J Appl Biomed 15:63-70, 2017 | DOI: 10.1016/j.jab.2016.09.002

Exercise-induced epigenetic regulations in inflammatory related cells

Małgorzata Zawadzka*, Paweł Piotr Jagodziński
Department of Biochemistry and Molecular Biology, Poznań University of Medical Sciences, Poland

Physical activity has been correlated with transient immune impairment. However, such activities lead to improvement in immunity rather than dysfunction. The major benefit of regular exercise is the reduction of low-grade inflammation which consequently prevents or attenuates metabolic diseases, such as atherosclerosis and type 2 diabetes, neurodegenerative disorders, cancer or even depression. As a major factor responsible for general improvements in the immune system, scientists have examined epigenetics. Epigenetic mechanisms include cytosine methylation, micro-RNA expression and post-transcriptional modifications of histones, which regulate tissue-specific gene expression in response to environmental stimulation. This review will summarize the recent data regarding the impact of exercise and the role of epigenetic mechanisms on gene expression changes in Peripheral Blood Mononuclear Cells (PBMCs).

Keywords: Epigenetic; Physical activity; Exercise; PBMCs; Inflammation; Immunity

Received: May 23, 2016; Accepted: September 22, 2016; Published: January 1, 2017  Show citation

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Zawadzka M, Jagodziński PP. Exercise-induced epigenetic regulations in inflammatory related cells. J Appl Biomed. 2017;15(1):63-70. doi: 10.1016/j.jab.2016.09.002.
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References

  1. Baggish, A.L., Hale, A., Weiner, R.B., Lewis, G.D., Systrom, D., Wang, F., Wang, T.J., Chan, S.Y., 2011. Dynamic regulation of circulating microRNA during acute exhaustive exercise and sustained aerobic exercise training. J. Physiol. 589 (16), 3983-3994. Go to original source... Go to PubMed...
  2. Baggish, A.L., Park, J., Min, P.K., Isaacs, S., Parker, B.A., Thompson, P.D., Troyanos, C., D'Hemecourt, P., Dyer, S., Thiel, M., Hale, A., Chan, S.C., 2014. Rapid upregulation and clearance of distinct circulating microRNAs after prolonged aerobic exercise. J. Appl. Physiol. 116 (5), 522-531. Go to original source... Go to PubMed...
  3. Bannister, A.J., Kouzarides, T., 2011. Regulation of chromatin by histone modifications. Cell Res. 21 (3), 381-395. Go to original source... Go to PubMed...
  4. Barres, R., Yan, J., Egan, B., Treebak, J.T., Rasmussen, M., Fritz, T., Caidahl, K., Krook, A., O'Gorman, D.J., Zierath, J.R., 2012. Acute exercise remodels promoter methylation in human skeletal muscle. Cell Metab. 15 (3), 405-411. Go to original source... Go to PubMed...
  5. Bartel, D.P., 2004. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116 (2), 281-297. Go to original source... Go to PubMed...
  6. Bauer, M., Heeg, K., Wagner, H., Lipford, G.B., 1999. DNA activates human immune cells through a CpG sequence-dependent manner. Immunology 97 (4), 699- 705. Go to original source... Go to PubMed...
  7. Berger, S.L., 2002. Histone modifications in transcriptional regulation. Curr. Opin. Genet Dev. 12 (2), 142-148. Go to original source... Go to PubMed...
  8. Bestor, T.H., 2000. The DNA methyltransferases of mammals. Hum. Mol. Genet. 9 (16), 2395-2402. Go to original source... Go to PubMed...
  9. Bogdanovi c, O., Veenstra, G.J.C., 2009. DNA methylation and methyl-CpG binding proteins: developmental requirements and function. Chromosoma 118 (5), 549-565. Go to original source... Go to PubMed...
  10. Bouchard, C., 2015. Exercise genomics - a paradigm shift is needed: a commentary. Br. J. Sports Med. 49, 1492-1496. Go to original source... Go to PubMed...
  11. Chalitchagorn, K., Shuangshoti, S., Hourpai, N., Kongruttanachok, N., Tangkijvanich, P., Thong-ngam, D., Voravud, N., Sriuranpong, V., Mutirangura, A., 2004. Distinctive pattern of LINE-1 methylation level in normal tissues and the association with carcinogenesis. Oncogene 23 (54), 8841-8846. Go to original source... Go to PubMed...
  12. Chuang, J.C., Jones, P.A., 2007. Epigenetics and microRNAs. Pediatr. Res. 61, 24R-29R. Go to original source... Go to PubMed...
  13. Ciafre, S.A., Galardi, S., Mangiola, A., Ferracin, M., Liu, C.G., Sabatino, G., Negrini, M., Maira, C.M., Croce, M.G., Farace, M.G., 2005. Extensive modulation of a set of microRNAs in primary glioblastoma. Biochem. Biophys. Res. Commun. 334 (4), 1351-1358. Go to original source... Go to PubMed...
  14. Çolak, T.K., Acar, G., Dereli, E.E., Özgül, B., Demirbüken, I., Alkaç, Ç., Polat, M.G., 2016. Association between the physical activity level and the quality of life of patients with type 2 diabetes mellitus. J. Phys. Ther. Sci. 28 (1), 142-147. Go to original source... Go to PubMed...
  15. Cooper, D.M., Radom-Aizik, S., Schwindt, C., Zaldivar Jr., F., 2007. Dangerous exercise: lessons learned from dysregulated inflammatory responses to physical activity. J. Appl. Physiol. 103 (2), 700-709. Go to original source... Go to PubMed...
  16. de Gonzalo-Calvo, D., Dávalos, A., Montero, A., García-González, Á., Tyshkovska, I., Medina, A.G., Díaz-Martínez, Á.E., 2015. Circulating inflammatory miRNA signature in response to different doses of aerobic exercise. J. Appl. Physiol. 199, 124-134. Go to original source... Go to PubMed...
  17. Delatte, B., Deplus, R., Fuks, F., 2014. Playing TETris with DNA modifications. EMBO J. 33 (11), 1198-1211. Go to original source... Go to PubMed...
  18. Denham, J., O'Brien, B.J., Marques, F.Z., Charchar, F.J., 2014. Changes in the leukocyte methylome and its effect on cardiovascular related genes after exercise. J. Appl. Physiol. 118, 475-488. Go to original source... Go to PubMed...
  19. Denham, J., Marques, F.Z., Bruns, E.L., O'Brien, B.J., Charchar, F.J., 2016. Epigenetic changes in leukocytes after 8 weeks of resistance exercise training. Eur. J. Appl. Physiol. 116 (6), 1245-1253. Go to original source... Go to PubMed...
  20. Ding, W., Li, J., Singh, J., Alif, R., Vazquez-Padron, R.I., Gomes, S.A., Hare, J.M., Shehadeh, L.A., 2014. MiR-30e targets IGF2-regulated osteogenesis in bone marrow derived mesenchymal stem cells, aortic smooth muscle cells, and APOE-/-mice. Circulation 130, A18084. Go to original source... Go to PubMed...
  21. Eulalio, A., Huntzinger, E., Izaurralde, E., 2008. Getting to the root of miRNAmediated gene silencing. Cell 132 (1), 9-14. Go to original source... Go to PubMed...
  22. Fabbri, M., Garzon, R., Cimmino, A., Liu, Z., Zanesi, N., Callegari, E., Liu, S., Alder, H., Costinean, S., Fernandez-Cymering, C., Volinia, S., Guler, G., Morrison, C.D., Chan, K.K., Marcucci, G., Calin, G.A., Huebner, K., Croce, C.M., 2007. MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proc. Natl. Acad. Sci. U. S.A. 104 (40), 15805- 15810. Go to original source... Go to PubMed...
  23. Feil, R., Fraga, M.F., 2012. Epigenetics and the environment: emerging patterns and implications. Nat. Rev. Genet. 13 (2), 97-109. Go to original source... Go to PubMed...
  24. Ferraro, E., Giammarioli, A.M., Chiandotto, S., Spoletini, I., Rosano, G., 2014. Exerciseinduced skeletal muscle remodeling and metabolic adaptation: redox signaling and role of autophagy. Antioxid. Redox Signal. 21 (1), 154-176. Go to original source... Go to PubMed...
  25. Fischle, W., Wang, Y., Allis, C.D., 2003. Histone and chromatin cross-talk. Curr. Opin. Cell Biol. 15 (2), 172-183. Go to original source... Go to PubMed...
  26. Flück, M., Waxham, M.N., Hamilton, M.T., Booth, F.W., 2000. Skeletal muscle Ca2 +-independent kinase activity increases during either hypertrophy or running. J. Appl. Physiol. 88 (1), 352-358. Go to original source... Go to PubMed...
  27. Fraga, M.F., Ballestar, E., Paz, M.F., Ropero, S., Setien, F., Ballestar, M.L., Heine-Suñer, D., Cigudosa, J.C., Urioste, M., Benitez, J., Boix-Chornet, M., Sanchez-Aqualera, A., Ling, C., Carlsson, E., Poulsen, P., Vaag, A., Stephan, Z., Spector, T.D., Wu, Y.Z., Plass, C., Esteller, M., 2005. Epigenetic differences arise during the lifetime of monozygotc twins. Proc. Natl. Acad. Sci. U. S. A. 102 (30), 10604-10609. Go to original source... Go to PubMed...
  28. Gehring, M., Reik, W., Henikoff, S., 2009. DNA demethylation by DNA repair. Trends Genet. 25 (2), 82-90. Go to original source... Go to PubMed...
  29. Gjevestad, G.O., Holven, K.B., Ulven, S.M., 2015. Effects of exercise on gene expression of inflammatory markers in human peripheral blood cells: a systematic review. Curr. Cardiovasc. Risk Rep. 9 (7), 1-17. Go to original source... Go to PubMed...
  30. Golbidi, S., Lather, L., 2012. Exercise and the cardiovascular system. Cardiol. Res. Pract. 2012, 210852. Go to original source... Go to PubMed...
  31. Gregory, R.I., Chendrimada, T.P., Cooch, N., Shiekhattar, R., 2005. Human RISC couples microRNA biogenesis and posttranscriptional gene silencing. Cell 123 (4), 631-640. Go to original source... Go to PubMed...
  32. Grunstein, M., 1997. Histone acetylation in chromatin structure and transcription. Nature 389 (6649), 349-352. Go to original source... Go to PubMed...
  33. He, Y., Ecker, J.R., 2014. Non-CG methylation in the human genome. Annu. Rev. Genomics Hum. Genet. 16, 55-77. Go to original source... Go to PubMed...
  34. He, L., Hannon, G.J., 2004. MicroRNAs: small RNAs with a big role in gene regulation. Nat. Rev. Genet. 5 (7), 522-531. Go to original source... Go to PubMed...
  35. Heneghan, H.M., Miller, N., Lowery, A.J., Sweeney, K.J., Newell, J., Kerin, M.J., 2010. Circulating microRNAs as novel minimally invasive biomarkers for breast cancer. Ann. Surg. 251 (3), 499-505. Go to original source... Go to PubMed...
  36. Hermann, A., Gowher, H., Jeltsh, A., 2004. Biochemistry and biology of mammalian DNA methylotransferases. Cell. Mol. Life Sci. 61 (19-20), 2571-2587. Go to original source... Go to PubMed...
  37. Hirasawa, R., Chiba, H., Kaneda, M., Tajima, S., Li, E., Jaenisch, R., Sasaki, H., 2008. Maternal and zygotic Dnmt1 are necessary and sufficient for the maintenance of DNA methylation imprints during preimplantation development. Genes Dev. 22 (12), 1607-1616. Go to original source... Go to PubMed...
  38. Hoesel, B., Schmid, J.A., 2013. The complexity of NF-kB signaling in inflammation and cancer. Mol. Cancer 12 (1), 1. Go to original source... Go to PubMed...
  39. Horsburgh, S., Todryk, S., Toms, C., Moran, C.N., Ansley, L., 2015. Exerciseconditioned plasma attenuates nuclear concentrations of DNA methyltransferase 3 B in human peripheral blood mononuclear cells. Physiol. Rep. 3 (12), e12621. Go to original source... Go to PubMed...
  40. Jjingo, D., Conley, A.B., Soojin, V.Y., Lunyak, V.V., Jordan, I.K., 2012. On the presence and role of human gene-body DNA methylation. Oncotarget 3 (4), 462-474. Go to original source... Go to PubMed...
  41. Jones, P.A., 2012. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat. Rev. Genet. 13 (7), 484-492. Go to original source... Go to PubMed...
  42. Kampert, J.B., Blair, S.N., Berlow, C.E., Kohl, H.W., 1996. Physical activity, physical fitness, and all-cause and cancer mortality: a prospective study of men and women. Ann. epidemiol. 6 (5), 452-457. Go to original source... Go to PubMed...
  43. Kawagoe, T., Sato, S., Jung, A., Yamamoto, M., Matsui, K., Kato, H., Uematsu, S., Takeuchi, O., Akira, S., 2007. Essential role of IRAK-4 protein and its kinase activity in Toll-like receptor-mediated immune responses but not in TCR signaling. J. Exp. Med. 204 (5), 1. Go to original source... Go to PubMed...
  44. Keller, C., Steensberg, A., Pilegaard, H., Osada, T., Saltin, B., Pedersen, B.K., Neufer, P. D., 2001. Transcriptional activation of the IL-6 gene in human contracting skeletal muscle: influence of muscle glycogen content. FASEB J. 15 (14), 2748- 2750. Go to original source... Go to PubMed...
  45. Khorasanizadeh, S., 2004. The nucleosome: from genomic organization to genomic regulation. Cell 116 (2), 259-272. Go to original source... Go to PubMed...
  46. Krokan, H.E., Nilsen, H., Skorpen, F., Otterlei, M., Slupphaug, G., 2000. Base excision repair of DNA in mammalian cells. FEBS 476 (1-2), 73-77. Go to original source... Go to PubMed...
  47. Lagos-Quintana, M., Rauhut, R., Lendeckel, W., Tuschl, T., 2001. Identification of novel genes coding for small expressed RNAs. Science 294 (5543), 853-858. Go to original source... Go to PubMed...
  48. Lee, S., Vasudevan, S., 2013. Post-transcriptional stimulation of gene expression by microRNAs. Adv. Exp. Med. Biol. 768, 97-126. Go to original source... Go to PubMed...
  49. Lewis, B.P., Burge, C.B., Bartel, D.P., 2005. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120 (1), 15-20. Go to original source... Go to PubMed...
  50. Li, Q.J., Chau, J., Ebert, P.J., Sylvester, G., Min, H., Liu, G., Braich, R., Monoharan, M., Soutschek, J., Skare, P., Klein, L.O., Davis, M.M., Chen, C.Z., 2007. miR-181a is an intrinsic modulator of T cell sensitivity and selection. Cell 129 (1), 147-161. Go to original source... Go to PubMed...
  51. Li, E., 2002. Chromatin modification and epigenetic reprogramming in mammalian development. Nat. Rev. Genet. 3 (9), 662-673. Go to original source... Go to PubMed...
  52. Lochmann, T.L., Thomas, R.R., Bennett Jr, J.P., Taylor, S.M., 2015. Epigenetic modifications of the PGC-1a promoter during exercise induced expression in mice. PLoS One 10 (6), e0129647. Go to original source... Go to PubMed...
  53. Lytle, J.R., Yario, T.A., Steitz, J.A., 2000. Target mRNAs are repressed as efficiently by microRNA-binding sites in the 50 UTR as in the 30 UTR. PNAS 104 (23), 9667- 9672. Go to original source... Go to PubMed...
  54. Ma, R., Jiang, T., Kang, X., 2012. Circulating microRNAs in cancer: origin, function and application. J. Exp. Clin. Cancer Res. 31 (1), 1. Go to original source... Go to PubMed...
  55. Mariathasan, S., Newton, K., Monack, D.M., Vucic, D., French, D.M., Lee, W.P., RooseGirma, M., Erickson, S., Dixit, V.M., 2004. Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature 430 (6996), 213- 218. Go to original source... Go to PubMed...
  56. Martinon, F., Tschopp, J., 2004. Inflammatory caspases: linking an intracellular innate immune system to autoinflammatory diseases. Cell 117 (5), 561-574. Go to original source... Go to PubMed...
  57. McFarlin, B.K., Flynn, M.G., Campbell, W.W., Craig, B.A., Robinson, J.P., Stewart, L.K., Timmerman, K.L., Coen, P.M., 2006. Physical activity status, but not age, influences inflammatory biomarkers and toll-like receptor 4. J. Gerontol. A Biol. Sci. Med. Sci. 61 (4), 388-393. Go to original source... Go to PubMed...
  58. McKinsey, T.A., Zhang, C.L., Lu, J., Olson, E.N., 2000. Signal-dependent nuclear export of a histone deacetylase regulates muscle differentiation. Nature 408 (6808), 106-111. Go to original source... Go to PubMed...
  59. Miousse, I.R., Koturbash, I., 2015. The fine LINE: methylation drawing the cancer landscape. Biomed. Res. Int. 2015, 131547. Go to original source... Go to PubMed...
  60. Mitchell, J.B., Dugas, J.P., McFarlin, B.K., Nelson, M.J., 2002. Effect of exercise, heat stress, and hydration on immune cell number and function. Med. Sci. Sports Exerc. 34 (12), 1941-1950. Go to original source... Go to PubMed...
  61. Mooren, F.C., Viereck, J., Krüger, K., Thum, T., 2014. Circulating microRNAs as potential biomarkers of aerobic exercise capacity. Am. J. Physiol. Heart Circ. Physiol. 306 (4), H557-H563. Go to original source... Go to PubMed...
  62. Nakajima, K., Takeoka, M., Mori, M., Hashimoto, S., Sakurai, A., Nose, H., Taniguchi, S., 2010. Exercise effects on methylation of ASC gene. Int. J. Sports Med. 31, 671- 675. Go to original source... Go to PubMed...
  63. Niculescu, M.D., Zeisel, S.H., 2002. Diet, methyl donors and DNA methylation: interactions between dietary folate, methionine and choline. J. Nutr. 132 (8), 2333S-2335S. Go to original source... Go to PubMed...
  64. Nielsen, H.G., 2013. Exercise and Immunity. Current Issues in Sports and Exercise Medicine 121-140.
  65. Nielsen, S., Åkerström, T., Rinnov, A., Yfanti, C., Scheele, C., Pedersen, B.K., Laye, M.J., 2014. The miRNA plasma signature in response to acute aerobic exercise and endurance training. PLoS One 9 (2), e87308. Go to original source... Go to PubMed...
  66. Nieman, D.C., Johanssen, L.M., Lee, J.W., 1989. Infectious episodes in runners before and after a roadrace. J. Sports Med. Phys. Fitness 29 (3), 289-296. Go to PubMed...
  67. Nieman, D.C., 1994. Exercise, infection, and immunity. Int. J. Sports Med. 15, 131-141. Go to original source... Go to PubMed...
  68. Normanno, N., De Luca, A., Bianco, C., Strizzi, L., Mancino, M., Maiello, M.R., Carotenuto, A., De Feo, G., Caponigro, F., Salomon, D.S., 2006. Epidermal growth factor receptor (EGFR) signaling in cancer. Gene 366 (1), 2-16. Go to original source... Go to PubMed...
  69. Pedersen, B.K., Fischer, C.P., 2007. Beneficial health effects of exercise - the role of IL6 as a myokine. Trends Pharmacol. Sci. 28 (4), 152-156. Go to original source... Go to PubMed...
  70. Pedersen, B.K., Ullum, H., 1994. NK cell response to physical activity: possible mechanism of action. Med. Sci. Sports Exerc. 26 (2), 140-146. Go to original source... Go to PubMed...
  71. Pedersen, B.K., Ostrowski, K., Rohde, T., Bruunsgaard, H., 1998. The cytokine response to strenuous exercise. Can. J. Physiol. Pharmacol. 76 (5), 501-511. Go to original source...
  72. Pedersen, B.K., 2000. Exercise and cytokines. Immunol. Cell Biol. 78, 532-535. Go to original source... Go to PubMed...
  73. Pekarsky, Y., Santanam, U., Cimmino, A., Palamarchuk, A., Efanov, A., Maximov, V., Volinia, S., Alder, H., Liu, C.G., Rassenti, L., Calin, G.A., Hagan, J.P., Kipps, T., Croce, C.M., 2006. Tcl1 expression in chronic lymphocytic leukemia is regulated by miR-29 and miR-181. Cancer Res. 66 (24), 11590-11593. Go to original source... Go to PubMed...
  74. Peterson, C.L., Laniel, M.A., 2004. Histones and histone modifications. Curr. Biol. 14 (14), R546-R551. Go to original source... Go to PubMed...
  75. Radom-Aizik, S., Zaldivar, F., Oliver, S., Galassetti, P., Cooper, D.M., 2010. Evidence for microRNA involvement in exercise-associated neutrophil gene expression changes. J. Appl. Physiol. 109 (1), 252-261. Go to original source... Go to PubMed...
  76. Radom-Aizik, S., Zaldivar, F., Leu, S.Y., Adams, G.R., Oliver, S., Cooper, D.M., 2012. Effects of exercise on microRNA expression in young males peripheral blood mononuclear cells. Clin. Transl. Sci. 5 (1), 32-38. Go to original source... Go to PubMed...
  77. Radom-Aizik, S., Zaldivar, F., Haddad, F., Cooper, D.M., 2013. Impact of brief exercise on peripheral blood NK cell gene and microRNA expression in young adults. J. Appl. Physiol. 114 (5), 628-636. Go to original source... Go to PubMed...
  78. Radom-Aizik, S., Zaldivar, F.P., Haddad, F., Cooper, D.M., 2014. Impact of brief exercise on circulating monocyte gene and microRNA expression: implications for atherosclerotic vascular disease. Brain Behav. Immun. 39, 121-129. Go to original source... Go to PubMed...
  79. Rice, J.C., Allis, C.D., 2001. Histone methylation versus histone acetylation: new insights into epigenetic regulation. Curr. Opin. Cell Biol. 13 (3), 263-273. Go to original source... Go to PubMed...
  80. Robson-Ansley, P.J., Saini, A., Toms, C., Ansley, L., Walshe, I.H., Nimmo, M.A., Curtin, J. A., 2013. Dynamic changes in dna methylation status in peripheral blood Mononuclear cells following an acute bout of exercise: potential impact of exercise-induced elevations in interleukin-6 concentration. J. Biol. Regul. Homeost. Agents 28 (3), 407-417.
  81. Ross, J.P., Rand, K.N., Molloy, P.L., 2010. Hypomethylation of repeated DNA sequences in cancer. Epigenomics 2 (2), 245-269. Go to original source... Go to PubMed...
  82. Rusca, N., Monticelli, S., 2011. MiR-146a in immunity and disease. Mol. Biol. Int. 2011, 437301. Go to original source... Go to PubMed...
  83. Sawada, S., Kon, M., Wada, S., Ushida, T., Suzuki, K., Akimoto, T., 2013. Profiling of circulating microRNAs after a bout of acute resistance exercise in humans. PLoS One 8 (7), e70823. Go to original source... Go to PubMed...
  84. Sikorski, K., Chmielewski, S., Przybył, Ł., Heemann, U., Baumann, M., Wesoły, J.Z., Bluyssen, H.A., 2011. STAT1-mediated signal integration between IFNł and LPS leads to increased EC and SMC activation and monocot adhesion. Am. J. Physiol. Cell Physiol. 300, 1137-1344. Go to original source... Go to PubMed...
  85. Stewart, L.K., Flynn, M.G., Campbell, W.W., Craig, B.A., Robinson, J.P., Timmerman, K. L., McFarlin, B.K., Coen, P.M., Talbert, E., 2007. The influence of exercise training on inflammatory cytokines and C-reactive protein. Med. Sci. Sports Exerc. 39 (10), 1714-1719. Go to original source... Go to PubMed...
  86. Strahl, B.D., Allis, C.D., 2000. The language of covalent histone modifications. Nature 403 (6765), 41-45. Go to original source... Go to PubMed...
  87. Suzuki, M.M., Bird, A., 2008. DNA methylation landscapes: provocative insights from epigenomics. Nat. Rev. Genet. 9 (6), 465-476. Go to original source... Go to PubMed...
  88. Tak, P.P., Firestein, G.S., 2001. NF-kB: a key role in inflammatory diseases. J. Clin. Invest. 107 (1), 7-11. Go to original source... Go to PubMed...
  89. Turner, B.M., 2000. Histone acetylation and an epigenetic code. Bioessays 22 (9), 836-845. Go to original source... Go to PubMed...
  90. Vasudevan, S., Tong, Y., Steitz, J.A., 2007. Switching from repression to activation: microRNAs can up-regulate translation. Science 318 (5858), 1931-1934. Go to original source... Go to PubMed...
  91. Waddington, C.H., 1942. The epigenotype. Endeavour 1, 18-20.
  92. Walsh, N.P., Gleeson, M., Shepard, R.J., Gleeson, M., Woods, J.A., Bishop, N.C., Fleshner, M., Green, C., Pedersen, B.K., Hoffman-Goetz, L., Rogers, C.J., Northoff, H., Abbasi, A., Simon, P., 2011. Position statement. Part one: immune function and exercise. Exerc. Immunol. Rev. 11, 6-63.
  93. Wang, Z., Wesche, H., Stevens, T., Walker, N., Yeh, W.C., 2009. IRAK-4 inhibitors for inflammation. Curr. Top. Med. Chem. 9 (8), 724-737. Go to original source... Go to PubMed...
  94. Wang, Y., Xu, Y., Sheng, H., Ni, X., Lu, J., 2016. Exercise amelioration of depressionlike behaviour in OVX mice is associated with suppression of NLRP3 inflammasome activation in hippocampus. Behav. Bran Res. 307, 18-24. Go to original source... Go to PubMed...
  95. White, A.J., Sandler, D.P., Bolick, S.C., Xu, Z., Taylor, J.A., DeRoo, L.A., 2013. Recreational and household physical activity at different time points and DNA global methylation. Eur. J. Cancer 49 (9), 2199-2206. Go to original source... Go to PubMed...
  96. Wolffe, A., 1998. Chro Matin: Structure and Function. Academic press, Cambridge.
  97. Wu, S.C., Zhang, Y., 2010. Active DNA demethylation: many roads lead to Rome. Nat. Rev. Mol. Cell Biol. 11 (9), 607-620. Go to original source... Go to PubMed...
  98. Xu, T., Zhou, Q., Che, L., Das, S., Wang, L., Jiang, J., Li, G., Xu, J., Yao, J., Wang, H., Dai, Y., Xiao, J., 2016. Circulating miR-21, miR-378, and miR-940 increase in response to an acute exhaustive exercise in chronic heart failure patients. Oncotarget 7 (11), 12414-12425. Go to original source... Go to PubMed...
  99. Zhang, Y., Reinberg, D., 2001. Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tails. Genes Dev. 15 (18), 2343-2360. Go to original source... Go to PubMed...
  100. Zhang, F.F., Cardarelli, R., Carroll, J., Zhang, S., Fulda, K.G., Gonzalez, K., Vishwanatha, J.K., Morabia, A., Santella, R.M., 2011. Physical activity and global genomic DNA methylation in a cancer-free population. Epigenetics 6 (3), 293-299. Go to original source... Go to PubMed...
  101. Zhang, Y., Hashimoto, S., Fujii, C., Hida, S., Ito, K., Matsumura, T., Sakaizawa, T., Morikawa, M., Masuki, S., Nose, H., Higuchi, K., Nakijama, K., Taniguchi, S., 2015. NFkB2 gene as a novel candidate that epigenetically responds to interval walking training. Int. J. Sports Med. 36 (9), 769-775. Go to original source... Go to PubMed...
  102. Zimmer, P., Baumann, F.T., Bloch, W., Schenk, A., Koliamitra, C., Jensen, P., Mierau, A., Hülsdünker, T., Reinart, A., Hallek, M., Elter, T., 2014. Impact of exercise on pro inflammatory cytokine levels and epigenetic modulations of tumor-competitive lymphocytes in Non-Hodgkin-Lymphoma patients-randomized controlled trial. Eur. J. Haematol. 93 (6), 527-532. Go to original source... Go to PubMed...
  103. Zimmer, P., Bloch, W., Schenk, A., Zopf, E.M., Hildebrandt, U., Streckmann, F., Beulertz, J., Koliamitra, C., Schollmayer, F., Baumann, F., 2015. Exercise-induced natural killer cell activation is driven by epigenetic modifications. Int. J. Sporst Go to original source... Go to PubMed...