Maternal pre-pregnancy BMI and gestational weight gain, offspring DNA methylation and later offspring adiposity: Findings from the Avon Longitudinal Study of Parents and Children

International Journal of Epidemiology

Volumn 44, Issue 4, 2015, Pages 1288-1304

  Sharp, Gemma C ^a   Lawlor, Debbie A ^a   Richmond, Rebecca C ^a   Fraser, Abigail ^a   Simpkin, Andrew ^a   Suderman, Matthew ^a   Shihab, Hashem A ^a   Lyttleton, Oliver ^a   McArdle, Wendy ^a   Ring, Susan M ^a   Gaunt, Tom R ^a   Smith, George Davey ^a   Relton, Caroline L ^a,b  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

ALSPAC; ARIES; Causality; Epigenetic; Epigenome wide association study; Longitudinal; Overnutrition; Overweight; Undernutrition

Indexed keywords

BODY MASS; CHILD HEALTH; DNA; GENETICS; MATERNAL EFFECT; METHYLATION; NUTRITIONAL STATUS; OBESITY; PATERNAL CARE; PREGNANCY; WEIGHT;

ADOLESCENT; ARTICLE; BODY MASS; CHILD; DNA METHYLATION; FEMALE; HUMAN; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MALE; MATERNAL OBESITY; MOTHER; NEWBORN; OBESITY; PARENT; PREGNANCY; PRIORITY JOURNAL; PROGENY; SCHOOL CHILD; STATISTICAL SIGNIFICANCE; UNDERWEIGHT; WEIGHT GAIN; BODY WEIGHT; GENETICS; GENOME-WIDE ASSOCIATION STUDY; MATERNAL NUTRITION; OVERNUTRITION; UNITED KINGDOM;

ADIPOSITY; ADOLESCENT; BODY MASS INDEX; CHILD; DNA METHYLATION; FEMALE; GENOME-WIDE ASSOCIATION STUDY; HUMANS; LONGITUDINAL STUDIES; MALE; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; OBESITY; OVERNUTRITION; PREGNANCY; THINNESS; UNITED KINGDOM; WEIGHT GAIN;

EID: 84936787346     PISSN: 03005771     EISSN: 14643685     Source Type: Journal    
DOI: 10.1093/ije/dyv042     Document Type: Article

References (49)

1. Lumey LH, Stein AD, Susser E. Prenatal famine and adult health. Ann Rev Public Halth 2011;32:237-62.
2. Fraser A, Tilling K, Macdonald-Wallis C et al. Association of maternal weight gain in pregnancy with offspring obesity and metabolic and vascular traits in childhood. Circulation 2010; 121:2557-64.
3. Lawlor DA, Relton C, Sattar N, Nelson SM. Maternal adiposity - a determinant of perinatal and offspring outcomes? Nat Rev Endocrinol 2012;8:679-88.
4. Lawlor DA. The Society for Social Medicine John Pemberton Lecture 2011. Developmental overnutrition-an old hypothesis with new importance? Int J Epidemiol 2013;42:7-29.
5. Lawlor DA, Lichtenstein P, Fraser A, Långström N. Does maternal weight gain in pregnancy have long-term effects on offspring adiposity? A sibling study in a prospective cohort of 146,894 men from 136,050 families. Am J Clin Nutr 2011;94:142-48.
6. Lawlor DA, Lichtenstein P, Långström N. Association of maternal diabetes mellitus in pregnancy with offspring adiposity into early adulthood: sibling study in a prospective cohort of 280,866 men from 248,293 families. Circulation 2011;123:258-65.
7. Kral JG, Biron S, Simard S et al. Large maternal weight loss from obesity surgery prevents transmission of obesity to children who were followed for 2 to 18 years. Pediatrics 2006;118:e1644-49.
8. Smith J, Cianflone K, Biron S et al. Effects of maternal surgical weight loss in mothers on intergenerational transmission of obesity. J Clin Endocrinol Metab. 2009;94:4275-83.
9. Berglind D, Willmer M, Näslund E, Tynelius P, Sørensen TIA, Rasmussen F. Differences in gestational weight gain between pregnancies before and after maternal bariatric surgery correlate with differences in birth weight but not with scores on the body mass index in early childhood. Pediatr Obes 2014;9:427-34
10. Willmer M, Berglind D, Sørensen TIA, Näslund E, Tynelius P, Rasmussen F. Surgically induced interpregnancy weight loss and prevalence of overweight and obesity in offspring. PloS One 2013;8(:e82247.
11. Lillycrop KA, Burdge GC. Epigenetic changes in early life and future risk of obesity. Int J Obes (Lond) 2011;35:72-83.
12. Mathers JC. Early nutrition: impact on epigenetics. Forum Nutr 2007;60:42-48.
13. Li CCY, Maloney CA, Cropley JE, Suter CM. Epigenetic programming by maternal nutrition: shaping future generations. Epigenomics 2010;2:539-49.
14. 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;105:17046-49.
15. Tobi EW, Lumey LH, Talens RP et al. DNA methylation differences after exposure to prenatal famine are common and timingand sex-specific. Hum Mol Genet 2009;18:4046-53.
16. Waterland RA, Kellermayer R, Laritsky E et al. Season of conception in rural Gambia affects DNA methylation at putative human metastable epialleles. PLoS Genet 2010;6:e1001252.
17. Dominguez-Salas P, Moore SE, Baker MS et al. Maternal nutrition at conception modulates DNA methylation of human metastable epialleles. Nat Communications 2014;5:3746.
18. Guénard F, Tchernof A, Deshaies Y et al. Methylation and expression of immune and inflammatory genes in the offspring of bariatric bypass surgery patients. J Obes 2013;2013:492170.
19. Michels KB, Harris HR, Barault L. Birthweight, maternal weight trajectories and global DNA methylation of LINE-1 repetitive elements. PloS One 2011;6:e25254.
20. Herbstman JB, Wang S, Perera FP et al. Predictors and consequences of global DNA methylation in cord blood and at three years. PLoS One 2013;8:e72824.
21. Morales E, Groom A, Lawlor DA, Relton CL. DNA methylation signatures in cord blood associated with maternal gestational weight gain: results from the ALSPAC cohort. BMC Res Notes 2014;7:278.
22. Liu X, Chen Q, Tsai H-J et al. Maternal preconception body mass index and offspring cord blood DNA methylation: exploration of early life origins of disease. Environ Mol Mutagen 2014; 55:223-30.
23. Gemma C, Sookoian S, Alvariñas J et al. Maternal pregestational BMI is associated with methylation of the PPARGC1A promoter in newborns. Obesity (Silver Spring) 2009;17:1032-39.
24. Godfrey KM, Sheppard A, Gluckman PD et al. Epigenetic gene promoter methylation at birth is associated with child's later adiposity. Diabetes 2011;60:1528-34.
25. Relton CL, Groom A, St Pourcain B et al. DNA methylation patterns in cord blood DNA and body size in childhood. PLoS One 2012;7:e31821.
26. Davey Smith G. Negative control exposures in epidemiologic studies. Epidemiology 2012;23:350-51; author reply 351-52.
27. Richmond R, Al-Amin A, Davey Smith G, Relton C. Approaches for drawing causal inferences from epidemiological birth cohorts: A review. Early Human Development. 2014;90:769-80.
28. Boyd A, Golding J, Macleod J et al. Cohort Profile: The 'children of the 90s'-the index offspring of the Avon Longitudinal Study of Parents and Children. Int J Epidemiol 2013;42:111-27.
29. Fraser A, Macdonald-Wallis C, Tilling K et al. Cohort Profile:The Avon Longitudinal Study of Parents and Children: ALSPAC mothers cohort. Int J Epidemiol 2013;42:97-110.
30. Macdonald-Wallis C, Lawlor DA, Palmer T, Tilling K. Multivariate multilevel spline models for parallel growth processes:application to weight and mean arterial pressure in pregnancy. Stat Med 2012;31:3147-64.
31. Institute of Medicine (US) and National Research Council (US) Committee to Reexamine IOM Pregnancy Weight Guidelines. Rasmussen K, Yaktine A (eds). Weight Gain During Pregnancy:Reexamining the Guidelines. Washington, DC: National Academies Press, 2009.
32. Bibikova M, Barnes B, Tsan C et al. High density DNA methylation array with single CpG site resolution. Genomics 2011;98:288-95.
33. Schalkwyk LC, Pidsley R, Wong CC et al. wateRmelon: Illumina 450 methylation array normalization and metrics. R package version 1.5.1. 2013.
34. Touleimat N, Tost J. Complete pipeline for Infinium(VR ) Human Methylation 450K BeadChip data processing using subset quantile normalization for accurate DNA methylation estimation. Epigenomics 2012;4:325-41.
35. Aryee MJ, Jaffe AE, Corrada-Bravo H et al. Minfi: a flexible and comprehensive Bioconductor package for the analysis of Infinium DNA methylation microarrays. Bioinformatics 2014; 30:1363-69.
36. Houseman EA, Accomando WP, Koestler DC et al. DNA methylation arrays as surrogate measures of cell mixture distribution. BMC Bioinformatics 2012;13:86.
37. Davey Smith G, Steer C, Leary S, Ness A. Is there an intrauterine influence on obesity? Evidence from parent child associations in the Avon Longitudinal Study of Parents and Children (ALSPAC). Arch Dis Child 2007;92:876-80.
38. Lawlor DA, Timpson NJ, Harbord RM et al. Exploring the developmental overnutrition hypothesis using parental-offspring associations and FTO as an instrumental variable. PLoS Med 2008;5:e33.
39. Du P, Zhang X, Huang C-C et al. Comparison of Beta-value and M-value methods for quantifying methylation levels by microarray analysis. BMC Bioinformatics 2010;11:587.
40. Laird N, Ware J. Random-effects for longitudinal data. Biometrics 1982;3:963-974.
41. Goldstein H. Multilevel mixed linear model analysis using iterative generalized least squares. Biometrika 1986;73:43-56.
42. Wrotniak BH, Shults J, Butts S, Stettler N. Gestational weight gain and risk of overweight in the offspring at age 7 y in a multicenter, multiethnic cohort study. Am J Clin Nutr 2008;87:1818-24.
43. Oken E, Taveras EM, Kleinman KP, Rich-Edwards JW, Gillman MW. Gestational weight gain and child adiposity at age 3 years. Am J Obstet Gynecol 2007;196:322.e1-8.
44. Moreira P, Padez C, Mourão-Carvalhal I, Rosado V. Maternal weight gain during pregnancy and overweight in Portuguese children. Int J Obes (Lond) 2007;31:608-14.
45. Lawlor DA, Fraser A, Macdonald-Wallis C et al. Maternal and offspring adiposity-related genetic variants and gestational weight gain. Am J Clin Nutr 2011;94:149-55.
46. Relton CL, Davey Smith G. Two-step epigenetic Mendelian randomization:a strategy for establishing the causal role of epigenetic processes in pathways to disease. Int J Epidemiol 2012;41:161-76.
47. Clark C, Palta P, Joyce CJ et al. A comparison of the whole genome approach of MeDIP-seq to the targeted approach of the Infinium HumanMethylation450 BeadChip(VR ) for methylome profiling. PloS One 2012;7:e50233.
48. Slieker RC, Bos SD, Goeman JJ et al. Identification and systematic annotation of tissue-specific differentially methylated regions using the Illumina 450k array. Epigenet Chromatin 2013; 6:26.
49. Patel R, Martin RM, Kramer MS et al. Familial associations of adiposity: findings from a cross-sectional study of 12,181 parental-offspring trios from Belarus. PloS One 2011;6(1):e14607.