Faster ticking rate of the epigenetic clock is associated with faster pubertal development in girls

Epigenetics

Volumn 13, Issue 1, 2018, Pages 85-94

  Binder, Alexandra M ^a   Corvalan, Camila ^b   Mericq, Verónica ^b   Pereira, Ana ^b   Santos, José Luis ^c   Horvath, Steve ^d   Shepherd, John ^e   Michels, Karin B ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CHILE   (Chile)

^c PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

breast density; DNA methylation; epigenetic clock; menarche; Puberty; thelarche

Indexed keywords

ANTHROPOMETRY; ARTICLE; BIRTH WEIGHT; BODY FAT; BODY MASS; BREAST DENSITY; BREAST DEVELOPMENT; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CHILD; COHORT ANALYSIS; DNA METHYLATION; DUAL ENERGY X RAY ABSORPTIOMETRY; EPIGENETICS; FEMALE; HUMAN; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MATERNAL AGE; PUBERTY; QUESTIONNAIRE; SCHOOL CHILD; URINALYSIS; ADOLESCENT; BREAST; CHILE; GENETIC EPIGENESIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; MENARCHE; PHOTON ABSORPTIOMETRY; SEXUAL MATURATION; TIME FACTOR;

ABSORPTIOMETRY, PHOTON; ADOLESCENT; BODY MASS INDEX; BREAST; BREAST DENSITY; CHILD; CHILE; EPIGENESIS, GENETIC; FEMALE; HUMANS; MENARCHE; SEXUAL MATURATION; TIME FACTORS;

EID: 85042229056     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.1080/15592294.2017.1414127     Document Type: Article

References (61)

1. Horvath S. DNA methylation age of human tissues and cell types. Genome Biol. 2013;14:3156. doi:10.1186/gb-2013-14-10-r115.
2. Hannum G, Guinney J, Zhao L, et al. Genome-wide methylation profiles reveal quantitative views of human aging rates. Mol Cell. 2013;49:359–367. doi:10.1016/j.molcel.2012.10.016. PMID:23177740
3. Quach A, Levine ME, Tanaka T, et al. Epigenetic clock analysis of diet, exercise, education, and lifestyle factors. Aging. 2017;9:419–446. PMID:28198702
4. Simpkin AJ, Hemani G, Suderman M, et al. Prenatal and early life influences on epigenetic age in children: a study of mother–offspring pairs from two cohort studies. Hum Mol Genet. 2016;25:191–201. doi:10.1093/hmg/ddv456. PMID:26546615
5. Marioni RE, Shah S, McRae AF, et al. DNA methylation age of blood predicts all-cause mortality in later life. Genome Biol. [Internet] 2015; [cited 2016 Oct 19];16. Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4350614/ PMID:25622821
6. Christiansen L, Lenart A, Tan Q, et al. DNA methylation age is associated with mortality in a longitudinal Danish twin study. Aging Cell. 2016;15:149–154. doi:10.1111/acel.12421. PMID:26594032
7. Zheng Y, Joyce BT, Colicino E, et al. Blood epigenetic age may predict cancer incidence and mortality. EBioMedicine. 2016;5:68–73. doi:10.1016/j.ebiom.2016.02.008. PMID:27077113
8. Perna L, Zhang Y, Mons U, et al. Epigenetic age acceleration predicts cancer, cardiovascular, and all-cause mortality in a German case cohort. Clin Epigenet. 2016;8:64. doi:10.1186/s13148-016-0228-z.
9. Levine ME, Hosgood HD, Chen B, et al. DNA methylation age of blood predicts future onset of lung cancer in the women's health initiative. Aging. 2015;7:690–700. doi:10.18632/aging.100809. PMID:26411804
10. Ambatipudi S, Horvath S, Perrier F, et al. DNA methylome analysis identifies accelerated epigenetic ageing associated with postmenopausal breast cancer susceptibility. Eur J Cancer Oxf Engl. 2017;75:299–307. doi:10.1016/j.ejca.2017.01.014.
11. Kelsey JL, Gammon MD, John EM. Reproductive factors and breast cancer. Epidemiol Rev. 1993;15:36–47. doi:10.1093/oxfordjournals.epirev.a036115. PMID:8405211
12. Bodicoat DH, Schoemaker MJ, Jones ME, et al. Timing of pubertal stages and breast cancer risk: the Breakthrough Generations Study. Breast Cancer Res BCR. 2014;16:R18. doi:10.1186/bcr3613.
13. Collaborative Group on Hormonal Factors in Breast Cancer. Menarche, menopause, and breast cancer risk: individual participant meta-analysis, including 118 964 women with breast cancer from 117 epidemiological studies. Lancet Oncol. 2012;13:1141–1151. doi:10.1016/S1470-2045(12)70425-4. PMID:23084519
14. Dossus L, Allen N, Kaaks R, et al. Reproductive risk factors and endometrial cancer: the European Prospective Investigation into Cancer and Nutrition. Int J Cancer. 2010;127:442–451. PMID:19924816
15. Gong T-T, Wu Q-J, Vogtmann E, et al. Age at menarche and risk of ovarian cancer: a meta-analysis of epidemiological studies. Int J Cancer J Int Cancer. 2013;132:2894–2900. doi:10.1002/ijc.27952.
16. Charalampopoulos D, McLoughlin A, Elks CE, et al. Age at menarche and risks of all-cause and cardiovascular death: a systematic review and meta-analysis. Am J Epidemiol. 2014;180:29–40. doi:10.1093/aje/kwu113. PMID:24920784
17. McCormack VA, dos Santos Silva I. Breast density and parenchymal patterns as markers of breast cancer risk: a meta-analysis. Cancer Epidemiol Biomark Prev Publ Am Assoc Cancer Res Cosponsored Am Soc Prev Oncol. 2006;15:1159–1169. doi:10.1158/1055-9965.EPI-06-0034.
18. Boyd NF, Guo H, Martin LJ, et al. Mammographic density and the risk and detection of breast cancer. N Engl J Med. 2007;356:227–236. doi:10.1056/NEJMoa062790. PMID:17229950
19. Yaghjyan L, Colditz GA, Collins LC, et al. Mammographic breast density and subsequent risk of breast cancer in postmenopausal women according to tumor characteristics. J Natl Cancer Inst. 2011;103:1179–1189. doi:10.1093/jnci/djr225. PMID:21795664
20. Pike MC, Krailo MD, Henderson BE, et al. “Hormonal” risk factors, “breast tissue age” and the age-incidence of breast cancer. Nature. 1983;303:767–770. doi:10.1038/303767a0. PMID:6866078
21. Colditz GA, Frazier AL. Models of breast cancer show that risk is set by events of early life: prevention efforts must shift focus. Cancer Epidemiol Biomark Prev Publ Am Assoc Cancer Res Cosponsored Am Soc Prev Oncol. 1995;4:567–571.
22. Boyd N, Martin L, Chavez S, et al. Breast-tissue composition and other risk factors for breast cancer in young women: a cross-sectional study. Lancet Oncol. 2009;10:569–580. doi:10.1016/S1470-2045(09)70078-6. PMID:19409844
23. Novotny R, Daida Y, Morimoto Y, et al. Puberty, body fat, and breast density in girls of several ethnic groups. Am J Hum Biol Off J Hum Biol Counc. 2011;23:359–365. doi:10.1002/ajhb.21145.
24. Simpkin AJ, Howe LD, Tilling K, et al. The epigenetic clock and physical development during childhood and adolescence: longitudinal analysis from a UK birth cohort. Int J Epidemiol. 2017;46:549–558. PMID:28089957
25. Ong KK, Ahmed ML, Dunger DB. Lessons from large population studies on timing and tempo of puberty (secular trends and relation to body size): the European trend. Mol Cell Endocrinol. 2006;254–255:8–12. doi:10.1016/j.mce.2006.04.018. PMID:16757103
26. McDowell MA, Brody DJ, Hughes JP. Has age at menarche changed? Results from the National Health and Nutrition Examination Survey (NHANES) 1999–2004. J Adolesc Health Off Publ Soc Adolesc Med. 2007;40:227–231. doi:10.1016/j.jadohealth.2006.10.002.
27. Morris DH, Jones ME, Schoemaker MJ, et al. Secular trends in age at menarche in women in the UK born 1908-93: results from the Breakthrough Generations Study. Paediatr Perinat Epidemiol. 2011;25:394–400. doi:10.1111/j.1365-3016.2011.01202.x. PMID:21649682
28. Junqueira Do Lago M, Faerstein E, De Souza Lopes C. Family socio-economic background modified secular trends in age at menarche: evidence from the Pró-Saúde Study (Rio de Janeiro, Brazil). Ann Hum Biol. 2003;30:347–352. doi:10.1080/0301446031000091783. PMID:12850966
29. Biro FM, Greenspan LC, Galvez MP. Puberty in girls of the 21st century. J Pediatr Adolesc Gynecol. 2012;25:289–294. doi:10.1016/j.jpag.2012.05.009. PMID:22841372
30. Burt Solorzano CM, McCartney CR. Obesity and the pubertal transition in girls and boys. Reprod Camb Engl. 2010;140:399–410.
31. Wolff MS, Teitelbaum SL, McGovern K, et al. Breast cancer and environment research program. Phthalate exposure and pubertal development in a longitudinal study of US girls. Hum Reprod Oxf Engl. 2014;29:1558–1566. doi:10.1093/humrep/deu081.
32. Wolff MS, Teitelbaum SL, McGovern K, et al. Environmental phenols and pubertal development in girls. Environ Int. 2015;84:174–180. doi:10.1016/j.envint.2015.08.008. PMID:26335517
33. Wolff MS, Pajak A, Pinney SM, et al. Associations of urinary phthalate and phenol biomarkers with menarche in a multiethnic cohort of young girls. Reprod Toxicol Elmsford N. 2017;67:56–64. doi:10.1016/j.reprotox.2016.11.009.
34. Mouritsen A, Aksglaede L, Soerensen K, et al. The pubertal transition in 179 healthy Danish children: associations between pubarche, adrenarche, gonadarche, and body composition. Eur J Endocrinol. 2013;168:129–136. doi:10.1530/EJE-12-0191. PMID:23093700
35. Aksglaede L, Sørensen K, Petersen JH, et al. Recent decline in age at breast development: the Copenhagen Puberty Study. Pediatrics. 2009;123:e932–e939. doi:10.1542/peds.2008-2491. PMID:19403485
36. Biro FM, Deardorff J. Identifying opportunities for cancer prevention during preadolescence and adolescence: puberty as a window of susceptibility. J Adolesc Health Off Publ Soc Adolesc Med. 2013;52:S15–S20. doi:10.1016/j.jadohealth.2012.09.019.
37. Schoemaker MJ, Jones ME, Allen S, et al. Childhood body size and pubertal timing in relation to adult mammographic density phenotype. Breast Cancer Res BCR. 2017;19:13. doi:10.1186/s13058-017-0804-y. PMID:28173872
38. Yaghjyan L, Colditz GA, Rosner B, et al. Reproductive factors related to childbearing and mammographic breast density. Breast Cancer Res Treat. 2016;158:351–359. doi:10.1007/s10549-016-3884-y. PMID:27351801
39. Rice MS, Bertrand KA, Lajous M, et al. Reproductive and lifestyle risk factors and mammographic density in Mexican women. Ann Epidemiol. 2015;25:868–873. doi:10.1016/j.annepidem.2015.08.006. PMID:26475982
40. Russo J, Moral R, Balogh GA, et al. The protective role of pregnancy in breast cancer. Breast Cancer Res BCR. 2005;7:131–142. doi:10.1186/bcr1029.
41. Gassen NC, Chrousos GP, Binder EB, et al. Life stress, glucocorticoid signaling, and the aging epigenome: Implications for aging-related diseases. Neurosci Biobehav Rev. 2017;74:356–365. doi:10.1016/j.neubiorev.2016.06.003. PMID:27343999
42. Foster H, Hagan J, Brooks-Gunn J. Growing up fast: stress exposure and subjective “weathering” in emerging adulthood. Journal of Health and Social Behavior. 2008;49:162–177. doi:10.1177/002214650804900204. PMID:18649500
43. Wu T, Mendola P, Buck GM. Ethnic differences in the presence of secondary sex characteristics and menarche among US girls: the Third National Health and Nutrition Examination Survey, 1988-1994. Pediatrics. 2002;110:752–757. doi:10.1542/peds.110.4.752. PMID:12359790
44. Biro FM, Greenspan LC, Galvez MP, et al. Onset of breast development in a longitudinal cohort. Pediatrics. 2013;132:1019–1027. doi:10.1542/peds.2012-3773. PMID:24190685
45. Shepherd JA, Malkov S, Fan B, et al. Breast density assessment in adolescent girls using dual-energy X-ray absorptiometry: a feasibility study. Cancer Epidemiol Biomark Prev Publ Am Assoc Cancer Res Cosponsored Am Soc Prev Oncol. 2008;17:1709–1713. doi:10.1158/1055-9965.EPI-08-0006.
46. Tanner J. Growth at adolescense. Oxford: Blackwell Scientific Publications; 1962.
47. Shepherd JA, Herve L, Landau J, et al. Clinical comparison of a novel breast DXA technique to mammographic density. Med Phys. 2006;33:1490–1498. doi:10.1118/1.2193691. PMID:16752583
48. Weaver CM, McCabe LD, McCabe GP, et al. Bone mineral and predictors of bone mass in white, Hispanic, and Asian early pubertal girls. Calcif Tissue Int. 2007;81:352–363. doi:10.1007/s00223-007-9074-5. PMID:17989943
49. Shepherd JA, Kerlikowske KM, Smith-Bindman R, et al. Measurement of breast density with dual X-ray absorptiometry: feasibility. Radiology. 2002;223:554–557. doi:10.1148/radiol.2232010482. PMID:11997567
50. Cediel G, Corvalán C, Aguirre C, et al. Serum 25-Hydroxyvitamin D associated with indicators of body fat and insulin resistance in prepubertal chilean children. Int J Obes. 2016;40:147–152. doi:10.1038/ijo.2015.148.
51. Teschendorff AE, Marabita F, Lechner M, et al. A beta-mixture quantile normalization method for correcting probe design bias in Illumina Infinium 450 k DNA methylation data. Bioinforma Oxf Engl. 2013;29:189–196. doi:10.1093/bioinformatics/bts680.
52. Houseman EA, Accomando WP, Koestler DC, et al. DNA methylation arrays as surrogate measures of cell mixture distribution. BMC Bioinformatics. 2012;13:86. doi:10.1186/1471-2105-13-86. PMID:22568884
53. Sánchez BN, Hu H, Litman HJ, et al. Statistical methods to study timing of vulnerability with sparsely sampled data on environmental toxicants. Environ Health Perspect. 2011;119:409–415. doi:10.1289/ehp.1102453. PMID:21362588
54. Chen Y-H, Ferguson KK, Meeker JD, et al. Statistical methods for modeling repeated measures of maternal environmental exposure biomarkers during pregnancy in association with preterm birth. Environ Health Glob Access Sci Source. 2015;14:9.
55. Horvath S, Gurven M, Levine ME, et al. An epigenetic clock analysis of race/ethnicity, sex, and coronary heart disease. Genome Biol. 2016;17:171. doi:10.1186/s13059-016-1030-0. PMID:27511193
56. Keim SA, Branum AM, Klebanoff MA, et al. Maternal body mass index and daughters’ age at menarche. Epidemiol Camb Mass. 2009;20:677–681. doi:10.1097/EDE.0b013e3181b093ce.
57. Terry MB, Ferris JS, Tehranifar P. Birth weight, postnatal growth, and age at menarche. Am J Epidemiol. 2009;170:72–79. doi:10.1093/aje/kwp095. PMID:19439580
58. Tamimi RM, Eriksson L, Lagiou P, et al. Birth weight and mammographic density among postmenopausal women in Sweden. Int J Cancer. 2010;126:985–991. PMID:19642103
59. Tehranifar P, Cohn BA, Flom JD. Early life socioeconomic environment and mammographic breast density. BMC Cancer. 2017;17:41. doi:10.1186/s12885-016-3010-x. PMID:28068940
60. Katsoulis M, La Vecchia C, Trichopoulou A, et al. Maternal height and breast cancer risk: results from a study nested within the EPIC-Greece cohort. Eur J Epidemiol. 2017;32:457–463. doi:10.1007/s10654-017-0245-z. PMID:28417273
61. Wickham H. ggplot2: Elegant graphics for data analysis. New York: Springer-Verlag; 2009.