Maternal pre-pregnancy obesity, offspring cord blood DNA methylation, and offspring cardiometabolic health in early childhood: an epigenome-wide association study

References

• Ogden CL, Carroll MD, Lawman HG, et al. Trends in obesity prevalence among children and adolescents in the United States, 1988–1994 Through 2013-2014. JAMA. 2016 Jun 7;315(21): 2292.
   PubMed Web of Science ®Google Scholar
• Ogden CL, Carroll MD, Kit BK, et al. Prevalence of obesity and trends in body mass index among US children and adolescents, 1999–2010. JAMA. 2012;307(5):483–490.
   PubMed Web of Science ®Google Scholar
• Fuemmeler BF, Wang L, Iversen ES, et al. Association between prepregnancy body mass index and gestational weight gain with size, tempo, and velocity of infant growth: analysis of the newborn epigenetic study cohort. Child Obes [Internet]. 2016 Jun [cited 2018 May 7];12(3): 210–218.
   PubMed Web of Science ®Google Scholar
• Oken E, Kleinman KP, Belfort MB, et al. Associations of gestational weight gain with short- and longer-term maternal and child health outcomes. Am J Epidemiol [Internet]. 2009 Jul 15 [cited 2018 May 7];170(2): 173–180.
   PubMed Web of Science ®Google Scholar
• Taveras EM, Rifas-Shiman SL, Belfort MB, et al. Weight status in the first 6 months of life and obesity at 3 years of age. Pediatrics [Internet]. 2009 Apr 1 [cited 2018 May 7];123(4): 1177–1183.
   PubMed Web of Science ®Google Scholar
• Barker DJ. Fetal origins of coronary heart disease. BMJ [Internet]. 1995 Jul 15 [cited 2018 May 7];311(6998): 171–174.
   PubMed Web of Science ®Google Scholar
• Claesson I-M, Sydsjö G, Olhager E, et al. Effects of a gestational weight gain restriction program for obese pregnant women: children’s weight development during the first five years of life. Child Obes [Internet]. 2016 Jun [cited 2018 May 7];12(3): 162–170.
   PubMed Web of Science ®Google Scholar
• Gregory EF, Goldshore MA, Henderson JL, et al. Infant growth following maternal participation in a gestational weight management intervention. Child Obes [Internet]. 2016 Jun [cited 2018 May 7];12(3): 219–225.
   PubMed Web of Science ®Google Scholar
• Tanvig M. Offspring body size and metabolic profile - effects of lifestyle intervention in obese pregnant women. Dan Med J [Internet]. 2014 Jul [cited 2018 May 7];61(7): B4893.
   PubMed Web of Science ®Google Scholar
• Dolinoy DC, Weidman JR, Waterland RA, et al. Maternal genistein alters coat color and protects Avy mouse offspring from obesity by modifying the fetal epigenome. Environ Health Perspect [Internet]. 2006 Apr [cited 2018 May 7];114(4): 567–572.
   PubMed Web of Science ®Google Scholar
• Woo Baidal JA, Locks LM, Cheng ER, et al. Risk factors for childhood obesity in the first 1,000 days. Am J Prev Med [Internet]. 2016 Jun [cited 2018 May 7];50(6): 761–779.
   PubMed Web of Science ®Google Scholar
• Branum AM, Kirmeyer SE, Gregory ECW. Prepregnancy body mass index by maternal characteristics and state: data from the birth certificate, 2014. Natl Vital Stat Rep [Internet]. 2016 Aug [cited 2018 May 7];65(6): 1–11.
   PubMedGoogle Scholar
• Waterland RA. Do maternal methyl supplements in mice affect DNA methylation of offspring? J Nutr [Internet]. 2003 Jan 1 [cited 2018 May 7];133(1): 238; author reply 239.
   PubMed Web of Science ®Google Scholar
• Heijmans BT, Tobi EW, Stein AD, et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci USA [Internet]. 2008 Nov 4 [cited 2018 May 7];105(44): 17046–17049.
   PubMed Web of Science ®Google Scholar
• Steegers-Theunissen RP, Obermann-Borst SA, Kremer D, et al. Periconceptional maternal folic acid use of 400 microg per day is related to increased methylation of the IGF2 gene in the very young child. Zhang C, editor. PLoS One. 2009 Nov 16 [cited.2018 May 7];4(11): e7845.
   PubMed Web of Science ®Google Scholar
• Hoyo C, Daltveit AK, Iversen E, et al. Erythrocyte folate concentrations, CpG methylation at genomically imprinted domains, and birth weight in a multiethnic newborn cohort. Epigenetics [Internet]. 2014 Aug 6 [cited 2018 May 7];9(8): 1120–1130.
   PubMed Web of Science ®Google Scholar
• Vidal AC, Murphy SK, Murtha AP, et al. Associations between antibiotic exposure during pregnancy, birth weight and aberrant methylation at imprinted genes among offspring. Int J Obes (Lond) [Internet]. 2013 Jul 28 [cited 2018 May 7];37(7): 907–913.
   PubMed Web of Science ®Google Scholar
• Sharp GC, Lawlor DA, Richmond RC, et al. 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. Int J Epidemiol. 2015;44(4):1288–1304.
   PubMed Web of Science ®Google Scholar
• Sharp GC, Salas LA, Monnereau C, et al. Maternal BMI at the start of pregnancy and offspring epigenome-wide DNA methylation: findings from the pregnancy and childhood epigenetics (PACE) consortium. Hum Mol Genet [Internet]. 2017;26(20): 4067–4085.
   PubMed Web of Science ®Google Scholar
• Michels KB, Harris HR, Barault L. Birthweight, maternal weight trajectories and global DNA methylation of LINE-1 repetitive elements. Fugmann SD, editor. PLoS One. 2011 Sep 28 [cited.2018 May 7];6(9): e25254.
   PubMed Web of Science ®Google Scholar
• Herbstman JB, Wang S, Perera FP, et al. Predictors and consequences of global DNA methylation in cord blood and at three years. El-Maarri O, editor. PLoS One. 2013 Sep 4 [cited 2018 May 7];8(9): e72824.
   PubMed Web of Science ®Google Scholar
• Liu X, Chen Q, Tsai HJ, 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(3):223–230.
   PubMed Web of Science ®Google Scholar
• Chen EY, Tan CMKou Y, et al. Enrichr: interactive and collaborative HTML5 gene list enrichment analysis tool. BMC Bioinformatics. 2013; Apr 15; 14:128.
   Google Scholar
• Kuleshov MV, Jones MRRouillard AD, et al. Enrichr: a comprehensive gene set enrichment analysis web server 2016 update. Nucleic Acids Res. 2016 Jul 8; 44(W1):W90-7.
   PubMed Web of Science ®Google Scholar
• van Dijk SJ, Peters TJ, Buckley M, et al. DNA methylation in blood from neonatal screening cards and the association with BMI and insulin sensitivity in early childhood. Int J Obes [Internet]. 2017;42(1): 28–35.
   Web of Science ®Google Scholar
• Maloney CA, Hay SM, Young LE, et al. A methyl-deficient diet fed to rat dams during the peri-conception period programs glucose homeostasis in adult male but not female offspring. J Nutr [Internet]. 2011 Jan 1 [cited 2018 May 8];141(1): 95–100.
   PubMed Web of Science ®Google Scholar
• Mueller BR, Bale TL. Early prenatal stress impact on coping strategies and learning performance is sex dependent. Physiol Behav [Internet]. 2007 May 16 [cited 2018 May 8];91(1): 55–65.
   PubMed Web of Science ®Google Scholar
• Bruce-Keller AJ, Fernandez-Kim S-O, Townsend RL, et al. Maternal obese-type gut microbiota differentially impact cognition, anxiety and compulsive behavior in male and female offspring in mice. Rosenfeld CS, editor. PLoS One [Internet]. 2017 Apr 25 [cited 2018 May 8];12(4): e0175577.
   PubMed Web of Science ®Google Scholar
• Soubry A, Schildkraut JM, Murtha A, et al. Paternal obesity is associated with IGF2 hypomethylation in newborns: results from a Newborn Epigenetics Study (NEST) cohort. BMC Med [Internet]. 2013 Feb 6 [cited 2018 May 8];11(1): 29.
   PubMedGoogle Scholar
• Soubry A, Murphy SK, Wang F, et al. Newborns of obese parents have altered DNA methylation patterns at imprinted genes. Int J Obes (Lond) [Internet]. 2015 Apr 25 [cited 2018 May 8];39(4): 650–657.
   PubMed Web of Science ®Google Scholar
• Ortmann B, Copeman J, Lehner PJ, et al. A critical role for tapasin in the assembly and function of multimeric MHC class I-TAP complexes. Science [Internet]. 1997 Aug 29 [cited 2018 May 8];277(5330): 1306–1309.
   PubMed Web of Science ®Google Scholar
• Tang Y, Wang J, Zhang Y, et al. Correlation between low tapasin expression and impaired CD8+ T‑cell function in patients with chronic hepatitis B. Mol Med Rep [Internet]. 2016 Oct [cited 2018 May 8];14(4): 3315–3322.
   PubMed Web of Science ®Google Scholar
• Shionoya Y, Kanaseki T, Miyamoto S, et al. Loss of tapasin in human lung and colon cancer cells and escape from tumor-associated antigen-specific CTL recognition. Oncoimmunology [Internet]. 2017 Feb 8 [cited 2018 May 8];6(2): e1274476.
   PubMed Web of Science ®Google Scholar
• Sokol L, Koelzer VH, Rau TT, et al. Loss of tapasin correlates with diminished CD8(+) T-cell immunity and prognosis in colorectal cancer. J Transl Med [Internet]. 2015 Aug 27 [cited 2018 May 8];13(1): 279.
   PubMedGoogle Scholar
• Jiang Q, Pan H, Ye D, et al. Downregulation of tapasin expression in primary human oral squamous cell carcinoma: association with clinical outcome. Tumour Biol [Internet]. 2010 Oct 8 [cited 2018 May 8];31(5): 451–459.
   PubMedGoogle Scholar
• Bukulmez H, Fife M, Tsoras M, et al. Tapasin gene polymorphism in systemic onset juvenile rheumatoid arthritis: a family-based case-control study. Arthritis Res Ther [Internet]. 2005 [cited 2018 May 8];7(2): R285–90.
   PubMed Web of Science ®Google Scholar
• Lee H-M, Sugino H, Aoki C, et al. Abnormal networks of immune response-related molecules in bone marrow cells from patients with rheumatoid arthritis as revealed by DNA microarray analysis. Arthritis Res Ther [Internet]. 2011 Jun 16 [cited 2018 May 8];13(3): R89.
   PubMed Web of Science ®Google Scholar
• Xiao X, Hao J, Wen Y, Wang W, Guo XZhang F. Genome-wide association studies and gene expression profiles of rheumatoid arthritis: an analysis. Bone Joint Res 2016 Jul;5(7):314–9.
   PubMed Web of Science ®Google Scholar
• Abarca-Heidemann K, Friederichs S, Klamp T, et al., Regulation of the expression of mouse TAP-associated glycoprotein (tapasin) by cytokines. Immunol Lett [Internet]. 2002 Oct 1 [cited 2018 May 8];83(3): 197–207. Available from: http://www.ncbi.nlm.nih.gov/pubmed/12095710
   PubMed Web of Science ®Google Scholar
• Mattos RT, Medeiros NI, Menezes CA, et al. Chronic low-grade inflammation in childhood obesity is associated with decreased IL-10 expression by monocyte subsets. Richard Y, editor. PLoS One. 2016 Dec 15 [cited 2018 May 8];11(12): e0168610.
   PubMed Web of Science ®Google Scholar
• Pachón-Peña G, Serena C, Ejarque M, et al. Obesity determines the immunophenotypic profile and functional characteristics of human mesenchymal stem cells from adipose tissue. Stem Cells Transl Med [Internet]. 2016 Apr [cited 2018 May 8];5(4): 464–475.
   PubMed Web of Science ®Google Scholar
• El Azreq M-A, Kadiri M, Boisvert M, et al. Discoidin domain receptor 1 promotes Th17 cell migration by activating the RhoA/ROCK/MAPK/ERK signaling pathway. Oncotarget [Internet]. 2016 Jul 19 [cited 2018 May 8];7(29): 44975–44990.
   PubMedGoogle Scholar
• Kadiri M, El Azreq M-A, Berrazouane S, et al. Human Th17 migration in three-dimensional collagen involves p38 MAPK. J Cell Biochem [Internet]. 2017 Sep [cited 2018 May 8];118(9): 2819–2827.
   PubMed Web of Science ®Google Scholar
• Ogino S, Nosho K, Baba Y, et al. A cohort study of STMN1 expression in colorectal cancer: body mass index and prognosis. Am J Gastroenterol. 2009;104(8):2047–2056.
   PubMed Web of Science ®Google Scholar
• Pekkala S, Munukka E, Kong L, et al. Toll-like receptor 5 in obesity: the role of gut microbiota and adipose tissue inflammation. Obesity. 2015;23(3):581–590.
   PubMed Web of Science ®Google Scholar
• Kim JY, Campbell LE, Shaibi GQ, et al. Gene expression profiling and association of circulating lactoferrin level with obesity-related phenotypes in Latino youth. Pediatr Obes [Internet]. 2015 Oct [cited 2018 May 8];10(5): 338–344.
   PubMed Web of Science ®Google Scholar
• Vijay-Kumar M, Aitken JD, Carvalho FA, et al. Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5. Science [Internet]. 2010 Apr 9 [cited 2018 May 8];328(5975): 228–231.
   PubMed Web of Science ®Google Scholar
• Rubin CI, Atweh GF. The role of stathmin in the regulation of the cell cycle. J Cell Biochem. 2004;93(2):242–250.
   PubMed Web of Science ®Google Scholar
• Soubry A, Hoyo C, Jirtle RL, et al. A paternal environmental legacy: evidence for epigenetic inheritance through the male germ line. Bioessays [Internet]. 2014 Apr [cited 2018 May 8];36(4): 359–371.
   PubMed Web of Science ®Google Scholar
• Soubry A, Guo L, Huang Z, et al. Obesity-related DNA methylation at imprinted genes in human sperm: results from the TIEGER study. Clin Epigenetics [Internet]. 2016 Dec 6 [cited 2018 May 8];8(1): 51.
   PubMedGoogle Scholar
• McCullough LE, Mendez MA, Miller EE, et al. Associations between prenatal physical activity, birth weight, and DNA methylation at genomically imprinted domains in a multiethnic newborn cohort. Epigenetics [Internet]. 2015 Jul 3 [cited 2018 May 7];10(7): 597–606.
   PubMed Web of Science ®Google Scholar
• Hoyo C, Murtha AP, Schildkraut JM, et al. Folic acid supplementation before and during pregnancy in the Newborn Epigenetics STudy (NEST). BMC Public Health [Internet]. 2011 Jan 21 [cited 2018 May 7]; 11(1): 46.
   PubMed Web of Science ®Google Scholar
• World Health Organization. Obesity: preventing and managing the global epidemic. Report of a WHO Consultation of Obesity. Geneva, 3-5 June 1997.
   Google Scholar
• Kuczmarski RJ, Ogden CL, Guo SS, Flegal KM, Mei Z, Wei R, Curtin LR, Roche AF, Johnson CL. 2000 CDC growth charts for the United States: Methods and development. National Center for Health Statistics. Vita Health Stat. 2000; 11(246)
   Google Scholar
• National High Blood Pressure Education Program Working Group on High Blood Pressure in Children and Adolescents. The fourth report on the diagnosis, evaluation, and treatment of high blood pressure in children and adolescents. Pediatrics. 2004;114(2):555–576.
   PubMed Web of Science ®Google Scholar
• Murphy SK, Adigun A, Huang Z, et al. Gender-specific methylation differences in relation to prenatal exposure to cigarette smoke. Gene [Internet]. 2012 Feb 15 [cited 2018 May 8];494(1): 36–43.
   PubMed Web of Science ®Google Scholar
• Joubert BR, Felix JF, Yousefi P, et al. DNA methylation in newborns and maternal smoking in pregnancy: genome-wide consortium meta-analysis. Am J Hum Genet. 2016;98(4):680–696.
   PubMed Web of Science ®Google Scholar
• Joubert BR, Håberg SE, Nilsen RM, et al. 450K epigenome-wide scan identifies differential DNA methylation in newborns related to maternal smoking during pregnancy. Environ Health Perspect [Internet]. 2012 Jul 31 [cited 2018 May 8];120(10): 1425–1431.
   PubMed Web of Science ®Google Scholar
• Bibikova M, Barnes B, Tsan C, et al. High density DNA methylation array with single CpG site resolution. Genomics [Internet]. 2011 Oct [cited 2018 May 8];98(4): 288–295.
   PubMed Web of Science ®Google Scholar
• 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 [Internet]. 2014 May 15 [cited 2018 May 8];30(10): 1363–1369.
   PubMed Web of Science ®Google Scholar
• Leek JT, Johnson WE, Parker HS, et al. Sva: surrogate variable analysis. R Package Version 3300. 2018.
   Google Scholar
• Tian Y, Morris TJ, Webster AP, et al. ChAMP: updated methylation analysis pipeline for Illumina BeadChips. Bioinformatics. 2017;33(24):3982–3984.
   PubMed Web of Science ®Google Scholar
• Houseman EA, Accomando WP, Koestler DC, et al. DNA methylation arrays as surrogate measures of cell mixture distribution. BMC Bioinformatics [Internet]. 2012 May 8 [cited 2018 May 8];13(1): 86.
   PubMedGoogle Scholar
• Reinius LE, Acevedo N, Joerink M, et al. Differential DNA methylation in purified human blood cells: implications for cell lineage and studies on disease susceptibility. Ting AH, editor. PLoS One. 2012 Jul 25 [cited 2018 May 8];7(7): e41361.
   PubMed Web of Science ®Google Scholar
• Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing [Internet]. J R Stat Soc Series B Stat Methodol. WileyRoyal Statistical Society; 1995 [cited 2018];57: 289–300.
   Web of Science ®Google Scholar
• 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 [Internet]. 2013 Feb [cited 2018 May 8];42(1): 111–127.
   PubMed Web of Science ®Google Scholar
• 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 [Internet]. 2013 Feb 1 [cited 2018 May 8];42(1): 97–110.
   PubMed Web of Science ®Google Scholar
• Relton CL, Gaunt T, McArdle W, et al. Data resource profile: accessible Resource for Integrated Epigenomic Studies (ARIES). Int J Epidemiol [Internet]. 2015 Aug [cited 2018 May 8];44(4): 1181–1190.
   PubMed Web of Science ®Google Scholar
• Min J, Hemani G, Davey Smith G, et al. Meffil: efficient normalisation and analysis of very large DNA methylation samples. Bioinformatics. 2018 Dec 1; 34(23):3983-3989.
   Google Scholar