Changes in the leukocyte methylome and its effect on cardiovascular-related genes after exercise

Journal of Applied Physiology

Volumn 118, Issue 4, 2015, Pages 475-488

  Denham, Joshua ^a   O'Brien, Brendan J ^a   Marques, Francine Z ^a   Charchar, Fadi J ^a  

^a UNIVERSITY OF BALLARAT   (Australia)

Author keywords

Cholesterol; DNA methylation; Epigenetics; MicroRNA; Sprint interval training

Indexed keywords

EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; LOW DENSITY LIPOPROTEIN; MICRORNA; MIRN21 MICRORNA, HUMAN; MIRN210 MICRORNA, HUMAN;

ADULT; CARDIOVASCULAR SYSTEM; CPG ISLAND; DNA METHYLATION; EXERCISE; GENE EXPRESSION; GENETIC EPIGENESIS; GENETICS; HUMAN; LEUKOCYTE; MALE; METABOLISM; PHYSIOLOGY; PROMOTER REGION; YOUNG ADULT;

ADULT; CARDIOVASCULAR SYSTEM; CPG ISLANDS; DNA METHYLATION; EPIDERMAL GROWTH FACTOR; EPIGENESIS, GENETIC; EXERCISE; GENE EXPRESSION; HUMANS; LEUKOCYTES; LIPOPROTEINS, LDL; MALE; MICRORNAS; PROMOTER REGIONS, GENETIC; RECEPTOR, EPIDERMAL GROWTH FACTOR; YOUNG ADULT;

EID: 84923005662     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00878.2014     Document Type: Article

References (68)

1. Abel JL, Rissman EF. Running-induced epigenetic and gene expression changes in the adolescent brain. Int J Dev Neurosci 31: 382-390, 2013.
2. Aoi W, Naito Y, Mizushima K, Takanami Y, Kawai Y, Ichikawa H, Yoshikawa T. The microRNA miR-696 regulates PGC-1α in mouse skeletal muscle in response to physical activity. Am J Physiol Endocrinol Metab 298: E799-E806, 2010.
3. Babraj JA, Vollaard NB, Keast C, Guppy FM, Cottrell G, Timmons JA. Extremely short duration high intensity interval training substantially improves insulin action in young healthy males. BMC Endocr Disord 9: 3, 2009.
4. Baggish AL, Hale A, Weiner RB, Lewis GD, Systrom D, Wang F, Wang TJ, Chan SY. Dynamic regulation of circulating microRNA during acute exhaustive exercise and sustained aerobic exercise training. J Physiol 589: 3983-3994, 2011.
5. Barres 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 15: 405-411, 2012.
6. Bestor TH. The DNA methyltransferases of mammals. Hum Mol Genet 9: 2395-2402, 2000.
7. Bollati V, Baccarelli A. Environmental epigenetics. Heredity (Edinb) 105: 105-112, 2010.
8. Bostjancic E, Zidar N, Glavac D. MicroRNA microarray expression profiling in human myocardial infarction. Dis Markers 27: 255-268, 2009.
9. Bryan AD, Magnan RE, Hooper AE, Harlaar N, Hutchison KE. Physical activity and differential methylation of breast cancer genes assayed from saliva: a preliminary investigation. Ann Behav Med 45: 89-98, 2013.
10. Burgomaster KA, Howarth KR, Phillips SM, Rakobowchuk M, Macdonald MJ, McGee SL, Gibala MJ. Similar metabolic adaptations during exercise after low volume sprint interval and traditional endurance training in humans. J Physiol 586: 151-160, 2008.
11. Bye A, Rosjo H, Aspenes ST, Condorelli G, Omland T, Wisloff U. Circulating microRNAs and aerobic fitness - the HUNT-Study. PLoS One 8: e57496, 2013.
12. Calvanese V, Fernández AF, Urdinguio RG, Suárez-Alvarez B, Mangas C, Pérez-García V, Bueno C, Montes R, Ramos-Mejía V, Martínez-Camblor P, Ferrero C, Assenov Y, Bock C, Menendez P, Carrera AC, Lopez-Larrea C, Fraga MF. A promoter DNA demethylation landscape of human hematopoietic differentiation. Nucleic Acids Res 40: 116-131, 2012.
13. Chapman MJ, Ginsberg HN, Amarenco P, Andreotti F, Borén J, Catapano AL, Descamps OS, Fisher E, Kovanen PT, Kuivenhoven JA, Lesnik P, Masana L, Nordestgaard BG, Ray KK, Reiner Z, Taskinen MR, Tokgözoglu L, Tybjærg-Hansen A, Watts GF, European Atherosclerosis Society Consensus Panel. Triglyceride-rich lipoproteins and high-density lipoprotein cholesterol in patients at high risk of cardiovascular disease: evidence and guidance for management. Eur Heart J 32: 1345-1361, 2011.
14. Chen KC, Juo SH. MicroRNAs in atherosclerosis. Kaohsiung J Med Sci 28: 631-640, 2012.
15. Cholesterol Treatment Trialists' CTT Collaborators, Mihaylova B, Emberson J, Blackwell L, Keech A, Simes J, Barnes EH, Voysey M, Gray A, Collins R, Baigent C. The effects of lowering LDL cholesterol with statin therapy in people at low risk of vascular disease: meta-analysis of individual data from 27 randomised trials. Lancet 380: 581-590, 2012.
16. Cocks M, Shaw CS, Shepherd SO, Fisher JP, Ranasinghe AM, Barker TA, Tipton KD, Wagenmakers AJ. Sprint interval and endurance training are equally effective in increasing muscle microvascular density and eNOS content in sedentary males. J Physiol 591: 641-656, 2013.
17. Comb M, Goodman HM. CpG methylation inhibits proenkephalin gene expression and binding of the transcription factor AP-2. Nucleic Acids Res 18: 3975-3982, 1990.
18. Dangardt FJ, McKenna WJ, Luscher TF, Deanfield JE. Exercise: friend or foe? Nat Rev Cardiol 10: 495-507, 2013.
19. Denham J, Marques FZ, O'Brien BJ, Charchar FJ. Exercise: putting action into our epigenome. Sports Med 44: 189-209, 2014.
20. Devlin C, Greco S, Martelli F, Ivan M. miR-210: More than a silent player in hypoxia. IUBMB Life 63: 94-100, 2011.
21. Dong S, Cheng Y, Yang J, Li J, Liu X, Wang X, Wang D, Krall TJ, Delphin ES, Zhang C. MicroRNA expression signature and the role of microRNA-21 in the early phase of acute myocardial infarction. J Biol Chem 284: 29514-29525, 2009.
22. Du P, Zhang X, Huang CC, Jafari N, Kibbe WA, Hou L, Lin SM. Comparison of Beta-value and M-value methods for quantifying methylation levels by microarray analysis. BMC Bioinformatics 11: 587, 2010.
23. Dweep H, Sticht C, Pandey P, Gretz N. miRWalk-database: prediction of possible miRNA binding sites by "walking" the genes of three genomes. J Biomed Inform 44: 839-847, 2011.
24. Faraonio R, Salerno P, Passaro F, Sedia C, Iaccio A, Bellelli R, Nappi TC, Comegna M, Romano S, Salvatore G, Santoro M, Cimino F. A set of miRNAs participates in the cellular senescence program in human diploid fibroblasts. Cell Death Differ 19: 713-721, 2012.
25. Gist NH, Fedewa MV, Dishman RK, Cureton KJ. Sprint interval training effects on aerobic capacity: a systematic review and metaanalysis. Sports Med 44: 269-279, 2014.
26. Hambrecht R, Adams V, Erbs S, Linke A, Krankel N, Shu Y, Baither Y, Gielen S, Thiele H, Gummert JF, Mohr FW, Schuler G. Regular physical activity improves endothelial function in patients with coronary artery disease by increasing phosphorylation of endothelial nitric oxide synthase. Circulation 107: 3152-3158, 2003.
27. Hazell TJ, Hamilton CD, Olver TD, Lemon PW. Running sprint interval training induces fat loss in women. Appl Physiol Nutr Metab 39: 944-950, 2014.
28. Heyn H, Esteller M. DNA methylation profiling in the clinic: applications and challenges. Nat Rev Genet 13: 679-692, 2012.
29. Huang da W, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37: 1-13, 2009.
30. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57, 2009.
31. Jackson AS, Pollock ML. Generalized equations for predicting body density of men. Br J Nutr 40: 497-504, 1978.
32. Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 13: 484-492, 2012.
33. Kass SU, Landsberger N, Wolffe AP. DNA methylation directs a time-dependent repression of transcription initiation. Curr Biol 7: 157-165, 1997.
34. Kim JH, Park SG, Song SY, Kim JK, Sung JH. Reactive oxygen species-responsive miR-210 regulates proliferation and migration of adi-pose-derived stem cells via PTPN2. Cell Death Dis 4: e588, 2013.
35. Klug M, Heinz S, Gebhard C, Schwarzfischer L, Krause SW, Andreesen R, Rehli M. Active DNA demethylation in human postmitotic cells correlates with activating histone modifications, but not transcription levels. Genome Biol 11: R63, 2010.
36. Laufs U, Werner N, Link A, Endres M, Wassmann S, Jurgens K, Miche E, Bohm M, Nickenig G. Physical training increases endothelial progenitor cells, inhibits neointima formation, and enhances angiogenesis. Circulation 109: 220-226, 2004.
37. Liew CC, Ma J, Tang HC, Zheng R, Dempsey AA. The peripheral blood transcriptome dynamically reflects system wide biology: a potential diagnostic tool. J Lab Clin Med 147: 126-132, 2006.
38. Lin Y, Liu X, Cheng Y, Yang J, Huo Y, Zhang C. Involvement of MicroRNAs in hydrogen peroxide-mediated gene regulation and cellular injury response in vascular smooth muscle cells. J Biol Chem 284: 7903-7913, 2009.
39. Liu G, Detloff MR, Miller KN, Santi L, Houle JD. Exercise modulates microRNAs that affect the PTEN/mTOR pathway in rats after spinal cord injury. Exp Neurol 233: 447-456, 2012.
40. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408, 2001.
41. Luttropp K, Nordfors L, Ekström TJ, Lind L. Physical activity is associated with decreased global DNA methylation in Swedish older individuals. Scand J Clin Lab Invest 73: 184-185, 2013.
42. Ma Z, Qi J, Meng S, Wen B, Zhang J. Swimming exercise traininginduced left ventricular hypertrophy involves microRNAs and synergistic regulation of the PI3K/AKT/mTOR signaling pathway. Eur J Appl Physiol 113: 2473-2486, 2013.
43. Makki N, Thiel KW, Miller FJ Jr. The epidermal growth factor receptor and its ligands in cardiovascular disease. Int J Mol Sci 14: 20597-20613, 2013.
44. Maksimovic J, Gordon L, Oshlack A. SWAN: subset-quantile within array normalization for illumina infinium HumanMethylation450 BeadChips. Genome Biol 13: R44, 2012.
45. Martin-Subero JI, Kreuz M, Bibikova M, Bentink S, Ammerpohl O, Wickham-Garcia E, Rosolowski M, Richter J, Lopez-Serra L, Ballestar E, Berger H, Agirre X, Bernd HW, Calvanese V, Cogliatti SB, Drexler HG, Fan JB, Fraga MF, Hansmann ML, Hummel M, Klapper W, Korn B, Küppers R, Macleod RA, Möller P, Ott G, Pott C, Prosper F, Rosenwald A, Schwaenen C, Schübeler D, Seifert M, Stürzenhofecker B, Weber M, Wessendorf S, Loeffler M, Trümper L, Stein H, Spang R, Esteller M, Barker D, Hasenclever D, Siebert R, Molecular Mechanisms in Malignant Lymphomas Network Project of the Deutsche Krebshilfe. New insights into the biology and origin of mature aggressive B-cell lymphomas by combined epigenomic, genomic, and transcriptional profiling. Blood 113: 2488-2497, 2009.
46. Milagro FI, Campión J, Cordero P, Goyenechea E, Gómez-Uriz AM, Abete I, Zulet MA, Martinez JA. A dual epigenomic approach for the search of obesity biomarkers: DNA methylation in relation to diet-induced weight loss. FASEB J 25: 1378-1389, 2011.
47. Nakajima K, Takeoka M, Mori M, Hashimoto S, Sakurai A, Nose H, Higuchi K, Itano N, Shiohara M, Oh T, Taniguchi S. Exercise effects on methylation of ASC gene. Int J Sports Med 31: 671-675, 2010.
48. Ndon JA, Snyder AC, Foster C, Wehrenberg WB. Effects of chronic intense exercise training on the leukocyte response to acute exercise. Int J Sports Med 13: 176-182, 1992.
49. Nitert MD, Dayeh T, Volkov P, Elgzyri T, Hall E, Nilsson E, Yang BT, Lang S, Parikh H, Wessman Y, Weishaupt H, Attema J, Abels M, Wierup N, Almgren P, Jansson PA, Rönn T, Hansson O, Eriksson KF, Groop L, Ling C. Impact of an exercise intervention on DNA methylation in skeletal muscle from first-degree relatives of patients with type 2 diabetes. Diabetes 61: 3322-3332, 2012.
50. Pareja-Galeano H, Sanchis-Gomar F, García-Giménez JL. Physical exercise and epigenetic modulation: elucidating intricate mechanisms. Sports Med 44: 429-436, 2014.
51. Pastor WA, Aravind L, Rao A. TETonic shift: biological roles of TET proteins in DNA demethylation and transcription. Nat Rev Mol Cell Biol 14: 341-356, 2013.
52. Raitoharju E, Lyytikäinen LP, Levula M, Oksala N, Mennander A, Tarkka M, Klopp N, Illig T, Kähönen M, Karhunen PJ, Laaksonen R, Lehtimäki T. miR-21, miR-210, miR-34a, and miR-146a/b are upregulated in human atherosclerotic plaques in the Tampere Vascular Study. Atherosclerosis 219: 211-217, 2011.
53. Rakobowchuk M, Stuckey MI, Millar PJ, Gurr L, Macdonald MJ. Effect of acute sprint interval exercise on central and peripheral artery distensibility in young healthy males. Eur J Appl Physiol 105: 787-795, 2009.
54. Rakobowchuk M, Tanguay S, Burgomaster KA, Howarth KR, Gibala MJ, MacDonald MJ. Sprint interval and traditional endurance training induce similar improvements in peripheral arterial stiffness and flowmediated dilation in healthy humans. Am J Physiol Regul Integr Comp Physiol 295: R236-R242, 2008.
55. Rönn T, Volkov P, Davegårdh C, Dayeh T, Hall E, Olsson AH, Nilsson E, Tornberg A, Dekker Nitert M, Eriksson KF, Jones HA, Groop L, Ling C. A six months exercise intervention influences the genome-wide DNA methylation pattern in human adipose tissue. PLoS Genet 9: e1003572, 2013.
56. Sandvei M, Jeppesen PB, Støen L, Litleskare S, Johansen E, Stensrud T, Enoksen E, Hautala A, Martinmäki K, Kinnunen H, Tulppo M, Jensen J. Sprint interval running increases insulin sensitivity in young healthy subjects. Arch Physiol Biochem 118: 139-147, 2012.
57. Sloth M, Sloth D, Overgaard K, Dalgas U. Effects of sprint interval training on VO2max and aerobic exercise performance: a systematic review and meta-analysis. Scand J Med Sci Sports 23: e341-e352, 2013.
58. Swirski FK, Nahrendorf M. Leukocyte behavior in atherosclerosis, myocardial infarction, and heart failure. Science 339: 161-166, 2013.
59. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, Agarwal S, Iyer LM, Liu DR, Aravind L, Rao A. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324: 930-935, 2009.
60. Urbich C, Kuehbacher A, Dimmeler S. Role of microRNAs in vascular diseases, inflammation, and angiogenesis. Cardiovasc Res 79: 581-588, 2008.
61. Weber C, Schober A, Zernecke A. MicroRNAs in arterial remodelling, inflammation and atherosclerosis. Curr Drug Targets 11: 950-956, 2010.
62. Weber M, Baker MB, Moore JP, Searles CD. MiR-21 is induced in endothelial cells by shear stress and modulates apoptosis and eNOS activity. Biochem Biophys Res Commun 393: 643-648, 2010.
63. White AJ, Sandler DP, Bolick SC, Xu Z, Taylor JA, DeRoo LA. Recreational and household physical activity at different time points and DNA global methylation. Eur J Cancer 49: 2199-2206, 2013.
64. Yao R, Ma Y, Du Y, Liao M, Li H, Liang W, Yuan J, Ma Z, Yu X, Xiao H, Liao Y. The altered expression of inflammation-related microRNAs with microRNA-155 expression correlates with Th17 differentiation in patients with acute coronary syndrome. Cell Mol Immunol 8: 486-495, 2011.
65. Zhang FF, Cardarelli R, Carroll J, Zhang S, Fulda KG, Gonzalez K, Vishwanatha JK, Morabia A, Santella RM. Physical activity and global genomic DNA methylation in a cancer-free population. Epigenetics 6: 293-299, 2011.
66. Zhang FF, Morabia A, Carroll J, Gonzalez K, Fulda K, Kaur M, Vishwanatha JK, Santella RM, Cardarelli R. Dietary patterns are associated with levels of global genomic DNA methylation in a cancerfree population. J Nutr 141: 1165-1171, 2011.
67. Zhang FF, Santella RM, Wolff M, Kappil MA, Markowitz SB, Morabia A. White blood cell global methylation and IL-6 promoter methylation in association with diet and lifestyle risk factors in a cancer-free population. Epigenetics 7: 606-614, 2012.
68. Zhao Q, Rank G, Tan YT, Li H, Moritz RL, Simpson RJ, Cerruti L, Curtis DJ, Patel DJ, Allis CD, Cunningham JM, Jane SM. PRMT5-mediated methylation of histone H4R3 recruits DNMT3A, coupling histone and DNA methylation in gene silencing. Nat Struct Mol Biol 16: 304-311, 2009.