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Exposures in early life: associations with DNA promoter methylation in breast tumors

Published online by Cambridge University Press:  10 December 2012

M.-H. Tao ,
C. Marian ,
P. G. Shields ,
N. Potischman ,
J. Nie ,
S. S. Krishnan ,
D. L. Berry ,
B. V. Kallakury ,
C. Ambrosone  and
S. B. Edge
...Show all authors
M.-H. Tao*
Affiliation:
Institute for Translational Epidemiology, Mount Sinai School of Medicine, New York, NY, USA
C. Marian
Affiliation:
Ohio State University Cancer Center, The Ohio State University, Columbus, OH, USA
P. G. Shields
Affiliation:
Ohio State University Cancer Center, The Ohio State University, Columbus, OH, USA
N. Potischman
Affiliation:
Applied Research Program, Division of Cancer Control and Population Sciences, National Cancer Institute, Bethesda, MD, USA
J. Nie
Affiliation:
Department of Social and Preventive Medicine, School of Public Health and Health Professions, University at Buffalo, Buffalo, NY, USA
S. S. Krishnan
Affiliation:
Ohio State University Cancer Center, The Ohio State University, Columbus, OH, USA
D. L. Berry
Affiliation:
Lombardi Cancer Center, Georgetown University, Washington, DC, USA
B. V. Kallakury
Affiliation:
Lombardi Cancer Center, Georgetown University, Washington, DC, USA
C. Ambrosone
Affiliation:
Department of Cancer Prevention and Control, Roswell Park Cancer Institute, Buffalo, NY, USA
S. B. Edge
Affiliation:
Department of Surgery, Roswell Park Cancer Institute, Buffalo, NY, USA
M. Trevisan
Affiliation:
Department of Social and Preventive Medicine, School of Public Health and Health Professions, University at Buffalo, Buffalo, NY, USA School of Biomedical Education, City College of New York, New York, NY, USA
J. Winston
Affiliation:
Potomac Hospital, Woodbridge, VA, USA
J. L. Freudenheim
Affiliation:
Department of Social and Preventive Medicine, School of Public Health and Health Professions, University at Buffalo, Buffalo, NY, USA
*
*Address for correspondence: Dr M.-H. Tao, Institute for Translational Epidemiology, Mount Sinai School of Medicine, PO BOX 1057, New York, NY 10029, USA. Email [email protected]
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Abstract

There is evidence that epigenetic changes occur early in breast carcinogenesis. We hypothesized that early-life exposures associated with breast cancer would be associated with epigenetic alterations in breast tumors. In particular, we examined DNA methylation patterns in breast tumors in association with several early-life exposures in a population-based case–control study. Promoter methylation of E-cadherin, p16 and RAR-β2 genes was assessed in archived tumor blocks from 803 cases with real-time methylation-specific PCR. Unconditional logistic regression was used for case–case comparisons of those with and without promoter methylation. We found no differences in the prevalence of DNA methylation of the individual genes by age at menarche, age at first live birth and weight at age 20. In case–case comparisons of premenopausal breast cancer, lower birth weight was associated with increased likelihood of E-cadherin promoter methylation (OR = 2.79, 95% CI, 1.15–6.82, for ⩽2.5 v. 2.6–2.9 kg); higher adult height with RAR-β2 methylation (OR = 3.34, 95% CI, 1.19–9.39, for ⩾1.65 v. <1.60 m); and not having been breastfed with p16 methylation (OR = 2.75, 95% CI, 1.14–6.62). Among postmenopausal breast cancers, birth order was associated with increased likelihood of p16 promoter methylation. Being other than first in the birth order was inversely associated with likelihood of ⩾1 of the three genes being methylated for premenopausal breast cancers, but positively associated with methylation in postmenopausal women. These results suggest that there may be alterations in methylation associated with early-life exposures that persist into adulthood and affect breast cancer risk.

Keywords

breast cancerearly-life exposureepidemiologyepigeneticspromoter methylation
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 4 , Issue 2 , April 2013 , pp. 182 - 190
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2012 

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References

1.Okasha, M, McCarron, P, Gunnell, D, Smith, GD. Exposures in childhood, adolescence and early adulthood and breast cancer risk: a systematic review of the literature. Breast Cancer Res Treat. 2003; 78, 223–276.CrossRefGoogle Scholar
2.Burdge, GC, Lillycrop, KA, Jackson, AA. Nutrition in early life, and risk of cancer and metabolic disease: alternative endings in an epigenetic tale? Br J Nutr. 2009; 101, 619–630.CrossRefGoogle Scholar
3.Russo, J, Russo, IH. Development of the human breast. Maturitas. 2004; 49, 2–15.CrossRefGoogle ScholarPubMed
4.Park, SK, Kang, D, McGlynn, KA, et al. Intrauterine environments and breast cancer risk: meta-analysis and systematic review. Breast Cancer Res. 2008; 10, R8.CrossRefGoogle ScholarPubMed
5.Xu, X, Dailey, AB, Peoples-Sheps, M, et al. Birth weight as a risk factor for breast cancer: a meta-analysis of 18 epidemiological studies. J Womens Health. 2009; 18, 1169–1178.CrossRefGoogle ScholarPubMed
6.Xue, F, Michels, KB. Intrauterine factors and risk of breast cancer: a systematic review and meta-analysis of current evidence. Lancet Oncol. 2007; 8, 1088–1100.CrossRefGoogle ScholarPubMed
7.Martin, RM, Middleton, N, Gunnell, D, Owen, CG, Smith, GD. Breast-feeding and cancer: the Boyd Orr Cohort and a systematic review with meta-analysis. J Natl Cancer Inst. 2005; 97, 1446–1457.CrossRefGoogle Scholar
8.Forman, MR, Cantwell, MM, Ronckers, C, Zhang, Y. Through the looking glass at early-life exposures and breast cancer risk. Cancer Invest. 2005; 23, 609–624.CrossRefGoogle Scholar
9.Ruder, EH, Dorgan, JF, Kranz, S, Kris-Etherton, PM, Hartman, TJ. Examining breast cancer growth and lifestyle risk factors: early life, childhood, and adolescence. Clin Breast Cancer. 2008; 8, 334–342.CrossRefGoogle ScholarPubMed
10.Barba, M, McCann, SE, Nie, J, et al. Perinatal exposures and breast cancer risk in the Western New York Exposures and Breast Cancer (WEB) Study. Cancer Causes Control. 2006; 17, 395–401.CrossRefGoogle ScholarPubMed
11.Green, J, Cairns, BJ, Casabonne, D, et al, for the Million Women Study collaborators.Height and cancer incidence in the Million Women Study: prospective cohort, and meta-analysis of prospective studies of height and total cancer risk. Lancet Oncol. 2011; 12, 785–794.CrossRefGoogle ScholarPubMed
12.Waterland, RA. Is epigenetics an important link between early life events and adult disease? Horm Res. 2009; (Suppl 1), 13–16.Google ScholarPubMed
13.Bernal, AJ, Jirtle, RL. Epigenomic disruption: the effects of early developmental exposures. Birth Defects Res (Part A). 2010; 88, 938–944.CrossRefGoogle ScholarPubMed
14.Szyf, M, Pakneshan, P, Rabbani, SA. DNA methylation and breast cancer. Biochem Pharmacol. 2004; 68, 1187–1197.CrossRefGoogle ScholarPubMed
15.Esteller, M. Epigenetics in cancer. N Engl J Med. 2008; 358, 1148–1159.CrossRefGoogle ScholarPubMed
16.Herman, JG, Merlo, A, Mao, L, et al. Inactivation of the CDKN2/p16/MTS1 gene is frequently associated with aberrant DNA methylation in all common human cancers. Cancer Res. 1995; 55, 4525–4530.Google ScholarPubMed
17.Arapshian, A, Kuppumbatti, YS, Mira-y-Lopez, R. Methylation of conserved CpG sites neighboring the beta retinoic acid response element may mediate retinoic acid receptor beta gene silencing in MCF-7 breast cancer cells. Oncogene. 2000; 19, 4066–4070.CrossRefGoogle ScholarPubMed
18.Caldeira, JR, Prando, EC, Quevedo, FC, et al. CDH1 promoter hypermethylation and E-cadherin protein expression in infiltrating breast cancer. BMC Cancer. 2006; 6, 48.CrossRefGoogle ScholarPubMed
19.Desaulniers, D, Xiao, GH, Lian, H, et al. Effects of mixtures of polychlorinated biphenyls, methylmercury, and organochlorine pesticides on hepatic DNA methylation in prepubertal female Sprague-Dawley rats. Int J Toxicol. 2009; 28, 294–307.CrossRefGoogle ScholarPubMed
20.Heijmans, BT, Tobi, EW, Stein, AD, et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci U S A. 2008; 105, 17046–17049.CrossRefGoogle ScholarPubMed
21.Tao, MH, Shields, PG, Nie, J, et al. DNA hypermethylation and clinicopathological features in breast cancer: the Western New York Exposures and Breast Cancer (WEB) Study. Breast Cancer Res Treat. 2009; 114, 559–568.CrossRefGoogle ScholarPubMed
22.Tao, MH, Marian, C, Nie, J, et al. Body mass and DNA promoter methylation in breast tumors in the Western New York Exposures and Breast Cancer Study. Am J Clin Nutr. 2011; 94, 831–838.CrossRefGoogle ScholarPubMed
23.Mellemkjaer, L, Olsen, ML, Sørensen, HT, et al. Birth weight and risk of early-onset breast cancer (Denmark). Cancer Causes Control. 2003; 14, 61–64.CrossRefGoogle ScholarPubMed
24.Innes, K, Byers, T, Schymura, M. Birth characteristics and subsequent risk for breast cancer in very young women. Am J Epidemiol. 2000; 152, 1121–1128.CrossRefGoogle ScholarPubMed
25.Fryer, AA, Emes, RD, Ismail, KM, et al. Quantitative, high-resolution epigenetic profiling of CpG loci identifies associations with cord blood plasma homocysteine and birth weight in humans. Epigenetics. 2011; 6, 86–94.CrossRefGoogle ScholarPubMed
26.La Merrill, M, Stein, CR, Landrigan, P, Engel, SM, Savitz, DA. Prepregnancy body mass index, smoking during pregnancy, and infant birth weight. Ann Epidemiol. 2011; 21, 413–420CrossRefGoogle ScholarPubMed
27.Flom, J, Ferris, J, Gonzalez, K, Santella, R, Terry, M. Prenatal tobacco smoke exposure and genome wide methylation in adulthood. Cancer Epidemiol Biomarkers Prev. 2011; 20, 2518–2523.CrossRefGoogle Scholar
28.Breton, CV, Byun, HM, Wenten, M, et al. Prenatal tobacco smoke exposure affects global and gene-specific DNA methylation. Am J Respir Crit Care Med. 2009; 180, 462–467.CrossRefGoogle ScholarPubMed
29.Shah, PS, Ohlsson, A. Knowledge Synthesis group on determinants of low birth weight and preterm births. Effects of prenatal multimicronutrient supplementation on pregnancy outcomes: a meta-analysis. CMAJ. 2009; 180, E99–E108.CrossRefGoogle Scholar
30.Attig, L, Gabory, A, Junien, C. Early nutrition and epigenetic programming: chasing shadows. Curr Opin Clin Nutr Metab Care. 2010; 13, 284–293.CrossRefGoogle ScholarPubMed
31.Freudenheim, JL, Marshall, JR, Graham, S, et al. Exposure to breastmilk in infancy and the risk of breast cancer. Epidemiology. 1995; 5, 324–331.CrossRefGoogle Scholar
32.Wise, LA, Titus-Ernstoff, L, Newcomb, PA, et al. Exposure to breast milk in infancy and risk of breast cancer. Cancer Causes Control. 2009; 20, 1083–1089.CrossRefGoogle ScholarPubMed
33.Michels, KB, Trichopoulos, D, Rosner, BA, et al. Being breastfed in infancy and breast cancer incidence in adult life: results from the two nurses’ health studies. Am J Epidemiol. 2001; 153, 275–283.CrossRefGoogle ScholarPubMed
34.Titus-Ernstoff, L, Egan, KM, Newcomb, PA, et al. Exposure to breast milk in infancy and adult breast cancer risk. J Natl Cancer Inst. 1998; 90, 921–924.CrossRefGoogle ScholarPubMed
35.Rodriguez-Palmero, M, Koletzko, B, Kunz, C, Jensen, R. Nutritional and biochemical properties of human milk: II. Lipids, micronutrients, and bioactive factors. Clin Perinatol. 1999; 26, 335–359.CrossRefGoogle ScholarPubMed
36.Knip, M, Virtanen, SM, Akerblom, HK. Infant feeding and the risk of type 1 diabetes. Am J Clin Nutr. 2010; 91, 1506S–1513S.CrossRefGoogle ScholarPubMed
37.Kang, GH, Lee, HJ, Hwang, KS, et al. Aberrant CpG island hypermethylation of chronic gastritis, in relation to aging, gender, intestinal metaplasia, and chronic inflammation. Am J Pathol. 2003; 163, 1551–1556.CrossRefGoogle ScholarPubMed
38.Issa, JP, Ahuja, N, Toyota, M, Bronner, MP, Brentnall, TA. Accelerated age-related CpG island methylation in ulcerative colitis. Cancer Res. 2001; 61, 3573–3577.Google ScholarPubMed
39.Hsieh, CC, Tzonou, A, Trichopoulos, D. Birth order and breast cancer risk. Cancer Causes Control. 1991; 2, 95–98.CrossRefGoogle ScholarPubMed
40.Fernandez, SV, Russo, J. Estrogen and xenoestrogens in breast cancer. Toxicol Pathol. 2010; 38, 110–122.CrossRefGoogle ScholarPubMed
41.Victora, CG, Adair, L, Fall, C, et al. Maternal and Child Undernutrition Study Group. Maternal and child undernutrition: consequences for adult health and human capital. Lancet. 2008; 371, 340–357.CrossRefGoogle Scholar
42.Hughes, LA, van den Brandt, PA, de Bruïne, AP, et al. Early life exposure to famine and colorectal cancer risk: a role for epigenetic mechanisms. PLoS One. 2009; 4, e7951.CrossRefGoogle Scholar
43.Li, L, Manor, O, Power, C. Early environment and child-to-adult growth trajectories in the 1958 British birth cohort. Am J Clin Nutr. 2004; 80, 185–192.CrossRefGoogle ScholarPubMed
44.Slanger, T, Mutschelknauss, E, Kropp, S, et al. Test-retest reliability of self-reported reproductive and lifestyle data in the context of a German case-control study on breast cancer and postmenopausal hormone therapy. Ann Epidemiol. 2007; 17, 993–998.CrossRefGoogle Scholar
45.Eads, CA, Danenberg, KD, Kawakami, K, et al. MethyLight: a high-throughput assay to measure DNA methylation. Nucleic Acids Res. 2000; 28, E32.CrossRefGoogle ScholarPubMed
46.Lee, ES, Issa, JP, Roberts, DB, et al. Quantitative promoter hypermethylation analysis of cancer-related genes in salivary gland carcinomas: comparison with methylation-specific PCR technique and clinical significance. Clin Cancer Res. 2008; 14, 2664–2672.CrossRefGoogle ScholarPubMed