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Associations of long interspersed nuclear element-1 DNA methylation with preterm birth in a prospective cohort study

Published online by Cambridge University Press:  29 February 2012

H. H. Burris*
Affiliation:
Department of Neonatology, Beth Israel Deaconess Medical Center, Division of Newborn Medicine, Children's Hospital Boston, Harvard Medical School, Boston, MA, USA
S. L. Rifas-Shiman
Affiliation:
Obesity Prevention Program, Department of Population Medicine, Harvard Medical School and Harvard Pilgrim Health Care Institute, Boston, MA, USA
A. Baccarelli
Affiliation:
Department of Environmental Health, Harvard School of Public Health, Boston, MA, USA
L. Tarantini
Affiliation:
Department of Preventive Medicine and Department of Environmental and Occupational Health, University of Milan and IRCCS Maggiore Hospital, Mangiagalli and Regina Elena Foundation, Milan, Italy
C. E. Boeke
Affiliation:
Department of Nutrition, Harvard School of Public Health, Boston, MA, USA Department of Epidemiology, Harvard School of Public Health, Boston, MA, USA
K. Kleinman
Affiliation:
Obesity Prevention Program, Department of Population Medicine, Harvard Medical School and Harvard Pilgrim Health Care Institute, Boston, MA, USA
A. A. Litonjua
Affiliation:
Channing Laboratory, Department of Medicine, Brigham and Women's Hospital, Harvard School of Public Health, Boston, MA, USA Division of Pulmonary and Critical Care, Brigham and Women's Hospital, Boston, MA, USA
J. W. Rich-Edwards
Affiliation:
Department of Epidemiology, Harvard School of Public Health, Boston, MA, USA Women's Health, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA
M. W. Gillman
Affiliation:
Obesity Prevention Program, Department of Population Medicine, Harvard Medical School and Harvard Pilgrim Health Care Institute, Boston, MA, USA Department of Nutrition, Harvard School of Public Health, Boston, MA, USA
*
*Address for correspondence: H. H. Burris, Department of Neonatology, Beth Israel Deaconess Medical Center, Division of Newborn Medicine, Children's Hospital Boston, Harvard Medical School, Boston, MA, USA (Email [email protected])

Abstract

Preterm birth affects over 12% of all infants born in the United States; yet the biology of early delivery remains unclear, including whether epigenetic mechanisms are involved. We examined associations of maternal and umbilical cord blood long interspersed nuclear element-1 (LINE-1) DNA methylation with length of gestation and odds of preterm birth in singleton pregnancies in Project Viva. In white blood cells from maternal blood during first trimester (n = 914) and second trimester (n = 922), and from venous cord blood at delivery (n = 557), we measured LINE-1 by pyrosequencing [expressed as %5 methyl cytosines within the LINE-1 region analyzed (%5mC)]. We ran linear regression models to analyze differences in gestation length, and logistic models for odds of preterm birth (<37 v. ⩾37 weeks’ gestation), across quartiles of LINE-1. Mean (s.d.) LINE-1 levels were 84.3 (0.6), 84.5 (0.4) and 84.6 (0.7) %5mC for first trimester, second trimester and cord blood, respectively. Mean (s.d.) gestational age was 39.5 (1.8) weeks, and 6.5% of infants were born preterm. After adjustment for maternal age, race/ethnicity, body mass index, education, smoking status and fetal sex, women with the highest v. lowest quartile of first trimester LINE-1 had longer gestations [0.45 weeks (95% CI 0.12, 0.78)] and lower odds of preterm birth [OR 0.40 (0.17, 0.94)], whereas associations with cord blood LINE-1 were in the opposite direction (−0.45 weeks, −0.83, −0.08) and [OR 4.55 (1.18, 17.5)]. In conclusion, higher early pregnancy LINE-1 predicts lower risk of preterm birth. In contrast, preterm birth is associated with lower LINE-1 in cord blood.

Type
Original Article
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2012

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References

1. Hamilton, BE, Martin, JA, Ventura, SJ. Births: preliminary data for 2009 (online). National Center for Health Statistics, 2010. http://www.cdc.gov/nchs/data/nvsr/nvsr59/nvsr59_03.pdf. Natl Vital Stat Rep. 2010; 59.Google ScholarPubMed
2. MacDorman, MF, Callaghan, WM, Mathews, TJ, Hoyert, DL, Kochanek, KD. Trends in preterm-related infant mortality by race and ethnicity, United States, 1999–2004. Int J Health Serv. 2007; 37, 635641.CrossRefGoogle ScholarPubMed
3. Stoll, BJ, Hansen, NI, Bell, EF, et al. . Neonatal outcomes of extremely preterm infants from the NICHD Neonatal Research Network. Pediatrics. 2010; 126, 443456.Google Scholar
4. Woythaler, MA, McCormick, MC, Smith, VC. Late preterm infants have worse 24-month neurodevelopmental outcomes than term infants. Pediatrics. 2010; 127, e622e629.CrossRefGoogle Scholar
5. Kramer, MS, Seguin, L, Lydon, J, Goulet, L. Socio-economic disparities in pregnancy outcome: why do the poor fare so poorly? Paediatr Perinat Epidemiol. 2000; 14, 194210.Google Scholar
6. David, RJ, Collins, JW Jr. Differing birth weight among infants of U.S.-born blacks, African-born blacks, and U.S.-born whites. N Engl J Med. 1997; 337, 12091214.Google Scholar
7. Hitti, J, Nugent, R, Boutain, D, et al. . Racial disparity in risk of preterm birth associated with lower genital tract infection. Paediatr Perinat Epidemiol. 2007; 21, 330337.CrossRefGoogle ScholarPubMed
8. Hillier, SL, Nugent, RP, Eschenbach, DA, et al. . Association between bacterial vaginosis and preterm delivery of a low-birth-weight infant. The Vaginal Infections and Prematurity Study Group. N Engl J Med. 1995; 333, 17371742.Google Scholar
9. Goldenberg, RL, Andrews, WW, Guerrant, RL, et al. . The preterm prediction study: cervical lactoferrin concentration, other markers of lower genital tract infection, and preterm birth. National Institute of Child Health and Human Development Maternal-Fetal Medicine Units Network. Am J Obstet Gynecol. 2000; 182, 631635.CrossRefGoogle ScholarPubMed
10. Savitz, DA, Dole, N, Terry, JW Jr, Zhou, H, Thorp, JM Jr. Smoking and pregnancy outcome among African-American and white women in central North Carolina. Epidemiology. 2001; 12, 636642.CrossRefGoogle ScholarPubMed
11. Behrman, RE, Butler, AS. Institute of Medicine (U.S.). Committee on Understanding Premature Birth and Assuring Healthy Outcomes. Preterm Birth: Causes, Consequences, and Prevention. National Academies Press, Washington, DC 2007.Google Scholar
12. Burris, HH, Collins, JW Jr. Race and preterm birth – the case for epigenetic inquiry. Ethn Dis. 2010; 20, 296299.Google Scholar
13. Bollati, V, Baccarelli, A. Environmental epigenetics. Heredity. 2010; 105, 105112.Google Scholar
14. Doerfler, W. DNA methylation and gene activity. Annu Rev Biochem. 1983; 52, 93124.Google Scholar
15. Hedges, DJ, Deininger, PL. Inviting instability: transposable elements, double-strand breaks, and the maintenance of genome integrity. Mutat Res. 2007; 616, 4659.CrossRefGoogle ScholarPubMed
16. Bestor, TH. The host defence function of genomic methylation patterns. Novartis Found Symp. 1998; 214, 187195. discussion 195-189, 228-132.Google Scholar
17. Yang, AS, Estecio, MR, Doshi, K, et al. . A simple method for estimating global DNA methylation using bisulfite PCR of repetitive DNA elements. Nucleic Acids Res. 2004; 32, e38.CrossRefGoogle ScholarPubMed
18. Li, TH, Schmid, CW. Differential stress induction of individual Alu loci: implications for transcription and retrotransposition. Gene. 2001; 276, 135141.CrossRefGoogle ScholarPubMed
19. Schulz, WA. L1 retrotransposons in human cancers. J Biomed Biotechnol. 2006; Article no. 83672, 12pp., 2006. doi:10.1155/JBB/2006/83672.Google ScholarPubMed
20. Bollati, V, Galimberti, D, Pergoli, L, et al. . DNA methylation in repetitive elements and Alzheimer disease. Brain Behav Immun. 2011; 25, 10781083.Google Scholar
21. Baccarelli, A, Wright, R, Bollati, V, et al. . Ischemic heart disease and stroke in relation to blood DNA methylation. Epidemiology. 2010; 21, 819828.CrossRefGoogle ScholarPubMed
22. Timmermans, S, Jaddoe, VW, Silva, LM, et al. . Folic acid is positively associated with uteroplacental vascular resistance: the Generation R Study. Nutr Metab Cardiovasc Dis. 2011; 21, 5461. Epub October 12, 2009.CrossRefGoogle ScholarPubMed
23. Timmermans, S, Jaddoe, VW, Hofman, A, Steegers-Theunissen, RP, Steegers, EA. Periconception folic acid supplementation, fetal growth and the risks of low birth weight and preterm birth: the Generation R Study. Br J Nutr. 2009, 19.Google ScholarPubMed
24. Hsiung, DT, Marsit, CJ, Houseman, EA, et al. . Global DNA methylation level in whole blood as a biomarker in head and neck squamous cell carcinoma. Cancer Epidemiol Biomarkers Prev. 2007; 16, 108114.Google Scholar
25. Ingrosso, D, Cimmino, A, Perna, AF, et al. . Folate treatment and unbalanced methylation and changes of allelic expression induced by hyperhomocysteinaemia in patients with uraemia. Lancet. 2003; 361, 16931699.Google Scholar
26. Bonamy, AK, Parikh, NI, Cnattingius, S, Ludvigsson, JF, Ingelsson, E. Birth characteristics and subsequent risks of maternal cardiovascular disease: effects of gestational age and fetal growth. Circulation. 2011; 124, 28392846.CrossRefGoogle ScholarPubMed
27. McGovern, PG, Llorens, AJ, Skurnick, JH, Weiss, G, Goldsmith, LT. Increased risk of preterm birth in singleton pregnancies resulting from in vitro fertilization-embryo transfer or gamete intrafallopian transfer: a meta-analysis. Fertil Steril. 2004; 82, 15141520.Google Scholar
28. Jackson, RA, Gibson, KA, Wu, YW, Croughan, MS. Perinatal outcomes in singletons following in vitro fertilization: a meta-analysis. Obstet Gynecol. 2004; 103, 551563.CrossRefGoogle ScholarPubMed
29. McDonald, SD, Murphy, K, Beyene, J, Ohlsson, A. Perinatel outcomes of singleton pregnancies achieved by in vitro fertilization: a systematic review and meta-analysis. J Obstet Gynaecol Can. 2005; 27, 449459.Google Scholar
30. Morgan, HD, Santos, F, Green, K, Dean, W, Reik, W. Epigenetic reprogramming in mammals. Hum Mol Genet. 2005; 14 (Spec. no. 1) R47R58.Google Scholar
31. Manipalviratn, S, DeCherney, A, Segars, J. Imprinting disorders and assisted reproductive technology. Fertil Steril. 2009; 91, 305315.CrossRefGoogle ScholarPubMed
32. Bollati, V, Schwartz, J, Wright, R, et al. . Decline in genomic DNA methylation through aging in a cohort of elderly subjects. Mech Ageing Dev. 2009; 130, 234239.Google Scholar
33. Zhu, ZZ, Sparrow, D, Hou, L, et al. . Repetitive element hypomethylation in blood leukocyte DNA and cancer incidence, prevalence, and mortality in elderly individuals: the Normative Aging Study. Cancer Causes Control. 2010; 22, 437447.Google Scholar
34. Gillman, MW, Rich-Edwards, JW, Rifas-Shiman, SL, et al. . Maternal age and other predictors of newborn blood pressure. J Pediatr. 2004; 144, 240245.Google Scholar
35. Stuebe, AM, Oken, E, Gillman, MW. Associations of diet and physical activity during pregnancy with risk for excessive gestational weight gain. Am J Obstet Gynecol. 2009; 201, e51e58.Google Scholar
36. Baccarelli, A, Wright, RO, Bollati, V, et al. . Rapid DNA methylation changes after exposure to traffic particles. Am J Respir Crit Care Med. 2009; 179, 572578.CrossRefGoogle ScholarPubMed
37. Tarantini, L, Bonzini, M, Apostoli, P, et al. . Effects of particulate matter on genomic DNA methylation content and iNOS promoter methylation. Environ Health Perspect. 2009; 117, 217222.Google Scholar
38. Laird, NM, Ware, JH. Random-effects models for longitudinal data. Biometrics. 1982; 38, 963974.Google Scholar
39. McElrath, TF, Hecht, JL, Dammann, O, et al. . Pregnancy disorders that lead to delivery before the 28th week of gestation: an epidemiologic approach to classification. Am J Epidemiol. 2008; 168, 980989.Google Scholar
40. Ananth, CV, Vintzileos, AM. Medically indicated preterm birth: recognizing the importance of the problem. Clin Perinatol. 2008; 35, 5367, viii.CrossRefGoogle ScholarPubMed
41. Lucchinetti, E, Feng, J, Silva, R, et al. . Inhibition of LINE-1 expression in the heart decreases ischemic damage by activation of Akt/PKB signaling. Physiol Genomics. 2006; 25, 314324.Google Scholar
42. Roberts, JM, Gammill, HS. Preeclampsia: recent insights. Hypertension. 2005; 46, 12431249.Google Scholar
43. Gravett, MG, Novy, MJ. Endocrine–immune interactions in pregnant non-human primates with intrauterine infection. Infect Dis Obstet Gynecol. 1997; 5, 142153.CrossRefGoogle ScholarPubMed
44. Pitiphat, W, Gillman, MW, Joshipura, KJ, et al. . Plasma C-reactive protein in early pregnancy and preterm delivery. Am J Epidemiol. 2005; 162, 11081113.Google Scholar
45. Baccarelli, A, Tarantini, L, Wright, RO, et al. . Repetitive element DNA methylation and circulating endothelial and inflammation markers in the VA normative aging study. Epigenetics. 2010; 5, 222228.CrossRefGoogle ScholarPubMed
46. Gasche, JA, Hoffmann, J, Boland, CR, Goel, A. Interleukin-6 promotes tumorigenesis by altering DNA methylation in oral cancer cells. Int J Cancer. 2011; 129, 10531063.Google Scholar
47. Crow, MK. Long interspersed nuclear elements (LINE-1): potential triggers of systemic autoimmune disease. Autoimmunity. 2010; 43, 716.Google Scholar
48. Cheng, MH, Wang, PH. Placentation abnormalities in the pathophysiology of preeclampsia. Expert Rev Mol Diagn. 2009; 9, 3749.Google Scholar
49. Fuke, C, Shimabukuro, M, Petronis, A, et al. . Age related changes in 5-methylcytosine content in human peripheral leukocytes and placentas: an HPLC-based study. Ann Hum Genet. 2004; 68, 196204.Google Scholar
50. Purisch, SE, DeFranco, EA, Muglia, LJ, et al. . Preterm birth in pregnancies complicated by major congenital malformations: a population-based study. Am J Obstet Gynecol. 2008; 199, 287, e1e8.Google Scholar
51. Kulkarni, A, Chavan-Gautam, P, Mehendale, S, Yadav, H, Joshi, S. Global DNA methylation patterns in placenta and its association with maternal hypertension in pre-eclampsia. DNA Cell Biol. 2011; 30, 7984.Google Scholar
52. Tabano, S, Colapietro, P, Cetin, I, et al. . Epigenetic modulation of the IGF2/H19 imprinted domain in human embryonic and extra-embryonic compartments and its possible role in fetal growth restriction. Epigenetics. 2010; 5, 313324.Google Scholar
53. Bollati, V, Fabris, S, Pegoraro, V, et al. . Differential repetitive DNA methylation in multiple myeloma molecular subgroups. Carcinogenesis. 2009; 30, 13301335.Google Scholar
54. Martin, JA, Hamilton, BE, Sutton, PD, et al. . Births: final data for 2008. Hyattsville, MD: National Center for Health Statistics. 2010. Natl Vital Stat Rep. 2010; 59.Google Scholar
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