Skip to main content
Top
Published in: BMC Medical Genetics 1/2017

Open Access 01-12-2017 | Research article

CpG Methylation across the adipogenic PPARγ gene and its relationship with birthweight and child BMI at 9 years

Authors: Vitaly Volberg, Paul Yousefi, Karen Huen, Kim Harley, Brenda Eskenazi, Nina Holland

Published in: BMC Medical Genetics | Issue 1/2017

Login to get access

Abstract

Background

To examine methylation of the peroxisome proliferator-activated receptor γ (PPARγ) gene and its relationship with child weight status, at birth and 9 years.

Methods

We measured PPARγ methylation across 23 CpG sites using the Infinium Illumina 450 k array for children from the Center for the Health Assessment of Mothers and Children of Salinas (CHAMACOS) cohort at birth (N = 373) and 9 years (N = 245).

Results

Methylation level correlation patterns across the 23 PPARγ CpG sites were conserved between birth and 9-year ages. We found high inter-CpG correlations between sites 1–3 (methylation block 1) and also between sites 18–23 (methylation block 2) for both time points, although these patterns were less pronounced at 9 years. Additionally, sites 1–3 (north shore) had the highest intra-CpG correlations over time (r = 0.24, 0.42, and 0.3; P = 0.002, P < 0.001, P < 0.001, respectively). PPARγ methylation levels tended to increase with age, and the largest differences were observed for north shore sites (7.4%). Adjusting for sex, both site 1 and site 20 (gene body) methylation at birth was significantly and inversely associated with birth weight (β = −0.13, P = 0.033; β = −0.09, P = 0.025, respectively). Similarly, we found that site 1 and site 20 methylation at 9 years was significantly and inversely associated with 9-year BMI z-score (β = −0.41, P = 0.015; β = −0.23, P = 0.045, respectively).

Conclusion

Our results indicate that PPARγ methylation is highly organized and conserved over time, and highlight the potential functional importance of north shore sites, adding to a better understanding of regional human methylome patterns. Overall, our results suggest that PPARγ methylation may be associated with child body size.
Appendix
Available only for authorised users
Literature
1.
go back to reference Waterland RA, Michels KB. Epigenetic epidemiology of the developmental origins hypothesis. Annu Rev Nutr. 2007;27:363–88.CrossRefPubMed Waterland RA, Michels KB. Epigenetic epidemiology of the developmental origins hypothesis. Annu Rev Nutr. 2007;27:363–88.CrossRefPubMed
2.
go back to reference Lustig RH. Obesity Before Birth: Maternal and Prenatal Influences on the Offspring. Springer Sceince. 2011;30:1–25. Lustig RH. Obesity Before Birth: Maternal and Prenatal Influences on the Offspring. Springer Sceince. 2011;30:1–25.
4.
7.
go back to reference Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet. 2003;33(Suppl):245–54.CrossRefPubMed Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet. 2003;33(Suppl):245–54.CrossRefPubMed
8.
go back to reference Baccarelli A, Rienstra M, Benjamin EJ. Cardiovascular epigenetics: basic concepts and results from animal and human studies. Circ Cardiovasc Genet. 2010;3(6):567–73.CrossRefPubMedPubMedCentral Baccarelli A, Rienstra M, Benjamin EJ. Cardiovascular epigenetics: basic concepts and results from animal and human studies. Circ Cardiovasc Genet. 2010;3(6):567–73.CrossRefPubMedPubMedCentral
9.
go back to reference Irizarry RA, Ladd-Acosta C, Wen B, Wu Z, Montano C, Onyango P, Cui H, Gabo K, Rongione M, Webster M, et al. The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Nat Genet. 2009;41(2):178–86.CrossRefPubMedPubMedCentral Irizarry RA, Ladd-Acosta C, Wen B, Wu Z, Montano C, Onyango P, Cui H, Gabo K, Rongione M, Webster M, et al. The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Nat Genet. 2009;41(2):178–86.CrossRefPubMedPubMedCentral
10.
go back to reference Saxonov S, Berg P, Brutlag DL. A genome-wide analysis of CpG dinucleotides in the human genome distinguishes two distinct classes of promoters. Proc Natl Acad Sci U S A. 2006;103(5):1412–7.CrossRefPubMedPubMedCentral Saxonov S, Berg P, Brutlag DL. A genome-wide analysis of CpG dinucleotides in the human genome distinguishes two distinct classes of promoters. Proc Natl Acad Sci U S A. 2006;103(5):1412–7.CrossRefPubMedPubMedCentral
11.
go back to reference Waterland RA, Travisano M, Tahiliani KG, Rached MT, Mirza S. Methyl donor supplementation prevents transgenerational amplification of obesity. Int J Obes (Lond). 2008;32(9):1373–9.CrossRef Waterland RA, Travisano M, Tahiliani KG, Rached MT, Mirza S. Methyl donor supplementation prevents transgenerational amplification of obesity. Int J Obes (Lond). 2008;32(9):1373–9.CrossRef
12.
go back to reference Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, Susser ES, et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci U S A. 2008;105:17046–9.CrossRefPubMedPubMedCentral Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, Susser ES, et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci U S A. 2008;105:17046–9.CrossRefPubMedPubMedCentral
13.
go back to reference Tobi EW, Lumey LH, Talens RP, Kremer D, Putter H, Stein AD, et al. DNA methylation differences after exposure to prenatal famine are common and timing- and sex-specific. Hum Mol Genet. 2009;18:4046–53.CrossRefPubMedPubMedCentral Tobi EW, Lumey LH, Talens RP, Kremer D, Putter H, Stein AD, et al. DNA methylation differences after exposure to prenatal famine are common and timing- and sex-specific. Hum Mol Genet. 2009;18:4046–53.CrossRefPubMedPubMedCentral
14.
go back to reference Guénard F, Tchernof A, Deshaies Y, Cianflone K, Kral JG, Marceau P, et al. Methylation and expression of immune and inflammatory genes in the offspring of bariatric bypass surgery patients. J Obes. 2013;2013:492170.CrossRefPubMedPubMedCentral Guénard F, Tchernof A, Deshaies Y, Cianflone K, Kral JG, Marceau P, et al. Methylation and expression of immune and inflammatory genes in the offspring of bariatric bypass surgery patients. J Obes. 2013;2013:492170.CrossRefPubMedPubMedCentral
15.
go back to reference Sharp GC, Lawlor DA, Richmond RC, Fraser A, Simpkin A, Suderman M, 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):1288–304.CrossRefPubMedPubMedCentral Sharp GC, Lawlor DA, Richmond RC, Fraser A, Simpkin A, Suderman M, 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):1288–304.CrossRefPubMedPubMedCentral
16.
go back to reference Richmond RC, Sharp GC, Ward ME, Fraser A, Lyttleton, McArdle WL, Ring SM, Gaunt TR, Lawlor DA, Davey Smith G, Relton CL. DNA Methylation and BMI: Investigating Identified Methylation Sites at HIF3A in a Causal Framework. Diabetes. 2016;65(5):1231–44.CrossRefPubMedPubMedCentral Richmond RC, Sharp GC, Ward ME, Fraser A, Lyttleton, McArdle WL, Ring SM, Gaunt TR, Lawlor DA, Davey Smith G, Relton CL. DNA Methylation and BMI: Investigating Identified Methylation Sites at HIF3A in a Causal Framework. Diabetes. 2016;65(5):1231–44.CrossRefPubMedPubMedCentral
17.
go back to reference Sharp GC, Lawlor DA, Richmond RC, Fraser A, Simpkin A, Suderman M, Shihab HA, Lyttleton O, McArdle W, Ring SM, 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):1288–304.CrossRefPubMedPubMedCentral Sharp GC, Lawlor DA, Richmond RC, Fraser A, Simpkin A, Suderman M, Shihab HA, Lyttleton O, McArdle W, Ring SM, 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):1288–304.CrossRefPubMedPubMedCentral
18.
go back to reference Aslibekyan S, Demerath EW, Mendelson M, Zhi D, Guan W, Liang L, Sha J, Pankow JS, Liu C, Irvin MR, et al. Epigenome-wide study identifies novel methylation loci associated with body mass index and waist circumference. Obesity (Silver Spring, Md). 2015;23(7):1493–501.CrossRef Aslibekyan S, Demerath EW, Mendelson M, Zhi D, Guan W, Liang L, Sha J, Pankow JS, Liu C, Irvin MR, et al. Epigenome-wide study identifies novel methylation loci associated with body mass index and waist circumference. Obesity (Silver Spring, Md). 2015;23(7):1493–501.CrossRef
19.
go back to reference Tontonoz P, Spiegelman BM. Fat and beyond: the diverse biology of PPARgamma. Annu Rev Biochem. 2008;77:289–312.CrossRefPubMed Tontonoz P, Spiegelman BM. Fat and beyond: the diverse biology of PPARgamma. Annu Rev Biochem. 2008;77:289–312.CrossRefPubMed
20.
go back to reference Vidal-Puig A, Jimenez-Linan M, Lowell BB, Hamann A, Hu E, Spiegelman B, Flier JS, Moller DE. Regulation of PPAR gamma gene expression by nutrition and obesity in rodents. J Clin Invest. 1996;97(11):2553–61.CrossRefPubMedPubMedCentral Vidal-Puig A, Jimenez-Linan M, Lowell BB, Hamann A, Hu E, Spiegelman B, Flier JS, Moller DE. Regulation of PPAR gamma gene expression by nutrition and obesity in rodents. J Clin Invest. 1996;97(11):2553–61.CrossRefPubMedPubMedCentral
21.
go back to reference Maeda N, Takahashi M, Funahashi T, Kihara S, Nishizawa H, Kishida K, Nagaretani H, Matsuda M, Komuro R, Ouchi N, et al. PPARgamma ligands increase expression and plasma concentrations of adiponectin, an adipose-derived protein. Diabetes. 2001;50(9):2094–9.CrossRefPubMed Maeda N, Takahashi M, Funahashi T, Kihara S, Nishizawa H, Kishida K, Nagaretani H, Matsuda M, Komuro R, Ouchi N, et al. PPARgamma ligands increase expression and plasma concentrations of adiponectin, an adipose-derived protein. Diabetes. 2001;50(9):2094–9.CrossRefPubMed
22.
go back to reference Kubota N, Terauchi Y, Miki H, Tamemoto H, Yamauchi T, Komeda K, Satoh S, Nakano R, Ishii C, Sugiyama T, et al. PPAR gamma mediates high-fat diet-induced adipocyte hypertrophy and insulin resistance. Mol Cell. 1999;4(4):597–609.CrossRefPubMed Kubota N, Terauchi Y, Miki H, Tamemoto H, Yamauchi T, Komeda K, Satoh S, Nakano R, Ishii C, Sugiyama T, et al. PPAR gamma mediates high-fat diet-induced adipocyte hypertrophy and insulin resistance. Mol Cell. 1999;4(4):597–609.CrossRefPubMed
23.
go back to reference Larsen TM, Toubro S, Astrup A. PPARgamma agonists in the treatment of type II diabetes: is increased fatness commensurate with long-term efficacy? Int J Obes Relat Metab Disord. 2003;27(2):147–61.CrossRefPubMed Larsen TM, Toubro S, Astrup A. PPARgamma agonists in the treatment of type II diabetes: is increased fatness commensurate with long-term efficacy? Int J Obes Relat Metab Disord. 2003;27(2):147–61.CrossRefPubMed
24.
go back to reference Toruner F, Akbay E, Cakir N, Sancak B, Elbeg S, Taneri F, Akturk M, Karakoc A, Ayvaz G, Arslan M. Effects of PPARgamma and PPARalpha agonists on serum leptin levels in diet-induced obese rats. Horm Metab Res. 2004;36(4):226–30.CrossRefPubMed Toruner F, Akbay E, Cakir N, Sancak B, Elbeg S, Taneri F, Akturk M, Karakoc A, Ayvaz G, Arslan M. Effects of PPARgamma and PPARalpha agonists on serum leptin levels in diet-induced obese rats. Horm Metab Res. 2004;36(4):226–30.CrossRefPubMed
25.
go back to reference Noer A, Sorensen AL, Boquest AC, Collas P. Stable CpG hypomethylation of adipogenic promoters in freshly isolated, cultured, and differentiated mesenchymal stem cells from adipose tissue. Mol Biol Cell. 2006;17(8):3543–56.CrossRefPubMedPubMedCentral Noer A, Sorensen AL, Boquest AC, Collas P. Stable CpG hypomethylation of adipogenic promoters in freshly isolated, cultured, and differentiated mesenchymal stem cells from adipose tissue. Mol Biol Cell. 2006;17(8):3543–56.CrossRefPubMedPubMedCentral
26.
go back to reference Fujiki K, Kano F, Shiota K, Murata M. Expression of the peroxisome proliferator activated receptor gamma gene is repressed by DNA methylation in visceral adipose tissue of mouse models of diabetes. BMC Biol. 2009;7:38.CrossRefPubMedPubMedCentral Fujiki K, Kano F, Shiota K, Murata M. Expression of the peroxisome proliferator activated receptor gamma gene is repressed by DNA methylation in visceral adipose tissue of mouse models of diabetes. BMC Biol. 2009;7:38.CrossRefPubMedPubMedCentral
27.
go back to reference Dave V, Yousefi P, Huen K, Volberg V, Holland N. Relationship between expression and methylation of obesity-related genes in children. Mutagenesis. 2015;30(3):411–20.CrossRefPubMedPubMedCentral Dave V, Yousefi P, Huen K, Volberg V, Holland N. Relationship between expression and methylation of obesity-related genes in children. Mutagenesis. 2015;30(3):411–20.CrossRefPubMedPubMedCentral
28.
go back to reference Eskenazi B, Gladstone EA, Berkowitz GS, Drew CH, Faustman EM, Holland NT, Lanphear B, Meisel SJ, Perera FP, Rauh VA, et al. Methodologic and logistic issues in conducting longitudinal birth cohort studies: lessons learned from the Centers for Children's Environmental Health and Disease Prevention Research. Environ Health Perspect. 2005;113(10):1419–29.CrossRefPubMedPubMedCentral Eskenazi B, Gladstone EA, Berkowitz GS, Drew CH, Faustman EM, Holland NT, Lanphear B, Meisel SJ, Perera FP, Rauh VA, et al. Methodologic and logistic issues in conducting longitudinal birth cohort studies: lessons learned from the Centers for Children's Environmental Health and Disease Prevention Research. Environ Health Perspect. 2005;113(10):1419–29.CrossRefPubMedPubMedCentral
29.
go back to reference Eskenazi B, Harley K, Bradman A, Weltzien E, Jewell NP, Barr DB, Furlong CE, Holland NT. Association of in utero organophosphate pesticide exposure and fetal growth and length of gestation in an agricultural population. Environ Health Perspect. 2004;112(10):1116–24.CrossRefPubMedPubMedCentral Eskenazi B, Harley K, Bradman A, Weltzien E, Jewell NP, Barr DB, Furlong CE, Holland NT. Association of in utero organophosphate pesticide exposure and fetal growth and length of gestation in an agricultural population. Environ Health Perspect. 2004;112(10):1116–24.CrossRefPubMedPubMedCentral
30.
go back to reference Kuczmarski RJ, Ogden CL, Guo SS, Grummer-Strawn LM, Flegal KM, Mei Z, Wei R, Curtin LR, Roche AF, Johnson CL. 2000 CDC Growth Charts for the United States: methods and development. Vital Health Stat 11. 2002;(246):1–190. Data from the national health survey. Kuczmarski RJ, Ogden CL, Guo SS, Grummer-Strawn LM, Flegal KM, Mei Z, Wei R, Curtin LR, Roche AF, Johnson CL. 2000 CDC Growth Charts for the United States: methods and development. Vital Health Stat 11. 2002;(246):1–190. Data from the national health survey.
31.
go back to reference Stettler N, Zemel BS, Kumanyika S, Stallings VA. Infant weight gain and childhood overweight status in a multicenter, cohort study. Pediatrics. 2002;109(2):194–9.CrossRefPubMed Stettler N, Zemel BS, Kumanyika S, Stallings VA. Infant weight gain and childhood overweight status in a multicenter, cohort study. Pediatrics. 2002;109(2):194–9.CrossRefPubMed
32.
go back to reference Yousefi P, Huen K, Aguilar Schall R, Decker A, Elboudwarej E, Quach H, Barcellos L, Holland N. Considerations for normalization of DNA methylation data by Illumina 450 k BeadChip assay in population studies. Epigenetics. 2013;8(11):1141–52.CrossRefPubMed Yousefi P, Huen K, Aguilar Schall R, Decker A, Elboudwarej E, Quach H, Barcellos L, Holland N. Considerations for normalization of DNA methylation data by Illumina 450 k BeadChip assay in population studies. Epigenetics. 2013;8(11):1141–52.CrossRefPubMed
33.
go back to reference Teschendorff AE, Menon U, Gentry-Maharaj A, Ramus SJ, Weisenberger DJ, Shen H, Campan M, Noushmehr H, Bell CG, Maxwell AP, et al. Age-dependent DNA methylation of genes that are suppressed in stem cells is a hallmark of cancer. Genome Res. 2010;20(4):440–6.CrossRefPubMedPubMedCentral Teschendorff AE, Menon U, Gentry-Maharaj A, Ramus SJ, Weisenberger DJ, Shen H, Campan M, Noushmehr H, Bell CG, Maxwell AP, et al. Age-dependent DNA methylation of genes that are suppressed in stem cells is a hallmark of cancer. Genome Res. 2010;20(4):440–6.CrossRefPubMedPubMedCentral
34.
go back to reference Yousefi P, Huen K, Quach H, Motwani G, Hubbard A, Eskenazi B, Holland N. Estimation of blood cellular heterogeneity in newborns and children for epigenome-wide association studies. Environ Mol Mutagen. 2015;56(9):751–8.CrossRefPubMedPubMedCentral Yousefi P, Huen K, Quach H, Motwani G, Hubbard A, Eskenazi B, Holland N. Estimation of blood cellular heterogeneity in newborns and children for epigenome-wide association studies. Environ Mol Mutagen. 2015;56(9):751–8.CrossRefPubMedPubMedCentral
35.
go back to reference Houwen B. The differential cell count. Lab Hematol. 2001;7:89–100. Houwen B. The differential cell count. Lab Hematol. 2001;7:89–100.
36.
go back to reference Aryee MJ, Jaffe AE, Corrada-Bravo H, Ladd-Acosta C, Feinberg AP, Hansen KD, Irizarry RA. Minfi: a flexible and comprehensive Bioconductor package for the analysis of Infinium DNA methylation microarrays. Bioinformatics (Oxford, England). 2014;30(10):1363–9.CrossRef Aryee MJ, Jaffe AE, Corrada-Bravo H, Ladd-Acosta C, Feinberg AP, Hansen KD, Irizarry RA. Minfi: a flexible and comprehensive Bioconductor package for the analysis of Infinium DNA methylation microarrays. Bioinformatics (Oxford, England). 2014;30(10):1363–9.CrossRef
37.
go back to reference Dallman P. Blood and blood-forming tissues. In: Rudolph Q, editor. Paediatrics. New York: Appleton; 1977. p. 1109–12. Dallman P. Blood and blood-forming tissues. In: Rudolph Q, editor. Paediatrics. New York: Appleton; 1977. p. 1109–12.
38.
go back to reference Nathan D, Oski F, Orkin S. Nathan and Oski’s Hematology of Infancy and Childhood, vol. 2. 6th ed. Philadelphia: Saunders; 2003. Nathan D, Oski F, Orkin S. Nathan and Oski’s Hematology of Infancy and Childhood, vol. 2. 6th ed. Philadelphia: Saunders; 2003.
39.
go back to reference Bakulski KM, Feinberg JI, Andrews SV, et al. DNA methylation of cord blood cell types: Applications for mixed cell birth studies. Epigenetics. 2016;11:354–62.CrossRefPubMed Bakulski KM, Feinberg JI, Andrews SV, et al. DNA methylation of cord blood cell types: Applications for mixed cell birth studies. Epigenetics. 2016;11:354–62.CrossRefPubMed
41.
go back to reference de Goede OM, Razzaghian HR, Price EM, et al. Nucleated red blood cells impact DNA methylation and expression analyses of cord blood hematopoietic cells. Clin Epigenetics. 2015;7(1):95.CrossRefPubMedPubMedCentral de Goede OM, Razzaghian HR, Price EM, et al. Nucleated red blood cells impact DNA methylation and expression analyses of cord blood hematopoietic cells. Clin Epigenetics. 2015;7(1):95.CrossRefPubMedPubMedCentral
43.
go back to reference Du P, Zhang X, Huang CC, Jafari N, Kibbe WA, Hou L, Lin SM. Comparison of Beta-value and M-value methods for quantifying methylation levels by microarray analysis. BMC Bioinformatics. 2010;11:587.CrossRefPubMedPubMedCentral Du P, Zhang X, Huang CC, Jafari N, Kibbe WA, Hou L, Lin SM. Comparison of Beta-value and M-value methods for quantifying methylation levels by microarray analysis. BMC Bioinformatics. 2010;11:587.CrossRefPubMedPubMedCentral
44.
go back to reference Shoemaker R, Deng J, Wang W, Zhang K. Allele-specific methylation is prevalent and is contributed by CpG-SNPs in the human genome. Genome Res. 2010;20(7):883–9.CrossRefPubMedPubMedCentral Shoemaker R, Deng J, Wang W, Zhang K. Allele-specific methylation is prevalent and is contributed by CpG-SNPs in the human genome. Genome Res. 2010;20(7):883–9.CrossRefPubMedPubMedCentral
45.
go back to reference Liu Y, Li X, Aryee MJ, Ekstrom TJ, Padyukov L, Klareskog L, Vandiver A, Moore AZ, Tanaka T, Ferrucci L, et al. GeMes, clusters of DNA methylation under genetic control, can inform genetic and epigenetic analysis of disease. Am J Hum Genet. 2014;94(4):485–95.CrossRefPubMedPubMedCentral Liu Y, Li X, Aryee MJ, Ekstrom TJ, Padyukov L, Klareskog L, Vandiver A, Moore AZ, Tanaka T, Ferrucci L, et al. GeMes, clusters of DNA methylation under genetic control, can inform genetic and epigenetic analysis of disease. Am J Hum Genet. 2014;94(4):485–95.CrossRefPubMedPubMedCentral
46.
go back to reference Volberg V, Harley KG, Aguilar RS, Rosas LG, Huen K, Yousefi P, Dave V, Phan N, Lustig RH, Eskenazi B, et al. Associations between perinatal factors and adiponectin and leptin in 9-year-old Mexican-American children. Pediatr Obes. 2013;8(6):454–63.CrossRefPubMed Volberg V, Harley KG, Aguilar RS, Rosas LG, Huen K, Yousefi P, Dave V, Phan N, Lustig RH, Eskenazi B, et al. Associations between perinatal factors and adiponectin and leptin in 9-year-old Mexican-American children. Pediatr Obes. 2013;8(6):454–63.CrossRefPubMed
47.
go back to reference Dulloo AG, Jacquet J, Seydoux J, Montani JP. The thrifty 'catch-up fat' phenotype: its impact on insulin sensitivity during growth trajectories to obesity and metabolic syndrome. Int J Obes (Lond). 2006;30 Suppl 4:S23–35.CrossRef Dulloo AG, Jacquet J, Seydoux J, Montani JP. The thrifty 'catch-up fat' phenotype: its impact on insulin sensitivity during growth trajectories to obesity and metabolic syndrome. Int J Obes (Lond). 2006;30 Suppl 4:S23–35.CrossRef
48.
go back to reference Ong KK, Preece MA, Emmett PM, Ahmed ML, Dunger DB. Size at birth and early childhood growth in relation to maternal smoking, parity and infant breast-feeding: longitudinal birth cohort study and analysis. Pediatr Res. 2002;52(6):863–7.CrossRefPubMed Ong KK, Preece MA, Emmett PM, Ahmed ML, Dunger DB. Size at birth and early childhood growth in relation to maternal smoking, parity and infant breast-feeding: longitudinal birth cohort study and analysis. Pediatr Res. 2002;52(6):863–7.CrossRefPubMed
49.
go back to reference Whitaker RC. Predicting preschooler obesity at birth: the role of maternal obesity in early pregnancy. Pediatrics. 2004;114(1):e29–36.CrossRefPubMed Whitaker RC. Predicting preschooler obesity at birth: the role of maternal obesity in early pregnancy. Pediatrics. 2004;114(1):e29–36.CrossRefPubMed
50.
go back to reference Hediger ML, Overpeck MD, McGlynn A, Kuczmarski RJ, Maurer KR, Davis WW. Growth and fatness at three to six years of age of children born small- or large-for-gestational age. Pediatrics. 1999;104(3):e33.CrossRefPubMed Hediger ML, Overpeck MD, McGlynn A, Kuczmarski RJ, Maurer KR, Davis WW. Growth and fatness at three to six years of age of children born small- or large-for-gestational age. Pediatrics. 1999;104(3):e33.CrossRefPubMed
51.
go back to reference Sofer T, Schifano ED, Hoppin JA, Hou L, Baccarelli AA. A-clustering: a novel method for the detection of co-regulated methylation regions, and regions associated with exposure. Bioinformatics (Oxford, England). 2013;29(22):2884–91.CrossRef Sofer T, Schifano ED, Hoppin JA, Hou L, Baccarelli AA. A-clustering: a novel method for the detection of co-regulated methylation regions, and regions associated with exposure. Bioinformatics (Oxford, England). 2013;29(22):2884–91.CrossRef
53.
go back to reference Huen K, Yousefi P, Street K, Eskenazi B, Holland N. PON1 as a model for integration of genetic, epigenetic, and expression data on candidate susceptibility genes. Envrionmental Epigenetics. 2015;1(1):1–11. Huen K, Yousefi P, Street K, Eskenazi B, Holland N. PON1 as a model for integration of genetic, epigenetic, and expression data on candidate susceptibility genes. Envrionmental Epigenetics. 2015;1(1):1–11.
54.
go back to reference Doi A, Park IH, Wen B, Murakami P, Aryee MJ, Irizarry R, Herb B, Ladd-Acosta C, Rho J, Loewer S, et al. Differential methylation of tissue- and cancer-specific CpG island shores distinguishes human induced pluripotent stem cells, embryonic stem cells and fibroblasts. Nat Genet. 2009;41(12):1350–3.CrossRefPubMedPubMedCentral Doi A, Park IH, Wen B, Murakami P, Aryee MJ, Irizarry R, Herb B, Ladd-Acosta C, Rho J, Loewer S, et al. Differential methylation of tissue- and cancer-specific CpG island shores distinguishes human induced pluripotent stem cells, embryonic stem cells and fibroblasts. Nat Genet. 2009;41(12):1350–3.CrossRefPubMedPubMedCentral
55.
go back to reference Edgar R, Tan PP, Portales-Casamar E, Pavlidis P. Meta-analysis of human methylomes reveals stably methylated sequences surrounding CpG islands associated with high gene expression. Epigenetics Chromatin. 2014;7(1):28.CrossRefPubMedPubMedCentral Edgar R, Tan PP, Portales-Casamar E, Pavlidis P. Meta-analysis of human methylomes reveals stably methylated sequences surrounding CpG islands associated with high gene expression. Epigenetics Chromatin. 2014;7(1):28.CrossRefPubMedPubMedCentral
56.
go back to reference Talens RP, Boomsma DI, Tobi EW, Kremer D, Jukema JW, Willemsen G, Putter H, Slagboom PE, Heijmans BT. Variation, patterns, and temporal stability of DNA methylation: considerations for epigenetic epidemiology. FASEB J. 2010;24(9):3135–44.CrossRefPubMed Talens RP, Boomsma DI, Tobi EW, Kremer D, Jukema JW, Willemsen G, Putter H, Slagboom PE, Heijmans BT. Variation, patterns, and temporal stability of DNA methylation: considerations for epigenetic epidemiology. FASEB J. 2010;24(9):3135–44.CrossRefPubMed
57.
go back to reference Fraga MF, Ballestar E, Paz MF, Ropero S, Setien F, Ballestar ML, Heine-Suner D, Cigudosa JC, Urioste M, Benitez J, et al. Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci U S A. 2005;102(30):10604–9.CrossRefPubMedPubMedCentral Fraga MF, Ballestar E, Paz MF, Ropero S, Setien F, Ballestar ML, Heine-Suner D, Cigudosa JC, Urioste M, Benitez J, et al. Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci U S A. 2005;102(30):10604–9.CrossRefPubMedPubMedCentral
58.
go back to reference Wong CC, Caspi A, Williams B, Craig IW, Houts R, Ambler A, Moffitt TE, Mill J. A longitudinal study of epigenetic variation in twins. Epigenetics. 2010;5(6):516–26.CrossRefPubMedPubMedCentral Wong CC, Caspi A, Williams B, Craig IW, Houts R, Ambler A, Moffitt TE, Mill J. A longitudinal study of epigenetic variation in twins. Epigenetics. 2010;5(6):516–26.CrossRefPubMedPubMedCentral
59.
go back to reference Bjornsson HT, Sigurdsson MI, Fallin MD, Irizarry RA, Aspelund T, Cui H, Yu W, Rongione MA, Ekstrom TJ, Harris TB, et al. Intra-individual change over time in DNA methylation with familial clustering. JAMA. 2008;299(24):2877–83.CrossRefPubMedPubMedCentral Bjornsson HT, Sigurdsson MI, Fallin MD, Irizarry RA, Aspelund T, Cui H, Yu W, Rongione MA, Ekstrom TJ, Harris TB, et al. Intra-individual change over time in DNA methylation with familial clustering. JAMA. 2008;299(24):2877–83.CrossRefPubMedPubMedCentral
60.
go back to reference Bollati V, Schwartz J, Wright R, Litonjua A, Tarantini L, Suh H, Sparrow D, Vokonas P, Baccarelli A. Decline in genomic DNA methylation through aging in a cohort of elderly subjects. Mech Ageing Dev. 2009;130(4):234–9.CrossRefPubMed Bollati V, Schwartz J, Wright R, Litonjua A, Tarantini L, Suh H, Sparrow D, Vokonas P, Baccarelli A. Decline in genomic DNA methylation through aging in a cohort of elderly subjects. Mech Ageing Dev. 2009;130(4):234–9.CrossRefPubMed
61.
go back to reference Maegawa S, Hinkal G, Kim HS, Shen L, Zhang L, Zhang J, Zhang N, Liang S, Donehower LA, Issa JP. Widespread and tissue specific age-related DNA methylation changes in mice. Genome Res. 2010;20(3):332–40.CrossRefPubMedPubMedCentral Maegawa S, Hinkal G, Kim HS, Shen L, Zhang L, Zhang J, Zhang N, Liang S, Donehower LA, Issa JP. Widespread and tissue specific age-related DNA methylation changes in mice. Genome Res. 2010;20(3):332–40.CrossRefPubMedPubMedCentral
62.
go back to reference Hall E, Volkov P, Dayeh T, Esguerra JL, Salo S, Eliasson L, Ronn T, Bacos K, Ling C. Sex differences in the genome-wide DNA methylation pattern and impact on gene expression, microRNA levels and insulin secretion in human pancreatic islets. Genome Biol. 2014;15(12):522.CrossRefPubMedPubMedCentral Hall E, Volkov P, Dayeh T, Esguerra JL, Salo S, Eliasson L, Ronn T, Bacos K, Ling C. Sex differences in the genome-wide DNA methylation pattern and impact on gene expression, microRNA levels and insulin secretion in human pancreatic islets. Genome Biol. 2014;15(12):522.CrossRefPubMedPubMedCentral
63.
go back to reference Drogan D, Boeing H, Janke J, Schmitt B, Zhou Y, Walter J, Pischon T, Tierling S. Regional distribution of body fat in relation to DNA methylation within the LPL, ADIPOQ and PPARgamma promoters in subcutaneous adipose tissue. Nutr Diabetes. 2015;5:e168.CrossRefPubMedPubMedCentral Drogan D, Boeing H, Janke J, Schmitt B, Zhou Y, Walter J, Pischon T, Tierling S. Regional distribution of body fat in relation to DNA methylation within the LPL, ADIPOQ and PPARgamma promoters in subcutaneous adipose tissue. Nutr Diabetes. 2015;5:e168.CrossRefPubMedPubMedCentral
64.
go back to reference Yan Z, Zhang H, Maher C, Arteaga-Solis E, Champagne FA, Wu L, McDonald JD, Yan B, Schwartz GJ, Miller RL. Prenatal polycyclic aromatic hydrocarbon, adiposity, peroxisome proliferator-activated receptor (PPAR) gamma methylation in offspring, grand-offspring mice. PLoS One. 2014;9(10):e110706.CrossRefPubMedPubMedCentral Yan Z, Zhang H, Maher C, Arteaga-Solis E, Champagne FA, Wu L, McDonald JD, Yan B, Schwartz GJ, Miller RL. Prenatal polycyclic aromatic hydrocarbon, adiposity, peroxisome proliferator-activated receptor (PPAR) gamma methylation in offspring, grand-offspring mice. PLoS One. 2014;9(10):e110706.CrossRefPubMedPubMedCentral
65.
go back to reference Nilsson E, Jansson PA, Perfilyev A, Volkov P, Pedersen M, Svensson MK, Poulsen P, Ribel-Madsen R, Pedersen NL, Almgren P, et al. Altered DNA methylation and differential expression of genes influencing metabolism and inflammation in adipose tissue from subjects with type 2 diabetes. Diabetes. 2014;63(9):2962–76.CrossRefPubMed Nilsson E, Jansson PA, Perfilyev A, Volkov P, Pedersen M, Svensson MK, Poulsen P, Ribel-Madsen R, Pedersen NL, Almgren P, et al. Altered DNA methylation and differential expression of genes influencing metabolism and inflammation in adipose tissue from subjects with type 2 diabetes. Diabetes. 2014;63(9):2962–76.CrossRefPubMed
66.
go back to reference Mohr S, Liew CC. The peripheral-blood transcriptome: new insights into disease and risk assessment. Trends Mol Med. 2007;13(10):422–32.CrossRefPubMed Mohr S, Liew CC. The peripheral-blood transcriptome: new insights into disease and risk assessment. Trends Mol Med. 2007;13(10):422–32.CrossRefPubMed
67.
go back to reference Liew CC, Ma J, Tang HC, Zheng R, Dempsey AA. The peripheral blood transcriptome dynamically reflects system wide biology: a potential diagnostic tool. J Lab Clin Med. 2006;147(3):126–32.CrossRefPubMed Liew CC, Ma J, Tang HC, Zheng R, Dempsey AA. The peripheral blood transcriptome dynamically reflects system wide biology: a potential diagnostic tool. J Lab Clin Med. 2006;147(3):126–32.CrossRefPubMed
69.
go back to reference Chadwick LH, Sawa A, Yang IV, et al. New insights and updated guidelines for epigenome-wide association studies. Neuroepigenetics. 2015;1:14–9.CrossRef Chadwick LH, Sawa A, Yang IV, et al. New insights and updated guidelines for epigenome-wide association studies. Neuroepigenetics. 2015;1:14–9.CrossRef
70.
go back to reference Dick KJ, Nelson CP, Tsaprouni L, et al. DNA methylation and body-mass index: a genome-wide analysis. Lancet. 2014;383:1990–8.CrossRefPubMed Dick KJ, Nelson CP, Tsaprouni L, et al. DNA methylation and body-mass index: a genome-wide analysis. Lancet. 2014;383:1990–8.CrossRefPubMed
71.
go back to reference Ghosh S, Dent R, Harper ME, Gorman SA, Stuart JS, McPherson R. Gene expression profiling in whole blood identifies distinct biological pathways associated with obesity. BMC Med Genomics. 2010;3:56.CrossRefPubMedPubMedCentral Ghosh S, Dent R, Harper ME, Gorman SA, Stuart JS, McPherson R. Gene expression profiling in whole blood identifies distinct biological pathways associated with obesity. BMC Med Genomics. 2010;3:56.CrossRefPubMedPubMedCentral
72.
go back to reference Charriere G, Cousin B, Arnaud E, Andre M, Bacou F, Penicaud L, Casteilla L. Preadipocyte conversion to macrophage. Evidence of plasticity. J Biol Chem. 2003;278(11):9850–5.CrossRefPubMed Charriere G, Cousin B, Arnaud E, Andre M, Bacou F, Penicaud L, Casteilla L. Preadipocyte conversion to macrophage. Evidence of plasticity. J Biol Chem. 2003;278(11):9850–5.CrossRefPubMed
Metadata
Title
CpG Methylation across the adipogenic PPARγ gene and its relationship with birthweight and child BMI at 9 years
Authors
Vitaly Volberg
Paul Yousefi
Karen Huen
Kim Harley
Brenda Eskenazi
Nina Holland
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Medical Genetics / Issue 1/2017
Electronic ISSN: 1471-2350
DOI
https://doi.org/10.1186/s12881-016-0365-4

Other articles of this Issue 1/2017

BMC Medical Genetics 1/2017 Go to the issue