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RESEARCH PAPERS

An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training

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Pages 1557-1569 | Received 02 Jul 2014, Accepted 23 Oct 2014, Published online: 27 Jan 2015

References

  • Matheson GO, Klügl M, Engebretsen L, Bendiksen F, Blair SN, Börjesson M, Budgett R, Derman W, Erdener U, Ioannidis JPA, et al. Prevention and management of non-communicable disease: the IOC consensus statement, Lausanne 2013. Sports Med 2013; 43:1075-88; PMID:24129783; http://dx.doi.org/10.1007/s40279-013-0104-3
  • Coffey VG, Hawley JA. The Molecular Bases of Training Adaptation. Sports Med 2007; 37:737-63; PMID:17722947; http://dx.doi.org/10.2165/00007256-200737090-00001
  • Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 2012; 13:484-92; PMID:22641018; http://dx.doi.org/10.1038/nrg3230
  • Heyn H, Esteller M. DNA methylation profiling in the clinic: applications and challenges. Nat Rev Genet 2012; 13:679-92; PMID:22945394; http://dx.doi.org/10.1038/nrg3270
  • Jones PA, Baylin SB. The epigenomics of cancer. Cell 2007; 128:683-92; PMID:17320506; http://dx.doi.org/10.1016/j.cell.2007.01.029
  • Feinberg AP. Epigenetics at the epicenter of modern medicine. JAMA 2008; 299:1345-50; PMID:18349095; http://dx.doi.org/10.1001/jama.299.11.1345
  • Teschendorff AE, West J, Beck S. Age-associated epigenetic drift: implications, and a case of epigenetic thrift? Human Molecular Genetics 2013; 22:R7-R15; PMID:23918660; http://dx.doi.org/10.1093/hmg/ddt375
  • Bjornsson HT, Sigurdsson MI, Fallin MD, Irizarry RA, Aspelund T, Cui H, Yu W, Rongione MA, Ekström TJ, Harris TB, et al. Intra-individual change over time in DNA methylation with familial clustering. JAMA 2008; 299:2877-83; PMID:18577732; http://dx.doi.org/10.1001/jama.299.24.2877
  • Feil R, Fraga MF. Epigenetics and the environment: emerging patterns and implications. Nat Rev Genet 2011; 13:97-109.
  • Lim U, Song M-A. Dietary and Lifestyle Factors of DNA Methylation. In: Methods in Molecular Biology. Totowa, NJ: Humana Press; 2012. pages 359-76. Available from: .
  • Jacobsen SC, Brøns C, Bork-Jensen J, Ribel-Madsen R, Yang B, Lara E, Hall E, Calvanese V, Nilsson E, Jørgensen SW, et al. Effects of short-term high-fat overfeeding on genome-wide DNA methylation in the skeletal muscle of healthy young men. Diabetologia 2012; 55:3341-9; PMID:22961225; http://dx.doi.org/10.1007/s00125-012-2717-8
  • Barrès R, Yan J, Egan B, Treebak JT, Rasmussen M, Fritz T, Caidahl K, Krook A, O’Gorman DJ, Zierath JR. Acute Exercise Remodels Promoter Methylation in Human Skeletal Muscle. Cell Metab 2012; 15:405-11; http://dx.doi.org/10.1016/j.cmet.2012.01.001
  • Nitert MD, Dayeh T, Volkov P, Elgzyri T, Hall E, Nilsson E, Yang BT, Lang S, Parikh H, Wessman Y, 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; PMID:23028138; http://dx.doi.org/10.2337/db11-1653
  • Rönn T, Volkov P, Davegårdh C, Dayeh T, Hall E, Olsson AH, Nilsson E, Tornberg Å, Dekker Nitert M, Eriksson K-F, et al. A Six Months Exercise Intervention Influences the Genome-wide DNA Methylation Pattern in Human Adipose Tissue. PLoS Genet 2013; 9:e1003572.
  • Williams RS, Neufer PD. Regulation of gene expression in skeletal muscle by contractile activity. In: Rowell LB, Shepherd JT, editors. Exercise: regulation and integration of multiple systems. Published for the American Physiological Society by Oxford University Press; 1996. pages 1124-50.
  • Karimi M, Johansson S, Stach D, Corcoran M, Grandér D, Schalling M, Bakalkin G, Lyko F, Larsson C, Ekström TJ. LUMA (LUminometric Methylation Assay)-a high throughput method to the analysis of genomic DNA methylation. Exp Cell Res 2006; 312:1989-95; PMID:16624287; http://dx.doi.org/10.1016/j.yexcr.2006.03.006
  • Ernst J, Kheradpour P, Mikkelsen TS, Shoresh N, Ward LD, Epstein CB, Zhang X, Wang L, Issner R, Coyne M, et al. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 2011; 473:43-9; PMID:21441907; http://dx.doi.org/10.1038/nature09906
  • Wiench M, John S, Baek S, Johnson TA, Sung M-H, Escobar T, Simmons CA, Pearce KH, Biddie SC, Sabo PJ, et al. DNA methylation status predicts cell type-specific enhancer activity. EMBO J 2011; 30:3028-39; PMID:21701563; http://dx.doi.org/10.1038/emboj.2011.210
  • Aran D, Sabato S, Hellman A. DNA methylation of distal regulatory sites characterizes dysregulation of cancer genes. Genome Biol 2013; 14:R21; PMID:23497655; http://dx.doi.org/10.1186/gb-2013-14-3-r21
  • Stadler MB, Murr R, Burger L, Ivanek R, Lienert F, Schöler A, van Nimwegen E, Wirbelauer C, Oakeley EJ, Gaidatzis D, et al. DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 2011; 480:490-5; PMID:22170606
  • Randi AM, Sperone A, Dryden NH, Birdsey GM. Regulation of angiogenesis by ETS transcription factors. Biochem Soc Trans 2009; 37:1248-53; PMID:19909256; http://dx.doi.org/10.1042/BST0371248
  • Chew A, Buck EA, Peretz S, Sirugo G, Rinaldo P, Isaya G. Cloning, expression, and chromosomal assignment of the human mitochondrial intermediate peptidase gene (MIPEP). Genomics 1997; 40:493-6; PMID:9073519; http://dx.doi.org/10.1006/geno.1996.4586
  • Wang L, Shen M, Wang F, Ma L. GRK5 ablation contributes to insulin resistance. Biochem Biophys Res Commun 2012; 429:99-104; PMID:23111327; http://dx.doi.org/10.1016/j.bbrc.2012.10.077
  • Liu Y, Aryee MJ, Padyukov L, Fallin MD, Hesselberg E, Runarsson A, Reinius L, Acevedo N, Taub M, Ronninger M, et al. Epigenome-wide association data implicate DNA methylation as an intermediary of genetic risk in rheumatoid arthritis. Nat Biotechnol 2013; 31:142-7; PMID:23334450; http://dx.doi.org/10.1038/nbt.2487
  • Mason CC, Hanson RL, Ossowski V, Bian L, Baier LJ, Krakoff J, Bogardus C. Bimodal distribution of RNA expression levels in human skeletal muscle tissue. BMC Genomics 2011; 12:98; PMID:21299892; http://dx.doi.org/10.1186/1471-2164-12-98
  • Meruvu S, Hugendubler L, Mueller E. Regulation of Adipocyte Differentiation by the Zinc Finger Protein ZNF638. J Biol Chem 2011; 286:26516-23; PMID:21602272; http://dx.doi.org/10.1074/jbc.M110.212506
  • Sakai T, Liu L, Teng X, Mukai-Sakai R, Shimada H, Kaji R, Mitani T, Matsumoto M, Toida K, Ishimura K, et al. Nucling recruits Apaf-1/pro-caspase-9 complex for the induction of stress-induced apoptosis. J Biol Chem 2004; 279:41131-40; PMID:15271982; http://dx.doi.org/10.1074/jbc.M402902200
  • Timmons JA, Knudsen S, Rankinen T, Koch LG, Sarzynski M, Jensen T, Keller P, Scheele C, Vollaard NBJ, Nielsen S, 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; PMID:20133430; http://dx.doi.org/10.1152/japplphysiol.01295.2009
  • Rakyan VK, Down TA, Balding DJ, Beck S. Epigenome-wide association studies for common human diseases. Nat Rev Genet 2011; 12:529-41; PMID:21747404; http://dx.doi.org/10.1038/nrg3000
  • Michels KB. Epigenetic epidemiology. Springer; 2012.
  • Houseman EA, Accomando WP, Koestler DC, Christensen BC, Marsit CJ, Nelson HH, Wiencke JK, Kelsey KT. DNA methylation arrays as surrogate measures of cell mixture distribution. BMC Bioinformatics 2012; 13:86; PMID:22568884; http://dx.doi.org/10.1186/1471-2105-13-86
  • Gustafsson T. Vascular remodelling in human skeletal muscle. Biochem Soc Trans 2011; 39:1628-32; PMID:22103498; http://dx.doi.org/10.1042/BST20110720
  • Harris RA, Wang T, Coarfa C, Nagarajan RP, Hong C, Downey SL, Johnson BE, Fouse SD, Delaney A, Zhao Y, et al. Comparison of sequencing-based methods to profile DNA methylation and identification of monoallelic epigenetic modifications. Nat Biotechnol 2010; 28:1097-105; PMID:20852635; http://dx.doi.org/10.1038/nbt.1682
  • Robinson MD, Stirzaker C, Statham AL, Coolen MW, Song JZ, Nair SS, Strbenac D, Speed TP, Clark SJ. Evaluation of affinity-based genome-wide DNA methylation data: effects of CpG density, amplification bias, and copy number variation. Genome Research 2010; 20:1719-29; PMID:21045081; http://dx.doi.org/10.1101/gr.110601.110
  • Bock C, Tomazou EM, Brinkman AB, Müller F, Simmer F, Gu H, Jäger N, Gnirke A, Stunnenberg HG, Meissner A. Quantitative comparison of genome-wide DNA methylation mapping technologies. Nat Biotechnol 2010; 28:1106-14; PMID:20852634; http://dx.doi.org/10.1038/nbt.1681
  • Keller P, Vollaard NBJ, Gustafsson T, Gallagher IJ, Sundberg CJ, Rankinen T, Britton SL, Bouchard C, Koch LG, Timmons JA. A transcriptional map of the impact of endurance exercise training on skeletal muscle phenotype. J Appl Physiol 2011; 110:46-59; PMID:20930125; http://dx.doi.org/10.1152/japplphysiol.00634.2010
  • Papandreou I, Cairns RA, Fontana L, Lim AL, Denko NC. HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption. Cell Metab 2006; 3:187-97; PMID:16517406; http://dx.doi.org/10.1016/j.cmet.2006.01.012
  • Lindholm ME, Fischer H, Poellinger L, Johnson RS, Gustafsson T, Sundberg CJ, Rundqvist H. Negative regulation of HIF in skeletal muscle of elite endurance athletes: a tentative mechanism promoting oxidative metabolism. Am J Physiol Regul Integr Comp Physiol 2014; 307:R248-55; PMID:24898836; http://dx.doi.org/10.1152/ajpregu.00036.2013
  • Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF, Ye Z, Lee LK, Stuart RK, Ching CW, et al. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 2009; 459:108-12; PMID:19295514; http://dx.doi.org/10.1038/nature07829
  • Gundersen K. Excitation-transcription coupling in skeletal muscle: the molecular pathways of exercise. Biol Rev Camb Philos Soc 2011; 86:564-600; PMID:21040371; http://dx.doi.org/10.1111/j.1469-185X.2010.00161.x
  • Amat R, Planavila A, Chen SL, Iglesias R, Giralt M, Villarroya F. SIRT1 controls the transcription of the peroxisome proliferator-activated receptor-gamma Co-activator-1alpha (PGC-1alpha) gene in skeletal muscle through the PGC-1alpha autoregulatory loop and interaction with MyoD. J Biol Chem 2009; 284:21872-80; PMID:19553684; http://dx.doi.org/10.1074/jbc.M109.022749
  • Potthoff MJ, Olson EN. MEF2: a central regulator of diverse developmental programs. Development 2007; 134:4131-40; PMID:17959722; http://dx.doi.org/10.1242/dev.008367
  • Yu W, Gius D, Onyango P, Muldoon-Jacobs K, Karp J, Feinberg AP, Cui H. Epigenetic silencing of tumour suppressor gene p15 by its antisense RNA. Nature 2008; 451:202-6; PMID:18185590; http://dx.doi.org/10.1038/nature06468
  • Fredriksson K, Tjäder I, Keller P, Petrovic N, Ahlman B, Scheele C, Wernerman J, Timmons JA, Rooyackers O. Dysregulation of mitochondrial dynamics and the muscle transcriptome in ICU patients suffering from sepsis induced multiple organ failure. PLoS ONE 2008; 3:e3686; PMID:18997871; http://dx.doi.org/10.1371/journal.pone.0003686
  • Mootha VK, Handschin C, Arlow D, Xie X, St Pierre J, Sihag S, Yang W, Altshuler D, Puigserver P, Patterson N, et al. Erralpha and Gabpa/b specify PGC-1alpha-dependent oxidative phosphorylation gene expression that is altered in diabetic muscle. Proc Natl Acad Sci USA 2004; 101:6570-5; PMID:15100410; http://dx.doi.org/10.1073/pnas.0401401101
  • Oettgen P. Regulation of vascular inflammation and remodeling by ETS factors. Circul Res 2006; 99:1159-66; PMID:17122446; http://dx.doi.org/10.1161/01.RES.0000251056.85990.db
  • Timmons JA, Sundberg CJ. Oligonucleotide microarray expression profiling: human skeletal muscle phenotype and aerobic exercise training. IUBMB Life 2006; 58:15-24; PMID:16540428; http://dx.doi.org/10.1080/15216540500507390
  • Hollenhorst PC, Shah AA, Hopkins C, Graves BJ. Genome-wide analyses reveal properties of redundant and specific promoter occupancy within the ETS gene family. Genes Dev 2007; 21:1882-94; PMID:17652178; http://dx.doi.org/10.1101/gad.1561707
  • Lu C, Thompson CB. Metabolic Regulation of Epigenetics. Cell Metab 2012; 16:9-17; PMID:22768835; http://dx.doi.org/10.1016/j.cmet.2012.06.001
  • Bibikova M, Barnes B, Tsan C, Ho V, Klotzle B, Le JM, Delano D, Zhang L, Schroth GP, Gunderson KL, et al. High density DNA methylation array with single CpG site resolution. Genomics 2011; 98:288-95; PMID:21839163; http://dx.doi.org/10.1016/j.ygeno.2011.07.007
  • Marabita F, Almgren M, Lindholm ME, Ruhrmann S, Fagerström-Billai F, Jagodic M, Sundberg CJ, Ekström TJ, Teschendorff AE, TegnEr J, et al. An evaluation of analysis pipelines for DNA methylation profiling using the Illumina HumanMethylation450 BeadChip platform. Epigenetics 2013; 8:333-46; PMID:23422812; http://dx.doi.org/10.4161/epi.24008
  • Teschendorff AE, Marabita F, Lechner M, Bartlett T, TegnEr J, Gomez-Cabrero D, Beck S. A beta-mixture quantile normalization method for correcting probe design bias in Illumina Infinium 450 k DNA methylation data. Bioinformatics (Oxford, England) 2013; 29:189-96; PMID:23175756; http://dx.doi.org/10.1093/bioinformatics/bts680
  • Smyth GK. Linear Models and Empirical Bayes Methods for Assessing Differential Expression in Microarray Experiments. Stat Appl Genet Mol Biol 2004; 3; PMID:16646809; http://dx.doi.org/10.2202/1544-6115.1027
  • Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics (Oxford, England) 2010; 26:139-40; PMID:19910308; http://dx.doi.org/10.1093/bioinformatics/btp616
  • Young MD, Wakefield MJ, Smyth GK, Oshlack A. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 2010; 11:R14; PMID:20132535; http://dx.doi.org/10.1186/gb-2010-11-2-r14
  • Luo W, Brouwer C. Pathview: an R/Bioconductor package for pathway-based data integration and visualization. Bioinformatics (Oxford, England) 2013; 29:1830-1; PMID:23740750; http://dx.doi.org/10.1093/bioinformatics/btt285
  • Lindholm ME, Huss M, Solnestam BW, Kjellqvist S, Lundeberg J, Sundberg CJ. The human skeletal muscle transcriptome: sex differences, alternative splicing, and tissue homogeneity assessed with RNA sequencing. FASEB J 2014.
  • Basso K, Margolin AA, Stolovitzky G, Klein U, Dalla-Favera R, Califano A. Reverse engineering of regulatory networks in human B cells. Nat Genet 2005; 37:382-90; PMID:15778709; http://dx.doi.org/10.1038/ng1532