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Exercise: Putting Action into Our Epigenome

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Abstract

Most human phenotypes are influenced by a combination of genomic and environmental factors. Engaging in regular physical exercise prevents many chronic diseases, decreases mortality risk and increases longevity. However, the mechanisms involved are poorly understood. The modulating effect of physical (aerobic and resistance) exercise on gene expression has been known for some time now and has provided us with an understanding of the biological responses to physical exercise. Emerging research data suggest that epigenetic modifications are extremely important for both development and disease in humans. In the current review, we summarise findings on the effect of exercise on epigenetic modifications and their effects on gene expression. Current research data suggest epigenetic modifications (DNA methylation and histone acetylation) and microRNAs (miRNAs) are responsive to acute aerobic and resistance exercise in brain, blood, skeletal and cardiac muscle, adipose tissue and even buccal cells. Six months of aerobic exercise alters whole-genome DNA methylation in skeletal muscle and adipose tissue and directly influences lipogenesis. Some miRNAs are related to maximal oxygen consumption (VO2max) and VO2max trainability, and are differentially expressed amongst individuals with high and low VO2max. Remarkably, miRNA expression profiles discriminate between low and high responders to resistance exercise (miR-378, -26a, -29a and -451) and correlate to gains in lean body mass (miR-378). The emerging field of exercise epigenomics is expected to prosper and additional studies may elucidate the clinical relevance of miRNAs and epigenetic modifications, and delineate mechanisms by which exercise confers a healthier phenotype and improves performance.

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References

  1. de la Chapelle A. Genetic predisposition to human disease: allele-specific expression and low-penetrance regulatory loci. Oncogene. 2009;28:3345–8.

    PubMed  Google Scholar 

  2. Diaz-Gallo LM, Palomino-Morales RJ, Gomez-Garcia M, et al. STAT4 gene influences genetic predisposition to ulcerative colitis but not Crohn’s disease in the Spanish population: a replication study. Hum Immunol. 2010;71:515–9.

    CAS  PubMed  Google Scholar 

  3. Ingles J, Yeates L, Hunt L, et al. Health status of cardiac genetic disease patients and their at-risk relatives. Int J Cardiol. 2013;165:448–53.

    PubMed  Google Scholar 

  4. Charchar FJ, Bloomer LD, Barnes TA, et al. Inheritance of coronary artery disease in men: an analysis of the role of the Y chromosome. Lancet. 2012;379:915–22.

    CAS  PubMed Central  PubMed  Google Scholar 

  5. Bannister AJ, Kouzarides T. Regulation of chromatin by histone modifications. Cell Res. 2011;21:381–95.

    CAS  PubMed  Google Scholar 

  6. Varley KE, Gertz J, Bowling KM, et al. Dynamic DNA methylation across diverse human cell lines and tissues. Genome Res. 2013;23:555–67.

    CAS  PubMed  Google Scholar 

  7. Wang X, Falkner B, Zhu H, et al. A genome-wide methylation study on essential hypertension in young African American males. PLoS One. 2013;8:e53938.

    CAS  PubMed Central  PubMed  Google Scholar 

  8. Bartlett TE, Zaikin A, Olhede SC, et al. Corruption of the intra-gene DNA methylation architecture is a hallmark of cancer. PLoS One. 2013;8:e68285.

    CAS  PubMed Central  PubMed  Google Scholar 

  9. Heyn H, Esteller M. DNA methylation profiling in the clinic: applications and challenges. Nat Rev Genet. 2012;13:679–92.

    CAS  PubMed  Google Scholar 

  10. van Empel VP, De Windt LJ, da Costa Martins PA. Circulating miRNAs: reflecting or affecting cardiovascular disease? Curr Hypertens Rep. 2012;14:498–509.

    PubMed  Google Scholar 

  11. Esteller M. Non-coding RNAs in human disease. Nat Rev Genet. 2011;12:861–74.

    CAS  PubMed  Google Scholar 

  12. Na HK, Oliynyk S. Effects of physical activity on cancer prevention. Ann N Y Acad Sci. 2011;1229:176–83.

    CAS  PubMed  Google Scholar 

  13. Jenkins NT, Martin JS, Laughlin MH, et al. Exercise-induced signals for vascular endothelial adaptations: implications for cardiovascular disease. Curr Cardiovasc Risk Rep. 2012;6:331–46.

    PubMed Central  PubMed  Google Scholar 

  14. Warburton DE, Nicol CW, Bredin SS. Health benefits of physical activity: the evidence. CMAJ. 2006;174:801–9.

    PubMed Central  PubMed  Google Scholar 

  15. Fraga MF, Ballestar E, Paz MF, et al. Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci USA. 2005;102:10604–9.

    CAS  PubMed  Google Scholar 

  16. Waterland RA, Michels KB. Epigenetic epidemiology of the developmental origins hypothesis. Annu Rev Nutr. 2007;27:363–88.

    CAS  PubMed  Google Scholar 

  17. Kouzarides T. Chromatin modifications and their function. Cell. 2007;128:693–705.

    CAS  PubMed  Google Scholar 

  18. Ren H, Collins V, Clarke SJ, et al. Epigenetic changes in response to tai chi practice: a pilot investigation of DNA methylation marks. Evid Based Complement Alternat Med. 2012;2012:841810.

    PubMed Central  PubMed  Google Scholar 

  19. Barres R, Yan J, Egan B, et al. Acute exercise remodels promoter methylation in human skeletal muscle. Cell Metabolism. 2012;15:405–11.

    CAS  PubMed  Google Scholar 

  20. McGee SL, Fairlie E, Garnham AP, et al. Exercise-induced histone modifications in human skeletal muscle. J Physiol. 2009;587:5951–8.

    CAS  PubMed  Google Scholar 

  21. Chandramohan Y, Droste SK, Arthur JS, et al. The forced swimming-induced behavioural immobility response involves histone H3 phospho-acetylation and c-Fos induction in dentate gyrus granule neurons via activation of the N-methyl-d-aspartate/extracellular signal-regulated kinase/mitogen- and stress-activated kinase signalling pathway. Eur J Neurosci. 2008;27:2701–13.

    PubMed  Google Scholar 

  22. Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet. 2003;33(Suppl):245–54.

    CAS  PubMed  Google Scholar 

  23. Fazzari MJ, Greally JM. Introduction to epigenomics and epigenome-wide analysis. Methods Mol Biol. 2010;620:243–65.

    CAS  PubMed  Google Scholar 

  24. Bernardo BC, Charchar FJ, Lin RC, et al. A microRNA guide for clinicians and basic scientists: background and experimental techniques. Heart Lung Circ. 2012;21:131–42.

    CAS  PubMed  Google Scholar 

  25. Eads CA, Danenberg KD, Kawakami K, et al. MethyLight: a high-throughput assay to measure DNA methylation. Nucleic Acids Res. 2000;28:E32.

    CAS  PubMed Central  PubMed  Google Scholar 

  26. Karimi M, Johansson S, Stach D, et al. LUMA (LUminometric Methylation Assay)—a high throughput method to the analysis of genomic DNA methylation. Exp Cell Res. 2006;312:1989–95.

    CAS  PubMed  Google Scholar 

  27. Irizarry RA, Ladd-Acosta C, Carvalho B, et al. Comprehensive high-throughput arrays for relative methylation (CHARM). Genome Res. 2008;18:780–90.

    CAS  PubMed  Google Scholar 

  28. de Ruijter AJ, van Gennip AH, Caron HN, et al. Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem J. 2003;370:737–49.

    PubMed  Google Scholar 

  29. Jirtle RL, Skinner MK. Environmental epigenomics and disease susceptibility. Nat Rev Genet. 2007;8:253–62.

    CAS  PubMed  Google Scholar 

  30. Li Y, Zhu J, Tian G, et al. The DNA methylome of human peripheral blood mononuclear cells. PLoS Biol. 2010;8:e1000533.

    PubMed Central  PubMed  Google Scholar 

  31. Deaton AM, Bird A. CpG islands and the regulation of transcription. Genes Dev. 2011;25:1010–22.

    CAS  PubMed  Google Scholar 

  32. Han H, Cortez CC, Yang X, et al. DNA methylation directly silences genes with non-CpG island promoters and establishes a nucleosome occupied promoter. Hum Mol Genet. 2011;20:4299–310.

    CAS  PubMed  Google Scholar 

  33. Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet. 2012;13:484–92.

    CAS  PubMed  Google Scholar 

  34. Defossez PA, Stancheva I. Biological functions of methyl-CpG-binding proteins. Prog Mol Biol Transl Sci. 2011;101:377–98.

    CAS  PubMed  Google Scholar 

  35. Klose RJ, Bird AP. Genomic DNA methylation: the mark and its mediators. Trends Biochem Sci. 2006;31:89–97.

    CAS  PubMed  Google Scholar 

  36. Fang F, Hodges E, Molaro A, et al. Genomic landscape of human allele-specific DNA methylation. Proc Natl Acad Sci USA. 2012;109:7332–7.

    CAS  PubMed  Google Scholar 

  37. Wutz A. Gene silencing in X-chromosome inactivation: advances in understanding facultative heterochromatin formation. Nat Rev Genet. 2011;12:542–53.

    CAS  PubMed  Google Scholar 

  38. Mermoud JE, Popova B, Peters AH, et al. Histone H3 lysine 9 methylation occurs rapidly at the onset of random X chromosome inactivation. Curr Biol. 2002;12:247–51.

    CAS  PubMed  Google Scholar 

  39. Wolff EM, Byun HM, Han HF, et al. Hypomethylation of a LINE-1 promoter activates an alternate transcript of the MET oncogene in bladders with cancer. PLoS Genet. 2010;6:e1000917.

    PubMed Central  PubMed  Google Scholar 

  40. Sunami E, de Maat M, Vu A, et al. LINE-1 hypomethylation during primary colon cancer progression. PLoS One. 2011;6:e18884.

    CAS  PubMed Central  PubMed  Google Scholar 

  41. Pavicic W, Joensuu EI, Nieminen T, et al. LINE-1 hypomethylation in familial and sporadic cancer. J Mol Med (Berl). 2012;90:827–35.

    CAS  Google Scholar 

  42. Lopez-Serra P, Esteller M. DNA methylation-associated silencing of tumor-suppressor microRNAs in cancer. Oncogene. 2012;31:1609–22.

    CAS  PubMed Central  PubMed  Google Scholar 

  43. Kuratomi G, Iwamoto K, Bundo M, et al. Aberrant DNA methylation associated with bipolar disorder identified from discordant monozygotic twins. Mol Psychiatry. 2008;13:429–41.

    CAS  PubMed  Google Scholar 

  44. Poulsen P, Esteller M, Vaag A, et al. The epigenetic basis of twin discordance in age-related diseases. Pediatr Res. 2007;61:38R–42R.

    PubMed  Google Scholar 

  45. Deaton AM, Webb S, Kerr AR, et al. Cell type-specific DNA methylation at intragenic CpG islands in the immune system. Genome Res. 2011;21:1074–86.

    CAS  PubMed  Google Scholar 

  46. Denis H, Ndlovu MN, Fuks F. Regulation of mammalian DNA methyltransferases: a route to new mechanisms. EMBO Rep. 2011;12:647–56.

    CAS  PubMed Central  PubMed  Google Scholar 

  47. Karpf AR, Matsui S. Genetic disruption of cytosine DNA methyltransferase enzymes induces chromosomal instability in human cancer cells. Cancer Res. 2005;65:8635–9.

    CAS  PubMed  Google Scholar 

  48. Okano M, Bell DW, Haber DA, et al. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell. 1999;99:247–57.

    CAS  PubMed  Google Scholar 

  49. Suetake I, Shinozaki F, Miyagawa J, et al. DNMT3L stimulates the DNA methylation activity of Dnmt3a and Dnmt3b through a direct interaction. J Biol Chem. 2004;279:27816–23.

    CAS  PubMed  Google Scholar 

  50. Niculescu MD, Zeisel SH. Diet, methyl donors and DNA methylation: interactions between dietary folate, methionine and choline. J Nutr. 2002;132:2333S–5S.

    CAS  PubMed  Google Scholar 

  51. Ito S, D’Alessio AC, Taranova OV, et al. Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature. 2010;466:1129–33.

    CAS  PubMed Central  PubMed  Google Scholar 

  52. Wu SC, Zhang Y. Active DNA demethylation: many roads lead to Rome. Nat Rev Mol Cell Biol. 2010;11:607–20.

    CAS  PubMed Central  PubMed  Google Scholar 

  53. Franchini DM, Schmitz KM, Petersen-Mahrt SK. 5-methylcytosine DNA demethylation: more than losing a methyl group. Annu Rev Genet. 2012;46:419–41.

    CAS  PubMed  Google Scholar 

  54. Da Sacco L, Masotti A. Recent insights and novel bioinformatics tools to understand the role of microRNAs binding to 5’ untranslated region. Int J Mol Sci. 2012;14:480–95.

    PubMed Central  PubMed  Google Scholar 

  55. Vasudevan S. Posttranscriptional upregulation by microRNAs. Wiley Interdiscip Rev RNA. 2012;3:311–30.

    CAS  PubMed  Google Scholar 

  56. Kim YK, Kim VN. Processing of intronic microRNAs. EMBO J. 2007;26:775–83.

    CAS  PubMed  Google Scholar 

  57. Rodriguez A, Griffiths-Jones S, Ashurst JL, et al. Identification of mammalian microRNA host genes and transcription units. Genome Res. 2004;14:1902–10.

    CAS  PubMed  Google Scholar 

  58. Saini HK, Griffiths-Jones S, Enright AJ. Genomic analysis of human microRNA transcripts. Proc Natl Acad Sci USA. 2007;104:17719–24.

    CAS  PubMed  Google Scholar 

  59. Yeom KH, Lee Y, Han J, et al. Characterization of DGCR8/Pasha, the essential cofactor for Drosha in primary miRNA processing. Nucl Acids Res. 2006;34:4622–9.

    CAS  PubMed  Google Scholar 

  60. Zeng Y, Yi R, Cullen BR. Recognition and cleavage of primary microRNA precursors by the nuclear processing enzyme Drosha. EMBO J. 2005;24:138–48.

    CAS  PubMed  Google Scholar 

  61. Yi R, Qin Y, Macara IG, et al. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev. 2003;17:3011–6.

    CAS  PubMed  Google Scholar 

  62. Hutvagner G, McLachlan J, Pasquinelli AE, et al. A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science. 2001;293:834–8.

    CAS  PubMed  Google Scholar 

  63. Chendrimada TP, Gregory RI, Kumaraswamy E, et al. TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature. 2005;436:740–4.

    CAS  PubMed Central  PubMed  Google Scholar 

  64. Winter J, Jung S, Keller S, et al. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol. 2009;11:228–34.

    CAS  PubMed  Google Scholar 

  65. Okamura K, Ishizuka A, Siomi H, et al. Distinct roles for argonaute proteins in small RNA-directed RNA cleavage pathways. Genes Dev. 2004;18:1655–66.

    CAS  PubMed  Google Scholar 

  66. Sood P, Krek A, Zavolan M, et al. Cell-type-specific signatures of microRNAs on target mRNA expression. Proc Natl Acad Sci USA. 2006;103:2746–51.

    CAS  PubMed  Google Scholar 

  67. Gu S, Jin L, Zhang F, et al. Biological basis for restriction of microRNA targets to the 3’ untranslated region in mammalian mRNAs. Nat Struct Mol Biol. 2009;16:144–50.

    CAS  PubMed Central  PubMed  Google Scholar 

  68. Lim LP, Lau NC, Garrett-Engele P, et al. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature. 2005;433:769–73.

    CAS  PubMed  Google Scholar 

  69. Betancur JG, Yoda M, Tomari Y. miRNA-like duplexes as RNAi triggers with improved specificity. Front Genet. 2012;3:127.

    CAS  PubMed Central  PubMed  Google Scholar 

  70. Marques MA, Combes M, Roussel B, et al. Impact of a mechanical massage on gene expression profile and lipid mobilization in female gluteofemoral adipose tissue. Obes Facts. 2011;4:121–9.

    CAS  PubMed  Google Scholar 

  71. Nikitina EG, Urazova LN, Stegny VN. MicroRNAs and human cancer. Exp Oncol. 2012;34:2–8.

    CAS  PubMed  Google Scholar 

  72. Fernandez-Valverde SL, Taft RJ, Mattick JS. MicroRNAs in beta-cell biology, insulin resistance, diabetes and its complications. Diabetes. 2011;60:1825–31.

    CAS  PubMed  Google Scholar 

  73. Zampetaki A, Willeit P, Drozdov I, et al. Profiling of circulating microRNAs: from single biomarkers to re-wired networks. Cardiovasc Res. 2012;93:555–62.

    CAS  PubMed  Google Scholar 

  74. McAlexander MA, Phillips MJ, Witwer KW. Comparison of methods for miRNA extraction from plasma and quantitative recovery of RNA from cerebrospinal fluid. Front Genet. 2013;4:83.

    CAS  PubMed Central  PubMed  Google Scholar 

  75. Pritchard CC, Cheng HH, Tewari M. MicroRNA profiling: approaches and considerations. Nat Rev Genet. 2012;13:358–69.

    CAS  PubMed  Google Scholar 

  76. Cotman CW, Engesser-Cesar C. Exercise enhances and protects brain function. Exerc Sport Sci Rev. 2002;30:75–9.

    PubMed  Google Scholar 

  77. Hillman CH, Erickson KI, Kramer AF. Be smart, exercise your heart: exercise effects on brain and cognition. Nat Rev Neurosci. 2008;9:58–65.

    CAS  PubMed  Google Scholar 

  78. Podewils LJ, Guallar E, Kuller LH, et al. Physical activity, APOE genotype, and dementia risk: findings from the Cardiovascular Health Cognition Study. Am J Epidemiol. 2005;161:639–51.

    PubMed  Google Scholar 

  79. Smith JA, Kohn TA, Chetty AK, et al. 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:E698–704.

    CAS  PubMed  Google Scholar 

  80. Collins A, Hill LE, Chandramohan Y, et al. Exercise improves cognitive responses to psychological stress through enhancement of epigenetic mechanisms and gene expression in the dentate gyrus. PLoS One. 2009;4:e4330.

    PubMed Central  PubMed  Google Scholar 

  81. Abel JL, Rissman EF. Running-induced epigenetic and gene expression changes in the adolescent brain. Int J Dev Neurosci. 2013;31(6):382-90.

    Google Scholar 

  82. Elsner VR, Lovatel GA, Moyses F, et al. Exercise induces age-dependent changes on epigenetic parameters in rat hippocampus: a preliminary study. Exp Gerontol. 2012;48:136–9.

    PubMed  Google Scholar 

  83. Mattson MP, Maudsley S, Martin B. BDNF and 5-HT: a dynamic duo in age-related neuronal plasticity and neurodegenerative disorders. Trends Neurosci. 2004;27:589–94.

    CAS  PubMed  Google Scholar 

  84. Gomez-Pinilla F, Ying Z, Roy RR, et al. Voluntary exercise induces a BDNF-mediated mechanism that promotes neuroplasticity. J Neurophysiol. 2002;88:2187–95.

    CAS  PubMed  Google Scholar 

  85. Gomez-Pinilla F, Zhuang Y, Feng J, et al. Exercise impacts brain-derived neurotrophic factor plasticity by engaging mechanisms of epigenetic regulation. Eur J Neurosci. 2011;33:383–90.

    CAS  PubMed Central  PubMed  Google Scholar 

  86. Elsner VR, Lovatel GA, Bertoldi K, et al. Effect of different exercise protocols on histone acetyltransferases and histone deacetylases activities in rat hippocampus. Neuroscience. 2011;192:580–7.

    CAS  PubMed  Google Scholar 

  87. Abel JL, Rissman EF. Running-induced epigenetic and gene expression changes in the adolescent brain. Int J Dev Neurosci. 2013;31:382–90.

    CAS  PubMed Central  PubMed  Google Scholar 

  88. McGee SL, Hargreaves M. Histone modifications and exercise adaptations. J Appl Physiol. 2011;110:258–63.

    CAS  PubMed  Google Scholar 

  89. Mejat A, Ramond F, Bassel-Duby R, et al. Histone deacetylase 9 couples neuronal activity to muscle chromatin acetylation and gene expression. Nat Neurosci. 2005;8:313–21.

    CAS  PubMed  Google Scholar 

  90. Cohen TJ, Barrientos T, Hartman ZC, et al. The deacetylase HDAC4 controls myocyte enhancing factor-2-dependent structural gene expression in response to neural activity. FASEB J. 2009;23:99–106.

    CAS  PubMed  Google Scholar 

  91. Mukwevho E, Kohn TA, Lang D, et al. Caffeine induces hyperacetylation of histones at the MEF2 site on the Glut4 promoter and increases MEF2A binding to the site via a CaMK-dependent mechanism. Am J Physiol Endocrinol Metab. 2008;294:E582–8.

    CAS  PubMed  Google Scholar 

  92. Bouchard C, Sarzynski MA, Rice TK, et al. Genomic predictors of the maximal O(2) uptake response to standardized exercise training programs. J Appl Physiol. 2011;110:1160–70.

    CAS  PubMed  Google Scholar 

  93. Timmons JA, Knudsen S, Rankinen T, et al. Using molecular classification to predict gains in maximal aerobic capacity following endurance exercise training in humans. J Appl Physiol. 2010;108:1487–96.

    CAS  PubMed  Google Scholar 

  94. 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.

    CAS  PubMed  Google Scholar 

  95. Puthucheary Z, Skipworth JR, Rawal J, et al. The ACE gene and human performance: 12 years on. Sports Med. 2011;41:433–48.

    PubMed  Google Scholar 

  96. Bouchard C. Genomic predictors of trainability. Exp Physiol. 2012;97:347–52.

    CAS  PubMed  Google Scholar 

  97. Terruzzi I, Senesi P, Montesano A, et al. Genetic polymorphisms of the enzymes involved in DNA methylation and synthesis in elite athletes. Physiol Genomics. 2011;43:965–73.

    CAS  PubMed  Google Scholar 

  98. Ehlert T, Simon P, Moser DA. Epigenetics in sports. Sports Med. 2013;43:93–110.

    PubMed  Google Scholar 

  99. Raleigh SM. Epigenetic regulation of the ACE gene might be more relevant to endurance physiology than the I/D polymorphism. J Appl Physiol. 2012;112:1082–3.

    CAS  PubMed  Google Scholar 

  100. Egan B, Carson BP, Garcia-Roves PM, et al. Exercise intensity-dependent regulation of peroxisome proliferator-activated receptor coactivator-1 mRNA abundance is associated with differential activation of upstream signalling kinases in human skeletal muscle. J Physiol. 2010;588:1779–90.

    CAS  PubMed  Google Scholar 

  101. Drummond MJ, McCarthy JJ, Fry CS, et al. Aging differentially affects human skeletal muscle microRNA expression at rest and after an anabolic stimulus of resistance exercise and essential amino acids. Am J Physiol Endocrinol Metab. 2008;295:E1333–40.

    CAS  PubMed  Google Scholar 

  102. Russell AP, Lamon S, Boon H, et al. Regulation of miRNAs in human skeletal muscle following acute endurance exercise and short term endurance training. J Physiol. 2013;591(Pt 18):4637-53.

    Google Scholar 

  103. Imamura T, Yamamoto S, Ohgane J, et al. Non-coding RNA directed DNA demethylation of Sphk1 CpG island. Biochem Biophys Res Commun. 2004;322:593–600.

    CAS  PubMed  Google Scholar 

  104. Mohammad F, Pandey GK, Mondal T, et al. Long noncoding RNA-mediated maintenance of DNA methylation and transcriptional gene silencing. Development. 2012;139:2792–803.

    CAS  PubMed  Google Scholar 

  105. Lee IM, Paffenbarger RS Jr. Associations of light, moderate, and vigorous intensity physical activity with longevity. The Harvard Alumni Health Study. Am J Epidemiol. 2000;151:293–9.

    CAS  PubMed  Google Scholar 

  106. Monninkhof EM, Elias SG, Vlems FA, et al. Physical activity and breast cancer: a systematic review. Epidemiology. 2007;18:137–57.

    PubMed  Google Scholar 

  107. Quadrilatero J, Hoffman-Goetz L. Physical activity and colon cancer. A systematic review of potential mechanisms. J Sports Med Phys Fitness. 2003;43:121–38.

    CAS  PubMed  Google Scholar 

  108. Lee IM, Hsieh CC, Paffenbarger RS Jr. Exercise intensity and longevity in men. The Harvard Alumni Health Study. JAMA. 1995;273:1179–84.

    CAS  PubMed  Google Scholar 

  109. Gibala MJ, Little JP, Macdonald MJ, et al. Physiological adaptations to low-volume, high-intensity interval training in health and disease. J Physiol. 2012;590:1077–84.

    CAS  PubMed  Google Scholar 

  110. Paulsen G, Myklestad D, Raastad T. The influence of volume of exercise on early adaptations to strength training. J Strength Cond Res. 2003;17:115–20.

    PubMed  Google Scholar 

  111. Ringholm S, Bienso RS, Kiilerich K, et al. Bed rest reduces metabolic protein content and abolishes exercise-induced mRNA responses in human skeletal muscle. Am J Physiol Endocrinol Metab. 2011;301:e649–58.

    CAS  PubMed  Google Scholar 

  112. Alibegovic AC, Sonne MP, Hojbjerre L, et al. Insulin resistance induced by physical inactivity is associated with multiple transcriptional changes in skeletal muscle in young men. Am J Physiol Endocrinol Metab. 2010;299:e752–63.

    CAS  PubMed  Google Scholar 

  113. Nitert MD, Dayeh T, Volkov P, et al. Impact of an exercise Intervention on DNA methylation in skeletal muscle from first-degree relatives of patients with type 2 diabetes. Diabetes. 2012;61:3322–32.

    CAS  PubMed  Google Scholar 

  114. Ronn T, Volkov P, Davegardh C, et al. A six months exercise intervention influences the genome-wide DNA methylation pattern in human adipose tissue. PLoS Genet. 2013;9:e1003572.

    PubMed Central  PubMed  Google Scholar 

  115. Zhang FF, Cardarelli R, Carroll J, et al. Physical activity and global genomic DNA methylation in a cancer-free population. Epigenetics. 2011;6:293–9.

    CAS  PubMed  Google Scholar 

  116. Zhang FF, Santella RM, Wolff M, et al. White blood cell global methylation and IL-6 promoter methylation in association with diet and lifestyle risk factors in a cancer-free population. Epigenetics. 2012;7:606–14.

    CAS  PubMed  Google Scholar 

  117. Maeda T, Oyama J, Higuchi Y, et al. The physical ability of Japanese female elderly with cerebrovascular disease correlates with the telomere length and subtelomeric methylation status in their peripheral blood leukocytes. Gerontology. 2011;57:137–43.

    PubMed  Google Scholar 

  118. Nakajima K, Takeoka M, Mori M, et al. Exercise effects on methylation of ASC gene. Int J Sports Med. 2010;31:671–5.

    CAS  PubMed  Google Scholar 

  119. Zeng H, Irwin ML, Lu L, et al. Physical activity and breast cancer survival: an epigenetic link through reduced methylation of a tumor suppressor gene L3MBTL1. Breast Cancer Res Treat. 2012;133:127–35.

    CAS  PubMed  Google Scholar 

  120. Lott SA, Burghardt PR, Burghardt KJ, et al. The influence of metabolic syndrome, physical activity and genotype on catechol-O-methyl transferase promoter-region methylation in schizophrenia. Pharmacogenomics J. 2013;13:264–71.

    CAS  PubMed Central  PubMed  Google Scholar 

  121. Libby P. Inflammation in atherosclerosis. Nature. 2002;420:868–74.

    CAS  PubMed  Google Scholar 

  122. Marx J. Cancer research. Inflammation and cancer: the link grows stronger. Science. 2004;306:966–8.

    Google Scholar 

  123. Franks AL, Slansky JE. Multiple associations between a broad spectrum of autoimmune diseases, chronic inflammatory diseases and cancer. Anticancer Res. 2012;32:1119–36.

    CAS  PubMed Central  PubMed  Google Scholar 

  124. Cannizzo ES, Clement CC, Sahu R, et al. Oxidative stress, inflamm-aging and immunosenescence. J Proteomics. 2011;74:2313–23.

    CAS  PubMed  Google Scholar 

  125. Gleeson M, Bishop NC, Stensel DJ, et al. The anti-inflammatory effects of exercise: mechanisms and implications for the prevention and treatment of disease. Nat Rev Immunol. 2011;11:607–15.

    CAS  PubMed  Google Scholar 

  126. Walsh NP, Gleeson M, Shephard RJ, et al. Position statement. Part one: Immune function and exercise. Exerc Immunol Rev. 2011;17:6–63.

    PubMed  Google Scholar 

  127. Tomaszewski M, Charchar FJ, Przybycin M, et al. Strikingly low circulating CRP concentrations in ultramarathon runners independent of markers of adiposity: how low can you go? Arterioscler Thromb Vasc Biol. 2003;23:1640–4.

    CAS  PubMed  Google Scholar 

  128. Heyn H, Li N, Ferreira HJ, et al. Distinct DNA methylomes of newborns and centenarians. Proc Natl Acad Sci USA. 2012;109:10522–7.

    CAS  PubMed  Google Scholar 

  129. Gopalakrishnan S, Van Emburgh BO, Robertson KD. DNA methylation in development and human disease. Mutat Res. 2008;647:30–8.

    CAS  PubMed Central  PubMed  Google Scholar 

  130. Robertson KD. DNA methylation and human disease. Nat Rev Genet. 2005;6:597–610.

    CAS  PubMed  Google Scholar 

  131. Blackburn EH. Structure and function of telomeres. Nature. 1991;350:569–73.

    CAS  PubMed  Google Scholar 

  132. Oeseburg H, de Boer RA, van Gilst WH, et al. Telomere biology in healthy aging and disease. Pflugers Arch. 2010;459:259–68.

    CAS  PubMed Central  PubMed  Google Scholar 

  133. Cawthon RM, Smith KR, O’Brien E, et al. Association between telomere length in blood and mortality in people aged 60 years or older. Lancet. 2003;361:393–5.

    CAS  PubMed  Google Scholar 

  134. Denham J, Nelson CP, O’Brien BJ, et al. Longer leukocyte telomeres are associated with ultra-endurance exercise independent of cardiovascular risk factors. PLoS One. 2013;8:e69377.

    CAS  PubMed Central  PubMed  Google Scholar 

  135. Kaliman P, Parrizas M, Lalanza JF, et al. Neurophysiological and epigenetic effects of physical exercise on the aging process. Ageing Res Rev. 2011;10:475–86.

    PubMed  Google Scholar 

  136. Sanchis-Gomar F, Garcia-Gimenez JL, Perez-Quilis C, et al. Physical exercise as an epigenetic modulator: Eustress, the “positive stress” as an effector of gene expression. J Strength Cond Res. 2012;26:3469–72.

    PubMed  Google Scholar 

  137. Ntanasis-Stathopoulos J, Tzanninis JG, Philippou A, et al. Epigenetic regulation on gene expression induced by physical exercise. J Musculoskelet Neuronal Interact. 2013;13:133–46.

    CAS  PubMed  Google Scholar 

  138. White AJ, Sandler DP, Bolick SC, et al. Recreational and household physical activity at different time points and DNA global methylation. Eur J Cancer. Epub 2013 Mar 6.

  139. Luttropp K, Nordfors L, Ekstrom TJ, et al. Physical activity is associated with decreased global DNA methylation in Swedish older individuals. Scand J Clin Lab Invest. 2013;73:184–5.

    CAS  PubMed  Google Scholar 

  140. Kanwal R, Gupta S. Epigenetics and cancer. J Appl Physiol. 2010;109:598–605.

    CAS  PubMed  Google Scholar 

  141. Chalitchagorn K, Shuangshoti S, Hourpai N, et al. Distinctive pattern of LINE-1 methylation level in normal tissues and the association with carcinogenesis. Oncogene. 2004;23:8841–6.

    CAS  PubMed  Google Scholar 

  142. Coyle YM, Xie XJ, Lewis CM, et al. Role of physical activity in modulating breast cancer risk as defined by APC and RASSF1A promoter hypermethylation in nonmalignant breast tissue. Cancer Epidemiol Biomarkers Prev. 2007;16:192–6.

    CAS  PubMed  Google Scholar 

  143. Yuasa Y, Nagasaki H, Akiyama Y, et al. DNA methylation status is inversely correlated with green tea intake and physical activity in gastric cancer patients. Int J Cancer. 2009;124:2677–82.

    CAS  PubMed  Google Scholar 

  144. Slattery ML, Curtin K, Sweeney C, et al. Diet and lifestyle factor associations with CpG island methylator phenotype and BRAF mutations in colon cancer. Int J Cancer. 2007;120:656–63.

    CAS  PubMed  Google Scholar 

  145. Hughes LA, Simons CC, van den Brandt PA, et al. Body size, physical activity and risk of colorectal cancer with or without the CpG island methylator phenotype (CIMP). PLoS One. 2011;6:e18571.

    CAS  PubMed Central  PubMed  Google Scholar 

  146. Bryan AD, Magnan RE, Hooper AE, et al. Physical activity and differential methylation of breast cancer genes assayed from saliva: a preliminary investigation. Ann Behav Med. 2013;45:89–98.

    PubMed  Google Scholar 

  147. Moleres A, Campion J, Milagro FI, et al. Differential DNA methylation patterns between high and low responders to a weight loss intervention in overweight or obese adolescents: the EVASYON study. FASEB J. 2013;27:2504–12.

    CAS  PubMed  Google Scholar 

  148. Carone BR, Fauquier L, Habib N, et al. Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell. 2010;143:1084–96.

    CAS  PubMed Central  PubMed  Google Scholar 

  149. Morgan HD, Sutherland HG, Martin DI, et al. Epigenetic inheritance at the agouti locus in the mouse. Nat Genet. 1999;23:314–8.

    CAS  PubMed  Google Scholar 

  150. Wolff GL, Kodell RL, Moore SR, et al. Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice. FASEB J. 1998;12:949–57.

    CAS  PubMed  Google Scholar 

  151. Anway MD, Cupp AS, Uzumcu M, et al. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science. 2005;308:1466–9.

    CAS  PubMed  Google Scholar 

  152. Guerrero-Bosagna C, Settles M, Lucker B, Skinner MK, et al. Epigenetic transgenerational actions of vinclozolin on promoter regions of the sperm epigenome. PLoS One. 2010;5(9).

  153. Cooney CA, Dave AA, Wolff GL. Maternal methyl supplements in mice affect epigenetic variation and DNA methylation of offspring. J Nutr. 2002;132:2393S–400S.

    CAS  PubMed  Google Scholar 

  154. Burdge GC, Slater-Jefferies J, Torrens C, et al. Dietary protein restriction of pregnant rats in the F0 generation induces altered methylation of hepatic gene promoters in the adult male offspring in the F1 and F2 generations. Br J Nutr. 2007;97:435–9.

    CAS  PubMed Central  PubMed  Google Scholar 

  155. Chen PY, Ganguly A, Rubbi L, et al. Intrauterine calorie restriction affects placental DNA methylation and gene expression. Physiol Genomics. 2013;45:565–76.

    CAS  PubMed  Google Scholar 

  156. Soubry A, Schildkraut JM, Murtha A, et al. Paternal obesity is associated with IGF2 hypomethylation in newborns: results from a Newborn Epigenetics Study (NEST) cohort. BMC Med. 2013;11:29.

    CAS  PubMed Central  PubMed  Google Scholar 

  157. Radom-Aizik S, Zaldivar F Jr, Leu SY, et al. Effects of exercise on microRNA expression in young males peripheral blood mononuclear cells. Clin Transl Sci. 2012;5:32–8.

    PubMed  Google Scholar 

  158. Radom-Aizik S, Zaldivar FP, Haddad F, et al. Impact of brief exercise on peripheral blood NK cell gene and microRNA expression in young adults. J Appl Physiol. 2013;114:628–36.

    CAS  PubMed  Google Scholar 

  159. Baggish AL, Hale A, Weiner RB, et al. Dynamic regulation of circulating microRNA during acute exhaustive exercise and sustained aerobic exercise training. J Physiol. 2011;589:3983–94.

    CAS  PubMed  Google Scholar 

  160. Nielsen S, Scheele C, Yfanti C, et al. Muscle specific microRNAs are regulated by endurance exercise in human skeletal muscle. J Physiol. 2010;588:4029–37.

    CAS  PubMed  Google Scholar 

  161. Cotman CW, Berchtold NC. Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci. 2002;25:295–301.

    CAS  PubMed  Google Scholar 

  162. Jacobs PL, Nash MS. Exercise recommendations for individuals with spinal cord injury. Sports Med. 2004;34:727–51.

    PubMed  Google Scholar 

  163. Liu G, Detloff MR, Miller KN, et al. Exercise modulates microRNAs that affect the PTEN/mTOR pathway in rats after spinal cord injury. Exp Neurol. 2012;233:447–56.

    CAS  PubMed Central  PubMed  Google Scholar 

  164. Mojtahedi S, Kordi M, Soleimani M, et al. Effect of different intensities of short term aerobic exercise on expression of miR-124 in the hippocampus of adult male rats. J Res Med Sci. 2012;14:16–20.

    CAS  Google Scholar 

  165. Fernandes T, Soci UP, Oliveira EM. Eccentric and concentric cardiac hypertrophy induced by exercise training: microRNAs and molecular determinants. Braz J Med Biol Res. 2011;44:836–47.

    CAS  PubMed  Google Scholar 

  166. Gielen S, Schuler G, Adams V. Cardiovascular effects of exercise training: molecular mechanisms. Circulation. 2010;122:1221–38.

    PubMed  Google Scholar 

  167. Soci UP, Fernandes T, Hashimoto NY, et al. MicroRNAs 29 are involved in the improvement of ventricular compliance promoted by aerobic exercise training in rats. Physiol Genomics. 2011;43:665–73.

    CAS  PubMed  Google Scholar 

  168. Fernandes T, Hashimoto NY, Magalhaes FC, et al. Aerobic exercise training-induced left ventricular hypertrophy involves regulatory microRNAs, decreased angiotensin-converting enzyme-angiotensin ii, and synergistic regulation of angiotensin-converting enzyme 2-angiotensin (1–7). Hypertension. 2011;58:182–9.

    CAS  PubMed Central  PubMed  Google Scholar 

  169. Ma Z, Qi J, Meng S, et al. Swimming exercise training-induced left ventricular hypertrophy involves microRNAs and synergistic regulation of the PI3K/AKT/mTOR signaling pathway. Eur J Appl Physiol. 2013;113(10):2473-86.

    Google Scholar 

  170. Moulton KS. Angiogenesis in atherosclerosis: gathering evidence beyond speculation. Curr Opin Lipidol. 2006;17:548–55.

    CAS  PubMed  Google Scholar 

  171. Fernandes T, Magalhaes FC, Roque FR, et al. Exercise training prevents the microvascular rarefaction in hypertension balancing angiogenic and apoptotic factors: role of microRNAs-16, -21, and -126. Hypertension. 2012;59:513–20.

    CAS  PubMed  Google Scholar 

  172. Wang S, Aurora AB, Johnson BA, et al. The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis. Dev Cell. 2008;15:261–71.

    PubMed Central  PubMed  Google Scholar 

  173. Fish JE, Santoro MM, Morton SU, et al. miR-126 regulates angiogenic signaling and vascular integrity. Dev Cell. 2008;15:272–84.

    CAS  PubMed Central  PubMed  Google Scholar 

  174. da Silva NDJ, Fernandes T, Soci UP, et al. Swimming training in rats increases cardiac MicroRNA-126 expression and angiogenesis. Med Sci Sports Exerc. 2012;44:1453–62.

    Google Scholar 

  175. Yang Y, Creer A, Jemiolo B, et al. Time course of myogenic and metabolic gene expression in response to acute exercise in human skeletal muscle. J Appl Physiol. 2005;98:1745–52.

    CAS  PubMed  Google Scholar 

  176. Phillips BE, Hill DS, Atherton PJ. Regulation of muscle protein synthesis in humans. Curr Opin Clin Nutr Metab Care. 2012;15:58–63.

    CAS  PubMed  Google Scholar 

  177. Raue U, Slivka D, Jemiolo B, et al. Myogenic gene expression at rest and after a bout of resistance exercise in young (18–30 yr) and old (80–89 yr) women. J Appl Physiol. 2006;101:53–9.

    CAS  PubMed  Google Scholar 

  178. Davidsen PK, Gallagher IJ, Hartman JW, et al. High responders to resistance exercise training demonstrate differential regulation of skeletal muscle microRNA expression. J Appl Physiol. 2011;110:309–17.

    PubMed  Google Scholar 

  179. Mueller M, Breil FA, Lurman G, et al. Different molecular and structural adaptations with eccentric and conventional strength training in elderly men and women. Gerontology. 2011;57:528–38.

    PubMed  Google Scholar 

  180. McCarthy JJ, Esser KA. MicroRNA-1 and microRNA-133a expression are decreased during skeletal muscle hypertrophy. J app physiol. 2007;102:306–13.

    CAS  Google Scholar 

  181. Drummond MJ, McCarthy JJ, Sinha M, et al. Aging and microRNA expression in human skeletal muscle: a microarray and bioinformatics analysis. Physiol Genomics. 2011;43:595–603.

    CAS  PubMed  Google Scholar 

  182. Liang R, Bates DJ, Wang E. Epigenetic control of microRNA expression and aging. Curr Genomics. 2009;10:184–93.

    CAS  PubMed  Google Scholar 

  183. Lu L, Zhou L, Chen EZ, et al. A novel YY1-miR-1 regulatory circuit in skeletal myogenesis revealed by genome-wide prediction of YY1-miRNA network. PLoS One. 2012;7:e27596.

    CAS  PubMed Central  PubMed  Google Scholar 

  184. Chen JF, Tao Y, Li J, et al. microRNA-1 and microRNA-206 regulate skeletal muscle satellite cell proliferation and differentiation by repressing Pax7. J Cell Biol. 2010;190:867–79.

    CAS  PubMed  Google Scholar 

  185. Sun Y, Ge Y, Drnevich J, et al. Mammalian target of rapamycin regulates miRNA-1 and follistatin in skeletal myogenesis. J Cell Biol. 2010;189:1157–69.

    CAS  PubMed  Google Scholar 

  186. Safdar A, Abadi A, Akhtar M, et al. miRNA in the regulation of skeletal muscle adaptation to acute endurance exercise in C57Bl/6 J male mice. PLoS One. 2009;4:e5610.

    PubMed Central  PubMed  Google Scholar 

  187. Rico-Sanz J, Rankinen T, Rice T, et al. Quantitative trait loci for maximal exercise capacity phenotypes and their responses to training in the HERITAGE Family Study. Physiol Genomics. 2004;16:256–60.

    CAS  PubMed  Google Scholar 

  188. Macarthur DG, North KN. Genes and human elite athletic performance. Hum Genet. 2005;116:331–9.

    CAS  PubMed  Google Scholar 

  189. McCarthy JJ, Esser KA, Peterson CA, et al. Evidence of MyomiR network regulation of β-myosin heavy chain gene expression during skeletal muscle atrophy. Physiol Genomics. 2009;39:219–26.

    CAS  PubMed  Google Scholar 

  190. Aoi W, Naito Y, Mizushima K, et al. The microRNA miR-696 regulates PGC-1α in mouse skeletal muscle in response to physical activity. Am J Physiol Endocrinol Metab. 2010;298:e799–806.

    CAS  PubMed  Google Scholar 

  191. Mendell JT, Olson EN. MicroRNAs in stress signaling and human disease. Cell. 2012;148:1172–87.

    CAS  PubMed Central  PubMed  Google Scholar 

  192. Chinsomboon J, Ruas J, Gupta RK, et al. The transcriptional coactivator PGC-1α mediates exercise-induced angiogenesis in skeletal muscle. Proc Natl Acad Sci USA. 2009;106:21401–6.

    CAS  PubMed  Google Scholar 

  193. Lin J, Wu H, Tarr PT, et al. Transcriptional co-activator PGC-1α drives the formation of slow-twitch muscle fibres. Nature. 2002;418:797–801.

    CAS  PubMed  Google Scholar 

  194. Aquilano K, Vigilanza P, Baldelli S, et al. Peroxisome proliferator-activated receptor gamma co-activator 1alpha (PGC-1α) and sirtuin 1 (SIRT1) reside in mitochondria: possible direct function in mitochondrial biogenesis. J Biol Chem. 2010;285:21590–9.

    CAS  PubMed  Google Scholar 

  195. Wu Z, Puigserver P, Andersson U, et al. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell. 1999;98:115–24.

    CAS  PubMed  Google Scholar 

  196. Baoutina A, Alexander IE, Rasko JE, et al. Potential use of gene transfer in athletic performance enhancement. Mol Ther. 2007;15:1751–66.

    CAS  PubMed  Google Scholar 

  197. Yamamoto H, Morino K, Nishio Y, et al. MicroRNA (miRNA)-494 regulates mitochondrial biogenesis in skeletal muscle through mitochondrial transcriptional factor A (mtTFA) and forkhead box j3 (Foxj3). Am J Physiol Endocrinol Metab. 2012;303:e1419–27.

    CAS  PubMed  Google Scholar 

  198. Bye A, Rosjo H, Aspenes ST, et al. Circulating microRNAs and aerobic fitness - The HUNT-Study. PLoS One. 2013;8:e57496.

    CAS  PubMed Central  PubMed  Google Scholar 

  199. Aoi W, Ichikawa H, Mune K, et al. Muscle-enriched microRNA miR-486 decreases in circulation in response to exercise in young men. Front Physiol. 2013;4:80.

    PubMed Central  PubMed  Google Scholar 

  200. Kanaan Z, Rai SN, Eichenberger MR, et al. Plasma miR-21: a potential diagnostic marker of colorectal cancer. Ann Surg. 2012;256:544–51.

    PubMed  Google Scholar 

  201. Uhlemann M, Mobius-Winkler S, Fikenzer S, et al. Circulating microRNA-126 increases after different forms of endurance exercise in healthy adults. Eur J Prev Cardiol. Epub 2012 Nov 13.

  202. Radom-Aizik S, Zaldivar F Jr, Oliver S, et al. Evidence for microRNA involvement in exercise-associated neutrophil gene expression changes. J Appl Physiol. 2010;109:252–61.

    CAS  PubMed  Google Scholar 

  203. Tonevitsky AG, Maltseva DV, Abbasi A, et al. Dynamically regulated miRNA-mRNA networks revealed by exercise. BMC Physiol. 2013;13:e9.

    Google Scholar 

  204. Sawada S, Kon M, Wada S, et al. Profiling of circulating microRNAs after a bout of acute resistance exercise in humans. PLoS One. 2013;8:e70823.

    CAS  PubMed Central  PubMed  Google Scholar 

  205. Marcus BH, Bock BC, Pinto BM, et al. Efficacy of an individualized, motivationally-tailored physical activity intervention. Ann Behav Med. 1998;20:174–80.

    CAS  PubMed  Google Scholar 

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Acknowledgments

The authors would like to thank the Victorian Government’s Infrastructure Support Program and the University of Ballarat ‘Self-sustaining Regions Research and Innovation Initiative’, an Australian Government Collaborative Research Network (CRN), for their support. Joshua Denham is supported by an Australian Postgraduate Award. Dr Francine Marques is supported by a National Health and Medical Research Council (NHMRC) and National Heart Foundation (NHF) fellowship. Professor Charchar is supported by the Lew Carty Charitable fund and NHMRC.

Conflict of interest

The authors have no potential conflicts of interest that are directly relevant to the content of this review.

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Denham, J., Marques, F.Z., O’Brien, B.J. et al. Exercise: Putting Action into Our Epigenome. Sports Med 44, 189–209 (2014). https://doi.org/10.1007/s40279-013-0114-1

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