Genome-Wide Sperm DNA Methylation Changes After 3 Months of Exercise Training in Humans

References

• Jones PA , TakaiD . The role of DNA methylation in mammalian epigenetics . Science293 ( 5532 ), 1068 – 1070 ( 2001 ).
   PubMed Web of Science ®Google Scholar
• Wu H , TaoJ , SunYE . Regulation and function of mammalian DNA methylation patterns: a genomic perspective . Brief. Funct. Genomics11 ( 3 ), 240 – 250 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Angers B , CastonguayE , MassicotteR . Environmentally induced phenotypes and DNA methylation: how to deal with unpredictable conditions until the next generation and after . Mol. Ecol.19 ( 7 ), 1283 – 1295 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Flores KB , WolschinF , AmdamGV . The role of methylation of DNA in environmental adaptation . Integr. Comp. Biol.53 ( 2 ), 359 – 372 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Cheung HH , LeeTL , DavisAJ , TaftDH , RennertOM , ChanWY . Genome-wide DNA methylation profiling reveals novel epigenetically regulated genes and non-coding rnas in human testicular cancer . Br. J. Cancer102 ( 2 ), 419 – 427 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Kanai Y . Genome-wide DNA methylation profiles in precancerous conditions and cancers . Cancer Sci.101 ( 1 ), 36 – 45 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Weber M , DaviesJJ , WittigDet al. Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells . Nat. Genet.37 ( 8 ), 853 – 862 ( 2005 ).
   PubMed Web of Science ®Google Scholar
• Zaina S , HeynH , CarmonaFJet al. DNA methylation map of human atherosclerosis . Circ. Cardiovasc. Genet.7 ( 5 ), 692 – 700 ( 2014 ).
   PubMedGoogle Scholar
• Sharma P , GargG , KumarAet al. Genome wide DNA methylation profiling for epigenetic alteration in coronary artery disease patients . Gene541 ( 1 ), 31 – 40 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Toperoff G , AranD , KarkJDet al. Genome-wide survey reveals predisposing diabetes Type 2-related DNA methylation variations in human peripheral blood . Hum. Mol. Genet.21 ( 2 ), 371 – 383 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Volkmar M , DedeurwaerderS , CunhaDAet al. DNA methylation profiling identifies epigenetic dysregulation in pancreatic islets from Type 2 diabetic patients . EMBO J.31 ( 6 ), 1405 – 1426 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Bakulski KM , DolinoyDC , SartorMAet al. Genome-wide DNA methylation differences between late-onset alzheimer’s disease and cognitively normal controls in human frontal cortex . J. Alzheimers Dis.29 ( 3 ), 571 – 588 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Wockner LF , NobleEP , LawfordBRet al. Genome-wide DNA methylation analysis of human brain tissue from schizophrenia patients . Transl. Psychiatry4 , e339 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Nishioka M , BundoM , KoikeSet al. Comprehensive DNA methylation analysis of peripheral blood cells derived from patients with first-episode schizophrenia . J. Hum. Genet.58 ( 2 ), 91 – 97 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Anway MD , CuppAS , UzumcuM , SkinnerMK . Epigenetic transgenerational actions of endocrine disruptors and male fertility . Science308 ( 5727 ), 1466 – 1469 ( 2005 ).
   PubMed Web of Science ®Google Scholar
• Manikkam M , TraceyR , Guerrero-BosagnaC , SkinnerMK . Plastics derived endocrine disruptors (bpa, dehp and dbp) induce epigenetic transgenerational inheritance of obesity, reproductive disease and sperm epimutations . PLoS ONE8 ( 1 ), e55387 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Manikkam M , Guerrero-BosagnaC , TraceyR , HaqueMM , SkinnerMK . Transgenerational actions of environmental compounds on reproductive disease and identification of epigenetic biomarkers of ancestral exposures . PLoS ONE7 ( 2 ), e31901 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Guerrero-Bosagna C , SavenkovaM , HaqueMM , NilssonE , SkinnerMK . Environmentally induced epigenetic transgenerational inheritance of altered sertoli cell transcriptome and epigenome: molecular etiology of male infertility . PLoS ONE8 ( 3 ), e59922 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Michaud EJ , Van VugtMJ , BultmanSJ , SweetHO , DavissonMT , WoychikRP . Differential expression of a new dominant agouti allele (AIAPY) is correlated with methylation state and is influenced by parental lineage . Genes Dev.8 ( 12 ), 1463 – 1472 ( 1994 ).
   PubMed Web of Science ®Google Scholar
• Carone BR , FauquierL , HabibNet al. Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals . Cell143 ( 7 ), 1084 – 1096 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Cooney CA , DaveAA , WolffGL . Maternal methyl supplements in mice affect epigenetic variation and DNA methylation of offspring . J. Nutr.132 ( 8 Suppl. ), S2393 – S2400 ( 2002 ).
   PubMed Web of Science ®Google Scholar
• Ng SF , LinRC , LaybuttDR , BarresR , OwensJA , MorrisMJ . Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring . Nature467 ( 7318 ), 963 – 966 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Jenkins TG , AstonKI , PfluegerC , CairnsBR , CarrellDT . Age-associated sperm DNA methylation alterations: possible implications in offspring disease susceptibility . PLoS Genet.10 ( 7 ), e1004458 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Milekic MH , XinY , O’DonnellAet al. Age-related sperm DNA methylation changes are transmitted to offspring and associated with abnormal behavior and dysregulated gene expression . Mol. Psychiatry doi:10.1038/mp.2014.84. ( 2014 ) ( Epub ahead of print ).
   PubMed Web of Science ®Google Scholar
• Denham J , O’BrienBJ , MarquesFZ , CharcharFJ . Changes in the leukocyte methylome and its effect on cardiovascular related genes after exercise . J. Appl. Physio. ( 1985 ) 118 ( 4 ), 475 – 488 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Nitert MD , DayehT , VolkovPet al. Impact of an exercise intervention on DNA methylation in skeletal muscle from first-degree relatives of patients with Type 2 diabetes . Diabetes61 ( 12 ), 3322 – 3332 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Rowlands DS , PageRA , SukalaWRet al. Multi-omic integrated networks connect DNA methylation and mirna with skeletal muscle plasticity to chronic exercise in Type 2 diabetic obesity . Physiol. Genomics46 ( 20 ), 747 – 765 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Lindholm ME , MarabitaF , Gomez-CabreroDet al. An integrative analysis reveals coordinated reprogramming of the epigenome and the transcriptome in human skeletal muscle after training . Epigenetics9 ( 12 ), 1557 – 1569 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Ronn T , VolkovP , DavegardhCet al. A six months exercise intervention influences the genome-wide DNA methylation pattern in human adipose tissue . PLoS Genet.9 ( 6 ), e1003572 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Khaled MB , MunibuddinA , KhanST , ChoudhariSP , DoiphodeR . Effect of traditional aerobic exercises versus sprint interval training on pulmonary function tests in young sedentary males: a randomised controlled trial . J. Clin. Diagn. Res7 ( 9 ), 1890 – 1893 ( 2013 ).
   PubMedGoogle Scholar
• Macpherson RE , HazellTJ , OlverTD , PatersonDH , LemonPW . Run sprint interval training improves aerobic performance but not maximal cardiac output . Med. Sci. Sports. Exerc43 ( 1 ), 115 – 122 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Cicioni-Kolsky D , LorenzenC , WilliamsMD , KempJG . Endurance and sprint benefits of high-intensity and supramaximal interval training . Eur. J. Sport Sci.13 ( 3 ), 304 – 311 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Sloth M , SlothD , OvergaardK , DalgasU . Effects of sprint interval training on VO2max and aerobic exercise performance: a systematic review and meta-analysis . Scand. J. Med. Sci. Sports23 ( 6 ), e341 – e352 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Denham J , FerosSA , O’BrienBJ . Four weeks of sprint interval training improves 5 km run performance . J. Strength Cond. Res. ( 2015 ) ( Epub ahead of print ).
   PubMedGoogle Scholar
• Mayer W , NiveleauA , WalterJ , FundeleR , HaafT . Demethylation of the zygotic paternal genome . Nature403 ( 6769 ), 501 – 502 ( 2000 ).
   PubMed Web of Science ®Google Scholar
• Kafri T , GaoX , RazinA . Mechanistic aspects of genome-wide demethylation in the preimplantation mouse embryo . Proc. Natl Acad. Sci. USA90 ( 22 ), 10558 – 10562 ( 1993 ).
   PubMed Web of Science ®Google Scholar
• Oswald J , EngemannS , LaneNet al. Active demethylation of the paternal genome in the mouse zygote . Curr. Biol.10 ( 8 ), 475 – 478 ( 2000 ).
   PubMed Web of Science ®Google Scholar
• Morgan HD , SantosF , GreenK , DeanW , ReikW . Epigenetic reprogramming in mammals . Hum. Mol. Genet.14 ( Spec. No. 1 ), R47 – R58 ( 2005 ).
   PubMedGoogle Scholar
• Reik W , DeanW , WalterJ . Epigenetic reprogramming in mammalian development . Science293 ( 5532 ), 1089 – 1093 ( 2001 ).
   PubMed Web of Science ®Google Scholar
• Luttropp K , NordforsL , EkstromTJ , LindL . Physical activity is associated with decreased global DNA methylation in swedish older individuals . Scand. J. Clin. Lab. Invest.73 ( 2 ), 184 – 185 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Barres R , YanJ , EganBet al. Acute exercise remodels promoter methylation in human skeletal muscle . Cell Metab.15 ( 3 ), 405 – 411 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Jenkins TG , AstonKI , CairnsBR , CarrellDT . Paternal aging and associated intraindividual alterations of global sperm 5-methylcytosine and 5-hydroxymethylcytosine levels . Fertil. Steril.100 ( 4 ), 945 – 951 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Barzideh J , ScottRJ , AitkenRJ . Analysis of the global methylation status of human spermatozoa and its association with the tendency of these cells to enter apoptosis . Andrologia45 ( 6 ), 424 – 429 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Guerrero-Bosagna C , SettlesM , LuckerB , SkinnerMK . Epigenetic transgenerational actions of vinclozolin on promoter regions of the sperm epigenome . PLoS ONE5 ( 9 ), pii : e13100 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Nilsson EE , SkinnerMK . Environmentally induced epigenetic transgenerational inheritance of disease susceptibility . Transl. Res.165 ( 1 ), 12 – 17 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Skinner MK , ManikkamM , HaqueMM , ZhangB , SavenkovaMI . Epigenetic transgenerational inheritance of somatic transcriptomes and epigenetic control regions . Genome Biol.13 ( 10 ), R91 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Zhang FF , MorabiaA , CarrollJet al. Dietary patterns are associated with levels of global genomic DNA methylation in a cancer-free population . J. Nutr.141 ( 6 ), 1165 – 1171 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Anderson OS , SantKE , DolinoyDC . Nutrition and epigenetics: an interplay of dietary methyl donors, one-carbon metabolism and DNA methylation . J. Nutr. Biochem.23 ( 8 ), 853 – 859 ( 2012 ).
   PubMed Web of Science ®Google Scholar