DNA hypermethylation of CD3+ T cells from cord blood of infants exposed to intrauterine growth restriction

Diabetologia

Volumn 59, Issue 8, 2016, Pages 1714-1723

  Williams, Lyda ^a   Seki, Yoshinori ^a   Delahaye, Fabien ^a   Cheng, Alex ^a   Fuloria, Mamta ^a   Hughes Einstein, Francine ^a   Charron, Maureen J ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Human; Metabolic syndrome; Prediction of type 2 diabetes

Indexed keywords

BIOLOGICAL MARKER; DNA METHYLTRANSFERASE 3B; GELATINASE B; HLA DPB1 ANTIGEN; INSULIN; LOW DENSITY LIPOPROTEIN RECEPTOR; LYMPHOID ENHANCER FACTOR 1; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL; POTASSIUM CHANNEL KCNQ1; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR 7 LIKE 1; TRANSCRIPTION FACTOR NFAT; WNT PROTEIN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CD3 ANTIGEN; DNA BINDING PROTEIN; HLA DP ANTIGEN; HLA-DPB1 ANTIGEN; LEF1 PROTEIN, HUMAN; NFATC1 PROTEIN, HUMAN; PRDM16 PROTEIN, HUMAN; TCF3 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ARTICLE; BINDING SITE; BROWN ADIPOSE TISSUE; CD3+ T LYMPHOCYTE; CONTROLLED STUDY; CPG ISLAND; DIABETOGENESIS; DNA METHYLATION; ENHANCER REGION; GCK GENE; GENE; GENE LOCUS; GENOME ANALYSIS; GENOME-WIDE ASSOCIATION STUDY; GESTATIONAL AGE; HELPER CELL; HUMAN; HUMAN CELL; IMMUNOREGULATION; INSULIN METABOLISM; INTRAUTERINE GROWTH RETARDATION; LYMPHOCYTE DIFFERENTIATION; MALE; METABOLIC DISORDER; NCOR2 GENE; NEWBORN; NFATC2 GENE; NON INSULIN DEPENDENT DIABETES MELLITUS; NORMAL HUMAN; PATHOGENESIS; PRDM16 GENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PTPRN2 GENE; QUANTITATIVE STUDY; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; TISSUE DIFFERENTIATION; UMBILICAL CORD BLOOD; VALIDATION STUDY; WNT SIGNALING PATHWAY; ADULT; CELL CULTURE; FEMALE; FETUS BLOOD; GENETICS; METABOLISM; PHYSIOLOGY; PREGNANCY; T LYMPHOCYTE;

ADULT; ANTIGENS, CD3; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELLS, CULTURED; DNA METHYLATION; DNA-BINDING PROTEINS; FEMALE; FETAL BLOOD; FETAL GROWTH RETARDATION; GESTATIONAL AGE; HLA-DP BETA-CHAINS; HUMANS; LYMPHOID ENHANCER-BINDING FACTOR 1; NFATC TRANSCRIPTION FACTORS; PREGNANCY; T-LYMPHOCYTES; TRANSCRIPTION FACTORS;

EID: 84968654858     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-016-3983-7     Document Type: Article

References (50)

1. Barker DJ (1992) The fetal origins of adult hypertension. J Hypertens Suppl 10:S39–S44
2. Law CM, Shiell AW, Newsome CA et al (2002) Fetal, infant, and childhood growth and adult blood pressure: a longitudinal study from birth to 22 years of age. Circulation 105:1088–1092
3. Hales CN, Barker DJ (1992) Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35:595–601
4. Boney CM, Verma A, Tucker R, Vohr BR (2005) Metabolic syndrome in childhood: association with birth weight, maternal obesity, and gestational diabetes mellitus. Pediatrics 115:290–296
5. Williams L, Seki Y, Vuguin PM, Charron MJ (2014) Animal models of in utero exposure to a high fat diet: a review. Biochim Biophys Acta 1842:507–519
6. Martin-Gronert MS, Ozanne SE (2010) Mechanisms linking suboptimal early nutrition and increased risk of type 2 diabetes and obesity. J Nutr 140:662–666
7. Mandruzzato G, Antsaklis A, Botet F et al (2008) Intrauterine restriction (IUGR). J Perinat Med 36:277–281
8. Roseboom T, de Rooij S, Painter R (2006) The Dutch famine and its long-term consequences for adult health. Early Hum Dev 82:485–491
9. Heijmans BT, Tobi EW, Stein AD et al (2008) Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci U S A 105:17046–17049
10. Delahaye F, Wijetunga NA, Heo HJ et al (2014) Sexual dimorphism in epigenomic responses of stem cells to extreme fetal growth. Nat Commun 5:5187
11. Kanneganti TD, Dixit VD (2012) Immunological complications of obesity. Nat Immunol 13:707–712
12. Kohlgruber A, Lynch L (2015) Adipose tissue inflammation in the pathogenesis of type 2 diabetes. Curr Diab Rep 15:92
13. Richardson VR, Smith KA, Carter AM (2013) Adipose tissue inflammation: feeding the development of type 2 diabetes mellitus. Immunobiology 218:1497–1504
14. McLaughlin T, Liu LF, Lamendola C et al (2014) T cell profile in adipose tissue is associated with insulin resistance and systemic inflammation in humans. Arterioscler Thromb Vasc Biol 34:2637–2643
15. Mukhopadhyay D, Weaver L, Tobin R et al (2014) Intrauterine growth restriction and prematurity influence regulatory T cell development in newborns. J Pediatr Surg 49:727–732
16. Williams PJ, Bulmer JN, Searle RF, Innes BA, Robson SC (2009) Altered decidual leucocyte populations in the placental bed in pre-eclampsia and foetal growth restriction: a comparison with late normal pregnancy. Reproduction 138:177–184
17. Jaeckle Santos LJ, Li C, Doulias PT, Ischiropoulos H, Worthen GS, Simmons RA (2014) Neutralizing Th2 inflammation in neonatal islets prevents beta-cell failure in adult IUGR rats. Diabetes 63:1672–1684
18. Michels KB, Binder AM, Dedeurwaerder S et al (2013) Recommendations for the design and analysis of epigenome-wide association studies. Nat Methods 10:949–955
19. + T cells: differentiation and functions. Clin Dev Immunol 2012:925135
20. National cord blood program (2015) www.nationalcordbloodprogram.org, accessed 23 March 2016
21. Suzuki M, Jing Q, Lia D, Pascual M, McLellan A, Greally JM (2010) Optimized design and data analysis of tag-based cytosine methylation assays. Genome Biol 11:R36
22. Smyth GK (2004) Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article 3
23. Johnson WE, Li C, Rabinovic A (2007) Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics 8:118–127
24. Ehrich M, Nelson MR, Stanssens P et al (2005) Quantitative high-throughput analysis of DNA methylation patterns by base-specific cleavage and mass spectrometry. Proc Natl Acad Sci U S A 102:15785–15790
25. Thompson RF, Suzuki M, Lau KW, Greally JM (2009) A pipeline for the quantitative analysis of CG dinucleotide methylation using mass spectrometry. Bioinformatics 25:2164–2170
26. Xi Y, Li W (2009) BSMAP: whole genome bisulfite sequence MAPping program. BMC Bioinf 10:232
27. Hoffman MM, Buske OJ, Wang J, Weng Z, Bilmes JA, Noble WS (2012) Unsupervised pattern discovery in human chromatin structure through genomic segmentation. Nat Methods 9:473–476
28. Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11:R14
29. Subramanian A, Tamayo P, Mootha VK et al (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 102:15545–15550
30. Jaffe AE, Murakami P, Lee H et al (2012) Bump hunting to identify differentially methylated regions in epigenetic epidemiology studies. Int J Epidemiol 41:200–209
31. Seale P, Bjork B, Yang W et al (2008) PRDM16 controls a brown fat/skeletal muscle switch. Nature 454:961–967
32. Chuikov S, Levi BP, Smith ML, Morrison SJ (2010) Prdm16 promotes stem cell maintenance in multiple tissues, partly by regulating oxidative stress. Nat Cell Biol 12:999–1006
33. Mottis A, Mouchiroud L, Auwerx J (2013) Emerging roles of the corepressors NCoR1 and SMRT in homeostasis. Genes Dev 27:819–835
34. Weng NP, Araki Y, Subedi K (2012) The molecular basis of the memory T cell response: differential gene expression and its epigenetic regulation. Nat Rev Immunol 12:306–315
35. Macian F (2005) NFAT proteins: key regulators of T cell development and function. Nat Rev Immunol 5:472–484
36. Yui MA, Rothenberg EV (2014) Developmental gene networks: a triathlon on the course to T cell identity. Nat Rev Immunol 14:529–545
37. Cole MF, Johnstone SE, Newman JJ, Kagey MH, Young RA (2008) Tcf3 is an integral component of the core regulatory circuitry of embryonic stem cells. Genes Dev 22:746–755
38. Wong C, Chen C, Wu Q, Liu Y, Zheng P (2015) A critical role for the regulated Wnt-Myc pathway in naive T cell survival. J Immunol 194:158–167
39. Mamidi A, Inui M, Manfrin A et al (2012) Signaling crosstalk between TGFβ and Dishevelled/Par1b. Cell Death Differ 19:1689–1697
40. Saadat I, Higashi H, Obuse C et al (2007) Helicobacter pylori CagA targets PAR1/MARK kinase to disrupt epithelial cell polarity. Nature 447:330–333
41. Ng MC, Hester JM, Wing MR et al (2012) Genome-wide association of BMI in African Americans. Obesity (Silver Spring) 20:622–627
42. Heuberger J, Birchmeier W (2010) Interplay of cadherin-mediated cell adhesion and canonical Wnt signaling. Cold Spring Harb Perspect Biol 2:a002915
43. Gehart H, Kumpf S, Ittner A, Ricci R (2010) MAPK signalling in cellular metabolism: stress or wellness? EMBO Rep 11:834–840
44. Aguilo F, Avagyan S, Labar A et al (2011) Prdm16 is a physiologic regulator of hematopoietic stem cells. Blood 117:5057–5066
45. Feinberg AP, Irizarry RA, Fradin D et al (2010) Personalized epigenomic signatures that are stable over time and covary with body mass index. Sci Transl Med 2:49ra67
46. Zhi YF, Huang YS, Li ZH, Zhang RM, Wang SR (2007) Hypermethylation in promoter area of LDLR gene in atherosclerosis patients. Fen Zi Xi Bao Sheng Wu Xue Bao 40:419–427 [article in Chinese]
47. Martinelli N, Girelli D, Lunghi B et al (2010) Polymorphisms at LDLR locus may be associated with coronary artery disease through modulation of coagulation factor VIII activity and independently from lipid profile. Blood 116:5688–5697
48. Tang L, Ye H, Hong Q et al (2014) Elevated CpG island methylation of GCK gene predicts the risk of type 2 diabetes in Chinese males. Gene 547:329–333
49. Hillman SL, Finer S, Smart MC et al (2015) Novel DNA methylation profiles associated with key gene regulation and transcription pathways in blood and placenta of growth-restricted neonates. Epigenetics 10:50–61
50. Barres R, Osler ME, Yan J et al (2009) Non-CpG methylation of the PGC-1alpha promoter through DNMT3B controls mitochondrial density. Cell Metab 10:189–198