Deoxyribonucleic acid methylation and gene expression of PPARGC1A in human muscle is influenced by high-fat overfeeding in a birth-weight-dependent manner

Journal of Clinical Endocrinology and Metabolism

Volumn 95, Issue 6, 2010, Pages 3048-3056

  Brøns, Charlotte ^a,b   Jacobsen, Stine ^a   Nilsson, Emma ^a   Rönn, Tina ^c   Jensen, Christine B ^a   Storgaard, Heidi ^a   Poulsen, Pernille ^a   Groop, Leif ^c   Ling, Charlotte ^c   Astrup, Arne ^b   Vaag, Allan ^a,c  

^a STENO DIABETES CENTER   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; HEAT SHOCK PROTEIN; INSULIN; PPARGC1A PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ADULT; ARTICLE; BIRTH WEIGHT; CLINICAL ARTICLE; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; CROSSOVER PROCEDURE; DNA METHYLATION; GENE; GENE EXPRESSION; HUMAN; INSULIN RESISTANCE; LIPID DIET; LOW BIRTH WEIGHT; MALE; MUSCLE BIOPSY; OXIDATIVE PHOSPHORYLATION; OXPHOS GENE; PPARGC1A GENE; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; REAL TIME POLYMERASE CHAIN REACTION; BIOSYNTHESIS; BLOOD; CALORIC INTAKE; DIET; DRUG EFFECT; FAT INTAKE; GENETICS; GLUCOSE BLOOD LEVEL; GLUCOSE CLAMP TECHNIQUE; HYPERINSULINISM; METABOLISM; NEWBORN; NON INSULIN DEPENDENT DIABETES MELLITUS; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKELETAL MUSCLE;

BIRTH WEIGHT; BLOOD GLUCOSE; CROSS-OVER STUDIES; DIABETES MELLITUS, TYPE 2; DIET; DIETARY FATS; DNA METHYLATION; ENERGY INTAKE; GENE EXPRESSION; GLUCOSE CLAMP TECHNIQUE; HEAT-SHOCK PROTEINS; HUMANS; HYPERINSULINISM; INFANT, LOW BIRTH WEIGHT; INFANT, NEWBORN; INSULIN; MALE; MUSCLE, SKELETAL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTION FACTORS; YOUNG ADULT;

EID: 77954523386     PISSN: 0021972X     EISSN: 0021972X     Source Type: Journal    
DOI: 10.1210/jc.2009-2413     Document Type: Article

References (40)

1. Harder T, Rodekamp E, Schellong K, Dudenhausen JW, Plagemann A 2007 Birth weight and subsequent risk of type 2 diabetes: a meta-analysis. Am J Epidemiol 165:849-857 (Pubitemid 46536657)
2. Hermann TS, Rask-Madsen C, Ihlemann N, Domínguez H, Jensen CB, Storgaard H, Vaag AA, Kober L, Torp-Pedersen C 2003 Normal insulin-stimulated endothelial function and impaired insulin-stimulated muscle glucose uptake in young adults with low birth weight. J Clin Endocrinol Metab 88:1252-1257 (Pubitemid 36337786)
3. Brøns C, Jensen CB, Storgaard H, Alibegovic A, Jacobsen S, Nilsson E, Astrup A, Quistorff B, Vaag A 2008 Mitochondrial function in skeletal muscle is normal and unrelated to insulin action in young men born with low birth weight. J Clin Endocrinol Metab 93:3885-3892
4. Ozanne SE, Jensen CB, Tingey KJ, Storgaard H, Madsbad S, Vaag AA 2005 Low birthweight is associated with specific changes in muscle insulin-signalling protein expression. Diabetologia 48:547-552 (Pubitemid 40487302)
5. Ozanne SE, Jensen CB, Tingey KJ, Martin-Gronert MS, Grunnet L, Brons C, Storgaard H, Vaag AA 2006 Decreased protein levels of key insulin signalling molecules in adipose tissue from young men with a low birthweight: potential link to increased risk of diabetes? Diabetologia 49:2993-2999
6. Gemma C, Sookoian S, Alvarinas J, Garcia SI, Quintana L, Kanevsky D, Gonzalez CD, Pirola CJ 2009 Maternal pregestational BMI is associated with methylation of the PPARGC1A promoter in newborns. Obesity (Silver Spring) 17:1032-1039
7. Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, Susser ES, Slagboom PE, Lumey LH 2008 Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci USA 105:17046-17049
8. Tobi EW, Lumey LH, Talens RP, Kremer D, Putter H, Stein AD, Slagboom PE, Heijmans BT 2009 DNA methylation differences after exposure to prenatal famine are common and timing- and sex-specific. Hum Mol Genet 18:4046-4053
9. Bird AP 1984 DNA methylation versus gene expression. J Embryol Exp Morphol 83(Suppl):31-40
10. Eden A, Gaudet F, Waghmare A, Jaenisch R 2003 Chromosomal instability and tumors promoted by DNA hypomethylation. Science 300:455 (Pubitemid 36444319)
11. Bird AP 1986 CpG-rich islands and the function of DNA methylation. Nature 321:209-213
12. Fraga MF, Ballestar E, Paz MF, Ropero S, Setien F, Ballestar ML, Heine-Suñer D, Cigudosa JC, Urioste M, Benitez J, Boix-Chornet M, Sanchez-Aguilera A, Ling C, Carlsson E, Poulsen P, Vaag A, Stephan Z, Spector TD, Wu YZ, Plass C, Esteller M 2005 Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci USA 102:10604-10609 (Pubitemid 41061601)
13. Rönn T, Poulsen P, Hansson O, Holmkvist J, Almgren P, Nilsson P, Tuomi T, Isomaa B, Groop L, Vaag A, Ling C 2008 Age influences DNA methylation and gene expression of COX7A1 in human skeletal muscle. Diabetologia 51:1159-1168
14. Ling C, Poulsen P, Simonsson S, Rönn T, Holmkvist J, Almgren P, Hagert P, Nilsson E, Mabey AG, Nilsson P, Vaag A, Groop L 2007 Genetic and epigenetic factors are associated with expression of respiratory chain component NDUFB6 in human skeletal muscle. J Clin Invest 117:3427-3435 (Pubitemid 350096998)
15. Christensen BC, Houseman EA, Marsit CJ, Zheng S, Wrensch MR, Wiemels JL, Nelson HH, Karagas MR, Padbury JF, Bueno R, Sugarbaker DJ, Yeh RF, Wiencke JK, Kelsey KT 2009 Aging and environmental exposures alter tissue-specific DNA methylation dependent upon CpG island context. PLoS Genet 5:e1000602
16. Mootha VK, Handschin C, Arlow D, Xie X, St Pierre J, Sihag S, Yang W, Altshuler D, Puigserver P, Patterson N, Willy PJ, Schulman IG, Heyman RA, Lander ES, Spiegelman BM 2004 Erralpha and Gabpa/b specify PGC-1α-dependent oxidative phosphorylation gene expression that is altered in diabetic muscle. Proc Natl Acad Sci USA 101:6570-6575
17. Koves TR, Li P, An J, Akimoto T, Slentz D, Ilkayeva O, Dohm GL, Yan Z, Newgard CB, Muoio DM 2005 Peroxisome proliferator-activated receptor-γ co-activator 1α-mediated metabolic remodeling of skeletal myocytes mimics exercise training and reverses lipid-induced mitochondrial inefficiency. J Biol Chem 280:33588-33598
18. Arany Z, Foo SY, Ma Y, Ruas JL, Bommi-Reddy A, Girnun G, Cooper M, Laznik D, Chinsomboon J, Rangwala SM, Baek KH, Rosenzweig A, Spiegelman BM 2008 HIF-independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC-1α. Nature 451:1008-1012
19. St-Pierre J, Drori S, Uldry M, Silvaggi JM, Rhee J, Jäger S, Handschin C, Zheng K, Lin J, Yang W, Simon DK, Bachoo R, Spiegelman BM 2006 Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 127:397-408
20. Ling C, Del Guerra S, Lupi R, Rönn T, Granhall C, Luthman H, Masiello P, Marchetti P, Groop L, Del Prato S 2008 Epigenetic regulation of PPARGC1A in human type 2 diabetic islets and effect on insulin secretion. Diabetologia 51:615-622
21. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J, Puigserver P, Carlsson E, Ridderstråle M, Laurila E, Houstis N, Daly MJ, Patterson N, Mesirov JP, Golub TR, Tamayo P, Spiegelman B, Lander ES, Hirschhorn JN, Altshuler D, Groop LC 2003 PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34:267-273
22. Patti ME, Butte AJ, Crunkhorn S, Cusi K, Berria R, Kashyap S, Miyazaki Y, Kohane I, Costello M, Saccone R, Landaker EJ, Goldfine AB, Mun E, DeFronzo R, Finlayson J, Kahn CR, Mandarino LJ 2003 Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: potential role of PGC1and NRF1. Proc Natl Acad Sci USA 100:8466-8471
23. Palsgaard J, Brøns C, Friedrichsen M, Dominguez H, Jensen M, Storgaard H, Spohr C, Torp-Pedersen C, Borup R, De Meyts P, Vaag A 2009 Gene expression in skeletal muscle biopsies from people with type 2 diabetes and relatives: differential regulation of insulin signaling pathways. PLOS One 4:e6575
24. Barrès R, Osler ME, Yan J, Rune A, Fritz T, Caidahl K, Krook A, Zierath JR 2009 Non-CpG methylation of the PGC-1α promoter through DNMT3B controls mitochondrial density. Cell Metab 10: 189-198
25. Ling C, Poulsen P, Carlsson E, Ridderstrale M, Almgren P, Wojtaszewski J, Beck-Nielsen H, Groop L, Vaag A 2004 Multiple environmental and genetic factors influence skeletal muscle PGC-1alpha and PGC-1beta gene expression in twins. J Clin Invest 114: 1518-1526
26. Bouchard L, Rabasa-Lhoret R, Faraj M, Lavoie ME, Mill J, Pérusse L, Vohl MC 2010 Differential epigenomic and transcriptomic responses in subcutaneous adipose tissue between low and high responders to caloric restriction. Am J Clin Nutr 91:309-320
27. Milagro FI, Campión J, García-Díaz DF, Goyenechea E, Paternain L, Martínez JA 2009 High fat diet-induced obesity modifies the methylation pattern of leptin promoter in rats. J Physiol Biochem 65:1-9
28. Camus AM, Béréziat JC, Shuker DE, Hietanen E, Wild CP, Montesano R, Bartsch H 1990 Effects of a high fat diet on liver DNA methylation in rats exposed to N-nitrosodimethylamine. Carcinogenesis 11:2093-2095
29. el-Bayoumy K, Prokopczyk B, Peterson LA, Desai D, Amin S, Reddy BS, Hoffmann D, Wynder E 1996 Effects of dietary fat content on the metabolism of NNK and on DNA methylation induced by NNK. Nutr Cancer 26:1-10
30. Crunkhorn S, Dearie F, Mantzoros C, Gami H, da Silva WS, Espinoza D, Faucette R, Barry K, Bianco AC, Patti ME 2007 Peroxisome proliferator activator receptor γ coactivator-1 expression is reduced in obesity: potential pathogenic role of saturated fatty acids and p38 mitogen-activated protein kinase activation. J Biol Chem 282:15439-15450
31. Sparks LM, Xie H, Koza RA, Mynatt R, Hulver MW, Bray GA, Smith SR 2005 A high-fat diet coordinately downregulates genes required for mitochondrial oxidative phosphorylation in skeletal muscle. Diabetes 54:1926-1933
32. Rasmussen EL, Malis C, Jensen CB, Jensen JE, Storgaard H, Poulsen P, Pilgaard K, Schou JH, Madsbad S, Astrup A, Vaag A 2005 Altered fat tissue distribution in young adult men who had low birth weight. Diabetes Care 28:151-153
33. Brøns C, Jensen CB, Storgaard H, Hiscock NJ, White A, Appel JS, Jacobsen S, Nilsson E, Larsen CM, Astrup A, Quistorff B, Vaag A 2009 Impact of short-term high-fat feeding on glucose and insulin metabolism in young healthy men. J Physiol 587:2387-2397
34. Vaag A, Alford F, Henriksen FL, Christopher M, Beck-Nielsen H 1995 Multiple defects of both hepatic and peripheral intracellular glucose processing contribute to the hyperglycaemia of NIDDM. Diabetologia 38:326-336
35. Li LC, Dahiya R 2002 MethPrimer: designing primers for methylation PCRs. Bioinformatics 18:1427-1431
36. Lewin J, Schmitt AO, Adorján P, Hildmann T, Piepenbrock C 2004 Quantitative DNA methylation analysis based on four-dye trace data from direct sequencing of PCR amplificates. Bioinformatics 20:3005-3012
37. Weindruch R, Sohal RS 1997 Seminars in medicine of the Beth Israel Deaconess Medical Center. Caloric intake and aging. N Engl J Med 337:986-994
38. Ramchandani S, Bhattacharya SK, Cervoni N, Szyf M 1999 DNA methylation is a reversible biological signal. Proc Natl Acad Sci USA 96:6107-6112
39. De Filippis E, Alvarez G, Berria R, Cusi K, Everman S, Meyer C, Mandarino LJ 2008 Insulin-resistant muscle is exercise resistant: evidence for reduced response of nuclear-encoded mitochondrial genes to exercise. Am J Physiol Endocrinol Metab 294:E607-E614
40. Eckhardt F, Lewin J, Cortese R, Rakyan VK, Attwood J, Burger M, Burton J, Cox TV, Davies R, Down TA, Haefliger C, Horton R, Howe K, Jackson DK, Kunde J, Koenig C, Liddle J, Niblett D, Otto T, Pettett R, Seemann S, Thompson C, West T, Rogers J, Olek A, Berlin K, Beck S 2006 DNA methylation profiling of human chromosomes 6, 20 and 22. Nat Genet 38:1378-1385