Handbook of Nutrition, Diet, and Epigenetics pp 165-185| Cite as
Reference work entry
First Online: 05 January 2019
Abstract
Peroxisome proliferator-activated receptor-γ coactivator-1α (PGC-1α) is an essential orchestrator in energy homeostasis, serving as a substantial node linking nutritional signals to metabolism. Recent studies indicate that peroxisome proliferator-activated receptor-γ coactivator-1α (PGC-1α) promoter DNA methylation is associated with various disorders and plays an important role in metabolic programming. Dietary and nutritional disequilibrium is recognized as a crucial factor which influences the process of epigenetic modification. In this article, we summarize the current knowledge on the impact of both prenatal and postnatal nutritional factors on the peroxisome proliferator-activated receptor-γ coactivator-1α (PGC-1α) DNA methylation and their relationship to metabolic disorders, and discuss the unresolved questions that warrant further research.
Keywords
Peroxisome proliferator-activated receptor-γ coactivator-1α DNA methylation Diet Nutrition Metabolic disorders Maternal BMI/high-fat diet Maternal hyperglycemia Low birth weight Type 2 diabetes Nonalcoholic fatty liver disease Obesity Fatty acids Bioactive/toxic components in foodsList of Abbreviations
References
- Barker DJ et al (1993) Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia 36:62–67CrossRefGoogle Scholar
- Barres R et al (2009) Non-CpG methylation of the PGC-1alpha promoter through DNMT3B controls mitochondrial density. Cell Metab 10:189–198. https://doi.org/10.1016/j.cmet.2009.07.011CrossRefPubMedGoogle Scholar
- Barres R et al (2012) Acute exercise remodels promoter methylation in human skeletal muscle. Cell Metab 15:405–411. https://doi.org/10.1016/j.cmet.2012.01.001CrossRefPubMedGoogle Scholar
- Barres R et al (2013) Weight loss after gastric bypass surgery in human obesity remodels promoter methylation. Cell Rep 3:1020–1027. https://doi.org/10.1016/j.celrep.2013.03.018CrossRefPubMedGoogle Scholar
- Benton CR et al (2008a) Modest PGC-1alpha overexpression in muscle in vivo is sufficient to increase insulin sensitivity and palmitate oxidation in subsarcolemmal, not intermyofibrillar, mitochondria. J Biol Chem 283:4228–4240. https://doi.org/10.1074/jbc.M704332200CrossRefPubMedGoogle Scholar
- Benton CR et al (2008b) PGC-1alpha-mediated regulation of gene expression and metabolism: implications for nutrition and exercise prescriptions. Appl Physiol Nutr Metab 33:843–862. https://doi.org/10.1139/h08-074CrossRefPubMedGoogle Scholar
- Bhuiyan AR et al (2010) Relationship of low birth weight to pulsatile arterial function in asymptomatic younger adults: the Bogalusa heart study. Am J Hypertens 23:168–173. https://doi.org/10.1038/ajh.2009.218CrossRefPubMedGoogle Scholar
- Bonen A (2009) PGC-1alpha-induced improvements in skeletal muscle metabolism and insulin sensitivity. Appl Physiol Nutr Metab 34:307–314. https://doi.org/10.1139/h09-008CrossRefPubMedGoogle Scholar
- Boque N et al (2013) Prevention of diet-induced obesity by apple polyphenols in Wistar rats through regulation of adipocyte gene expression and DNA methylation patterns. Mol Nutr Food Res 57:1473–1478. https://doi.org/10.1002/mnfr.201200686CrossRefPubMedGoogle Scholar
- Bray GA (2004) Medical consequences of obesity. J Clin Endocrinol Metab 89:2583–2589. https://doi.org/10.1210/jc.2004-0535CrossRefPubMedGoogle Scholar
- Brons C et al (2010) Deoxyribonucleic acid methylation and gene expression of PPARGC1A in human muscle is influenced by high-fat overfeeding in a birth-weight-dependent manner. J Clin Endocrinol Metab 95:3048–3056. https://doi.org/10.1210/jc.2009-2413CrossRefPubMedGoogle Scholar
- Burdge GC, Lillycrop KA (2014) Fatty acids and epigenetics. Curr Opin Clin Nutr Metab Care 17:156–161. https://doi.org/10.1097/mco.0000000000000023CrossRefPubMedGoogle Scholar
- Burgueno AL et al (2013) Maternal high-fat intake during pregnancy programs metabolic-syndrome-related phenotypes through liver mitochondrial DNA copy number and transcriptional activity of liver PPARGC1A. J Nutr Biochem 24:6–13. https://doi.org/10.1016/j.jnutbio.2011.12.008CrossRefPubMedGoogle Scholar
- Choi SW, Friso S (2010) Epigenetics: a new bridge between nutrition and health. Adv Nutr 1:8–16. https://doi.org/10.3945/an.110.1004CrossRefPubMedPubMedCentralGoogle Scholar
- Choi CS et al (2008) Paradoxical effects of increased expression of PGC-1alpha on muscle mitochondrial function and insulin-stimulated muscle glucose metabolism. Proc Natl Acad Sci U S A 105:19926–19931. https://doi.org/10.1073/pnas.0810339105CrossRefPubMedPubMedCentralGoogle Scholar
- Clarke-Harris R et al (2014) PGC1alpha promoter methylation in blood at 5-7 years predicts adiposity from 9 to 14 years (EarlyBird 50). Diabetes 63:2528–2537. https://doi.org/10.2337/db13-0671CrossRefPubMedGoogle Scholar
- Clausen TD et al (2008) High prevalence of type 2 diabetes and pre-diabetes in adult offspring of women with gestational diabetes mellitus or type 1 diabetes: the role of intrauterine hyperglycemia. Diabetes Care 31:340–346. https://doi.org/10.2337/dc07-1596CrossRefPubMedGoogle Scholar
- Clausen TD et al (2009) Overweight and the metabolic syndrome in adult offspring of women with diet-treated gestational diabetes mellitus or type 1 diabetes. J Clin Endocrinol Metab 94:2464–2470. https://doi.org/10.1210/jc.2009-0305CrossRefPubMedGoogle Scholar
- Damm P (2009) Future risk of diabetes in mother and child after gestational diabetes mellitus. Int J Gynaecol Obstet 104(Suppl 1):S25–S26. https://doi.org/10.1016/j.ijgo.2008.11.025CrossRefPubMedGoogle Scholar
- Esterbauer H et al (1999) Human peroxisome proliferator activated receptor gamma coactivator 1 (PPARGC1) gene: cDNA sequence, genomic organization, chromosomal localization, and tissue expression. Genomics 62:98–102. https://doi.org/10.1006/geno.1999.5977CrossRefPubMedGoogle Scholar
- Fernandez-Marcos PJ, Auwerx J (2011) Regulation of PGC-1alpha, a nodal regulator of mitochondrial biogenesis. Am J Clin Nutr 93:884S–8890. https://doi.org/10.3945/ajcn.110.001917CrossRefPubMedPubMedCentralGoogle Scholar
- Gemma C et al (2009) Maternal pregestational BMI is associated with methylation of the PPARGC1A promoter in newborns. Obesity (Silver Spring) 17:1032–1039. https://doi.org/10.1038/oby.2008.605CrossRefGoogle Scholar
- Gillberg L et al (2013) Does DNA methylation of PPARGC1A influence insulin action in first degree relatives of patients with type 2 diabetes? PLoS One 8:e58384. https://doi.org/10.1371/journal.pone.0058384CrossRefPubMedPubMedCentralGoogle Scholar
- Gillberg L et al (2014) PPARGC1A DNA methylation in subcutaneous adipose tissue in low birth weight subjects–impact of 5 days of high-fat overfeeding. Metabolism 63:263–271. https://doi.org/10.1016/j.metabol.2013.10.003CrossRefPubMedGoogle Scholar
- Hales CN et al (1991) Fetal and infant growth and impaired glucose tolerance at age 64. BMJ 303:1019–1022CrossRefGoogle Scholar
- Heijmans BT et al (2008) Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci U S A 105:17046–17049. https://doi.org/10.1073/pnas.0806560105CrossRefPubMedPubMedCentralGoogle Scholar
- Jacobsen SC et al (2012) Effects of short-term high-fat overfeeding on genome-wide DNA methylation in the skeletal muscle of healthy young men. Diabetologia 55:3341–3349. https://doi.org/10.1007/s00125-012-2717-8CrossRefPubMedGoogle Scholar
- Jiang Y et al (2015) BPA-induced DNA hypermethylation of the master mitochondrial gene PGC-1alpha contributes to cardiomyopathy in male rats. Toxicology 329:21–31. https://doi.org/10.1016/j.tox.2015.01.001CrossRefPubMedGoogle Scholar
- Jorgensen SW et al (2015) Metabolic response to 36 hours of fasting in young men born small vs appropriate for gestational age. Diabetologia 58:178–187. https://doi.org/10.1007/s00125-014-3406-6CrossRefPubMedGoogle Scholar
- Kelstrup L et al (2016) Gene expression and DNA methylation of PPARGC1A in muscle and adipose tissue from adult offspring of women with diabetes in pregnancy. Diabetes. https://doi.org/10.2337/db16-0227
- Laker RC et al (2013) Epigenetic origins of metabolic disease: the impact of the maternal condition to the offspring epigenome and later health consequences. Food Sci Human Wellness 2:1–11CrossRefGoogle Scholar
- Laker RC et al (2014) Exercise prevents maternal high-fat diet-induced hypermethylation of the Pgc-1alpha gene and age-dependent metabolic dysfunction in the offspring. Diabetes 63:1605–1611. https://doi.org/10.2337/db13-1614CrossRefPubMedPubMedCentralGoogle Scholar
- Lawlor DA et al (2011) 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 123:258–265. https://doi.org/10.1161/circulationaha.110.980169CrossRefPubMedPubMedCentralGoogle Scholar
- Lehnen H et al (2013) Epigenetics of gestational diabetes mellitus and offspring health: the time for action is in early stages of life. Mol Hum Reprod 19:415–422. https://doi.org/10.1093/molehr/gat020CrossRefPubMedPubMedCentralGoogle Scholar
- Liao L et al (2011) The influence of down-regulation of suppressor of cellular signaling proteins by RNAi on glucose transport of intrauterine growth retardation rats. Pediatr Res 69:497–503. https://doi.org/10.1203/PDR.0b013e31821769bdCrossRefPubMedGoogle Scholar
- Lindholm D et al (2012) PGC-1alpha: a master gene that is hard to master. Cell Mol Life Sci 69:2465–2468. https://doi.org/10.1007/s00018-012-1043-0CrossRefPubMedGoogle Scholar
- Ling C, GROOP L (2009) Epigenetics: a molecular link between environmental factors and type 2 diabetes. Diabetes 58:2718–2725. https://doi.org/10.2337/db09-1003CrossRefPubMedPubMedCentralGoogle Scholar
- Ling C et al (2004) Multiple environmental and genetic factors influence skeletal muscle PGC-1alpha and PGC-1beta gene expression in twins. J Clin Invest 114:1518–1526. https://doi.org/10.1172/jci21889CrossRefPubMedPubMedCentralGoogle Scholar
- Ling C et al (2008) Epigenetic regulation of PPARGC1A in human type 2 diabetic islets and effect on insulin secretion. Diabetologia 51:615–622. https://doi.org/10.1007/s00125-007-0916-5CrossRefPubMedPubMedCentralGoogle Scholar
- Logroscino G et al (1996) Dietary lipids and antioxidants in Parkinson's disease: a population-based, case-control study. Ann Neurol 39:89–94. https://doi.org/10.1002/ana.410390113CrossRefPubMedGoogle Scholar
- Miura S et al (2003) Overexpression of peroxisome proliferator-activated receptor gamma coactivator-1alpha down-regulates GLUT4 mRNA in skeletal muscles. J Biol Chem 278:31385–31390. https://doi.org/10.1074/jbc.M304312200CrossRefPubMedGoogle Scholar
- O'rahilly S (2009) Human genetics illuminates the paths to metabolic disease. Nature 462:307–314. https://doi.org/10.1038/nature08532CrossRefPubMedGoogle Scholar
- Petronis A (2010) Epigenetics as a unifying principle in the aetiology of complex traits and diseases. Nature 465:721–727. https://doi.org/10.1038/nature09230CrossRefPubMedGoogle Scholar
- Plagemann A et al (2010) Epigenetic malprogramming of the insulin receptor promoter due to developmental overfeeding. J Perinat Med 38:393–400. https://doi.org/10.1515/jpm.2010.051CrossRefPubMedGoogle Scholar
- Ribel-Madsen R et al (2012) Genome-wide analysis of DNA methylation differences in muscle and fat from monozygotic twins discordant for type 2 diabetes. PLoS One 7:e51302. https://doi.org/10.1371/journal.pone.0051302CrossRefPubMedPubMedCentralGoogle Scholar
- Segar EM et al (2009) Programming of growth, insulin resistance and vascular dysfunction in offspring of late gestation diabetic rats. Clin Sci (Lond) 117:129–138. https://doi.org/10.1042/cs20080550CrossRefGoogle Scholar
- Sookoian S et al (2010) Epigenetic regulation of insulin resistance in nonalcoholic fatty liver disease: impact of liver methylation of the peroxisome proliferator-activated receptor gamma coactivator 1alpha promoter. Hepatology 52:1992–2000. https://doi.org/10.1002/hep.23927CrossRefPubMedGoogle Scholar
- Su X et al (2015) PGC-1alpha promoter methylation in Parkinson's disease. PLoS One 10:e0134087. https://doi.org/10.1371/journal.pone.0134087CrossRefPubMedPubMedCentralGoogle Scholar
- Vaag AA et al (2012) The thrifty phenotype hypothesis revisited. Diabetologia 55(8):2085. https://doi.org/10.1007/s00125-012-2589-yCrossRefPubMedPubMedCentralGoogle Scholar
- Xie X et al (2015a) Placental DNA methylation of peroxisome-proliferator-activated receptor-gamma co-activator-1alpha promoter is associated with maternal gestational glucose level. Clin Sci (Lond) 129:385–394. https://doi.org/10.1042/cs20140688CrossRefGoogle Scholar
- Xie X et al (2015b) IUGR with infantile overnutrition programs an insulin-resistant phenotype through DNA methylation of peroxisome proliferator-activated receptor-gamma coactivator-1alpha in rats. Pediatr Res 77:625–632. https://doi.org/10.1038/pr.2015.32CrossRefPubMedGoogle Scholar
- Ye J et al (2012) Downregulating SOCS3 with siRNA ameliorates insulin signaling and glucose metabolism in hepatocytes of IUGR rats with catch-up growth. Pediatr Res 72:550–559. https://doi.org/10.1038/pr.2012.123CrossRefPubMedGoogle Scholar
- Zeng Y et al (2013) Maternal protein restriction in rats leads to reduced PGC-1alpha expression via altered DNA methylation in skeletal muscle. Mol Med Rep 7:306–312. https://doi.org/10.3892/mmr.2012.1134CrossRefPubMedGoogle Scholar
- Zheng RD et al (2013) Effects of SOCS 1/3 gene silencing on the expression of C/EBPalpha and PPARgamma during differentiation and maturation of rat preadipocytes. Pediatr Res 73:263–267. https://doi.org/10.1038/pr.2012.190CrossRefPubMedGoogle Scholar
Δεν υπάρχουν σχόλια:
Δημοσίευση σχολίου