The genetic underpinnings of variation in ages at menarche and natural menopause among women from the multi-ethnic Population Architecture using Genomics and Epidemiology (PAGE) Study: A trans-ethnic meta-analysis

PLoS ONE

Volumn 13, Issue 7, 2018, Pages

  Fernández Rhodes, Lindsay ^a,b   Malinowski, Jennifer R ^c   Wang, Yujie ^a   Tao, Ran ^d   Pankratz, Nathan ^e   Jeff, Janina M ^f   Yoneyama, Sachiko ^a   Carty, Cara L ^g   Setiawan, V Wendy ^h   Le Marchand, Loic ⁱ   Haiman, Christopher ^h   Corbett, Steven ^j   Demerath, Ellen ^k   Heiss, Gerardo ^a   Gross, Myron ^e   Buzkova, Petra ^l   Crawford, Dana C ^m   Hunt, Steven C ⁿ   Rao, D C ^o   Schwander, Karen ^o   Chakravarti, Aravinda ^p   Gottesman, Omri ^q   Abul Husn, Noura S ^q   Bottinger, Erwin P ^q   Loos, Ruth J F ^q   Raffel, Leslie J ^r   Yao, Jie ^s   Guo, Xiuqing ^s   Bielinski, Suzette J ^t   Rotter, Jerome I ^s   Vaidya, Dhananjay ^u   Chen, Yii Der Ida ^s   Castañeda, Sheila F ^v   Daviglus, Martha ^w   Kaplan, Robert ^x   Talavera, Gregory A ^v   Ryckman, Kelli K ^y   Peters, Ulrike ^g   Ambite, Jose Luis ^z   Buyske, Steven ^aa   Hindorff, Lucia ^ab   Kooperberg, Charles ^g   Matise, Tara ^aa   Franceschini, Nora ^a   North, Kari E ^a   more..

^a IL   (United States)

^b UNIVERSITY OF NORTH CAROLINA AT CHAPEL HILL   (United States)

^c Write InSciTe   (United States)

^d VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^e UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^f ILLUMINA INC   (United States)

^g Fred Hutchinson Cancer Research Center   (United States)

^h UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

ⁱ UNIVERSITY OF HAWAII CANCER CENTER   (United States)

^j Kansas Health Institute   (United States)

^k UNIVERSITY OF MINNESOTA   (United States)

^l UNIVERSITY OF WASHINGTON   (United States)

^m CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

ⁿ WEILL CORNELL MEDICAL COLLEGE   (Qatar)

^o WASHINGTON UNIVERSITY   (United States)

^p JOHNS HOPKINS UNIVERSITY   (United States)

^q MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^r UNIVERSITY OF CALIFORNIA   (United States)

^s HARBOR UCLA MEDICAL CENTER   (United States)

^t MAYO CLINIC   (United States)

^u JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^v SAN DIEGO STATE UNIVERSITY   (United States)

^w UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^x ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^y UNIVERSITY OF IOWA   (United States)

^z UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^aa RUTGERS UNIVERSITY   (United States)

^ab NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ALASKA NATIVE; ALLELE; AMERICAN INDIAN; ARTICLE; ASIAN AMERICAN; CROSS-SECTIONAL STUDY; ETHNIC GROUP; ETHNICITY; EUROPEAN; FEMALE; GENOMICS; HISPANIC; HUMAN; HUMAN EXPERIMENT; LINEAR REGRESSION ANALYSIS; MEDICAL RECORD; MENOPAUSE; META ANALYSIS; RACE; STRATIFICATION; AGE; BIOLOGICAL VARIATION; ETHNOLOGY; GENE LOCUS; GENETICS; GENOTYPE; MENARCHE; PHENOTYPE; SINGLE NUCLEOTIDE POLYMORPHISM;

AGE FACTORS; ALLELES; BIOLOGICAL VARIATION, POPULATION; FEMALE; GENETIC LOCI; GENOTYPE; HUMANS; MENARCHE; MENOPAUSE; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE;

EID: 85050732362     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0200486     Document Type: Article

References (64)

1. McDowell MA, Brody DJ, Hughes JP (2007) Has age at menarche changed? Results from the National Health and Nutrition Examination Survey (NHANES) 1999–2004. J Adolesc Health 40: 227–231. https://doi.org/10.1016/j.jadohealth.2006.10.002 PMID: 17321422
2. Buttke DE, Sircar K, Martin C (2012) Exposures to endocrine-disrupting chemicals and age of menarche in adolescent girls in NHANES (2003–2008). Environ Health Perspect 120: 1613–1618. PMID: 23124194
3. McGuinn LA, Ghazarian AA, Joseph Su L, Ellison GL (2015) Urinary bisphenol A and age at menarche among adolescent girls: evidence from NHANES 2003–2010. Environ Res 136: 381–386. https://doi.org/10.1016/j.envres.2014.10.037 PMID: 25460659
4. Canoy D, Beral V, Balkwill A, Wright FL, Kroll ME, Reeves GK, et al. (2015) Age at menarche and risks of coronary heart and other vascular diseases in a large UK cohort. Circulation 131: 237–244. https://doi.org/10.1161/CIRCULATIONAHA.114.010070 PMID: 25512444
5. Bodicoat DH, Schoemaker MJ, Jones ME, McFadden E, Griffin J, Ashworth A, et al. (2014) Timing of pubertal stages and breast cancer risk: the Breakthrough Generations Study. Breast Cancer Res 16: R18. https://doi.org/10.1186/bcr3613 PMID: 24495528
6. Ali AT (2014) Reproductive factors and the risk of endometrial cancer. Int J Gynecol Cancer 24: 384–393. https://doi.org/10.1097/IGC.0000000000000075 PMID: 24463639
7. Gold EB (2011) The timing of the age at which natural menopause occurs. Obstet Gynecol Clin North Am 38: 425–440. https://doi.org/10.1016/j.ogc.2011.05.002 PMID: 21961711
8. Gold EB, Bromberger J, Crawford S, Samuels S, Greendale GA, Harlow SD, et al. (2001) Factors associated with age at natural menopause in a multiethnic sample of midlife women. Am J Epidemiol 153: 865–874. PMID: 11323317
9. Henderson KD, Bernstein L, Henderson B, Kolonel L, Pike MC (2008) Predictors of the timing of natural menopause in the Multiethnic Cohort Study. Am J Epidemiol 167: 1287–1294. https://doi.org/10.1093/aje/kwn046 PMID: 18359953
10. Campbell Jenkins BW, Addison C, Wilson G, Liu J, Fortune M, Robinson K, et al. (2011) Association of the joint effect of menopause and hormone replacement therapy and cancer in African American women: the Jackson Heart Study. Int J Environ Res Public Health 8: 2491–2504. https://doi.org/10.3390/ijerph8062491 PMID: 21776241
11. Kallen AN, Pal L (2011) Cardiovascular disease and ovarian function. Curr Opin Obstet Gynecol 23: 258–267. https://doi.org/10.1097/GCO.0b013e3283488a21 PMID: 21681091
12. Nichols HB, Trentham-Dietz A, Hampton JM, Titus-Ernstoff L, Egan KM, Willett WC, et al. (2006) From menarche to menopause: trends among US Women born from 1912 to 1969. Am J Epidemiol 164: 1003–1011. https://doi.org/10.1093/aje/kwj282 PMID: 16928728
13. Elks CE, Perry JR, Sulem P, Chasman DI, Franceschini N, He C, 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. https://doi.org/10.1038/ng.714 PMID: 21102462
14. Ong KK, Elks CE, Li S, Zhao JH, Luan J, Andersen LB, et al. (2009) Genetic variation in LIN28B is associated with the timing of puberty. Nat Genet.
15. He C, Kraft P, Chen C, Buring JE, Pare G, Hankinson SE, et al. (2009) Genome-wide association studies identify loci associated with age at menarche and age at natural menopause. Nat Genet.
16. He C, Zhang C, Hunter DJ, Hankinson SE, Buck Louis GM, Hediger ML, et al. (2010) Age at menarche and risk of type 2 diabetes: results from 2 large prospective cohort studies. Am J Epidemiol 171: 334–344. https://doi.org/10.1093/aje/kwp372 PMID: 20026580
17. Perry JR, Stolk L, Franceschini N, Lunetta KL, Zhai G, McArdle PF, et al. (2009) Meta-analysis of genome-wide association data identifies two loci influencing age at menarche. Nat Genet.
18. Stolk L, Perry JR, Chasman DI, He C, Mangino M, Sulem P, et al. (2012) Meta-analyses identify 13 loci associated with age at menopause and highlight DNA repair and immune pathways. Nat Genet 44: 260–268. https://doi.org/10.1038/ng.1051 PMID: 22267201
19. Stolk L, Zhai G, van Meurs JB, Verbiest MM, Visser JA, Estrada K, et al. (2009) Loci at chromosomes 13, 19 and 20 influence age at natural menopause. Nat Genet.
20. Perry JR, Day F, Elks CE, Sulem P, Thompson DJ, Ferreira T, et al. (2014) Parent-of-origin-specific allelic associations among 106 genomic loci for age at menarche. Nature 514: 92–97. https://doi.org/10.1038/nature13545 PMID: 25231870
21. Liu YZ, Guo YF, Wang L, Tan LJ, Liu XG, Pei YF, et al. (2009) Genome-wide association analyses identify SPOCK as a key novel gene underlying age at menarche. PLoS Genet 5: e1000420. https://doi.org/10.1371/journal.pgen.1000420 PMID: 19282985
22. Day FR, Thompson DJ, Helgason H, Chasman DI, Finucane H, Sulem P, et al. (2017) Genomic analyses identify hundreds of variants associated with age at menarche and support a role for puberty timing in cancer risk. Nat Genet.
23. Day FR, Ruth KS, Thompson DJ, Lunetta KL, Pervjakova N, Chasman DI, et al. (2015) Large-scale genomic analyses link reproductive aging to hypothalamic signaling, breast cancer susceptibility and BRCA1-mediated DNA repair. Nat Genet 47: 1294–1303. https://doi.org/10.1038/ng.3412 PMID: 26414677
24. Demerath EW, Liu CT, Franceschini N, Chen G, Palmer JR, Smith EN, et al. (2013) Genome-wide association study of age at menarche in African-American women. Hum Mol Genet 22: 3329–3346. https://doi.org/10.1093/hmg/ddt181 PMID: 23599027
25. Chen CT, Liu CT, Chen GK, Andrews JS, Arnold AM, Dreyfus J, et al. (2014) Meta-analysis of loci associated with age at natural menopause in African-American women. Hum Mol Genet 23: 3327–3342. https://doi.org/10.1093/hmg/ddu041 PMID: 24493794
26. Tanikawa C, Okada Y, Takahashi A, Oda K, Kamatani N, Kubo M, et al. (2013) Genome wide association study of age at menarche in the Japanese population. PLoS One 8: e63821. https://doi.org/10.1371/journal.pone.0063821 PMID: 23667675
27. Pyun JA, Kim S, Cho NH, Koh I, Lee JY, Shin C, et al. (2014) Genome-wide association studies and epistasis analyses of candidate genes related to age at menarche and age at natural menopause in a Korean population. Menopause 21: 522–529. https://doi.org/10.1097/GME.0b013e3182a433f7 PMID: 24045676
28. Shi J, Zhang B, Choi JY, Gao YT, Li H, Lu W, et al. (2016) Age at menarche and age at natural menopause in East Asian women: a genome-wide association study. Age (Dordr) 38: 513–523.
29. Spencer KL, Malinowski J, Carty CL, Franceschini N, Fernandez-Rhodes L, Young A, et al. (2013) Genetic variation and reproductive timing: African American women from the Population Architecture using Genomics and Epidemiology (PAGE) Study. PLoS One 8: e55258. https://doi.org/10.1371/journal.pone.0055258 PMID: 23424626
30. Carty CL, Spencer KL, Setiawan VW, Fernandez-Rhodes L, Malinowski J, Buyske S, et al. (2013) Replication of genetic loci for ages at menarche and menopause in the multi-ethnic Population Architecture using Genomics and Epidemiology (PAGE) study. Human Reproduction 28: 1695–1706. https://doi.org/10.1093/humrep/det071 PMID: 23508249
31. Chen CT, Fernandez-Rhodes L, Brzyski RG, Carlson CS, Chen Z, Heiss G, et al. (2011) Replication of loci influencing ages at menarche and menopause in Hispanic women: the Women’s Health Initiative SHARe Study. Hum Mol Genet.
32. Morris AP (2011) Transethnic meta-analysis of genomewide association studies. Genet Epidemiol 35: 809–822. https://doi.org/10.1002/gepi.20630 PMID: 22125221
33. Zakharov S, Wang X, Liu J, Teo YY (2015) Improving power for robust trans-ethnic meta-analysis of rare and low-frequency variants with a partitioning approach. Eur J Hum Genet 23: 238–244. https://doi.org/10.1038/ejhg.2014.78 PMID: 24801758
34. Matise TC, Ambite JL, Buyske S, Carlson CS, Cole SA, Crawford DC, et al. (2011) The Next PAGE in understanding complex traits: design for the analysis of Population Architecture Using Genetics and Epidemiology (PAGE) Study. Am J Epidemiol 174: 849–859. https://doi.org/10.1093/aje/kwr160 PMID: 21836165
35. Voight BF, Kang HM, Ding J, Palmer CD, Sidore C, Chines PS, et al. (2012) The metabochip, a custom genotyping array for genetic studies of metabolic, cardiovascular, and anthropometric traits. PLoS Genet 8: e1002793. https://doi.org/10.1371/journal.pgen.1002793 PMID: 22876189
36. Pulley J, Clayton E, Bernard GR, Roden DM, Masys DR (2010) Principles of human subjects protections applied in an opt-out, de-identified biobank. Clin Transl Sci 3: 42–48. https://doi.org/10.1111/j.1752-8062.2010.00175.x PMID: 20443953
37. Roden DM, Pulley JM, Basford MA, Bernard GR, Clayton EW, Balser JR, et al. (2008) Development of a large-scale de-identified DNA biobank to enable personalized medicine. Clin Pharmacol Ther 84: 362–369. https://doi.org/10.1038/clpt.2008.89 PMID: 18500243
38. Malinowski J, Farber-Eger E, Crawford DC (2014) Development of a data-mining algorithm to identify ages at reproductive milestones in electronic medical records. Pac Symp Biocomput: 376–387. PMID: 24297563
39. Liu EY, Buyske S, Aragaki AK, Peters U, Boerwinkle E, Carlson C, et al. (2012) Genotype imputation of Metabochip SNPs using a study-specific reference panel of ~4,000 haplotypes in African Americans from the Women’s Health Initiative. Genet Epidemiol 36: 107–117. https://doi.org/10.1002/gepi.21603PMID: 22851474
40. Weale ME (2010) Quality control for genome-wide association studies. Methods Mol Biol 628: 341–372. https://doi.org/10.1007/978-1-60327-367-1_19 PMID: 20238091
41. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, et al. (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81: 559–575. https://doi.org/10.1086/519795 PMID: 17701901
42. Lin DY, Tao R, Kalsbeek WD, Zeng DL, Gonzalez F, Fernandez-Rhodes L, et al. (2014) Genetic Association Analysis under Complex Survey Sampling: The Hispanic Community Health Study/Study of Latinos. Am J Hum Genet 95: 675–688. https://doi.org/10.1016/j.ajhg.2014.11.005 PMID: 25480034
43. Chen MH, Yang Q (2010) GWAF: an R package for genome-wide association analyses with family data. Bioinformatics 26: 580–581. https://doi.org/10.1093/bioinformatics/btp710 PMID: 20040588
44. Patterson N, Price AL, Reich D (2006) Population structure and eigenanalysis. PLoS Genet 2: e190. https://doi.org/10.1371/journal.pgen.0020190 PMID: 17194218
45. Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 38: 904–909. https://doi.org/10.1038/ng1847 PMID: 16862161
46. Buyske S, Wu Y, Carty CL, Cheng I, Assimes TL, Dumitrescu L, et al. (2012) Evaluation of the metabochip genotyping array in African Americans and implications for fine mapping of GWAS-identified loci: the PAGE study. PLoS One 7: e35651. https://doi.org/10.1371/journal.pone.0035651 PMID: 22539988
47. Willer CJ, Li Y, Abecasis GR (2010) METAL: fast and efficient meta-analysis of genomewide association scans. Bioinformatics 26: 2190–2191. https://doi.org/10.1093/bioinformatics/btq340 PMID: 20616382
48. Han B, Eskin E (2011) Random-Effects Model Aimed at Discovering Associations in Meta-Analysis of Genome-wide Association Studies. Am J Hum Genet 88: 586–598. https://doi.org/10.1016/j.ajhg.2011.04.014 PMID: 21565292
49. Yang J, Lee SH, Goddard ME, Visscher PM (2011) GCTA: a tool for genome-wide complex trait analysis. Am J Hum Genet 88: 76–82. https://doi.org/10.1016/j.ajhg.2010.11.011 PMID: 21167468
50. Yang J, Ferreira T, Morris AP, Medland SE, Madden PA, Heath AC, et al. (2012) Conditional and joint multiple-SNP analysis of GWAS summary statistics identifies additional variants influencing complex traits. Nat Genet 44: 369–375, S361-363. https://doi.org/10.1038/ng.2213 PMID: 22426310
51. Fernandez-Rhodes L, Gong J, Haessler J, Franceschini N, Graff M, Nishimura KK, et al. (2017) Transethnic fine-mapping of genetic loci for body mass index in the diverse ancestral populations of the Population Architecture using Genomics and Epidemiology (PAGE) Study reveals evidence for multiple signals at established loci. Hum Genet.
52. Locke AE, Kahali B, Berndt SI, Justice AE, Pers TH, Day FR, et al. (2015) Genetic studies of body mass index yield new insights for obesity biology. Nature 518: 197–206. https://doi.org/10.1038/nature14177PMID: 25673413
53. Lee JY, Lee BS, Shin DJ, Woo Park K, Shin YA, Joong Kim K, et al. (2013) A genome-wide association study of a coronary artery disease risk variant. J Hum Genet 58: 120–126. https://doi.org/10.1038/jhg.2012.124 PMID: 23364394
54. Huang J, Ellinghaus D, Franke A, Howie B, Li Y (2012) 1000 Genomes-based imputation identifies novel and refined associations for the Wellcome Trust Case Control Consortium phase 1 Data. Eur J Hum Genet 20: 801–805. https://doi.org/10.1038/ejhg.2012.3 PMID: 22293688
55. Liu L, Ebana Y, Nitta JI, Takahashi Y, Miyazaki S, Tanaka T, et al. (2017) Genetic Variants Associated With Susceptibility to Atrial Fibrillation in a Japanese Population. Can J Cardiol 33: 443–449. https://doi.org/10.1016/j.cjca.2016.10.029 PMID: 28129963
56. Steiner M, Dunn E, Born L (2003) Hormones and mood: from menarche to menopause and beyond. J Affect Disord 74: 67–83. PMID: 12646300
57. Global Lipids Genetics C, Willer CJ, Schmidt EM, Sengupta S, Peloso GM, Gustafsson S, et al. (2013) Discovery and refinement of loci associated with lipid levels. Nat Genet 45: 1274–1283. https://doi.org/10.1038/ng.2797 PMID: 24097068
58. Conomos MP, Laurie CA, Stilp AM, Gogarten SM, McHugh CP, Nelson SC, et al. (2016) Genetic Diversity and Association Studies in US Hispanic/Latino Populations: Applications in the Hispanic Community Health Study/Study of Latinos. Am J Hum Genet 98: 165–184. https://doi.org/10.1016/j.ajhg.2015.12.001 PMID: 26748518
59. Wang W, Zhao LJ, Liu YZ, Recker RR, Deng HW (2006) Genetic and environmental correlations between obesity phenotypes and age at menarche. Int J Obes (Lond) 30: 1595–1600.
60. Fernandez-Rhodes L, Demerath EW, Cousminer DL, Tao R, Dreyfus JG, Esko T, et al. (2013) Association of adiposity genetic variants with menarche timing in 92,105 women of European descent. Am J Epidemiol 178: 451–460. https://doi.org/10.1093/aje/kws473 PMID: 23558354
61. Cousminer DL, Stergiakouli E, Berry DJ, Ang W, Groen-Blokhuis MM, Korner A, et al. (2014) Genome-wide association study of sexual maturation in males and females highlights a role for body mass and menarche loci in male puberty. Hum Mol Genet 23: 4452–4464. https://doi.org/10.1093/hmg/ddu150PMID: 24770850
62. Day FR, Bulik-Sullivan B, Hinds DA, Finucane HK, Murabito JM, Tung JY, et al. (2015) Shared genetic aetiology of puberty timing between sexes and with health-related outcomes. Nat Commun 6: 8842. https://doi.org/10.1038/ncomms9842 PMID: 26548314
63. Bulik-Sullivan B, Finucane HK, Anttila V, Gusev A, Day FR, Loh PR, et al. (2015) An atlas of genetic correlations across human diseases and traits. Nat Genet 47: 1236–1241. https://doi.org/10.1038/ng. 3406 PMID: 26414676
64. Barban N, Jansen R, de Vlaming R, Vaez A, Mandemakers JJ, Tropf FC, et al. (2016) Genome-wide analysis identifies 12 loci influencing human reproductive behavior. Nat Genet.