Maternal obesity and diabetes induces latent metabolic defects and widespread epigenetic changes in isogenic mice

References

• Alfaradhi MZ, Ozanne SE. Developmental programming in response to maternal overnutrition. Front Genet 2011; 2:27; http://dx.doi.org/10.3389/fgene.2011.00027; PMID: 22303323
   PubMedGoogle Scholar
• McMillen IC, Robinson JS. Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev 2005; 85:571 - 633; http://dx.doi.org/10.1152/physrev.00053.2003; PMID: 15788706
   PubMed Web of Science ®Google Scholar
• Armitage JA, Taylor PD, Poston L. Experimental models of developmental programming: consequences of exposure to an energy rich diet during development. J Physiol 2005; 565:3 - 8; http://dx.doi.org/10.1113/jphysiol.2004.079756; PMID: 15695245
   PubMed Web of Science ®Google Scholar
• Jawerbaum A, White V. Animal models in diabetes and pregnancy. Endocr Rev 2010; 31:680 - 701; http://dx.doi.org/10.1210/er.2009-0038; PMID: 20534704
   PubMed Web of Science ®Google Scholar
• Carmody JS, Wan P, Accili D, Zeltser LM, Leibel RL. Respective contributions of maternal insulin resistance and diet to metabolic and hypothalamic phenotypes of progeny. Obesity (Silver Spring) 2011; 19:492 - 9; http://dx.doi.org/10.1038/oby.2010.245; PMID: 20948526
   PubMed Web of Science ®Google Scholar
• White CL, Purpera MN, Morrison CD. Maternal obesity is necessary for programming effect of high-fat diet on offspring. Am J Physiol Regul Integr Comp Physiol 2009; 296:R1464 - 72; http://dx.doi.org/10.1152/ajpregu.91015.2008; PMID: 19244583
   PubMed Web of Science ®Google Scholar
• Gallou-Kabani C, Junien C. Nutritional epigenomics of metabolic syndrome: new perspective against the epidemic. Diabetes 2005; 54:1899 - 906; http://dx.doi.org/10.2337/diabetes.54.7.1899; PMID: 15983188
   PubMed Web of Science ®Google Scholar
• Li CCY, Cropley JE, Cowley MJ, Preiss T, Martin DIK, Suter CM. A sustained dietary change increases epigenetic variation in isogenic mice. PLoS Genet 2011; 7:e1001380; http://dx.doi.org/10.1371/journal.pgen.1001380; PMID: 21541011
   PubMedGoogle Scholar
• Bird A. DNA methylation patterns and epigenetic memory. Genes Dev 2002; 16:6 - 21; http://dx.doi.org/10.1101/gad.947102; PMID: 11782440
   PubMed Web of Science ®Google Scholar
• Feinberg AP, Irizarry RA. Evolution in health and medicine Sackler colloquium: Stochastic epigenetic variation as a driving force of development, evolutionary adaptation, and disease. Proc Natl Acad Sci U S A 2010; 107:Suppl 1 1757 - 64; http://dx.doi.org/10.1073/pnas.0906183107; PMID: 20080672
   PubMed Web of Science ®Google Scholar
• Feinberg AP, Irizarry RA, Fradin D, Aryee MJ, Murakami P, Aspelund T, et al. Personalized epigenomic signatures that are stable over time and covary with body mass index. Sci Transl Med 2010; 2:49ra67; http://dx.doi.org/10.1126/scitranslmed.3001262; PMID: 20844285
   PubMed Web of Science ®Google Scholar
• Wolff GL. Body Composition and Coat Color Correlation in Different Phenotypes of “Viable Yellow” Mice. Science 1965; 147:1145 - 7; http://dx.doi.org/10.1126/science.147.3662.1145; PMID: 14242032
   PubMed Web of Science ®Google Scholar
• Yen TT, Gill AM, Frigeri LG, Barsh GS, Wolff GL. Obesity, diabetes, and neoplasia in yellow A(vy)/- mice: ectopic expression of the agouti gene. FASEB J 1994; 8:479 - 88; PMID: 8181666
   PubMed Web of Science ®Google Scholar
• Duhl DM, Vrieling H, Miller KA, Wolff GL, Barsh GS. Neomorphic agouti mutations in obese yellow mice. Nat Genet 1994; 8:59 - 65; http://dx.doi.org/10.1038/ng0994-59; PMID: 7987393
   PubMed Web of Science ®Google Scholar
• Frigeri LG, Wolff GL, Teguh C. Differential responses of yellow Avy/A and agouti A/a (BALB/c X VY) F1 hybrid mice to the same diets: glucose tolerance, weight gain, and adipocyte cellularity. Int J Obes 1988; 12:305 - 20; PMID: 3058616
   PubMed Web of Science ®Google Scholar
• Yen TT, Allan JA, Yu PL, Acton MA, Pearson DV. Triacylglycerol contents and in vivo lipogenesis of ob/ob, db/db and Avy/a mice. Biochim Biophys Acta 1976; 441:213 - 20; http://dx.doi.org/10.1016/0005-2760(76)90164-8; PMID: 952988
   PubMed Web of Science ®Google Scholar
• Wolff GL, Roberts DW, Mountjoy KG. Physiological consequences of ectopic agouti gene expression: the yellow obese mouse syndrome. Physiol Genomics 1999; 1:151 - 63; PMID: 11015573
   PubMed Web of Science ®Google Scholar
• Kennedy AJ, Ellacott KL, King VL, Hasty AH. Mouse models of the metabolic syndrome. Dis Model Mech 2010; 3:156 - 66; http://dx.doi.org/10.1242/dmm.003467; PMID: 20212084
   PubMed Web of Science ®Google Scholar
• Samuelsson AM, Matthews PA, Argenton M, Christie MR, McConnell JM, Jansen EH, et al. Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance: a novel murine model of developmental programming. Hypertension 2008; 51:383 - 92; http://dx.doi.org/10.1161/HYPERTENSIONAHA.107.101477; PMID: 18086952
   PubMed Web of Science ®Google Scholar
• Nivoit P, Morens C, Van Assche FA, Jansen E, Poston L, Remacle C, et al. Established diet-induced obesity in female rats leads to offspring hyperphagia, adiposity and insulin resistance. Diabetologia 2009; 52:1133 - 42; http://dx.doi.org/10.1007/s00125-009-1316-9; PMID: 19288075
   PubMed Web of Science ®Google Scholar
• Taylor PD, McConnell J, Khan IY, Holemans K, Lawrence KM, Asare-Anane H, et al. Impaired glucose homeostasis and mitochondrial abnormalities in offspring of rats fed a fat-rich diet in pregnancy. Am J Physiol Regul Integr Comp Physiol 2005; 288:R134 - 9; http://dx.doi.org/10.1152/ajpregu.00355.2004; PMID: 15388492
   PubMed Web of Science ®Google Scholar
• Kleiner DE, Brunt EM, Van Natta M, Behling C, Contos MJ, Cummings OW, et al, Nonalcoholic Steatohepatitis Clinical Research Network. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 2005; 41:1313 - 21; http://dx.doi.org/10.1002/hep.20701; PMID: 15915461
   PubMed Web of Science ®Google Scholar
• Maffei M, Halaas J, Ravussin E, Pratley RE, Lee GH, Zhang Y, et al. Leptin levels in human and rodent: measurement of plasma leptin and ob RNA in obese and weight-reduced subjects. Nat Med 1995; 1:1155 - 61; http://dx.doi.org/10.1038/nm1195-1155; PMID: 7584987
   PubMed Web of Science ®Google Scholar
• Pinese M, Scarlett CJ, Kench JG, Colvin EK, Segara D, Henshall SM, et al. Messina: a novel analysis tool to identify biologically relevant molecules in disease. PLoS One 2009; 4:e5337; http://dx.doi.org/10.1371/journal.pone.0005337; PMID: 19399185
   PubMedGoogle Scholar
• Zhou Y, Rui L. Major urinary protein regulation of chemical communication and nutrient metabolism. Vitam Horm 2010; 83:151 - 63; http://dx.doi.org/10.1016/S0083-6729(10)83006-7; PMID: 20831945
   PubMed Web of Science ®Google Scholar
• Deaton AM, Bird A. CpG islands and the regulation of transcription. Genes Dev 2011; 25:1010 - 22; http://dx.doi.org/10.1101/gad.2037511; PMID: 21576262
   PubMed Web of Science ®Google Scholar
• Flanagan JM, Popendikyte V, Pozdniakovaite N, Sobolev M, Assadzadeh A, Schumacher A, et al. Intra- and interindividual epigenetic variation in human germ cells. Am J Hum Genet 2006; 79:67 - 84; http://dx.doi.org/10.1086/504729; PMID: 16773567
   PubMed Web of Science ®Google Scholar
• Mill J, Tang T, Kaminsky Z, Khare T, Yazdanpanah S, Bouchard L, et al. Epigenomic profiling reveals DNA-methylation changes associated with major psychosis. Am J Hum Genet 2008; 82:696 - 711; http://dx.doi.org/10.1016/j.ajhg.2008.01.008; PMID: 18319075
   PubMed Web of Science ®Google Scholar
• Rakyan VK, Beyan H, Down TA, Hawa MI, Maslau S, Aden D, et al. Identification of type 1 diabetes-associated DNA methylation variable positions that precede disease diagnosis. PLoS Genet 2011; 7:e1002300; http://dx.doi.org/10.1371/journal.pgen.1002300; PMID: 21980303
   PubMed Web of Science ®Google Scholar
• Einstein F, Thompson RF, Bhagat TD, Fazzari MJ, Verma A, Barzilai N, et al. Cytosine methylation dysregulation in neonates following intrauterine growth restriction. PLoS One 2010; 5:e8887; http://dx.doi.org/10.1371/journal.pone.0008887; PMID: 20126273
   PubMed Web of Science ®Google Scholar
• Srinivasan M, Katewa SD, Palaniyappan A, Pandya JD, Patel MS. Maternal high-fat diet consumption results in fetal malprogramming predisposing to the onset of metabolic syndrome-like phenotype in adulthood. Am J Physiol Endocrinol Metab 2006; 291:E792 - 9; http://dx.doi.org/10.1152/ajpendo.00078.2006; PMID: 16720630
   PubMed Web of Science ®Google Scholar
• Gluckman PD, Hanson MA, Buklijas T, Low FM, Beedle AS. Epigenetic mechanisms that underpin metabolic and cardiovascular diseases. Nat Rev Endocrinol 2009; 5:401 - 8; http://dx.doi.org/10.1038/nrendo.2009.102; PMID: 19488075
   PubMed Web of Science ®Google Scholar
• Lillycrop KA, Phillips ES, Jackson AA, Hanson MA, Burdge GC. Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr 2005; 135:1382 - 6; PMID: 15930441
   PubMed Web of Science ®Google Scholar
• Park JH, Stoffers DA, Nicholls RD, Simmons RA. Development of type 2 diabetes following intrauterine growth retardation in rats is associated with progressive epigenetic silencing of Pdx1. J Clin Invest 2008; 118:2316 - 24; PMID: 18464933
   PubMed Web of Science ®Google Scholar
• Bogdarina I, Welham S, King PJ, Burns SP, Clark AJ. Epigenetic modification of the renin-angiotensin system in the fetal programming of hypertension. Circ Res 2007; 100:520 - 6; http://dx.doi.org/10.1161/01.RES.0000258855.60637.58; PMID: 17255528
   PubMed Web of Science ®Google Scholar
• 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; http://dx.doi.org/10.1073/pnas.0806560105; PMID: 18955703
   PubMed Web of Science ®Google Scholar
• El Hajj N, Pliushch G, Schneider E, Dittrich M, Muller T, Korenkov M, et al. Metabolic programming of MEST DNA methylation by intrauterine exposure to gestational diabetes mellitus. Diabetes 2013; 62:1320 - 8; http://dx.doi.org/10.2337/db12-0289; PMID: 23209187
   PubMed Web of Science ®Google Scholar
• Gemma C, Sookoian S, Alvariñas J, García SI, Quintana L, Kanevsky D, et al. Maternal pregestational BMI is associated with methylation of the PPARGC1A promoter in newborns. Obesity (Silver Spring) 2009; 17:1032 - 9; http://dx.doi.org/10.1038/oby.2008.605; PMID: 19148128
   PubMed Web of Science ®Google Scholar
• Krakowiak P, Walker CK, Bremer AA, Baker AS, Ozonoff S, Hansen RL, et al. Maternal metabolic conditions and risk for autism and other neurodevelopmental disorders. Pediatrics 2012; 129:e1121 - 8; http://dx.doi.org/10.1542/peds.2011-2583; PMID: 22492772
   PubMed Web of Science ®Google Scholar
• Lowe A, Bråbäck L, Ekeus C, Hjern A, Forsberg B. Maternal obesity during pregnancy as a risk for early-life asthma. J Allergy Clin Immunol 2011; 128:1107 - 9, e1-2; http://dx.doi.org/10.1016/j.jaci.2011.08.025; PMID: 21958587
   PubMed Web of Science ®Google Scholar
• Carone BR, Fauquier L, Habib N, Shea JM, Hart CE, Li R, et al. Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 2010; 143:1084 - 96; http://dx.doi.org/10.1016/j.cell.2010.12.008; PMID: 21183072
   PubMed Web of Science ®Google Scholar
• Ng S-F, Lin RC, Laybutt DR, Barres R, Owens JA, Morris MJ. Chronic high-fat diet in fathers programs β-cell dysfunction in female rat offspring. Nature 2010; 467:963 - 6; http://dx.doi.org/10.1038/nature09491; PMID: 20962845
   PubMed Web of Science ®Google Scholar
• Szendroedi J, Phielix E, Roden M. The role of mitochondria in insulin resistance and type 2 diabetes mellitus. Nat Rev Endocrinol 2012; 8:92 - 103; http://dx.doi.org/10.1038/nrendo.2011.138; PMID: 21912398
   PubMed Web of Science ®Google Scholar
• Hochberg Z, Feil R, Constancia M, Fraga M, Junien C, Carel JC, et al. Child health, developmental plasticity, and epigenetic programming. Endocr Rev 2011; 32:159 - 224; http://dx.doi.org/10.1210/er.2009-0039; PMID: 20971919
   PubMed Web of Science ®Google Scholar
• Gabory A, Attig L, Junien C. Sexual dimorphism in environmental epigenetic programming. Mol Cell Endocrinol 2009; 304:8 - 18; http://dx.doi.org/10.1016/j.mce.2009.02.015; PMID: 19433243
   PubMed Web of Science ®Google Scholar
• Matthews VB, Allen TL, Risis S, Chan MH, Henstridge DC, Watson N, et al. Interleukin-6-deficient mice develop hepatic inflammation and systemic insulin resistance. Diabetologia 2010; 53:2431 - 41; http://dx.doi.org/10.1007/s00125-010-1865-y; PMID: 20697689
   PubMed Web of Science ®Google Scholar
• Guo W, Jiang L, Bhasin S, Khan SM, Swerdlow RH. DNA extraction procedures meaningfully influence qPCR-based mtDNA copy number determination. Mitochondrion 2009; 9:261 - 5; http://dx.doi.org/10.1016/j.mito.2009.03.003; PMID: 19324101
   PubMed Web of Science ®Google Scholar
• Reich M, Liefeld T, Gould J, Lerner J, Tamayo P, Mesirov JP. GenePattern 2.0. Nat Genet 2006; 38:500 - 1; http://dx.doi.org/10.1038/ng0506-500; PMID: 16642009
   PubMed Web of Science ®Google Scholar
• Smyth GK. Limma: linear models for microarray data. In: Gentleman R, Carey V, Dudoit S, Irizarry RA, Huber W, eds. Bioinformatics and computational biology solutions using r and bioconductor. New York: Springer, 2005:397-420.
   Google Scholar
• Clark SJ, Harrison J, Paul CL, Frommer M. High sensitivity mapping of methylated cytosines. Nucleic Acids Res 1994; 22:2990 - 7; http://dx.doi.org/10.1093/nar/22.15.2990; PMID: 8065911
   PubMed Web of Science ®Google Scholar