Genome-wide association study identifies a new locus JMJD1C at 10q21 that may influence serum androgen levels in men

Human Molecular Genetics

Volumn 21, Issue 23, 2012, Pages 5222-5228

  Jin, Guangfu ^a   Sun, Jielin ^a   Kim, Seong Tae ^a   Feng, Junjie ^a   Wang, Zhong ^a   Tao, Sha ^a   Chen, Zhuo ^a   Purcell, Lina ^a   Smith, Shelly ^a   Isaacs, William B ^b   Rittmaster, Roger S ^c   Lilly Zheng, S ^a   Condreay, Lynn D ^c   Xu, Jianfeng ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b DEPARTMENT OF PATHOLOGY   (United States)

^c GLAXOSMITHKLINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; ANDROSTANOLONE; DNA; DUTASTERIDE; PLACEBO; PROSTATE SPECIFIC ANTIGEN; SEX HORMONE BINDING GLOBULIN; STEROID 5ALPHA REDUCTASE INHIBITOR; TESTOSTERONE;

ADULT; AGED; ANDROGEN BLOOD LEVEL; ARTICLE; CANCER RISK; CANCER STAGING; CHROMOSOME 10Q; DOUBLE BLIND PROCEDURE; EUROPE; GENE LOCUS; GENETIC ASSOCIATION; GENOTYPE; GLEASON SCORE; HUMAN; MAJOR CLINICAL STUDY; MALE; MULTICENTER STUDY (TOPIC); PRIORITY JOURNAL; PROSTATE CANCER; RANDOMIZED CONTROLLED TRIAL (TOPIC); RISK REDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; TESTOSTERONE BLOOD LEVEL; TREATMENT OUTCOME;

AGED; ANDROGENS; CHROMOSOMES, HUMAN, PAIR 10; CHROMOSOMES, HUMAN, PAIR 17; CHROMOSOMES, HUMAN, X; DIHYDROTESTOSTERONE; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; HUMANS; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; MALE; MIDDLE AGED; OXIDOREDUCTASES, N-DEMETHYLATING; POLYMORPHISM, SINGLE NUCLEOTIDE; TESTOSTERONE;

EID: 84869077514     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds361     Document Type: Article

References (40)

1. Mooradian, A.D., Morley, J.E. and Korenman, S.G. (1987) Biological actions of androgens. Endocr. Rev., 8, 1-28.
2. Penning, T.M. (2010) New frontiers in androgen biosynthesis and metabolism. Curr. Opin. Endocrinol. Diabetes Obes., 17, 233-239.
3. Labrie, F. (2004) Adrenal androgens and intracrinology. Semin. Reprod. Med., 22, 299-309.
4. Imamoto, T., Suzuki, H., Yano, M., Kawamura, K., Kamiya, N., Araki, K., Komiya, A., Nihei, N., Naya, Y. and Ichikawa, T. (2008) The role of testosterone in the pathogenesis of prostate cancer. Int. J. Urol., 15, 472-480.
5. Ring, H.Z., Lessov, C.N., Reed, T., Marcus, R., Holloway, L., Swan, G.E. and Carmelli, D. (2005) Heritability of plasma sex hormones and hormone binding globulin in adult male twins. J. Clin. Endocrinol. Metab., 90, 3653-3658.
6. Kuijper, E.A., Lambalk, C.B., Boomsma, D.I., van der Sluis, S., Blankenstein, M.A., de Geus, E.J. and Posthuma, D. (2007) Heritability of reproductive hormones in adult male twins. Hum. Reprod., 22, 2153-2159.
7. Ohlsson, C., Wallaschofski, H., Lunetta, K.L., Stolk, L., Perry, J.R., Koster, A., Petersen, A.K., Eriksson, J., Lehtimaki, T., Huhtaniemi, I.T. et al. (2011) Genetic determinants of serum testosterone concentrations in men. PLoS Genet., 7, e1002313.
8. Ding, E.L., Song, Y., Malik, V.S. and Liu, S. (2006) Sex differences of endogenous sex hormones and risk of type 2 diabetes: a systematic review and meta-analysis. JAMA, 295, 1288-1299.
9. Ruige, J.B., Mahmoud, A.M., De Bacquer, D. and Kaufman, J.M. (2011) Endogenous testosterone and cardiovascular disease in healthy men: a meta-analysis. Heart, 97, 870-875.
10. Brand, J.S., van der Tweel, I., Grobbee, D.E., Emmelot-Vonk, M.H. and van der Schouw, Y.T. (2011) Testosterone, sex hormone-binding globulin and the metabolic syndrome: a systematic review and meta-analysis of observational studies. Int. J. Epidemiol., 40, 189-207.
11. Chasman, D.I., Pare, G., Mora, S., Hopewell, J.C., Peloso, G., Clarke, R., Cupples, L.A., Hamsten, A., Kathiresan, S., Malarstig, A. et al. (2009) Forty-three loci associated with plasma lipoprotein size, concentration, and cholesterol content in genome-wide analysis. PLoS Genet., 5, e1000730.
12. Teslovich, T.M., Musunuru, K., Smith, A.V., Edmondson, A.C., Stylianou, I.M., Koseki, M., Pirruccello, J.P., Ripatti, S., Chasman, D.I., Willer, C.J. et al. (2010) Biological, clinical and population relevance of 95 loci for blood lipids. Nature, 466, 707-713.
13. Yuan, X., Waterworth, D., Perry, J.R., Lim, N., Song, K., Chambers, J.C., Zhang, W., Vollenweider, P., Stirnadel, H., Johnson, T. et al. (2008) Population-based genome-wide association studies reveal six loci influencing plasma levels of liver enzymes. Am. J. Hum. Genet., 83, 520-528.
14. Kim, S.M., Kim, J.Y., Choe, N.W., Cho, I.H., Kim, J.R., Kim, D.W., Seol, J.E., Lee, S.E., Kook, H., Nam, K.I. et al. (2010) Regulation of mouse steroidogenesis by WHISTLE and JMJD1C through histone methylation balance. Nucleic Acids Res., 38, 6389-6403.
15. Siiteri, P.K., Murai, J.T., Hammond, G.L., Nisker, J.A., Raymoure, W.J. and Kuhn, R.W. (1982) The serum transport of steroid hormones. Recent Prog. Horm. Res., 38, 457-510.
16. Rosner, W., Hryb, D.J., Kahn, S.M., Nakhla, A.M. and Romas, N.A. (2010) Interactions of sex hormone-binding globulin with target cells. Mol. Cell Endocrinol., 316, 79-85.
17. Hsing, A.W., Chu, L.W. and Stanczyk, F.Z. (2008) Androgen and prostate cancer: is the hypothesis dead? Cancer Epidemiol. Biomarkers Prev., 17, 2525-2530.
18. Roddam, A.W., Allen, N.E., Appleby, P. and Key, T.J. (2008) Endogenous sex hormones and prostate cancer: a collaborative analysis of 18 prospective studies. J. Natl Cancer Inst., 100, 170-183.
19. Cousin, P., Dechaud, H., Grenot, C., Lejeune, H. and Pugeat, M. (1998) Human variant sex hormone-binding globulin (SHBG) with an additional carbohydrate chain has a reduced clearance rate in rabbit. J. Clin. Endocrinol. Metab., 83, 235-240.
20. Dunning, A.M., Dowsett, M., Healey, C.S., Tee, L., Luben, R.N., Folkerd, E., Novik, K.L., Kelemen, L., Ogata, S., Pharoah, P.D. et al. (2004) Polymorphisms associated with circulating sex hormone levels in postmenopausal women. J. Natl Cancer Inst., 96, 936-945.
21. Cousin, P., Calemard-Michel, L., Lejeune, H., Raverot, G., Yessaad, N., Emptoz-Bonneton, A., Morel, Y. and Pugeat, M. (2004) Influence of SHBG gene pentanucleotide TAAAA repeat and D327N polymorphism on serum sex hormone-binding globulin concentration in hirsute women. J. Clin. Endocrinol. Metab., 89, 917-924.
22. Haiman, C.A., Riley, S.E., Freedman, M.L., Setiawan, V.W., Conti, D.V. and Le Marchand, L. (2005) Common genetic variation in the sex steroid hormone-binding globulin (SHBG) gene and circulating shbg levels among postmenopausal women: the Multiethnic Cohort. J. Clin. Endocrinol. Metab., 90, 2198-2204.
23. Thompson, D.J., Healey, C.S., Baynes, C., Kalmyrzaev, B., Ahmed, S., Dowsett, M., Folkerd, E., Luben, R.N., Cox, D., Ballinger, D. et al. (2008) Identification of common variants in the SHBG gene affecting sex hormone-binding globulin levels and breast cancer risk in postmenopausal women. Cancer Epidemiol. Biomarkers Prev., 17, 3490-3498.
24. Ding, E.L., Song, Y., Manson, J.E., Hunter, D.J., Lee, C.C., Rifai, N., Buring, J.E., Gaziano, J.M. and Liu, S. (2009) Sex hormone-binding globulin and risk of type 2 diabetes in women and men. N. Engl. J. Med., 361, 1152-1163.
25. Vanbillemont, G., Bogaert, V., De Bacquer, D., Lapauw, B., Goemaere, S., Toye, K., Van Steen, K., Taes, Y. and Kaufman, J.M. (2009) Polymorphisms of the SHBG gene contribute to the interindividual variation of sex steroid hormone blood levels in young, middle-aged and elderly men. Clin. Endocrinol., 70, 303-310.
26. Wickham, E.P. 3rd, Ewens, K.G., Legro, R.S., Dunaif, A., Nestler, J.E. and Strauss, J.F. 3rd (2011) Polymorphisms in the SHBG gene influence serum SHBG levels in women with polycystic ovary syndrome. J. Clin. Endocrinol. Metab., 96, E719-E727.
27. Turk, A., Kopp, P., Colangelo, L.A., Urbanek, M., Wood, K., Liu, K., Skinner, H.G. and Gapstur, S.M. (2008) Associations of serum sex hormone binding globulin (SHBG) levels with SHBG gene polymorphisms in the CARDIA Male Hormone Study. Am. J. Epidemiol., 167, 412-418.
28. Eriksson, A.L., Lorentzon, M., Mellstrom, D., Vandenput, L., Swanson, C., Andersson, N., Hammond, G.L., Jakobsson, J., Rane, A., Orwoll, E.S. et al. (2006) SHBG gene promoter polymorphisms in men are associated with serum sex hormone-binding globulin, androgen and androgen metabolite levels, and hip bone mineral density. J. Clin. Endocrinol. Metab., 91, 5029-5037.
29. Ahn, J., Schumacher, F.R., Berndt, S.I., Pfeiffer, R., Albanes, D., Andriole, G.L., Ardanaz, E., Boeing, H., Bueno-de-Mesquita, B., Chanock, S.J. et al. (2009) Quantitative trait loci predicting circulating sex steroid hormones in men from the NCI-Breast and Prostate Cancer Cohort Consortium (BPC3). Hum. Mol. Genet., 18, 3749-3757.
30. Huhtaniemi, I.T., Pye, S.R., Holliday, K.L., Thomson, W., O'Neill, T.W., Platt, H., Payne, D., John, S.L., Jiang, M., Bartfai, G. et al. (2010) Effect of polymorphisms in selected genes involved in pituitary-testicular function on reproductive hormones and phenotype in aging men. J. Clin. Endocrinol. Metab., 95, 1898-1908.
31. Melzer, D., Perry, J.R., Hernandez, D., Corsi, A.M., Stevens, K., Rafferty, I., Lauretani, F., Murray, A., Gibbs, J.R., Paolisso, G. et al. (2008) A genome-wide association study identifies protein quantitative trait loci (pQTLs). PLoS Genet., 4, e1000072.
32. Hogeveen, K.N., Talikka, M. and Hammond, G.L. (2001) Human sex hormone-binding globulin promoter activity is influenced by a (TAAAA)n repeat element within an Alu sequence. J. Biol. Chem., 276, 36383-36390.
33. Martinez-Garay, I., Jablonka, S., Sutajova, M., Steuernagel, P., Gal, A. and Kutsche, K. (2002) A new gene family (FAM9) of low-copy repeats in Xp22.3 expressed exclusively in testis: implications for recombinations in this region. Genomics, 80, 259-267.
34. Andriole, G., Bostwick, D., Brawley, O., Gomella, L., Marberger, M., Tindall, D., Breed, S., Somerville, M. and Rittmaster, R. (2004) Chemoprevention of prostate cancer in men at high risk: rationale and design of the REduction by DUtasteride of Prostate Cancer Events (REDUCE) trial. J. Urol., 172, 1314-1317.
35. Andriole, G.L., Bostwick, D.G., Brawley, O.W., Gomella, L.G., Marberger, M., Montorsi, F., Pettaway, C.A., Tammela, T.L., Teloken, C., Tindall, D.J. et al. (2010) Effect of dutasteride on the risk of prostate cancer. N. Engl. J. Med., 362, 1192-1202.
36. Marchini, J., Howie, B., Myers, S., McVean, G. and Donnelly, P. (2007) A new multipoint method for genome-wide association studies by imputation of genotypes. Nat. Genet., 39, 906-913.
37. Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M.A., Bender, D., Maller, J., Sklar, P., de Bakker, P.I., Daly, M.J. et al. (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet., 81, 559-575.
38. Price, A.L., Patterson, N.J., Plenge, R.M., Weinblatt, M.E., Shadick, N.A. and Reich, D. (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nat. Genet., 38, 904-909.
39. McNutt, L.A., Wu, C., Xue, X. and Hafner, J.P. (2003) Estimating the relative risk in cohort studies and clinical trials of common outcomes. Am. J. Epidemiol., 157, 940-943.
40. Coviello, A.D., Haring, R., Wellons, M., Vaidya, D., Lehtimaki, T., Keildson, S., Lunetta, K.L., HE, C., Fornage, M., Lagou, V. et al. (2012) A genome-wide association meta-analysis of circulating sex hormonebinding globulin reveals multiple loci implicated in sex steroid hormone regulation. PLoS Genet., 8, e1002805.