Genetic and epigenetic sex-specific adaptations to endurance exercise

References

• BLIEGE BIRD R, BIRD D W. Why women hunt risk and contemporary foraging in a western desert aboriginal community. Curr Anthropol. 2008;49:655–693.
   PubMed Web of Science ®Google Scholar
• Hurtado AM, Hawkes K, Hill K, et al. Female subsistence strategies among Ache hunter-gatherers of eastern Paraguay. Hum Ecol. 1985;13:1–28.
   Web of Science ®Google Scholar
• Haizlip KM, Harrison BC, Leinwand LA. Sex-based differences in skeletal muscle kinetics and fiber-type composition. Physiology (Bethesda). 2015;30:30–39.
   PubMed Web of Science ®Google Scholar
• Maughan R, Watson JS, Weir J. Strength and cross‐sectional area of human skeletal muscle. J Physiol. 1983;338:37–49.
   PubMed Web of Science ®Google Scholar
• Carter SL, Rennie C, Tarnopolsky MA. Substrate utilization during endurance exercise in men and women after endurance training. Am J Physiol Endocrinol Metab. 2001b;280:E898–907.
   PubMed Web of Science ®Google Scholar
• Carter S, Rennie C, Hamilton S, et al. Changes in skeletal muscle in males and females following endurance training. Can J Physiol Pharmacol. 2001a;79:386–392.
   PubMed Web of Science ®Google Scholar
• Tarnopolsky MA, Rennie CD, Robertshaw HA, et al. Influence of endurance exercise training and sex on intramyocellular lipid and mitochondrial ultrastructure, substrate use, and mitochondrial enzyme activity. Am J Physiol Regul Integr Comp Physiol. 2007;292:R1271–R1278.
   PubMed Web of Science ®Google Scholar
• Friedlander AL, Casazza GA, Horning MA, et al. Training-induced alterations of carbohydrate metabolism in women: women respond differently from men. J Appl Physiol. 1998;85:1175–1186.
   PubMed Web of Science ®Google Scholar
• Horton TJ, Pagliassotti MJ, Hobbs K, et al. Fuel metabolism in men and women during and after long-duration exercise. J Appl Physiol. 1998;85:1823–1832.
   PubMed Web of Science ®Google Scholar
• Spina RJ, Ogawa T, Kohrt WM, et al. Differences in cardiovascular adaptations to endurance exercise training between older men and women. J Appl Physiol. 1993;75:849–855.
   PubMed Web of Science ®Google Scholar
• Pedersen BK, Saltin B. Evidence for prescribing exercise as therapy in chronic disease. Scand J Med Sci Sports. 2006;16:3–63.
   PubMed Web of Science ®Google Scholar
• Devries MC. Sex-based differences in endurance exercise muscle metabolism: impact on exercise and nutritional strategies to optimize health and performance in women. Exp Physiol. 2016;101:243–249.
   PubMed Web of Science ®Google Scholar
• Tarnopolsky M, Atkinson S, Phillips S, et al. Carbohydrate loading and metabolism during exercise in men and women. J Appl Physiol. 1995;78:1360–1368.
   PubMed Web of Science ®Google Scholar
• Tarnopolsky MA. Gender differences in substrate metabolism during endurance exercise. Can J Appl Physiol. 2000;25:312–327.
   PubMedGoogle Scholar
• Devries MC, Hamadeh MJ, Phillips SM, et al. Menstrual cycle phase and sex influence muscle glycogen utilization and glucose turnover during moderate-intensity endurance exercise. Am J Physiol Regul Integr Comp Physiol. 2006;291:R1120–R1128.
   PubMed Web of Science ®Google Scholar
• Mannion AF, Dumas GA, Cooper RG, et al. Muscle fibre size and type distribution in thoracic and lumbar regions of erector spinae in healthy subjects without low back pain: normal values and sex differences. J Anat. 1997;190:505–513.
   PubMed Web of Science ®Google Scholar
• Miller AEJ, Macdougall J, Tarnopolsky M, et al. Gender differences in strength and muscle fiber characteristics. Eur J Appl Physiol Occup Physiol. 1993;66:254–262.
   PubMed Web of Science ®Google Scholar
• Hunter SK. Sex differences in human fatigability: mechanisms and insight to physiological responses. Acta Physiol (Oxf). 2014;210:768–789.
   PubMed Web of Science ®Google Scholar
• Lundsgaard AM, Kiens B. Gender differences in skeletal muscle substrate metabolism – molecular mechanisms and insulin sensitivity. Front Endocrinol (Lausanne). 2014;5:195.
   Web of Science ®Google Scholar
• Kashyap PC, Chia N, Nelson H, et al. Microbiome at the frontier of personalized medicine. Mayo Clin Proc. 2017;92: 1855–1864. Elsevier.
   PubMed Web of Science ®Google Scholar
• Buford TW, Roberts MD, Church TS. Toward exercise as personalized medicine. Sports Med. 2013;43:157–165.
   PubMed Web of Science ®Google Scholar
• Sadée W, Dai Z. Pharmacogenetics/genomics and personalized medicine. Hum Mol Genet. 2005;14:R207–R214.
   PubMed Web of Science ®Google Scholar
• 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;108:1487–1496.
   PubMed Web of Science ®Google Scholar
• Eynon N, Voisin S, Lucia A, et al. Preface: genomics and biology of exercise is undergoing a paradigm shift. BMC Genomics. 2017;18:825.
   PubMed Web of Science ®Google Scholar
• Bouchard C, Rankinen T. Individual differences in response to regular physical activity. Med Sci Sports Exerc. 2001;33: S446–51. discussion S452-3.
   PubMed Web of Science ®Google Scholar
• Vollaard NB, Constantin-Teodosiu D, Fredriksson K, et al. Systematic analysis of adaptations in aerobic capacity and submaximal energy metabolism provides a unique insight into determinants of human aerobic performance. J Appl Physiol (1985). 2009;106:1479–1486.
   PubMed Web of Science ®Google Scholar
• 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;591:4637–4653.
   PubMed Web of Science ®Google Scholar
• Timmons JA, Larsson O, Jansson E, et al. Human muscle gene expression responses to endurance training provide a novel perspective on Duchenne muscular dystrophy. Faseb J. 2005;19:750–760.
   PubMed Web of Science ®Google Scholar
• Lindholm ME, Marabita F, Gomez-Cabrero D, et al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training. Epigenetics. 2014b;9:1557–1569.
   PubMed Web of Science ®Google Scholar
• Barrès R, Yan J, Egan B, et al. Acute exercise remodels promoter methylation in human skeletal muscle. Cell Metab. 2012;15:405–411.
   PubMed Web of Science ®Google Scholar
• Brown WM. Exercise-associated DNA methylation change in skeletal muscle and the importance of imprinted genes: a bioinformatics meta-analysis. Br J Sports Med. 2015;49:1567–1578.
   PubMed Web of Science ®Google Scholar
• Coggan AR, Spina RJ, King DS, et al. Skeletal muscle adaptations to endurance training in 60- to 70-yr-old men and women. J Appl Physiol. 1992;72:1780–1786.
   PubMed Web of Science ®Google Scholar
• Gershoni M, Pietrokovski S. The landscape of sex-differential transcriptome and its consequent selection in human adults. BMC Biol. 2017;15:7.
   PubMed Web of Science ®Google Scholar
• Chen C-Y, Lopes-Ramos CM, Kuijjer ML, et al. Sexual dimorphism in gene expression and regulatory networks across human tissues. bioRxiv. 2016;082289.
   Google Scholar
• Liu D, Sartor MA, Nader GA, et al. Skeletal muscle gene expression in response to resistance exercise: sex specific regulation. BMC Genomics. 2010a;11:659.
   PubMed Web of Science ®Google Scholar
• Welle S, Tawil R, Thornton CA. Sex-related differences in gene expression in human skeletal muscle. PLoS One. 2008;3:e1385.
   PubMed Web of Science ®Google Scholar
• Maher AC, Fu MH, Isfort RJ, et al. Sex differences in global mRNA content of human skeletal muscle. PLoS One. 2009;4:e6335.
   PubMed Web of Science ®Google Scholar
• Roth SM, Ferrell RE, Peters DG, et al. Influence of age, sex, and strength training on human muscle gene expression determined by microarray. Physiol Genomics. 2002;10:181–190.
   PubMed Web of Science ®Google Scholar
• Lindholm ME, Huss M, Solnestam BW, et al. The human skeletal muscle transcriptome: sex differences, alternative splicing, and tissue homogeneity assessed with RNA sequencing. Faseb J. 2014a;28:4571–4581.
   PubMed Web of Science ®Google Scholar
• Hargreaves M. Exercise and gene expression. Prog Mol Biol Transl Sci. 2015;135:457–469.
   PubMed Web of Science ®Google Scholar
• Baar K, Wende AR, Jones TE, et al. Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1. Faseb J. 2002;16:1879–1886.
   PubMed Web of Science ®Google Scholar
• Roepstorff C, Thiele M, Hillig T, et al. Higher skeletal muscle alpha2AMPK activation and lower energy charge and fat oxidation in men than in women during submaximal exercise. J Physiol. 2006b;574:125–138.
   PubMed Web of Science ®Google Scholar
• Fu M-H-H, Maher AC, Hamadeh MJ, et al. Exercise, sex, menstrual cycle phase, and 17β-estradiol influence metabolism-related genes in human skeletal muscle. Physiol Genomics. 2009;40:34–47.
   PubMed Web of Science ®Google Scholar
• Peters SJ, Samjoo IA, Devries MC, et al. Perilipin family (PLIN) proteins in human skeletal muscle: the effect of sex, obesity, and endurance training. Appl Physiol Nutr Metab. 2012;37:724–735.
   PubMed Web of Science ®Google Scholar
• Roepstorff C, Schjerling P, Vistisen B, et al. Regulation of oxidative enzyme activity and eukaryotic elongation factor 2 in human skeletal muscle: influence of gender and exercise. Acta Physiol Scand. 2005;184:215–224.
   PubMedGoogle Scholar
• Roepstorff C, Donsmark M, Thiele M, et al. Sex differences in hormone-sensitive lipase expression, activity, and phosphorylation in skeletal muscle at rest and during exercise. Am J Physiol Endocrinol Metab. 2006a;291:E1106–14.
   PubMed Web of Science ®Google Scholar
• Lindholm ME, Giacomello S, Solnestam BW, et al. The impact of endurance training on human skeletal muscle memory, global isoform expression and novel transcripts. PLoS Genet. 2016;12:e1006294.
   PubMed Web of Science ®Google Scholar
• Zadro JR, Shirley D, Andrade TB, et al. The beneficial effects of physical activity: is it down to your genes? A systematic review and meta-analysis of twin and family studies. Sports Med Open. 2017;3:4.
   PubMedGoogle Scholar
• International human genome sequencing C, Lander ES, Linton LM, et al. Initial sequencing and analysis of the human genome. Nature. 2001;409:860.
   PubMed Web of Science ®Google Scholar
• Wang G, Padmanabhan S, Wolfarth B, et al. Genomics of elite sporting performance: what little we know and necessary advances. Adv Genet. 2013;47:550–5. Elsevier.
   PubMed Web of Science ®Google Scholar
• Mattsson CM, Wheeler MT, Waggott D, et al. Sports genetics moving forward: lessons learned from medical research. Physiol Genomics. 2016;48:175–182.
   PubMed Web of Science ®Google Scholar
• Ma F. The Association of Sport Performance with ACE and ACTN3 Genetic Polymorphisms: A Systematic Review and Meta-Analysis. PloS one. 2013;8:e54685.
   Google Scholar
• Druzhevskaya AM, Ahmetov II, Astratenkova IV, et al. Association of the ACTN3 R577X polymorphism with power athlete status in Russians. Eur J Appl Physiol. 2008;103:631–634.
   PubMed Web of Science ®Google Scholar
• Clarkson PM, Devaney JM, Gordish-Dressman H, et al. ACTN3 genotype is associated with increases in muscle strength in response to resistance training in women. J Appl Physiol. 2005;99:154–163.
   PubMed Web of Science ®Google Scholar
• Eynon N, Hanson ED, Lucia A, et al. Genes for elite power and sprint performance: ACTN3 leads the way. Sports Med. 2013;43:803–817.
   PubMed Web of Science ®Google Scholar
• Yang N, Macarthur DG, Gulbin JP, et al. ACTN3 Genotype Is Associated with Human Elite Athletic Performance. Am J Hum Genet. 2003;73:627–631.
   PubMed Web of Science ®Google Scholar
• Shang X, Huang C, Chang Q, et al. Association between the ACTN3 R577X polymorphism and female endurance athletes in China. Int J Sports Med. 2010;31:913–916.
   PubMed Web of Science ®Google Scholar
• Macarthur DG, North KN. A gene for speed? the evolution and function of α‐actinin‐3. Bioessays. 2004;26:786–795.
   PubMed Web of Science ®Google Scholar
• Williams AG, Rayson MP, Jubb M, et al. The ACE gene and muscle performance. Nature. 2000;403:614.
   PubMed Web of Science ®Google Scholar
• Yan X, Dvir N, Jacques M, et al. The ACE I/D gene variant predicts ACE enzyme content in blood but not the ACE, UCP2 and UCP3 protein content in human skeletal muscle in the Gene SMART study. J Appl Physiol (1985). 2018.
   Web of Science ®Google Scholar
• Min S-K, Takahashi K, Ishigami H, et al. Is there a gender difference between ACE gene and race distance? Appl Physiol Nutr Metab. 2009;34:926–932.
   PubMed Web of Science ®Google Scholar
• Ma F, Yang Y, Li X, et al. The Association of Sport Performance with ACE and ACTN3 Genetic Polymorphisms: A Systematic Review and Meta-Analysis. PLoS ONE. 2013;8:e54685.
   PubMed Web of Science ®Google Scholar
• Woods DR, Humphries SE, Montgomery HE. The ACE I/D Polymorphism and Human Physical Performance. Trends Endocrinol Metab. 2000;11:416–420.
   PubMed Web of Science ®Google Scholar
• Myerson S, Hemingway H, Budget R, et al. Human angiotensin I-converting enzyme gene and endurance performance. J Appl Physiol. 1999;87:1313–1316.
   PubMed Web of Science ®Google Scholar
• Gómez-Gallego F, Santiago C, Morán M, et al. The I allele of the ACE gene is associated with improved exercise capacity in women with McArdle disease. Br J Sports Med. 2008;42:134–140.
   PubMed Web of Science ®Google Scholar
• Montgomery HE, Marshall R, Hemingway H, et al. Human gene for physical performance. Nature. 1998;393:221.
   PubMed Web of Science ®Google Scholar
• Puthucheary Z, Skipworth JRA, Rawal J, et al. The ACE Gene and Human Performance. Sports Med. 2011;41:433–448.
   PubMed Web of Science ®Google Scholar
• Charbonneau DE, Hanson ED, Ludlow AT, et al. ACE Genotype and the Muscle Hypertrophic and Strength Responses to Strength Training. Med Sci Sports Exerc. 2008;40:677–683.
   PubMed Web of Science ®Google Scholar
• Higaki J, Baba S, Katsuya T, et al. Deletion allele of angiotensin-converting enzyme gene increases risk of essential hypertension in Japanese men: the Suita Study. Circulation. 2000;101:2060–2065.
   PubMed Web of Science ®Google Scholar
• Bouchard C, Sarzynski MA, Rice TK, et al. Genomic predictors of the maximal O2 uptake response to standardized exercise training programs. J Appl Physiol. 2011;110:1160–1170.
   PubMed Web of Science ®Google Scholar
• Verweij N, VAN DE VEGTE YJ, VAN DER HARST P. Genetic study links components of the autonomous nervous system to heart-rate profile during exercise. Nat Commun. 2018;9:898.
   PubMed Web of Science ®Google Scholar
• Willems SM, Wright DJ, Day FR, et al. Large-scale GWAS identifies multiple loci for hand grip strength providing biological insights into muscular fitness. Nat Commun. 2017;8:16015.
   PubMed Web of Science ®Google Scholar
• Ramirez J, Duijvenboden SV, Ntalla I, et al. Thirty loci identified for heart rate response to exercise and recovery implicate autonomic nervous system. Nat Commun. 2018;9:1947.
   PubMed Web of Science ®Google Scholar
• Khramtsova EA, Davis LK, Stranger BE. The role of sex in the genomics of human complex traits. Nature Reviews Genetics. 2019;20:173-90
   Google Scholar
• Bird A. Perceptions of epigenetics. Nature. 2007;447:396.
   PubMed Web of Science ®Google Scholar
• Voisin S, Eynon N, Yan X, et al. Exercise training and DNA methylation in humans. Acta Physiol (Oxf). 2015;213:39–59.
   PubMed Web of Science ®Google Scholar
• Handy DE, Castro R, Loscalzo J. Epigenetic modifications: basic mechanisms and role in cardiovascular disease. Circulation. 2011;123:2145–2156.
   PubMed Web of Science ®Google Scholar
• Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet. 2003;33(Suppl):245–254.
   PubMed Web of Science ®Google Scholar
• Hicks SD, Jacob P, Middleton FA, et al. Distance running alters peripheral microRNAs implicated in metabolism, fluid balance, and myosin regulation in a sex-specific manner. Physiol Genomics. 2018;50:658–667.
   PubMed Web of Science ®Google Scholar
• Sugathan A, Waxman DJ. Genome-wide analysis of chromatin states reveals distinct mechanisms of sex-dependent gene regulation in male and female mouse liver. Mol Cell Biol. 2013;33:3594–3610.
   PubMed Web of Science ®Google Scholar
• Guo L, Liang T, Yu J, et al. A comprehensive analysis of miRNA/isomiR expression with gender difference. PloS One. 2016;11:e0154955.
   PubMed Web of Science ®Google Scholar
• Mccarthy NS, Melton PE, Cadby G, et al. Meta-analysis of human methylation data for evidence of sex-specific autosomal patterns. BMC Genomics. 2014;15:981.
   PubMed Web of Science ®Google Scholar
• Boks MP, Derks EM, Weisenberger DJ, et al. The relationship of DNA methylation with age, gender and genotype in twins and healthy controls. PloS One. 2009;4:e6767.
   PubMed Web of Science ®Google Scholar
• Liu J, Morgan M, Hutchison K, et al. A study of the influence of sex on genome wide methylation. PloS One. 2010b;5:e10028.
   PubMed Web of Science ®Google Scholar
• Tsai H-W, Grant PA, Rissman EF. Sex differences in histone modifications in the neonatal mouse brain. Epigenetics. 2009;4:47–53.
   PubMed Web of Science ®Google Scholar
• Nielsen S, Hvid T, Kelly M, et al. Muscle specific miRNAs are induced by testosterone and independently upregulated by age. Front Physiol. 2013;4:394.
   PubMed Web of Science ®Google Scholar
• El-Maarri O, Becker T, Junen J, et al. Gender specific differences in levels of DNA methylation at selected loci from human total blood: a tendency toward higher methylation levels in males. Hum Genet. 2007;122:505–514.
   PubMed Web of Science ®Google Scholar
• Howlett KF, Mcgee SL. Epigenetic regulation of skeletal muscle metabolism. Clin Sci (Lond). 2016;130:1051–1063.
   PubMed Web of Science ®Google Scholar
• Ntanasis-Stathopoulos J, Tzanninis J, Philippou A, et al. Epigenetic regulation on gene expression induced by physical exercise. J Musculoskelet Neuronal Interact. 2013;13:133–146.
   PubMed Web of Science ®Google Scholar
• Zacharewicz E, Lamon S, Russell AP. MicroRNAs in skeletal muscle and their regulation with exercise, ageing, and disease. Front Physiol. 2013;4:266.
   PubMed Web of Science ®Google Scholar
• Denham J, Marques FZ, O‘Brien BJ, et al. Exercise: putting action into our epigenome. Sports Med. 2014;44:189–209.
   PubMed Web of Science ®Google Scholar
• Pareja-Galeano H, Sanchis-Gomar F, García-Giménez JL. Physical Exercise and Epigenetic Modulation: elucidating Intricate Mechanisms. Sports Med. 2014;44:429–436.
   PubMed Web of Science ®Google Scholar
• Panzeri I, Pospisilik JA. Epigenetic control of variation and stochasticity in metabolic disease. Mol Metab. 2018;14:26–38.
   PubMed Web of Science ®Google Scholar
• Kanwal R, Gupta K, Gupta S. Cancer epigenetics: an introduction. Methods Mol Biol. 2015;1238:3–25.
   PubMedGoogle Scholar
• Fogelholm M. Physical activity, fitness and fatness: relations to mortality, morbidity and disease risk factors. A systematic review. Obesity Rev. 2010;11:202–221.
   PubMed Web of Science ®Google Scholar
• Bird AP, Wolffe AP. Methylation-Induced Repression— belts, Braces, and Chromatin. Cell. 1999;99:451–454.
   PubMed Web of Science ®Google Scholar
• 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;61:3322–3332.
   PubMed Web of Science ®Google Scholar
• Barrès R, Osler ME, Yan J, et al. Non-CpG methylation of the PGC-1α promoter through DNMT3B controls mitochondrial density. Cell Metab. 2009;10:189–198.
   PubMed Web of Science ®Google Scholar
• Xiao Y, Word B, Starlard-Davenport A, et al. Age and gender affect DNMT3a and DNMT3b expression in human liver. Cell Biol Toxicol. 2008;24:265–272.
   PubMed Web of Science ®Google Scholar
• Tsumagari K, Baribault C, Terragni J, et al. Early de novo DNA methylation and prolonged demethylation in the muscle lineage. Epigenetics. 2013;8:317–332.
   PubMed Web of Science ®Google Scholar
• Hadad N, Masser DR, Logan S, et al. Absence of genomic hypomethylation or regulation of cytosine-modifying enzymes with aging in male and female mice. Epigenetics Chromatin. 2016;9:30.
   PubMed Web of Science ®Google Scholar
• Davegårdh C, Wedin EH, Broholm C, et al. Sex influences DNA methylation and gene expression in human skeletal muscle myoblasts and myotubes. Stem Cell Res Ther. 2019;10:26.
   PubMed Web of Science ®Google Scholar
• EL KHATTABI LA, Backer S, Pinard A, et al. A genome-wide search for new imprinted genes in the human placenta identifies DSCAM as the first imprinted gene on chromosome 21. Eur J Hum Genet. 2019;27:49.
   PubMed Web of Science ®Google Scholar
• Reik W, Walter J. Genomic imprinting: parental influence on the genome. Nat Rev Genet. 2001;2:21.
   PubMed Web of Science ®Google Scholar
• Abramowitz LK, Bartolomei MS. Genomic imprinting: recognition and marking of imprinted loci. Curr Opin Genet Dev. 2012;22:72–78.
   PubMed Web of Science ®Google Scholar
• Kong A, Steinthorsdottir V, Masson G, et al. Parental origin of sequence variants associated with complex diseases. Nature. 2009;462:868–874.
   PubMed Web of Science ®Google Scholar
• Chalk TE, M BROWN W. Exercise epigenetics and the fetal origins of disease. Epigenomics. 2014;6:469–472.
   PubMed Web of Science ®Google Scholar
• Gilbert JS, Nijland MJ. Sex differences in the developmental origins of hypertension and cardiorenal disease. Am J Physiol Regul Integr Comp Physiol. 2008;295:R1941–R1952.
   PubMed Web of Science ®Google Scholar
• Intapad S, Ojeda NB, Dasinger JH, et al. Sex differences in the developmental origins of cardiovascular disease. Physiology. 2014;29:122–132.
   PubMed Web of Science ®Google Scholar
• Li B, Carey M, Workman JL. The role of chromatin during transcription. Cell. 2007;128:707–719.
   PubMed Web of Science ®Google Scholar
• Mcgee SL, Hargreaves M. Histone modifications and exercise adaptations. J Appl Physiol. 2011;110:258–263.
   PubMed Web of Science ®Google Scholar
• 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–E704.
   PubMed Web of Science ®Google Scholar
• Mckinsey TA, Zhang C-L, Lu J, et al. Signal-dependent nuclear export of a histone deacetylase regulates muscle differentiation. Nature. 2000;408:106.
   PubMed Web of Science ®Google Scholar
• Mcgee SL, Hargreaves M. Exercise and skeletal muscle glucose transporter 4 expression: molecular mechanisms. Clin Exp Pharmacol Physiol. 2006;33:395–399.
   PubMed Web of Science ®Google Scholar
• Mcgee SL, Fairlie E, Garnham AP, et al. Exercise-induced histone modifications in human skeletal muscle. J Physiol. 2009;587:5951–5958.
   PubMed Web of Science ®Google Scholar
• Gaur V, Connor T, Sanigorski A, et al. Disruption of the class IIa HDAC corepressor complex increases energy expenditure and lipid oxidation. Cell Rep. 2016;16:2802–2810.
   PubMed Web of Science ®Google Scholar
• Vissing K, Mcgee SL, Roepstorff C, et al. Effect of sex differences on human MEF2 regulation during endurance exercise. Am J Physiol Endocrinol Metab. 2008;294:E408–15.
   PubMed Web of Science ®Google Scholar
• Kim MY, Hsiao SJ, Kraus WL. A role for coactivators and histone acetylation in estrogen receptor alpha-mediated transcription initiation. Embo J. 2001;20:6084–6094.
   PubMed Web of Science ®Google Scholar
• Sun J-M, Chen HY, Davie JR. Effect of estradiol on histone acetylation dynamics in human breast cancer cells. J Biol Chem. 2001;276:49435-42.
   Web of Science ®Google Scholar
• Ribas V, Drew BG, Zhou Z, et al. Skeletal muscle action of estrogen receptor alpha is critical for the maintenance of mitochondrial function and metabolic homeostasis in females. Sci Transl Med. 2016;8:334ra54.
   PubMed Web of Science ®Google Scholar
• Mcdonnell E, Crown SB, Fox DB, et al. Lipids reprogram metabolism to become a major carbon source for histone acetylation. Cell Rep. 2016;17:1463–1472.
   PubMed Web of Science ®Google Scholar
• Guo H, Ingolia NT, Weissman JS, et al. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature. 2010;466:835–840.
   PubMed Web of Science ®Google Scholar
• Humphreys DT, Westman BJ, Martin DI, et al. MicroRNAs control translation initiation by inhibiting eukaryotic initiation factor 4E/cap and poly(A) tail function. Proc Natl Acad Sci U S A. 2005;102:16961–16966.
   PubMed Web of Science ®Google Scholar
• Pillai RS, Bhattacharyya SN, Artus CG, et al. Inhibition of translational initiation by Let-7 MicroRNA in human cells. Science. 2005;309:1573–1576.
   PubMed Web of Science ®Google Scholar
• Tonevitsky AG, Maltseva DV, Abbasi A, et al. Dynamically regulated miRNA-mRNA networks revealed by exercise. BMC Physiol. 2013;13:9.
   PubMedGoogle Scholar
• Kirby TJ, Mccarthy JJ. MicroRNAs in skeletal muscle biology and exercise adaptation. Free Radic Biol Med. 2013;64:95–105.
   PubMed Web of Science ®Google Scholar
• Russell AP, Lamon S. Exercise, Skeletal Muscle and Circulating microRNAs. Prog Mol Biol Transl Sci. 2015;135:471–496.
   PubMed Web of Science ®Google Scholar
• Mccarthy JJ. The MyomiR Network in Skeletal Muscle Plasticity. Exerc Sport Sci Rev. 2011;39:150–154.
   PubMed Web of Science ®Google Scholar
• 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;57:528–538.
   PubMed Web of Science ®Google Scholar
• Nielsen S, Scheele C, Yfanti C, et al. Muscle specific microRNAs are regulated by endurance exercise in human skeletal muscle. J Physiol. 2010;588:4029–4037.
   PubMed Web of Science ®Google Scholar
• Aguiar AS, Speck AE, Amaral IM, et al. The exercise sex gap and the impact of the estrous cycle on exercise performance in mice. Sci Rep. 2018;8:10742.
   PubMed Web of Science ®Google Scholar
• Costello JT, Bieuzen F, Bleakley CM. Where are all the female participants in Sports and Exercise Medicine research? Eur J Sport Sci. 2014;14:847–851.
   PubMed Web of Science ®Google Scholar
• Yan X, Eynon N, Papadimitriou ID, et al. The gene SMART study: method, study design, and preliminary findings. BMC Genomics. 2017;18:821.
   PubMed Web of Science ®Google Scholar