and gout in Japan [in Japanese]. Nippon Rinsho 66, 647-652 (2008).
8. Z. Miao, C. Li, Y. Chen, S. Zhao, Y. Wang, Z. Wang, X. Chen, F. Xu, F. Wang, R. Sun, J. Hu, W. Song, S. Yan, C. Y. Wang, Dietary and lifestyle changes associated with high prevalence of hyperuricemia and gout in the Shandong coastal cities of Eastern China. J. Rheumatol. 35, 1859-1864 (2008).
9. T. R. Mikuls, J. T. Farrar, W. B. Bilker, S. Fernandes, H. R. Schumacher Jr., K. G. Saag, Gout epidemiology: Results from the UK General Practice Research Database, 1990-1999. Ann. Rheum. Dis. 64, 267-272 (2005)
10. P. J. Cannon, W. B. Stason, F. E. Demartini, S. C. Sommers, J. H. Laragh, Hyperuricemia in primary and renal hypertension. N. Engl. J. Med. 275, 457-464 (1966).
11. J. P. Forman, H. Choi, G. C. Curhan, Uric acid and insulin sensitivity and risk of incident hypertension. Arch. Intern. Med. 169, 155-162 (2009).
12. Y. H. Lin, H. L. Hsu, Y. C. Huang, M. Lee, W. Y. Huang, Y. C. Huang, T. H. Lee, J. D. Lee, Gouty arthritis in acute cerebrovascular disease. Cerebrovasc. Dis. 28, 391-396 (2009).
13. J. H. Chen, S. Y. Chuang, H. J. Chen, W. T. Yeh, W. H. Pan, Serum uric acid level as an independent risk factor for all-cause, cardiovascular, and ischemic stroke mortality: A Chinese cohort study. Arthritis Rheum. 61, 225-232 (2009).
14. Y. P. Siu, K. T. Leung, M. K. Tong, T. H. Kwan, Use of allopurinol in slowing the progression of renal disease through its ability to lower serum uric acid level. Am. J. Kidney Dis. 47, 51-59 (2006).
15. K. M. Talaat, A. R. el-Sheikh, The effect of mild hyperuricemia on urinary transforming growth factor b and the progression of chronic kidney disease. Am. J. Nephrol. 27, 435-440 (2007).
16. A. Enomoto, H. Kimura, A. Chairoungdua, Y. Shigeta, P. Jutabha, S. H. Cha, M. Hosoyamada, M. Takeda, T. Sekine, T. Igarashi, H. Matsuo, Y. Kikuchi, T. Oda, K. Ichida, T. Hosoya, K. Shimokata, T. Niwa, Y. Kanai, H. Endou, Molecular identification of a renal urate anion exchanger that regulates blood urate levels. Nature 417, 447-452 (2002).
17. S. Li, S. Sanna, A. Maschio, F. Busonero, G. Usala, A. Mulas, S. Lai, M. Dei, M. Orrù, G. Albai, S. Bandinelli, D. Schlessinger, E. Lakatta, A. Scuteri, S. S. Najjar, J. Guralnik, S. Naitza, L. Crisponi, A. Cao, G. Abecasis, L. Ferrucci, M. Uda, W. M. Chen, R. Nagaraja, The GLUT9 gene is associated with serum uric acid levels in Sardinia and Chianti cohorts. PLoS Genet. 3, e194 (2007).
18. A. Döring, C. Gieger, D. Mehta, H. Gohlke, H. Prokisch, S. Coassin, G. Fischer, K. Henke, N. Klopp, F. Kronenberg, B. Paulweber, A. Pfeufer, D. Rosskopf, H. Völzke, T. Illig, T. Meitinger, H. E. Wichmann, C. Meisinger, SLC2A9 influences uric acid concentrations with pronounced sex-specific effects. Nat. Genet. 40, 430-436 (2008).
19. V. Vitart, I. Rudan, C. Hayward, N. K. Gray, J. Floyd, C. N. Palmer, S. A. Knott, I. Kolcic, O. Polasek, J. Graessler, J. F. Wilson, A. Marinaki, P. L. Riches, X. Shu, B. Janicijevic, N. Smolej-Narancic, B. Gorgoni, J. Morgan, S. Campbell, Z. Biloglav, L. Barac-Lauc, M. Pericic, I. M. Klaric, L. Zgaga, T. Skaric-Juric, S. H. Wild, W. A. Richardson, P. Hohenstein, C. H. Kimber, A. Tenesa, L. A. Donnelly, L. D. Fairbanks, M. Aringer, P. M. McKeigue, S. H. Ralston, A. D. Morris, P. Rudan, N. D. Hastie, H. Campbell, A. F. Wright, SLC2A9 is a newly identified urate transporter influencing serum urate concentration, urate excretion and gout. Nat. Genet. 40, 437-442 (2008).
20. H. Matsuo, T. Chiba, S. Nagamori, A. Nakayama, H. Domoto, K. Phetdee, P. Wiriyasermkul, Y. Kikuchi, T. Oda, J. Nishiyama, T.Nakamura, Y.Morimoto, K. Kamakura, Y. Sakurai, S. Nonoyama, Y. Kanai, N. Shinomiya, Mutations in glucose transporter 9 gene SLC2A9 cause renal hypouricemia. Am. J. Hum. Genet. 83, 744-751 (2008).
21. L. S. Cheng, S. L. Chiang, H. P. Tu, S. J. Chang, T. N. Wang, A. M. Ko, R. Chakraborty, Y. C. Ko, Genomewide scan for gout in Taiwanese aborigines reveals linkage to chromosome 4q25. Am. J. Hum. Genet. 75, 498-503 (2004).
22. A. Dehghan, A. Köttgen, Q. Yang, S. J. Hwang, W. L. Kao, F. Rivadeneira, E. Boerwinkle, D. Levy, A. Hofman, B. C. Astor, E. J. Benjamin, C. M. van Duijn, J. C. Witteman, J. Coresh, C. S. Fox, Association of three genetic loci with uric acid concentration and risk of gout: A genome-wide association study. Lancet 372, 1953-1961 (2008).
23. M. Kolz, T. Johnson, S. Sanna, A. Teumer, V. Vitart, M. Perola, M. Mangino, E. Albrecht, C. Wallace, M. Farrall, A. Johansson, D. R. Nyholt, Y. Aulchenko, J. S. Beckmann, S. Bergmann, M. Bochud, M. Brown, H. Campbell; EUROSPAN Consortium, J. Connell, A. Dominiczak,G. Homuth, C. Lamina, M. I. McCarthy; ENGAGE Consortium, T. Meitinger, V. Mooser, P. Munroe, M. Nauck, J. Peden, H. Prokisch, P. Salo, V. Salomaa, N. J. Samani, D. Schlessinger, M. Uda, U. Völker, G. Waeber, D. Waterworth, R.Wang-Sattler, A. F. Wright, J.Adamski, J. B.Whitfield,U. Gyllensten, J. F. Wilson, I. Rudan, P. Pramstaller, H. Watkins; PROCARDIS Consortium, A. Doering, H. E. Wichmann; KORA Study, T. D. Spector, L. Peltonen, H. Völzke, R. Nagaraja, P. Vollenweider, M. Caulfield; WTCCC, T. Illig, C. Gieger, Meta-analysis of 28,141 individuals identifies common variants within five new loci that influence uric acid concentrations. PLoS Genet. 5, e1000504 (2009).
24. M. Maliepaard, G. L. Scheffer, I. F. Faneyte, M. A. van Gastelen, A. C. Pijnenborg, A. H. Schinkel, M. J. van De Vijver, R. J. Scheper, J. H. Schellens, Subcellular localization and distribution of the breast cancer resistance protein transporter in normal human tissues. Cancer Res. 61, 3458-3464 (2001).
25. M. Huls, C. D. Brown, A. S. Windass, R. Sayer, J. J. van den Heuvel, S. Heemskerk, F. G. Russel, R. Masereeuw, The breast cancer resistance protein transporter ABCG2 is expressed in the human kidney proximal tubule apical membrane. Kidney Int. 73, 220-225 (2008).
26. G. Pan, N. Giri, W. F. Elmquist, Abcg2/Bcrp1 mediates the polarized transport of antiretroviral nucleosides abacavir and zidovudine. Drug Metab. Dispos. 35, 1165-1173 (2007).
27. K. Takenaka, J. A. Morgan, G. L. Scheffer, M. Adachi, C. F. Stewart, D. Sun, M. Leggas, K. F. Ejendal, C. A. Hrycyna, J. D. Schuetz, Substrate overlap between Mrp4 and Abcg2/Bcrp affects purine analogue drug cytotoxicity and tissue distribution. Cancer Res. 67, 6965-6972 (2007).
28. C. de Wolf, R. Jansen, H. Yamaguchi, M. de Haas, K. van de Wetering, J. Wijnholds, J. Beijnen, P. Borst, Contribution of the drug transporter ABCG2 (breast cancer resistance protein) to resistance against anticancer nucleosides. Mol. Cancer Ther. 7, 3092-3102 (2008).
29. C. Kondo, H. Suzuki, M. Itoda, S. Ozawa, J. Sawada, D. Kobayashi, I. Ieiri, K. Mine, K. Ohtsubo, Y. Sugiyama, Functional analysis of SNPs variants of BCRP/ABCG2. Pharm. Res. 21, 1895-1903 (2004).
30. D. A. Sica, A. Schoolwerth, Elements of normal renal structure and function: Renal handling of organic anions and cations, in Brenner and Rector's The Kidney, B. M. Brenner, Ed. (Saunders, Philadelphia, ed. 7, 2004), pp. 645-649.
31. L. B. Sorensen, Role of the intestinal tract in the elimination of uric acid. Arthritis Rheum. 8, 694-706 (1965).
32. Supplementary Materials and Methods are presented as Supplementary Material on Science Translational Medicine Online.
33. M. Suzuki, H. Suzuki, Y. Sugimoto, Y. Sugiyama, ABCG2 transports sulfated conjugates of steroids and xenobiotics. J. Biol. Chem. 278, 22644 -22649 (2003).
34. K. Maekawa, M. Itoda, K. Sai, Y. Saito, N. Kaniwa, K. Shirao, T. Hamaguchi, H. Kunitoh, N. Yamamoto, T. Tamura, H. Minami, K. Kubota, A. Ohtsu, T. Yoshida, N. Saijo, N. Kamatani, S. Ozawa, J. Sawada, Genetic variation and haplotype structure of the ABC transporter gene ABCG2 in a Japanese population. Drug Metab. Pharmacokinet. 21, 109-121 (2006).
35. H. Wang, E. W. Lee, X. Cai, Z. Ni, L. Zhou, Q. Mao, Membrane topology of the human breast cancer resistance protein (BCRP/ABCG2) determined by epitope insertion and immunofluorescence. Biochemistry 47, 13778 -13787 (2008).
36. N. Kartner, J. R. Riordan, V. Ling, Cell surface P-glycoprotein associated with multidrug resistance in mammalian cell lines. Science 221, 1285-1288 (1983).
37. S. G. Aller, J. Yu, A. Ward, Y. Weng, S. Chittaboina, R. Zhuo, P. M. Harrell, Y. T. Trinh, Q. Zhang, I. L. Urbatsch, G. Chang, Structure of P-glycoprotein reveals a molecular basis for polyspecific drug binding. Science 323, 1718-1722 (2009).
38. S. P. Cole, G. Bhardwaj, J. H. Gerlach, J. E. Mackie, C. E. Grant, K. C. Almquist, A. J. Stewart, E. U. Kurz, A. M. Duncan, R. G. Deeley, Overexpression of a transporter gene in a multidrugresistant human lung cancer cell line. Science 258, 1650-1654 (1992).
39. C. C. Paulusma, P. J. Bosma, G. J. Zaman, C. T. Bakker, M. Otter, G. L. Scheffer, R. J. Scheper, P. Borst, R. P. Oude Elferink, Congenital jaundice in rats with a mutation in a multidrug resistance-associated protein gene. Science 271, 1126- 1128 (1996).
40. M. Kool, M. de Haas, G. L. Scheffer, R. J. Scheper, M. J. van Eijk, J. A. Juijn, F. Baas, P. Borst, Analysis of expression of cMOAT (MRP2), MRP3, MRP4, and MRP5, homologues of the multidrug resistance-associated protein gene (MRP1), in human cancer cell lines. Cancer Res. 57, 3537-3547 (1997).
41. A. Tamura, K. Wakabayashi, Y. Onishi, M. Takeda, Y. Ikegami, S. Sawada, M. Tsuji, Y. Matsuda, T. Ishikawa, Re-evaluation and functional classification of non-synonymous single nucleotide polymorphisms of the human ATP-binding cassette transporter ABCG2 . Cancer Sci. 98, 231-239 (2007).
42. W. Zhang, B. N. Yu, Y. J. He, L. Fan, Q. Li, Z. Q. Liu, A. Wang, Y. L. Liu, Z. R. Tan, Fen-Jiang, Y. F. Huang, H. H. Zhou, Role of BCRP 421C>A polymorphism on rosuvastatin pharmacokinetics in healthy Chinese males. Clin. Chim. Acta 373, 99-103 (2006). Downloaded from stm.sciencemag.org on June 13, 2014
43. G. Cusatis, V. Gregorc, J. Li, A. Spreafico, R. G. Ingersoll, J. Verweij, V. Ludovini, E. Villa, M. Hidalgo, A. Sparreboom, S. D. Baker, Pharmacogenetics of ABCG2 and adverse reactions to gefitinib. J. Natl. Cancer Inst. 98, 1739-1742 (2006).
44. A. E. van Herwaarden, J. W. Jonker, E. Wagenaar, R. F. Brinkhuis, J. H. Schellens, J. H. Beijnen, A. H. Schinkel, The breast cancer resistance protein (Bcrp1/Abcg2) restricts exposure to the dietary carcinogen 2-amino-1-methyl-6- phenylimidazo[4,5-b]pyridine. Cancer Res. 63, 6447-6452 (2003).
45. J. W. Jonker, M. Buitelaar, E. Wagenaar, M. A. Van Der Valk, G. L. Scheffer, R. J. Scheper, T. Plosch, F. Kuipers, R. P. Elferink, H. Rosing, J. H. Beijnen, A. H. Schinkel, The breast cancer resistance protein protects against a major chlorophyll-derived dietary phototoxin and protoporphyria. Proc. Natl. Acad. Sci. U.S.A. 99, 15649-15654 (2002).
46. X. W. Wu, C. C. Lee, D. M. Muzny, C. T. Caskey, Urate oxidase: Primary structure and evolutionary implications. Proc. Natl. Acad. Sci. U.S.A. 86, 9412-9416 (1989).
47. C. C. Lee, X.W.Wu, R. A. Gibbs, R. G. Cook,D.M.Muzny, C. T. Caskey, Generation of cDNA probes directed by amino acid sequence: Cloning of urate oxidase. Science 239, 1288-1291 (1988).
48. R. G. Cutler, Urate and ascorbate: Their possible roles as antioxidants in determining longevity of mammalian species. Arch. Gerontol. Geriatr. 3, 321-348 (1984).
49. R. J. Torres, J. G. Puig, Hypoxanthine-guanine phosophoribosyltransferase (HPRT) deficiency: Lesch-Nyhan syndrome. Orphanet. J. Rare Dis. 2, 48 (2007).
50. E. Zoref-Shani, S. Feinstein, Y. Frishberg, Y. Bromberg, O. Sperling, Kelley-Seegmiller syndrome due to a unique variant of hypoxanthine-guanine phosphoribosyltransferase: Reduced affinity for 5-phosphoribosyl-1-pyrophosphate manifested only at low, physiological substrate concentrations. Biochim. Biophys. Acta 1500, 197-203 (2000).
51. B. J. Roessler, J. M. Nosal, P. R. Smith, S. A. Heidler, T. D. Palella, R. L. Switzer, M. A. Becker, Human X-linked phosphoribosylpyrophosphate synthetase superactivity is associated with distinct point mutations in the PRPS1 gene. J. Biol. Chem. 268, 26476-26481 (1993).
52. M. A. Becker, L. J. Meyer, A. W. Wood, J. E. Seegmiller, Purine overproduction in man associated with increased phosphoribosylpyrophosphate synthetase activity. Science 179, 1123-1126 (1973).
53. N. Kamatani, M. Moritani, H. Yamanaka, F. Takeuchi, T. Hosoya, M. Itakura, Localization of a gene for familial juvenile hyperuricemic nephropathy causing underexcretion-type gout to 16p12 by genome-wide linkage analysis of a large family. Arthritis Rheum. 43, 925-929 (2000).
54. T. C. Hart, M. C. Gorry, P. S. Hart, A. S. Woodard, Z. Shihabi, J. Sandhu, B. Shirts, L. Xu, H. Zhu, M. M. Barmada, A. J. Bleyer, Mutations of the UMOD gene are responsible for medullary cystic kidney disease 2 and familial juvenile hyperuricaemic nephropathy. J. Med. Genet. 39, 882-892 (2002).
55. O. M. Woodward, A. Köttgen, J. Coresh, E. Boerwinkle, W. B. Guggino, M. Köttgen, Identification of a urate transporter, ABCG2, with a common functional polymorphism causing gout. Proc. Natl. Acad. Sci. U.S.A. 106, 10338-10342 (2009).
56. S. Nejentsev,N. Walker, D. Riches, M. Egholm, J. A. Todd, Rare variants of IFIH1, a gene implicated in antiviral responses, protect against type 1 diabetes. Science 324, 387-389 (2009).
57. H. Matsuo, K. Kamakura, M. Saito, M. Okano, T. Nagase, Y. Tadano, K. Kaida, A. Hirata, N. Miyamoto, T. Masaki, R. Nakamura, K. Motoyoshi, H. Tanaka, S. Tsuji, Familial paroxysmal dystonic choreoathetosis: Clinical findings in a large Japanese family and genetic linkage to 2q. Arch. Neurol. 56, 721-726 (1999).
58. H. Matsuo, K. Kamakura, S. Matsushita, T. Ohmori, M. Okano, Y. Tadano, S. Tsuji, S. Higuchi, Mutational analysis of the anion exchanger 3 gene in familial paroxysmal dystonic choreoathetosis linked to chromosome 2q. Am. J. Med. Genet. 88, 733-737 (1999).
59. T. Takada, H. M. Weiss, O. Kretz, G. Gross, Y. Sugiyama, Hepatic transport of PKI166, an epidermal growth factor receptor kinase inhibitor of the pyrrolo-pyrimidine class, and its main metabolite, ACU154, Drug Metab. Dispos. 32, 1272-1278 (2004).
60. K. Narushima, T. Takada, Y. Yamanashi, H. Suzuki, Niemann-Pick C1-like 1 mediates a-tocopherol transport. Mol. Pharmacol. 74, 42-49 (2008).
61. Y. Kitamura, M. Moriguchi, H. Kaneko, H. Morisaki, T. Morisaki, K. Toyama, N. Kamatani, Determination of probability distribution of diplotype configuration (diplotype distribution) for each subject from genotypic data using the EM algorithm. Ann. Hum. Genet. 66, 183-193 (2002).