Genome-wide association analysis confirms and extends the association of SLC2A9 with serum uric acid levels to mexican americans

Frontiers in Genetics

Volumn 4, Issue DEC, 2013, Pages

  Voruganti, Venkata Saroja ^a,b   Kent, Jack W ^a   Debnath, Subrata ^c   Cole, Shelley A ^a   Haack, Karin ^a   Göring, Harald H H ^a   Carless, Melanie A ^a   Curran, Joanne E ^a   Johnson, Matthew P ^a   Almasy, Laura ^a   Dyer, Thomas D ^a   MacCluer, Jean W ^a   Moses, Eric K ^a,d   Abboud, Hanna E ^c   Mahaney, Michael C ^a   Blangero, John ^a   Comuzzie, Anthony G ^a  

^a SOUTHWEST FOUNDATION FOR BIOMEDICAL RESEARCH   (United States)

^b University of North Carolina   (United States)

^c UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^d UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Hyperuricemia; Joint linkage association analysis; Kinship; Variance components decomposition approach

Indexed keywords

EID: 84892383574     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2013.00279     Document Type: Article

References (70)

1. Abecasis, G. R., Cherny, S. S., Cookson, W. O., and Cardon, L. R. (2002). Merlin-rapid analysis of dense genetic maps using sparse gene flow trees. Nat. Genet. 30, 97-101. doi: 10.1038/ng786.
2. Almasy, L., and Blangero, J. (1998). Multipoint quantitative-trait linkage analysis in general pedigrees. Am. J. Hum. Genet. 62, 1198-1211. doi: 10.1086/301844.
3. Arar, N. H., Voruganti, V. S., Nath, S. D., Thameem, F., Bauer, R., Cole, S. A., et al. (2008). A genome-wide search for linkage to chronic kidney disease in a community-based sample: the SAFHS. Nephrol. Dial. Transplant. 23, 3184-3191. doi: 10.1093/ndt/gfn215.
4. Boerwinkle, E., Chakroborty, R., and Sing, C. F. (1986). The use of measured genotype information in the analysis of quantitative phenotypes in man. I. Models and analytical methods. Ann. Hum. Genet. 50, 181-194. doi: 10.1111/j.1469-1809.1986.tb01037.x.
5. Brandstätter, A., Kiechl, S., Kollerits, B., Hunt, S. C., Heid, I. M., Coassin, S., et al. (2008). Sex-specific association of the putative fructose transporter SLC2A9 variants with uric acid levels is modified by BMI. Diabetes Care 31, 1662-1667. doi: 10.2337/dc08-0349.
6. Cameron, J. S., and Simmonds, H. A. (2005). Hereditary hyperuricemia and renal disease. Semin. Nephrol. 25, 9-18. doi: 10.1016/j.semnephrol.2004.09.003.
7. Caulfield, M. J., Munroe, P. B., O'Neill, D., Witkowska, K., Charchar, F. J., Doblado, M., et al. (2008). SLC2A9 is a high-capacity urate transporters in humans. PLoS Med. 5:e197. doi: 10.1371/journal.pmed.0050197.
8. Charles, B. A., Shriner, D., Doumatey, A., Chen, G., Zhou, J., Huang, H., et al. (2011). A genome-wide association study of serum uric acid in African Americans. BMD Med. Genomics 4, 4-17. doi: 10.1186/1755-8794-4-17.
9. Cheeseman, C. (2009). Solute carrier family 2, member 9 and uric acid homeostasis. Curr. Opin. Nephrol. Hypertens. 18, 428-432. doi: 10.1097/MNH.0b013e32832ee3de.
10. Cirillo, P., Sato, W., Reungjui, S., Heinig, M., Gesch, M., Sautin, Y., et al. (2006). Uric acid, the metabolic syndrome, and renal disease. J. Am. Soc. Nephrol. 17, S165-S168. doi: 10.1681/ASN.2006080909.
11. Culleton, B. F. (2001). Uric acid and cardiovascular disease: a renal-cardiac relationship? Curr. Opin. Nephrol. Hypertens. 10, 371-375. doi: 10.1097/00041552-200105000-00012.
12. Cummings, N., Dyer, T. D., Kotea, N., Kowlessur, S., Chitson, P., Zimmet, P., et al. (2010). Genome-wide scan identifies a quantitative trait locus at 4p15.3 for serum urate. Eur. J. Hum. Genet. 18, 1243-1247. doi: 10.1038/ejhg.2010.97.
13. Dehghan, A., Köttgen, A., Yang, Q., Hwang, S. J., Kao, W. L., Rivadeneira, F., et al. (2008). Association of three genetic loci with uric acid concentration and risk of gout: a genome-wide association study. Lancet 372, 1953-1961. doi: 10.1016/S0140-6736(08)61343-4.
14. Dixon, A. S. (1960). Familial hyperuricemic nephropathy. Proc. R. Soc. Med. 53, 967-968.
15. Domagk, G. F., and Schlicke, H. H. (1968). A colorimetric method using uricase and peroxidase for the determination of uric acid. Anal. Biochem. 22, 219-224. doi: 10.1016/0003-2697(68)90309-6.
16. Doria, A., and Krolewski, A. S. (2011). Lowering' serum uric acid levels to prevent kidney failure. Nat. Rev. Nephrol. 7, 495-496.
17. Döring, A., Gieger, C., Mehta, D., Gohlke, H., Prokisch, H., Coassin, S., et al. (2008). SLC2A9 influences uric acid concentrations with pronounced sex-specific effects. Nat. Genet. 40, 430-436. doi: 10.1038/ng.107.
18. Ejaz, A. A., Dass, B., Kambhampati, G., Ejaz, N. I., Maroz, N., Dhatt, G. S., et al. (2012). Lowering serum uric acid to prevent acute kidney injury. Med. Hypotheses 78, 796-799. doi: 10.1016/j.mehy.2012.03.011.
19. Feig, D. I. (2009). Uric acid: a novel mediator and marker of risk in chronic kidney disease? Curr. Opin. Nephrol. Hypertens. 18, 526-530. doi: 10.1097/MNH.0b013e328330d9d0.
20. Flegal, K. M., Ezzati, T. M., Harris, M. I., Haynes, S. G., Juarez, R. Z., Knowler, W. C., et al. (1991). Prevalence of diabetes in Mexican Americans, Cubans, and Puerto Ricans from the Hispanic Health and Nutrition Examination Survey, 1982-1984. Diabetes Care. 14, 628-638. doi: 10.2337/diacare.14.7.628.
21. Friedlander, Y., Kark, J. D., and Stein, Y. (1988). Family resemblance for serum uric acid in a Jerusalem sample of families. Hum. Genet. 79, 58-63. doi: 10.1007/BF00291711.
22. Go, A. S. (2013). Heart disease and stroke statistics-2013 update: a report from the American Heart Association. Circulation 127, e6. doi: 10.1161/CIR.0b013e31828124ad.
23. Gotsman, I., Kereb, A., Lotan, C., and Zwas, D. R. (2012). Changes in uric acid levels and allopurinol use' in chronic heart failure: association with improved survival. J. Card. Fail. 18, 694-701. doi: 10.1016/j.cardfail.2012.06.528.
24. Guan, M., Zhou, D., Ma, W., Chen, Y., Zhang, J., and Zou, H. (2011). Association of an intronic SNP of SLC2A9 gene with serum uric acid levels in the Chinese male Han population by high-resolution melting method. Clin. Rheumatol. 30, 29-35. doi: 10.1007/s10067-010-1597-x.
25. Johnson, R. J., Kang, D. H., Feig, D., Kivlighn, S., Kanellis, J., Watanabe, S., et al. (2003). Is there a pathogenetic role for uric acid in hypertension and cardiovascular and renal disease? Hypertension 41, 1183-1190. doi: 10.1161/01.HYP.0000069700.62727.C5.
26. Johnson, R. J., Lanaspa, M. A., and Gaucher, E. A. (2011). Uric acid: a danger signal from the RNA world that may have a role in the epidemic of obesity, metabolic syndrome, and cardiorenal disease: evolutionary considerations. Semin. Nephrol. 31, 394-399. doi: 10.1016/j.semnephrol.2011.08.002.
27. Karns, R., Zhang, G., Sun, G., Rao Indugula, S., Cheng, H., Havas-Augustin, D., et al. (2012). Genome-wide association of serum uric acid concentration: replication of sequence variants in an island populations of the Adriatic coast of Croatia. Ann. Hum. Genet. 75, 121-127. doi: 10.1111/j.1469-1809.2011.00698.x.
28. Kolz, M., Johnson, T., Sanna, S., Teumer, A., Vitart, V., Perola, M., et al. (2009). Meta-analysis of 28,141 individuals identifies common variants within five new loci that influence uric acid concentrations. PLoS Genet. 5:e1000504. doi: 10.1371/journal.pgen.1000504.
29. Köttgen, A., Albrecht, E., Teumer, A., Vitart, V., Krumsiek, J., Hundertmark, C., et al. (2013). Genome-wide association analyses identify 18 new loci associated with serum urate concentrations. Nat. Genet. 45, 145-154. doi: 10.1038/ng.2500.
30. Le, M. T., Shafiu, M., Mu, W., and Johnson, R. J. (2008). SLC2A9-a fructose transporter identified as a novel uric acid transporter. Nephrol. Dial. Transplant. 23, 2746-2749. doi: 10.1093/ndt/gfn349.
31. Li, S., Sanna, S., Maschio, A., Busonero, F., Usala, G., Mulas, A., et al. (2007). The GLUT9 gene is associated with serum uric acid levels in Sardinia and Chianti cohorts. PLoS Genet. 3:e194. doi: 10.1371/journal.pgen.0030194.
32. Liebman, S. E., Taylor, J. G., and Bushinsky, D. A. (2007). Uric acid nephrolithiasis. Curr. Rheumatol. Rep. 9, 251-257. doi: 10.1007/s11926-007-0040-z.
33. Liu, W. C., Hung, C. C., Chen, S. C., Lin, M. Y., Chen, L. I., Hwang, D. Y., et al. (2011). The rs1014290 polymorphisms of the SLC2A9 gene is associated with type 2 diabetes mellitus in Han Chinese. Exp. Diabetes Res. 2011:527520. doi: 10.1155/2011/527520.
34. MacCluer, J. W., Stern, M. P., Almasy, L., Atwood, L. A., Blangero, J., Comuzzie, A. G., et al. (1999). Genetics of atherosclerosis risk factors in Mexican Americans. Nutr. Rev. 57, S59-S65. doi: 10.1111/j.1753-4887.1999.tb01790.x.
35. Maher, B. (2008). Personal genomes: the case of the missing heritability. Nature 456, 18-21. doi: 10.1038/456018a.
36. Manolio, T. A., Collins, F. S., Cox, N. J., Goldstein, D. B., Hindorff, L. A., Hunter, D. J., et al. (2009). Finding the missing heritability of complex diseases. Nature 461, 747-753. doi: 10.1038/nature08494.
37. Matsuo, H., Chiba, T., Nagamori, S., Nakayama, A., Domoto, H., Phetdee, K., et al. (2008). Mutations in glucose transporter 9 gene SLC2A9 cause renal hypouricemia. Am. J. Hum. Genet. 83, 744-751. doi: 10.1016/j.ajhg.2008.11.001.
38. McArdle, P. F., Parsa, A., Chang, Y. P., Weir, M. R., O'Connell, J. R., Mitchell, B. D., et al. (2008). Association of a common nonsynonymous variant in GLUT9 with serum uric acid levels in old order amish. Arthritis Rheum. 58, 2874-2881. doi: 10.1002/art.23752.
39. Mitchell, B. D., Almasy, L. A., Rainwater, D. L., Schneider, J. L., Blangero, J., Stern, M. P., et al. (1999). Diabetes and hypertension in Mexican American families: relation to cardiovascular risk. Am. J. Epidemiol. 149, 1047-1056. doi: 10.1093/oxfordjournals.aje.a009750.
40. Nakagawa, T., Kang, D.-H., Feig, D., Sanchez-Lozada, L. G., Srinivas, T. R., Ejaz, A. A., et al. (2006). Unearthing uric acid: an ancient factor with recently found significance in renal and CVD. Kidney Int. 69, 1722-1725. doi: 10.1038/sj.ki.5000391.
41. Nakagawa, T., Tuttle, K. R., Short, R. A., and Johnson, R. J. (2005). Hypothesis: fructoseinduced hyperuricemia as a causal mechanism for the epidemic of the metabolic syndrome. Nat. Clin. Pract. Nephrol. 1, 80-86. doi: 10.1038/ncpneph0019.
42. Nakayama, A., Matsuo, H., Takada, T., Ichida, K., Nakamura, T., Ikebuchi, Y., et al. (2011). ABCG2 is a high-capacity urate transporter and its genetic impairment increases serum uric acid levels in humans. Nucleosides Nucleotides Nucleic Acids 30, 1091-1097. doi: 10.1080/15257770.2011.633953.
43. Nath, S. D., Voruganti, V. S., Arar, N. H., Thameem, F., Lopez-Alvarenga, J. C., Bauer, R., et al. (2007). Genome scan for determinants of serum uric acid variability. J. Am. Soc. Nephrol. 18, 3156-3163. doi: 10.1681/ASN.2007040426.
44. Parsa, A., Brown, E., Weir, M. R., Fink, J. C., Shuldiner, A. R., Mitchell, B. D., et al. (2012). Genotype-based changes in serum uric acid affect blood pressure. Kidney Int. 81, 502-507. doi: 10.1038/ki.2011.414.
45. Pasalic, D., Marinkovic, N., and Feher-Turkovic, L. (2012). Uric acid as one of the important factors in multifactorial disorders: facts and controversies. Biochem. Med. (Zagrab) 22, 63-75. doi: 10.11613/BM.2012.007.
46. Preitner, F., Bonny, O., Laverriere, A., Rotman, S., Firsov, D., Da Costa, A., et al. (2009). Glut9 is a major regulator of urate homeostasis and its genetic inactivation induces hyperuricosuria and urate nephropathy. Proc. Natl. Acad. Sci. U.S.A. 106, 15501-15506. doi: 10.1073/pnas.0904411106.
47. Rajendra, N. S., Ireland, S., George, J., Beich, J. J., Lang, C. C., and Struthers, A. D. (2011). Mechanistic insights into the therapeutic use of high-dose allopurinol manqlna pectoris. J. Am. Coli. Cardiol. 58, 820-828. doi: 10.1016/j.jacc.2010.12.052.
48. Rao, D. C., Laskarzewski, P. M., Morrison, J. A., Kelly, K., and Glueck, C. J. (1982). The clinical Lipid Research Clinic Family Study: familial determinants of plasma uric acid. Hum. Genet. 60, 257-261. doi: 10.1007/BF00303013.
49. Rice, T., Vogler, G. P., Perry, T. S., Laskarzewski, P. M., Province, M. A., and Rao, D. C. (1990). Heterogenity in the familial aggregation of fasting uric acid levels in five North American populations: the Lipid Research Clinics Family Study. Am. J. Med. Genet. 36, 219-225. doi: 10.1002/ajmg.1320360216.
50. Rule, A. D., de Andrade, M., Matsumoto, M., Mosley, T. H., Kardia, S., and Turner, S. T. (2011). Association between SLC2A9 transporter gene variants and uric acid phenotypes in African. American and white families. Rheumatology (Oxford) 50, 871-878. doi: 10.1093/rheumatology/keq425.
51. Rule, A. D., Fridley, B. L., Hunt, S. C., Asmann, Y., Boerwinkle, E., Pankow, J. S., et al. (2009). Genome-wide linkage analysis for uric acid in families enriched for hypertension. Nephrol. Dial. Transplant. 24, 2414-2420. doi: 10.1093/ndt/gfp080.
52. Sánchez-Lozada, L. G., Tapia, E., Avila-Casado, C., Soto, V., Franco, M., Santamaría, J., et al. (2002). Mild hyperuricemia induces glomerular hypertension in normal rats. Am. J. Physiol. Renal Physiol. 283, F1105-F1110. doi: 10.1152/ajprenal.00170.2002.
53. Self, S. G., and Liang, K.-Y. (1987). Asymptotic properties of maximum likelihood estimators and likelihood ratio tests under nonstandard conditions. J. Am. Stat. Assoc. 82, 605-610. doi: 10.1080/01621459.1987.10478472.
54. Sobel, E., and Lange, K. (1996). Descent graphs in pedigree analysis: Applications to haplotyping, location scores, and marker-sharing statistics. Ann. Hum. Genet. 58, 1323-1337.
55. Stark, K., Reinhard, W., Neureuther, K., Wiedmann, S., Sedlacek, K., Baessler, A., et al. (2008). Association of common polymorphisms in GLUT9 gene with gout but not with coronary artery disease in a large case-control study. PLoS ONE 3:e1948. doi: 10.1371/journal.pone.0001948.
56. Tabara, Y., Kohara, K., Kawamoto, R., Hiura, Y., Nishimura, K., Morisaki, T., et al. (2010). Association of four genetic loci with uric acid levels and reduced renal function: the J-SHIPP Suita study. Am. J. Nephrol. 32, 279-286. doi: 10.1159/000318943.
57. Tang, W., Miller, M. B., Rich, S. S., North, K. E., Pankow, J. S., Borecki, I. B., et al. (2003). Linkage analysis of a composite factor for the multiple metabolic syndrome. The National Heart, Lung and Blood Institute Family Heart Study. Diabetes 52, 2840-2847. doi: 10.2337/diabetes.52.11.2840.
58. Tin, A., Woodward, O. M., Kao, W. H., Liu, C. T., Lu, X., Nalls, M. A., et al. (2011). Genome-wide association study for serum urate concentrations and gout among African Americans identifies genomic risk loci and a novel URAT 1 loss-of-function allele. Hum. Mol. Genet. 20, 4056-4068. doi: 10.1093/hmg/ddr307.
59. Tu, H. P., Chen, C. J., Tovosia, S., Ko, A. M., Lee, C. H., Ou, T. T., et al. (2010). Associations of a non-synonymous variant in SLC2A9 with gouty arthritis and uric acid levels in Han Chinese subjects and Solomon Islanders. Ann. Rheum. Dis. 69, 887-890. doi: 10.1136/ard.2009.113357.
60. Vitart, V., Rudan, I., Hayward, C., Gray, N. K., Floyd, J., Palmer, C. N., et al. (2008). SLC2A9 is a newly identified urate transporter influencing serum urate concentration, urate excretion and gout. Nat. Genet. 40, 437-442. doi: 10.1038/ng.106.
61. Voruganti, V. S., Nath, S. D., Cole, S. A., Thameem, F., Jowett, J. B., Bauer, R., et al. (2009a). Genetics of variation in serum uric acid and cardiovascular risk factors in Mexican-Americans. J. Clin. Endocrinol. Metab. 94, 632-638. doi: 10.1210/jc.2008-0682.
62. Voruganti, V. S., Goring, H. H. H., Mottl, A., Franceschini, N., Haack, K., Laston, S., et al. (2009b). Genetic influence on variation in serum uric acid in American Indians: the Strong Heart Family Study. Hum. Genet. 126, 667-676. doi: 10.1007/s00439-009-0716-8.
63. Wallace, C., Newhouse, S. J., Braund, P., Zhang, F., Tobin, M., Falchi, M., et al. (2008). Genome-wide association study identifies genes for biomarkers of cardiovascular disease: serum urate and dyslipidemia. Am. J. Hum. Genet. 82, 139-149. doi: 10.1016/j.ajhg.2007.11.001.
64. Wilk, J. B., Djousse, L., Borecki, I., Atwood, L. D., Hunt, S. C., Rich, S. S., et al. (2000). Segregation analysis of serum uric acid in the NHLBI Family Heart Study. Hum. Genet. 106, 355-359. doi: 10.1007/s004390051050.
65. Woodward, O. M., Kottgen, A., Coresh, J., Boerwinkle, E., Guggino, W. B., and Kottgen, M. (2009). Identification of a urate transporter, ABCG2, with a common functional polymorphism causing gout. Proc. Natl. Acad. Sci. U.S.A. 106, 10338-10342. doi: 10.1073/pnas.0901249106.
66. Yang, Q., Guo, C. Y., Cupples, A., Levy, D., Wilson, P. W., and Fox, C. S. (2005). Genome-wide search for genes affecting serum uric acid levels: the Framingham Heart Study. Metabolism 54, 1435-1441. doi: 10.1016/j.metabol.2005.05.007.
67. Yang, Q., Köttgen, A., Dehghan, A., Smith, A. V., Glazer, N. L., Chen, M. H., et al. (2010). Multiple genetic loci influence serum urate levels and their relationship with gout and cardiovascular disease risk factors. Circ. Cardiovasc. Genet. 3, 523-530. doi: 10.1161/CIRCGENETICS.109.934455.
68. Yelken, B., Caliskan, Y., Gorgulu, N., Altun, I., Yimaz, A., Yazici, H., et al. (2012). Reduction of uric acid levels with allopurinol treatment improves endothelial function in patients with chronic kidney disease. Clin. Nephrol. 77, 275-282. doi: 10.5414/CN107352.
69. Zemunik, T., Boban, M., Lauc, G., Jankovi'c, S., Rotim, K., Vatavuk, Z., et al. (2009). Genome-wide association study of biochemical traits in Korcula Island, Croatia. Croat. Med. J. 50, 23-33. doi: 10.3325/cmj.2009.50.23.
70. Zhang, L., Spencer, K. L., Voruganti, V. S., Jorgensen, N. W., Fornage, M., Best, L. G., et al. (2013). Association of functional polymorphisms rs2231142 (Q141K) in the ABCG2 gene with serum uric acid and gout in 4 US populations: the PAGE study. Am. J. Epidemiol. doi: 10.1093/aje/kws330. [Epub ahead of print].