All Title Author
Keywords Abstract

PLOS ONE  2013 

Genome Wide Association Study of Age at Menarche in the Japanese Population

DOI: 10.1371/journal.pone.0063821

Full-Text   Cite this paper   Add to My Lib

Abstract:

Age at menarche (AAM) is a complex trait involving both genetic and environmental factors. To identify the genetic factors associated with AAM, we conducted a large-scale meta-analysis of genome-wide association studies using more than 15,000 Japanese female samples. Here, we identified an association between SNP (single nucleotide polymorphism) rs364663 at the LIN28B locus and AAM, with a P-value of 5.49×10?7 and an effect size of 0.089 (year). We also evaluated 33 SNPs that were previously reported to be associated with AAM in women of European ancestry. Among them, two SNPs rs4452860 and rs7028916 in TMEM38B indicated significant association with AAM in the same directions as reported in previous studies (P = 0.0013 with an effect size of 0.051) even after Bonferroni correction for the 33 SNPs. In addition, six loci in or near CCDC85A, LOC100421670, CA10, ZNF483, ARNTL, and RXRG exhibited suggestive association with AAM (P<0.05). Our findings elucidated the impact of genetic variations on AAM in the Japanese population.

References

[1]  Tena-Sempere M (2006) GPR54 and kisspeptin in reproduction. Hum Reprod Update 12: 631–639.
[2]  Susman EJ, Nottelmann ED, Inoff-Germain GE, Dorn LD, Cutler GB Jr, et al. (1985) The relation of relative hormonal levels and physical development and social-emotional behavior in young adolescents. Journal of Youth and Adolescence 14: 245–264.
[3]  Kaltiala-Heino R, Kosunen E, Rimpela M (2003) Pubertal timing, sexual behaviour and self-reported depression in middle adolescence. J Adolesc 26: 531–545.
[4]  Kaltiala-Heino R, Rimpela M, Rissanen A, Rantanen P (2001) Early puberty and early sexual activity are associated with bulimic-type eating pathology in middle adolescence. J Adolesc Health 28: 346–352.
[5]  Freedman DS, Khan LK, Serdula MK, Dietz WH, Srinivasan SR, et al. (2003) The relation of menarcheal age to obesity in childhood and adulthood: the Bogalusa heart study. BMC pediatrics 3: 3.
[6]  Kjaer K, Hagen C, Sand? S, Esh?j O (1992) Epidemiology of menarche and menstrual disturbances in an unselected group of women with insulin-dependent diabetes mellitus compared to controls. Journal of Clinical Endocrinology & Metabolism 75: 524–529.
[7]  Velie EM, Nechuta S, Osuch JR (2005) Lifetime reproductive and anthropometric risk factors for breast cancer in postmenopausal women. Breast Dis 24: 17–35.
[8]  Cooper GS, Ephross SA, Weinberg CR, Baird DD, Whelan EA, et al. (1999) Menstrual and reproductive risk factors for ischemic heart disease. Epidemiology 10: 255–259.
[9]  Fujiwara S, Kasagi F, Yamada M, Kodama K (1997) Risk factors for hip fracture in a Japanese cohort. Journal of Bone and Mineral Research 12: 998–1004.
[10]  Onland-Moret N, Peeters P, Van Gils C, Clavel-Chapelon F, Key T, et al. (2005) Age at menarche in relation to adult height. Am J Epidemiol 162: 623–632.
[11]  Anderson CA, Duffy DL, Martin NG, Visscher PM (2007) Estimation of variance components for age at menarche in twin families. Behav Genet 37: 668–677.
[12]  Towne B, Czerwinski SA, Demerath EW, Blangero J, Roche AF, et al. (2005) Heritability of age at menarche in girls from the Fels Longitudinal Study. American journal of physical anthropology 128: 210–219.
[13]  Treloar SA, Martin NG (1990) Age at menarche as a fitness trait: nonadditive genetic variance detected in a large twin sample. Am J Hum Genet 47: 137–148.
[14]  Anderson CA, Zhu G, Falchi M, Van Den Berg SM, Treloar SA, et al. (2008) A genome-wide linkage scan for age at menarche in three populations of European descent. Journal of Clinical Endocrinology & Metabolism 93: 3965.
[15]  Stavrou I, Zois C, Ioannidis JP, Tsatsoulis A (2002) Association of polymorphisms of the oestrogen receptor alpha gene with the age of menarche. Hum Reprod 17: 1101–1105.
[16]  Stavrou I, Zois C, Chatzikyriakidou A, Georgiou I, Tsatsoulis A (2006) Combined estrogen receptor alpha and estrogen receptor beta genotypes influence the age of menarche. Hum Reprod 21: 554–557.
[17]  Guo Y, Xiong DH, Yang TL, Guo YF, Recker RR, et al. (2006) Polymorphisms of estrogen-biosynthesis genes CYP17 and CYP19 may influence age at menarche: a genetic association study in Caucasian females. Hum Mol Genet 15: 2401–2408.
[18]  Xita N, Tsatsoulis A, Stavrou I, Georgiou I (2005) Association of SHBG gene polymorphism with menarche. Mol Hum Reprod 11: 459–462.
[19]  Rothenbuhler A, Fradin D, Heath S, Lefevre H, Bouvattier C, et al. (2006) Weight-adjusted genome scan analysis for mapping quantitative trait Loci for menarchal age. The Journal of clinical endocrinology and metabolism 91: 3534–3537.
[20]  Guo Y, Shen H, Xiao P, Xiong DH, Yang TL, et al. (2006) Genomewide linkage scan for quantitative trait loci underlying variation in age at menarche. The Journal of clinical endocrinology and metabolism 91: 1009–1014.
[21]  Elks CE, Perry JR, Sulem P, Chasman DI, Franceschini N, et al. (2010) Thirty new loci for age at menarche identified by a meta-analysis of genome-wide association studies. Nat Genet 42: 1077–1085.
[22]  Sulem P, Gudbjartsson DF, Rafnar T, Holm H, Olafsdottir EJ, et al. (2009) Genome-wide association study identifies sequence variants on 6q21 associated with age at menarche. Nat Genet 41: 734–738.
[23]  Ong KK, Elks CE, Li S, Zhao JH, Luan J, et al. (2009) Genetic variation in LIN28B is associated with the timing of puberty. Nature genetics 41: 729–733.
[24]  He C, Kraft P, Chen C, Buring JE, Pare G, et al. (2009) Genome-wide association studies identify loci associated with age at menarche and age at natural menopause. Nature genetics 41: 724–728.
[25]  Perry JR, Stolk L, Franceschini N, Lunetta KL, Zhai G, et al. (2009) Meta-analysis of genome-wide association data identifies two loci influencing age at menarche. Nat Genet 41: 648–650.
[26]  Nakamura Y (2007) The BioBank Japan Project. Clin Adv Hematol Oncol 5: 696–697.
[27]  Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, et al. (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 38: 904–909.
[28]  The International HapMap Consortium (2003) The International HapMap Project. Nature 426: 789–796.
[29]  Li Y, Willer C, Sanna S, Abecasis G (2009) Genotype imputation. Annu Rev Genomics Hum Genet 10: 387–406.
[30]  Li J, Guo YF, Pei Y, Deng HW (2012) The impact of imputation on meta-analysis of genome-wide association studies. PLoS One 7: e34486.
[31]  Okada Y, Kubo M, Ohmiya H, Takahashi A, Kumasaka N, et al. (2012) Common variants at CDKAL1 and KLF9 are associated with body mass index in east Asian populations. Nat Genet 44: 302–306.
[32]  Okada Y, Sim X, Go MJ, Wu JY, Gu D, et al. (2012) Meta-analysis identifies multiple loci associated with kidney function-related traits in east Asian populations. Nat Genet 44: 904–909.
[33]  Okada Y, Hirota T, Kamatani Y, Takahashi A, Ohmiya H, et al. (2011) Identification of nine novel loci associated with white blood cell subtypes in a Japanese population. PLoS Genet 7: e1002067.
[34]  Okada Y, Kamatani Y, Takahashi A, Matsuda K, Hosono N, et al. (2010) A genome-wide association study in 19 633 Japanese subjects identified LHX3-QSOX2 and IGF1 as adult height loci. Hum Mol Genet 19: 2303–2312.
[35]  Okada Y, Kamatani Y, Takahashi A, Matsuda K, Hosono N, et al. (2010) Common variations in PSMD3-CSF3 and PLCB4 are associated with neutrophil count. Hum Mol Genet 19: 2079–2085.
[36]  He C, Kraft P, Chasman DI, Buring JE, Chen C, et al. (2010) A large-scale candidate gene association study of age at menarche and age at natural menopause. Human genetics 128: 515–527.
[37]  Kumar V, Kato N, Urabe Y, Takahashi A, Muroyama R, et al. (2011) Genome-wide association study identifies a susceptibility locus for HCV-induced hepatocellular carcinoma. Nat Genet In press
[38]  Kumar V, Kato N, Urabe Y, Takahashi A, Muroyama R, et al. (2011) Genome-wide association study identifies a susceptibility locus for HCV-induced hepatocellular carcinoma. Nat Genet 43: 455–458.
[39]  Tanikawa C, Urabe Y, Matsuo K, Kubo M, Takahashi A, et al. (2012) A genome-wide association study identifies two susceptibility loci for duodenal ulcer in the Japanese population. Nat Genet In press
[40]  Mbarek H, Ochi H, Urabe Y, Kumar V, Kubo M, et al. (2011) A genome-wide association study of chronic hepatitis B identified novel risk locus in a Japanese population. Hum Mol Genet 20: 3884–3892.
[41]  Urabe Y, Tanikawa C, Takahashi A, Okada Y, Morizono T, et al. (2012) A Genome-Wide Association Study of Nephrolithiasis in the Japanese Population Identifies Novel Susceptible Loci at 5q35. 3, 7p14. 3, and 13q14. 1. PLoS Genet 8: e1002541.
[42]  Cui R, Okada Y, Jang SG, Ku JL, Park JG, et al. (2011) Common variant in 6q26–q27 is associated with distal colon cancer in an Asian population. Gut 60: 799–805.
[43]  Ambros V, Horvitz HR (1984) Heterochronic mutants of the nematode Caenorhabditis elegans. Science 226: 409–416.
[44]  Heo I, Joo C, Cho J, Ha M, Han J, et al. (2008) Lin28 mediates the terminal uridylation of let-7 precursor MicroRNA. Molecular cell 32: 276–284.
[45]  Viswanathan SR, Daley GQ, Gregory RI (2008) Selective blockade of microRNA processing by Lin28. Science's STKE 320: 97.
[46]  Zhu H, Shah S, Shyh-Chang N, Shinoda G, Einhorn WS, et al. (2010) Lin28a transgenic mice manifest size and puberty phenotypes identified in human genetic association studies. Nat Genet 42: 626–630.
[47]  Guo Y, Chen Y, Ito H, Watanabe A, Ge X, et al. (2006) Identification and characterization of lin-28 homolog B (LIN28B) in human hepatocellular carcinoma. Gene 384: 51–61.
[48]  Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, et al. (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318: 1917–1920.
[49]  Gudbjartsson DF, Walters GB, Thorleifsson G, Stefansson H, Halldorsson BV, et al. (2008) Many sequence variants affecting diversity of adult human height. Nat Genet 40: 609–615.
[50]  Lettre G, Jackson AU, Gieger C, Schumacher FR, Berndt SI, et al. (2008) Identification of ten loci associated with height highlights new biological pathways in human growth. Nat Genet 40: 584–591.
[51]  Krude H, Schutz B, Biebermann H, Von Moers A, Schnabel D, et al. (2002) Choreoathetosis, hypothyroidism, and pulmonary alterations due to human NKX2-1 haploinsufficiency. Journal of Clinical Investigation 109: 475–480.
[52]  Eriksson N, Benton GM, Do CB, Kiefer AK, Mountain JL, et al. (2012) Genetic variants associated with breast size also influence breast cancer risk. BMC Med Genet 13: 53.
[53]  Bhalla K, Luo Y, Buchan T, Beachem MA, Guzauskas GF, et al. (2008) Alterations in CDH15 and KIRREL3 in patients with mild to severe intellectual disability. Am J Hum Genet 83: 703–713.
[54]  Guerin A, Stavropoulos DJ, Diab Y, Chénier S, Christensen H, et al.. (2012) Interstitial deletion of 11q-implicating the KIRREL3 gene in the neurocognitive delay associated with Jacobsen syndrome. American Journal of Medical Genetics Part A.
[55]  Elks CE, Perry JR, Sulem P, Chasman DI, Franceschini N, et al. (2010) Thirty new loci for age at menarche identified by a meta-analysis of genome-wide association studies. Nat Genet 42: 1077–1085.
[56]  Melzer D, Perry JR, Hernandez D, Corsi AM, Stevens K, et al. (2008) A genome-wide association study identifies protein quantitative trait loci (pQTLs). PLoS Genet 4: e1000072.
[57]  Yazawa M, Ferrante C, Feng J, Mio K, Ogura T, et al. (2007) TRIC channels are essential for Ca2+ handling in intracellular stores. Nature 448: 78–82.
[58]  Volodarsky M, Markus B, Cohen I, Staretz-Chacham O, Flusser H, et al. (2013) A Deletion Mutation in TMEM38B Associated with Autosomal Recessive Osteogenesis Imperfecta. Hum Mutat
[59]  Parent AS, Teilmann G, Juul A, Skakkebaek NE, Toppari J, et al. (2003) The timing of normal puberty and the age limits of sexual precocity: variations around the world, secular trends, and changes after migration. Endocr Rev 24: 668–693.
[60]  Okada Y, Takahashi A, Ohmiya H, Kumasaka N, Kamatani Y, et al. (2011) Genome-wide association study for C-reactive protein levels identified pleiotropic associations in the IL6 locus. Hum Mol Genet 20: 1224–1231.
[61]  Yamaguchi-Kabata Y, Nakazono K, Takahashi A, Saito S, Hosono N, et al. (2008) Japanese population structure, based on SNP genotypes from 7003 individuals compared to other ethnic groups: effects on population-based association studies. The American Journal of Human Genetics 83: 445–456.

Full-Text

comments powered by Disqus