Impact of an exercise intervention on DNA methylation in skeletal muscle from first-degree relatives of patients with type 2 diabetes

Diabetes

Volumn 61, Issue 12, 2012, Pages 3322-3332

  Nitert, Marloes Dekker ^a   Dayeh, Tasnim ^a   Volkov, Peter ^a   Elgzyri, Targ ^a   Hall, Elin ^a   Nilsson, Emma ^a   Yang, Beatrice T ^a   Lang, Stefan ^a   Parikh, Hemang ^b   Wessman, Ylva ^a   Weishaupt, Holger ^c   Attema, Joanne ^c   Abels, Mia ^a   Wierup, Nils ^a   Almgren, Peter ^a   Jansson, Per Anders ^d   Rönn, Tina ^a   Hansson, Ola ^a   Eriksson, Karl Fredrik ^a   Groop, Leif ^a   Ling, Charlotte ^a   more..

^a LUND UNIVERSITY   (Sweden)

^b NATIONAL CANCER INSTITUTE   (United States)

^c LUND UNIVERSITY   (Sweden)

^d UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPONECTIN; ADIPOR1 PROTEIN; BDKRB2 PROTEIN; CALCIUM; FOLIC ACID; GLUCOSE; HEMOGLOBIN A1C; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; HOMOCYSTEINE; HOXC6 PROTEIN; INSULIN; KETONE BODY; LEPTIN; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MEF2A PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MYO18B PROTEIN; NDUFC2 PROTEIN; PRKAB1 PROTEIN; PROTEIN; RETINOL; SEX HORMONE BINDING GLOBULIN; SONIC HEDGEHOG PROTEIN; TESTOSTERONE; THADA PROTEIN; TRANSCRIPTION FACTOR RUNX1; TRIACYLGLYCEROL; TRIB1 PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ADULT; ARTICLE; BIRTH WEIGHT; BODY FAT; BODY MASS; BODY WEIGHT; CALCIUM SIGNALING; CHOLESTEROL BLOOD LEVEL; CLINICAL ARTICLE; CONTROLLED STUDY; DIABETIC PATIENT; DIASTOLIC BLOOD PRESSURE; DIET RESTRICTION; DNA DETERMINATION; DNA METHYLATION; EPIGENETICS; EXERCISE; FAMILY HISTORY; FOLIC ACID BLOOD LEVEL; GENE EXPRESSION; GENE REPRESSION; GENETIC PREDISPOSITION; GLUCOSE BLOOD LEVEL; GLUTATHIONE METABOLISM; GLYCOSAMINOGLYCAN METABOLISM; HEMOGLOBIN BLOOD LEVEL; HORMONE BLOOD LEVEL; HUMAN; INSULIN BLOOD LEVEL; MALE; MELANOGENESIS; MONOZYGOTIC TWINS; NON INSULIN DEPENDENT DIABETES MELLITUS; OOCYTE MATURATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BLOOD LEVEL; PROTEIN DEGRADATION; PULSE RATE; RELATIVE; REPORTER GENE; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SYSTOLIC BLOOD PRESSURE; TESTOSTERONE BLOOD LEVEL; TRIACYLGLYCEROL BLOOD LEVEL; TWIN DISCORDANCE; WAIST CIRCUMFERENCE; WAIST HIP RATIO;

ADULT; CORE BINDING FACTOR ALPHA 2 SUBUNIT; DIABETES MELLITUS, TYPE 2; DNA METHYLATION; EXERCISE; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MADS DOMAIN PROTEINS; MALE; MUSCLE, SKELETAL; MYOGENIC REGULATORY FACTORS; NEOPLASM PROTEINS; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, ADIPONECTIN;

EID: 84870319843     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db11-1653     Document Type: Article

References (50)

1. McCarthy MI. Genomics, type 2 diabetes, and obesity. N Engl J Med 2010;363:2339-2350
2. Lyssenko V, Almgren P, Anevski D, et al.; Botnia study group. Predictors of and longitudinal changes in insulin sensitivity and secretion preceding onset of type 2 diabetes. Diabetes 2005;54:166-174 (Pubitemid 40105109)
3. Hu FB, Manson JE, Stampfer MJ, et al. Diet, lifestyle, and the risk of type 2 diabetes mellitus in women. N Engl J Med 2001;345:790-797
4. Tuomilehto J, Lindström J, Eriksson JG, et al.; Finnish Diabetes Prevention Study Group. Prevention of type 2 diabetes mellitus by changes in lifestyle among subjects with impaired glucose tolerance. N Engl J Med 2001;344:1343-1350 (Pubitemid 32378388)
5. Knowler WC, Barrett-Connor E, Fowler SE, et al.; Diabetes Prevention Program Research Group. Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin. N Engl J Med 2002;346:393-403 (Pubitemid 34437694)
6. Ling C, Groop L. Epigenetics: a molecular link between environmental factors and type 2 diabetes. Diabetes 2009;58:2718-2725
7. Brøns C, Jacobsen S, Nilsson E, et al. Deoxyribonucleic acid methylation and gene expression of PPARGC1A in human muscle is influenced by highfat overfeeding in a birth-weight-dependent manner. J Clin Endocrinol Metab 2010;95:3048-3056
8. Bouchard L, Rabasa-Lhoret R, Faraj M, et al. Differential epigenomic and transcriptomic responses in subcutaneous adipose tissue between low and high responders to caloric restriction. Am J Clin Nutr 2010;91:309-320
9. 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;135:1382-1386 (Pubitemid 40799599)
10. Plagemann A, Harder T, Brunn M, et al. Hypothalamic proopiomelanocortin promoter methylation becomes altered by early overfeeding: an epigenetic model of obesity and the metabolic syndrome. J Physiol 2009;587:4963-4976
11. Milagro FI, Campión J, Cordero P, et al. A dual epigenomic approach for the search of obesity biomarkers: DNA methylation in relation to dietinduced weight loss. FASEB J 2011;25:1378-1389
12. Köbberling J, Tillil H. Genetic and nutritional factors in the etiology and pathogenesis of diabetes mellitus. World Rev Nutr Diet 1990;63:102-115
13. Isomaa B, Forsén B, Lahti K, et al. A family history of diabetes is associated with reduced physical fitness in the Prevalence, Prediction and Prevention of Diabetes (PPP)-Botnia study. Diabetologia 2010;53:1709-1713
14. Kacerovsky-Bielesz G, Chmelik M, Ling C, et al. Short-term exercise training does not stimulate skeletal muscle ATP synthesis in relatives of humans with type 2 diabetes. Diabetes 2009;58:1333-1341
15. Song JS, Johnson WE, Zhu X, et al. Model-based analysis of two-color arrays (MA2C). Genome Biol 2007;8:R178
16. R Development Core Team. R: A Language and Environment for Statistical Comp. Vienna, Austria, R Foundation for Statistical Computing, 2011
17. Irizarry RA, Hobbs B, Collin F, et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003;4:249-264
18. Klug M, Rehli M. Functional analysis of promoter CpG methylation using a CpG-free luciferase reporter vector. Epigenetics 2006;1:127-130
19. Wierup N, Kuhar M, Nilsson BO, Mulder H, Ekblad E, Sundler F. Cocaineand amphetamine-regulated transcript (CART) is expressed in several islet cell types during rat development. J Histochem Cytochem 2004;52:169-177 (Pubitemid 38146575)
20. Koopman R, Schaart G, Hesselink MK. Optimisation of oil red O staining permits combination with immunofluorescence and automated quantification of lipids. Histochem Cell Biol 2001;116:63-68 (Pubitemid 32695819)
21. Reik W. Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 2007;447:425-432 (Pubitemid 46816749)
22. Lyssenko V, Jonsson A, Almgren P, et al. Clinical risk factors, DNA variants, and the development of type 2 diabetes. N Engl J Med 2008;359:2220-2232
23. Ling C, Poulsen P, Simonsson S, et al. Genetic and epigenetic factors are associated with expression of respiratory chain component NDUFB6 in human skeletal muscle. J Clin Invest 2007;117:3427-3435 (Pubitemid 350096998)
24. Rönn T, Poulsen P, Hansson O, et al. Age influences DNA methylation and gene expression of COX7A1 in human skeletal muscle. Diabetologia 2008;51:1159-1168
25. Ling C, Del Guerra S, Lupi R, et al. Epigenetic regulation of PPARGC1A in human type 2 diabetic islets and effect on insulin secretion. Diabetologia 2008;51:615-622
26. Barrès R, Osler ME, Yan J, et al. Non-CpG methylation of the PGC-1alpha promoter through DNMT3B controls mitochondrial density. Cell Metab 2009;10:189-198
27. Yang BT, Dayeh TA, Kirkpatrick CL, et al. Insulin promoter DNA methylation correlates negatively with insulin gene expression and positively with HbA(1c) levels in human pancreatic islets. Diabetologia 2011;54:360-367
28. Bell CG, Finer S, Lindgren CM, et al.; International Type 2 Diabetes 1q Consortium. Integrated genetic and epigenetic analysis identifies haplotype-specific methylation in the FTO type 2 diabetes and obesity susceptibility locus. PLoS ONE 2010;5:e14040
29. Sandovici IS, Dekker-Nitert NH, Ackers-Johnson M, et al. M. and Ozanne, SE.: Dynamic epigenetic regulation by early-diet and aging of the type 2 diabetes susceptibility gene Hnf4a in pancreatic islets. Proc Natl Acad Sci USA 2011;108:5449-5454
30. Hardie DG. AMPK: a key regulator of energy balance in the single cell and the whole organism. Int J Obes (Lond) 2008;32(Suppl. 4):S7-S12
31. Wojtaszewski JF, Lynge J, Jakobsen AB, Goodyear LJ, Richter EA. Differential regulation of MAP kinase by contraction and insulin in skeletal muscle: metabolic implications. Am J Physiol 1999;277:E724-E732 (Pubitemid 29522626)
32. Cubas P, Vincent C, Coen E. An epigenetic mutation responsible for natural variation in floral symmetry. Nature 1999;401:157-161 (Pubitemid 29436317)
33. Chong S, Whitelaw E. Epigenetic germline inheritance. Curr Opin Genet Dev 2004;14:692-696 (Pubitemid 39505376)
34. Anway MD, Cupp AS, Uzumcu M, Skinner MK. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 2005;308:1466-1469 (Pubitemid 40791300)
35. Ng SF, Lin RC, Laybutt DR, Barres R, Owens JA, Morris MJ. Chronic highfat diet in fathers programs b-cell dysfunction in female rat offspring. Nature 2010;467:963-966
36. El-Osta A, Brasacchio D, Yao D, et al. Transient high glucose causes persistent epigenetic changes and altered gene expression during subsequent normoglycemia. J Exp Med 2008;205:2409-2417
37. 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;118:2316-2324 (Pubitemid 351872348)
38. Kriaucionis S, Bird A. DNA methylation and Rett syndrome. Hum Mol Genet 2003;12(Spec No 2):R221-R227 (Pubitemid 37259336)
39. Cassidy SB, Schwartz S, Miller JL, Driscoll DJ. Prader-Willi syndrome. Genet Med 2012;14:10-26
40. Mackay DJ, Temple IK. Transient neonatal diabetes mellitus type 1. Am J Med Genet C Semin Med Genet 2010;154C:335-342
41. Morgan HD, Sutherland HG, Martin DI, Whitelaw E. Epigenetic inheritance at the agouti locus in the mouse. Nat Genet 1999;23:314-318 (Pubitemid 29526429)
42. Keller P, Vollaard NB, Gustafsson T, et al. A transcriptional map of the impact of endurance exercise training on skeletal muscle phenotype. J Appl Physiol 2011;110:46-59
43. Smith JA, Collins M, Grobler LA, Magee CJ, Ojuka EO. Exercise and CaMK activation both increase the binding of MEF2A to the Glut4 promoter in skeletal muscle in vivo. Am J Physiol Endocrinol Metab 2007;292:E413-E420 (Pubitemid 46220565)
44. Smith JA, Kohn TA, Chetty AK, Ojuka EO. CaMK activation during exercise is required for histone hyperacetylation and MEF2A binding at the MEF2 site on the Glut4 gene. Am J Physiol Endocrinol Metab 2008;295:E698-E704
45. Olsson AH, Rönn T, Ladenvall C, et al. Two common genetic variants near nuclear-encoded OXPHOS genes are associated with insulin secretion in vivo. Eur J Endocrinol 2011;164:765-771
46. McGee SL, Sparling D, Olson AL, Hargreaves M. Exercise increases MEF2-and GEF DNA-binding activity in human skeletal muscle. FASEB J 2006;20:348-349 (Pubitemid 46671167)
47. Yamauchi T, Kamon J, Ito Y, et al. Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature 2003;423:762-769 (Pubitemid 36735700)
48. Taguchi T, Kishikawa H, Motoshima H, et al. Involvement of bradykinin in acute exercise-induced increase of glucose uptake and GLUT-4 translocation in skeletal muscle: studies in normal and diabetic humans and rats. Metabolism 2000;49:920-930 (Pubitemid 30483447)
49. Haugen F, Norheim F, Lian H, et al. IL-7 is expressed and secreted by human skeletal muscle cells. Am J Physiol Cell Physiol 2010;298:C807-C816
50. Deaton AM, Bird A. CpG islands and the regulation of transcription. Genes Dev 2011;25:1010-1022