Skip to main content
SpringerLink
Log in

MicroRNAs Mediate Beneficial Effects of Exercise in Heart

  • Chapter
  • First Online:
Exercise for Cardiovascular Disease Prevention and Treatment

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1000))

Abstract

MicroRNAs (miRNAs, miRs), a group of small non-coding RNAs, repress gene expressions at posttranscriptional level in most cases and are involved in cardiovascular physiology and disease pathogenesis. Increasing evidence has proved that miRNAs are potential regulators of exercise induced cardiac growth and mediate the benefits of exercise in a variety of cardiovascular diseases. In this chapter, we will review the regulatory effects of miRNAs in cardiac adaptations to exercise, and summarize their cardioprotective effects against myocardial infarction, ischemia/reperfusion injury, heart failure, diabetic cardiomyopathy, atherosclerosis, hypertension, and pulmonary hypertension. Also, we will introduce circulating miRNAs in response to acute and chronic exercise. Therefore, miRNAs may serve as novel therapeutic targets and potential biomarkers for cardiovascular diseases.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Institutional subscriptions

References

  1. Pagidipati NJ, Gaziano TA (2013) Estimating deaths from cardiovascular disease: a review of global methodologies of mortality measurement. Circulation 127(6):749–756

    Article  PubMed  PubMed Central  Google Scholar 

  2. Mozaffarian D, Benjamin EJ, Go AS et al (2016) Heart disease and stroke statistics-2016 update: a report from the American Heart Association. Circulation 133(4):e38–e360

    Article  PubMed  Google Scholar 

  3. Hill JA, Olson EN (2008) Cardiac plasticity. N Engl J Med 358(13):1370–1380

    Article  CAS  PubMed  Google Scholar 

  4. Ellison GM, Waring CD, Vicinanza C et al (2012) Physiological cardiac remodelling in response to endurance exercise training: cellular and molecular mechanisms. Heart 98(1):5–10

    Article  CAS  PubMed  Google Scholar 

  5. Tao L, Bei Y, Zhang H et al (2015) Exercise for the heart: signaling pathways. Oncotarget 6(25):20773–20784

    Article  PubMed  PubMed Central  Google Scholar 

  6. Shima T, Matsui T, Jesmin S et al (2016) Moderate exercise ameliorates dysregulated hippocampal glycometabolism and memory function in a rat model of type 2 diabetes. Diabetologia 60:597

    Article  PubMed  CAS  Google Scholar 

  7. Kwak MS, Kim D, Chung GE et al (2016) The preventive effect of sustained physical activity on incident nonalcoholic fatty liver disease. Liver Int 37:919

    Article  PubMed  CAS  Google Scholar 

  8. Kim HS, Ike A, Matthew J (2016) Effect of exercise on the development of new fatty liver and the resolution of existing fatty liver. J Hepatol 66:664–665

    Article  PubMed  Google Scholar 

  9. Deijle IA, Van Schaik SM, Van Wegen EE et al (2016) Lifestyle interventions to prevent cardiovascular events after stroke and transient ischemic attack: systematic review and meta-analysis. Stroke 48:174

    Article  PubMed  Google Scholar 

  10. Sandroff BM, Motl RW, Scudder MR et al (2016) Systematic, evidence-based review of exercise, physical activity, and physical fitness effects on cognition in persons with multiple sclerosis. Neuropsychol Rev 26(3):271–294

    Article  PubMed  Google Scholar 

  11. Todoric J, Antonucci L, Karin M (2016) Targeting inflammation in cancer prevention and therapy. Cancer Prev Res (Phila) 9(12):895–905

    Article  CAS  Google Scholar 

  12. Golbidi S, Laher I (2012) Exercise and the cardiovascular system. Cardiol Res Pract 2012:210852

    Article  PubMed  PubMed Central  Google Scholar 

  13. Thum T (2014) Noncoding RNAs and myocardial fibrosis. Nat Rev Cardiol 11(11):655–663

    Article  CAS  PubMed  Google Scholar 

  14. Ounzain S, Pedrazzini T (2015) The promise of enhancer-associated long noncoding RNAs in cardiac regeneration. Trends Cardiovasc Med 25(7):592–602

    Article  CAS  PubMed  Google Scholar 

  15. van Rooij E, Sutherland LB, Qi X et al (2007) Control of stress-dependent cardiac growth and gene expression by a microRNA. Science 316(5824):575–579

    Article  PubMed  CAS  Google Scholar 

  16. Tao L, Bei Y, Lin S et al (2015) Exercise training protects against acute myocardial infarction via improving myocardial energy metabolism and mitochondrial biogenesis. Cell Physiol Biochem 37(1):162–175

    Article  CAS  PubMed  Google Scholar 

  17. Fernandes T, Barauna VG, Negrao CE et al (2015) Aerobic exercise training promotes physiological cardiac remodeling involving a set of microRNAs. Am J Physiol Heart Circ Physiol 309(4):H543–H552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Nadruz W (2015) Myocardial remodeling in hypertension. J Hum Hypertens 29(1):1–6

    Article  CAS  PubMed  Google Scholar 

  19. Bernardo BC, Weeks KL, Pretorius L et al (2010) Molecular distinction between physiological and pathological cardiac hypertrophy: experimental findings and therapeutic strategies. Pharmacol Ther 128(1):191–227

    Article  CAS  PubMed  Google Scholar 

  20. MacDougall JD, Tuxen D, Sale DG et al (1985) Arterial blood pressure response to heavy resistance exercise. J Appl Physiol (1985) 58(3):785–790

    Article  CAS  Google Scholar 

  21. McMullen JR, Jennings GL (2007) Differences between pathological and physiological cardiac hypertrophy: novel therapeutic strategies to treat heart failure. Clin Exp Pharmacol Physiol 34(4):255–262

    Article  CAS  PubMed  Google Scholar 

  22. Abel ED, Doenst T (2011) Mitochondrial adaptations to physiological vs. pathological cardiac hypertrophy. Cardiovasc Res 90(2):234–242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Volpe M (2014) Natriuretic peptides and cardio-renal disease. Int J Cardiol 176(3):630–639

    Article  PubMed  Google Scholar 

  24. Shephard RJ, Balady GJ (1999) Exercise as cardiovascular therapy. Circulation 99(7):963–972

    Article  CAS  PubMed  Google Scholar 

  25. Ooi JY, Bernardo BC, McMullen JR (2014) The therapeutic potential of miRNAs regulated in settings of physiological cardiac hypertrophy. Future Med Chem 6(2):205–222

    Article  CAS  PubMed  Google Scholar 

  26. Gullestad L, Ueland T, Vinge LE et al (2012) Inflammatory cytokines in heart failure: mediators and markers. Cardiology 122(1):23–35

    Article  CAS  PubMed  Google Scholar 

  27. Hein S, Arnon E, Kostin S et al (2003) Progression from compensated hypertrophy to failure in the pressure-overloaded human heart: structural deterioration and compensatory mechanisms. Circulation 107(7):984–991

    Article  PubMed  Google Scholar 

  28. Kolwicz SC Jr, Purohit S, Tian R (2013) Cardiac metabolism and its interactions with contraction, growth, and survival of cardiomyocytes. Circ Res 113(5):603–616

    Article  CAS  PubMed  Google Scholar 

  29. Mohl W, Gangl C, Jusic A et al (2015) PICSO: from myocardial salvage to tissue regeneration. Cardiovasc Revasc Med 16(1):36–46

    Article  PubMed  Google Scholar 

  30. Bergmann O, Bhardwaj RD, Bernard S et al (2009) Evidence for cardiomyocyte renewal in humans. Science 324(5923):98–102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Kocher AA, Schlechta B, Gasparovicova A et al (2007) Stem cells and cardiac regeneration. Transpl Int 20(9):731–746

    Article  PubMed  Google Scholar 

  32. Bostrom P, Mann N, Wu J et al (2010) C/EBPbeta controls exercise-induced cardiac growth and protects against pathological cardiac remodeling. Cell 143(7):1072–1083

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Kubin T, Poling J, Kostin S et al (2011) Oncostatin M is a major mediator of cardiomyocyte dedifferentiation and remodeling. Cell Stem Cell 9(5):420–432

    Article  CAS  PubMed  Google Scholar 

  34. Waring CD, Vicinanza C, Papalamprou A et al (2014) The adult heart responds to increased workload with physiologic hypertrophy, cardiac stem cell activation, and new myocyte formation. Eur Heart J 35(39):2722–2731

    Article  CAS  PubMed  Google Scholar 

  35. Laughlin MH, Bowles DK, Duncker DJ (2012) The coronary circulation in exercise training. Am J Physiol Heart Circ Physiol 302(1):H10–H23

    Article  CAS  PubMed  Google Scholar 

  36. Leone AM, Valgimigli M, Giannico MB et al (2009) From bone marrow to the arterial wall: the ongoing tale of endothelial progenitor cells. Eur Heart J 30(8):890–899

    Article  PubMed  Google Scholar 

  37. Volaklis KA, Tokmakidis SP, Halle M (2013) Acute and chronic effects of exercise on circulating endothelial progenitor cells in healthy and diseased patients. Clin Res Cardiol 102(4):249–257

    Article  PubMed  Google Scholar 

  38. Silva DA, ND J, Fernandes T, Soci UP et al (2012) Swimming training in rats increases cardiac MicroRNA-126 expression and angiogenesis. Med Sci Sports Exerc 44(8):1453–1462

    Article  CAS  Google Scholar 

  39. Fish JE, Santoro MM, Morton SU et al (2008) miR-126 regulates angiogenic signaling and vascular integrity. Dev Cell 15(2):272–284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Care A, Catalucci D, Felicetti F et al (2007) MicroRNA-133 controls cardiac hypertrophy. Nat Med 13(5):613–618

    Article  CAS  PubMed  Google Scholar 

  41. Soci UP, Fernandes T, Hashimoto NY et al (2011) MicroRNAs 29 are involved in the improvement of ventricular compliance promoted by aerobic exercise training in rats. Physiol Genomics 43(11):665–673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. van Rooij E, Quiat D, Johnson BA et al (2009) A family of microRNAs encoded by myosin genes governs myosin expression and muscle performance. Dev Cell 17(5):662–673

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Soci UP, Fernandes T, Barauna VG et al (2016) Epigenetic control of exercise training-induced cardiac hypertrophy by miR-208. Clin Sci (Lond) 130:2005–2015

    Article  CAS  Google Scholar 

  44. Fernandes T, Hashimoto NY, Magalhaes FC et al (2011) Aerobic exercise training-induced left ventricular hypertrophy involves regulatory MicroRNAs, decreased angiotensin-converting enzyme-angiotensin ii, and synergistic regulation of angiotensin-converting enzyme 2-angiotensin (1-7). Hypertension 58(2):182–189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Mann N, Rosenzweig A (2012) Can exercise teach us how to treat heart disease? Circulation 126(22):2625–2635

    Article  PubMed  PubMed Central  Google Scholar 

  46. Ma Z, Qi J, Meng S et al (2013) Swimming exercise training-induced left ventricular hypertrophy involves microRNAs and synergistic regulation of the PI3K/AKT/mTOR signaling pathway. Eur J Appl Physiol 113(10):2473–2486

    Article  CAS  PubMed  Google Scholar 

  47. Liu X, Xiao J, Zhu H et al (2015) miR-222 is necessary for exercise-induced cardiac growth and protects against pathological cardiac remodeling. Cell Metab 21(4):584–595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Shi J, Bei Y, Kong X et al (2017) miR-17-3p contributes to exercise-induced cardiac growth and protects against myocardial ischemia-reperfusion injury. Theranostics 7(3):664–676

    Article  PubMed  PubMed Central  Google Scholar 

  49. van Rooij E, Sutherland LB, Thatcher JE et al (2008) Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis. Proc Natl Acad Sci U S A 105(35):13027–13032

    Article  PubMed  PubMed Central  Google Scholar 

  50. Brown MD (2003) Exercise and coronary vascular remodelling in the healthy heart. Exp Physiol 88(5):645–658

    Article  PubMed  Google Scholar 

  51. Nabel EG, Braunwald E (2012) A tale of coronary artery disease and myocardial infarction. N Engl J Med 366(1):54–63

    Article  CAS  PubMed  Google Scholar 

  52. Palojoki E, Saraste A, Eriksson A et al (2001) Cardiomyocyte apoptosis and ventricular remodeling after myocardial infarction in rats. Am J Physiol Heart Circ Physiol 280(6):H2726–H2731

    Article  CAS  PubMed  Google Scholar 

  53. Melo SF, Fernandes T, Barauna VG et al (2014) Expression of MicroRNA-29 and collagen in cardiac muscle after swimming training in myocardial-infarcted rats. Cell Physiol Biochem 33(3):657–669

    Article  CAS  PubMed  Google Scholar 

  54. Lawler PR, Filion KB, Eisenberg MJ (2011) Efficacy of exercise-based cardiac rehabilitation post-myocardial infarction: a systematic review and meta-analysis of randomized controlled trials. Am Heart J 162(4):571–584.e572

    Article  PubMed  Google Scholar 

  55. Wisloff U, Loennechen JP, Currie S et al (2002) Aerobic exercise reduces cardiomyocyte hypertrophy and increases contractility, Ca2+ sensitivity and SERCA-2 in rat after myocardial infarction. Cardiovasc Res 54(1):162–174

    Article  CAS  PubMed  Google Scholar 

  56. Melo SF, Barauna VG, Neves VJ et al (2015) Exercise training restores the cardiac microRNA-1 and -214 levels regulating Ca2+ handling after myocardial infarction. BMC Cardiovasc Disord 15:166

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  57. Icli B, Wara AK, Moslehi J et al (2013) MicroRNA-26a regulates pathological and physiological angiogenesis by targeting BMP/SMAD1 signaling. Circ Res 113(11):1231–1241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Carden DL, Granger DN (2000) Pathophysiology of ischaemia-reperfusion injury. J Pathol 190(3):255–266

    Article  CAS  PubMed  Google Scholar 

  59. Zhang KR, Liu HT, Zhang HF et al (2007) Long-term aerobic exercise protects the heart against ischemia/reperfusion injury via PI3 kinase-dependent and Akt-mediated mechanism. Apoptosis 12(9):1579–1588

    Article  CAS  PubMed  Google Scholar 

  60. Gomes EC, Silva AN, de Oliveira MR (2012) Oxidants, antioxidants, and the beneficial roles of exercise-induced production of reactive species. Oxidative Med Cell Longev 2012:756132

    Article  CAS  Google Scholar 

  61. Li J, Zhang H, Zhang C (2012) Role of inflammation in the regulation of coronary blood flow in ischemia and reperfusion: mechanisms and therapeutic implications. J Mol Cell Cardiol 52(4):865–872

    Article  CAS  PubMed  Google Scholar 

  62. Felli N, Fontana L, Pelosi E et al (2005) MicroRNAs 221 and 222 inhibit normal erythropoiesis and erythroleukemic cell growth via kit receptor down-modulation. Proc Natl Acad Sci U S A 102(50):18081–18086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Galardi S, Mercatelli N, Giorda E et al (2007) miR-221 and miR-222 expression affects the proliferation potential of human prostate carcinoma cell lines by targeting p27Kip1. J Biol Chem 282(32):23716–23724

    Article  CAS  PubMed  Google Scholar 

  64. Baggish AL, Hale A, Weiner RB et al (2011) Dynamic regulation of circulating microRNA during acute exhaustive exercise and sustained aerobic exercise training. J Physiol 589(16):3983–3994

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Liu SZ, Marcinek DJ (2016) Skeletal muscle bioenergetics in aging and heart failure. Heart Fail Rev 21:723

    Article  CAS  PubMed  Google Scholar 

  66. Souza RW, Fernandez GJ, Cunha JP et al (2015) Regulation of cardiac microRNAs induced by aerobic exercise training during heart failure. Am J Physiol Heart Circ Physiol 309(10):H1629–H1641

    Article  CAS  PubMed  Google Scholar 

  67. Hajdusek P, Kotrc M, Kautzner J et al (2016) Heart rate response to exercise in heart failure patients: the prognostic role of metabolic-chronotropic relation and heart rate recovery. Int J Cardiol 228:588–593

    Article  PubMed  Google Scholar 

  68. Aengevaeren VL, Hopman MT, Thijssen DH et al (2017) Endurance exercise-induced changes in BNP concentrations in cardiovascular patients versus healthy controls. Int J Cardiol 227:430–435

    Article  PubMed  Google Scholar 

  69. Giuliano C, Karahalios A, Neil C et al (2017) The effects of resistance training on muscle strength, quality of life and aerobic capacity in patients with chronic heart failure – a meta-analysis. Int J Cardiol 227:413–423

    Article  PubMed  Google Scholar 

  70. Wisloff U, Stoylen A, Loennechen JP et al (2007) Superior cardiovascular effect of aerobic interval training versus moderate continuous training in heart failure patients: a randomized study. Circulation 115(24):3086–3094

    Article  PubMed  Google Scholar 

  71. Haykowsky MJ, Liang Y, Pechter D et al (2007) A meta-analysis of the effect of exercise training on left ventricular remodeling in heart failure patients: the benefit depends on the type of training performed. J Am Coll Cardiol 49(24):2329–2336

    Article  PubMed  Google Scholar 

  72. Heymans S, Corsten MF, Verhesen W et al (2013) Macrophage microRNA-155 promotes cardiac hypertrophy and failure. Circulation 128(13):1420–1432

    Article  CAS  PubMed  Google Scholar 

  73. Aurora AB, Mahmoud AI, Luo X et al (2012) MicroRNA-214 protects the mouse heart from ischemic injury by controlling Ca(2)(+) overload and cell death. J Clin Invest 122(4):1222–1232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Baars T, Skyschally A, Klein-Hitpass L et al (2014) microRNA expression and its potential role in cardioprotection by ischemic postconditioning in pigs. Pflugers Arch 466(10):1953–1961

    Article  CAS  PubMed  Google Scholar 

  75. Li J, Rohailla S, Gelber N et al (2014) MicroRNA-144 is a circulating effector of remote ischemic preconditioning. Basic Res Cardiol 109(5):423

    Article  PubMed  CAS  Google Scholar 

  76. Tu Y, Wan L, Fan Y et al (2013) Ischemic postconditioning-mediated miRNA-21 protects against cardiac ischemia/reperfusion injury via PTEN/Akt pathway. PLoS One 8(10):e75872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Varga ZV, Zvara A, Farago N et al (2014) MicroRNAs associated with ischemia-reperfusion injury and cardioprotection by ischemic pre- and postconditioning: protectomiRs. Am J Physiol Heart Circ Physiol 307(2):H216–H227

    Article  CAS  PubMed  Google Scholar 

  78. Masoudi FA, Inzucchi SE (2007) Diabetes mellitus and heart failure: epidemiology, mechanisms, and pharmacotherapy. Am J Cardiol 99(4a):113b–132b

    Article  CAS  PubMed  Google Scholar 

  79. Raymond T, Raymond R, Lincoff AM (2013) Management of the patient with diabetes and coronary artery disease: a contemporary review. Futur Cardiol 9(3):387–403

    Article  CAS  Google Scholar 

  80. Cleland SJ (2012) Cardiovascular risk in double diabetes mellitus—when two worlds collide. Nat Rev Endocrinol 8(8):476–485

    Article  CAS  PubMed  Google Scholar 

  81. Shaw JE, Sicree RA, Zimmet PZ (2010) Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract 87(1):4–14

    Article  CAS  PubMed  Google Scholar 

  82. Wang H, Bei Y, Lu Y et al (2015) Exercise prevents cardiac injury and improves mitochondrial biogenesis in advanced diabetic cardiomyopathy with PGC-1alpha and Akt activation. Cell Physiol Biochem 35(6):2159–2168

    Article  CAS  PubMed  Google Scholar 

  83. Le Douairon Lahaye S, Bekono FR, Broderick T (2014) Physical activity and diabetic cardiomyopathy: myocardial adaptation depending on exercise load. Curr Diabetes Rev 10(6):371–390

    Article  PubMed  Google Scholar 

  84. Kalani A, Tyagi A, Tyagi N (2014) Exosomes: mediators of neurodegeneration, neuroprotection and therapeutics. Mol Neurobiol 49(1):590–600

    Article  CAS  PubMed  Google Scholar 

  85. Barile L, Lionetti V, Cervio E et al (2014) Extracellular vesicles from human cardiac progenitor cells inhibit cardiomyocyte apoptosis and improve cardiac function after myocardial infarction. Cardiovasc Res 103(4):530–541

    Article  CAS  PubMed  Google Scholar 

  86. Ibrahim AG, Cheng K, Marban E (2014) Exosomes as critical agents of cardiac regeneration triggered by cell therapy. Stem Cell Rep 2(5):606–619

    Article  CAS  Google Scholar 

  87. Chaturvedi P, Kalani A, Medina I et al (2015) Cardiosome mediated regulation of MMP9 in diabetic heart: role of mir29b and mir455 in exercise. J Cell Mol Med 19(9):2153–2161

    CAS  PubMed  PubMed Central  Google Scholar 

  88. Stellos K, Gatsiou A, Stamatelopoulos K et al (2016) Adenosine-to-inosine RNA editing controls cathepsin S expression in atherosclerosis by enabling HuR-mediated post-transcriptional regulation. Nat Med 22(10):1140–1150

    Article  CAS  PubMed  Google Scholar 

  89. Woollard KJ (2013) Immunological aspects of atherosclerosis. Clin Sci (Lond) 125(5):221–235

    Article  CAS  Google Scholar 

  90. Ahmed HM, Blaha MJ, Nasir K et al (2012) Effects of physical activity on cardiovascular disease. Am J Cardiol 109(2):288–295

    Article  PubMed  Google Scholar 

  91. Kraus WE, Houmard JA, Duscha BD et al (2002) Effects of the amount and intensity of exercise on plasma lipoproteins. N Engl J Med 347(19):1483–1492

    Article  CAS  PubMed  Google Scholar 

  92. XD W, Zeng K, Liu WL et al (2014) Effect of aerobic exercise on miRNA-TLR4 signaling in atherosclerosis. Int J Sports Med 35(4):344–350

    Google Scholar 

  93. Munroe PB, Barnes MR, Caulfield MJ (2013) Advances in blood pressure genomics. Circ Res 112(10):1365–1379

    Article  CAS  PubMed  Google Scholar 

  94. Amaral SL, Zorn TM, Michelini LC (2000) Exercise training normalizes wall-to-lumen ratio of the gracilis muscle arterioles and reduces pressure in spontaneously hypertensive rats. J Hypertens 18(11):1563–1572

    Article  CAS  PubMed  Google Scholar 

  95. Melo RM, Martinho E Jr, Michelini LC (2003) Training-induced, pressure-lowering effect in SHR: wide effects on circulatory profile of exercised and nonexercised muscles. Hypertension 42(4):851–857

    Article  CAS  PubMed  Google Scholar 

  96. Hagberg JM, Park JJ, Brown MD (2000) The role of exercise training in the treatment of hypertension: an update. Sports Med 30(3):193–206

    Article  CAS  PubMed  Google Scholar 

  97. Fernandes T, Magalhaes FC, Roque FR et al (2012) Exercise training prevents the microvascular rarefaction in hypertension balancing angiogenic and apoptotic factors: role of microRNAs-16, -21, and -126. Hypertension 59(2):513–520

    Article  CAS  PubMed  Google Scholar 

  98. Sun CY, She XM, Qin Y et al (2013) miR-15a and miR-16 affect the angiogenesis of multiple myeloma by targeting VEGF. Carcinogenesis 34(2):426–435

    Article  CAS  PubMed  Google Scholar 

  99. Diniz MG, Gomes CC, de Castro WH et al (2012) miR-15a/16-1 influences BCL2 expression in keratocystic odontogenic tumors. Cell Oncol (Dordr) 35(4):285–291

    Article  CAS  Google Scholar 

  100. Harmalkar M, Upraity S, Kazi S et al (2015) Tamoxifen-induced cell death of malignant glioma cells is brought about by oxidative-stress-mediated alterations in the expression of BCL2 family members and is enhanced on miR-21 inhibition. J Mol Neurosci 57(2):197–202

    Article  CAS  PubMed  Google Scholar 

  101. Salajegheh A, Vosgha H, Rahman MA et al (2016) Interactive role of miR-126 on VEGF-A and progression of papillary and undifferentiated thyroid carcinoma. Hum Pathol 51:75–85

    Article  CAS  PubMed  Google Scholar 

  102. Benza RL, Miller DP, Barst RJ et al (2012) An evaluation of long-term survival from time of diagnosis in pulmonary arterial hypertension from the REVEAL registry. Chest 142(2):448–456

    Article  PubMed  Google Scholar 

  103. Humbert M, Sitbon O, Chaouat A et al (2010) Survival in patients with idiopathic, familial, and anorexigen-associated pulmonary arterial hypertension in the modern management era. Circulation 122(2):156–163

    Article  PubMed  Google Scholar 

  104. Paolillo S, Farina S, Bussotti M et al (2012) Exercise testing in the clinical management of patients affected by pulmonary arterial hypertension. Eur J Prev Cardiol 19(5):960–971

    Article  PubMed  Google Scholar 

  105. Arena R, Cahalin LP, Borghi-Silva A et al (2015) The effect of exercise training on the pulmonary arterial system in patients with pulmonary hypertension. Prog Cardiovasc Dis 57(5):480–488

    Article  PubMed  Google Scholar 

  106. Grunig E, Maier F, Ehlken N et al (2012) Exercise training in pulmonary arterial hypertension associated with connective tissue diseases. Arthritis Res Ther 14(3):R148

    Article  PubMed  PubMed Central  Google Scholar 

  107. Colombo R, Siqueira R, Becker CU et al (2013) Effects of exercise on monocrotaline-induced changes in right heart function and pulmonary artery remodeling in rats. Can J Physiol Pharmacol 91(1):38–44

    Article  CAS  PubMed  Google Scholar 

  108. Ajit SK (2012) Circulating microRNAs as biomarkers, therapeutic targets, and signaling molecules. Sensors (Basel) 12(3):3359–3369

    Article  CAS  Google Scholar 

  109. Arroyo JD, Chevillet JR, Kroh EM et al (2011) Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci U S A 108(12):5003–5008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Turchinovich A, Weiz L, Langheinz A et al (2011) Characterization of extracellular circulating microRNA. Nucleic Acids Res 39(16):7223–7233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Mitchell PS, Parkin RK, Kroh EM et al (2008) Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci U S A 105(30):10513–10518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Laterza OF, Lim L, Garrett-Engele PW et al (2009) Plasma MicroRNAs as sensitive and specific biomarkers of tissue injury. Clin Chem 55(11):1977–1983

    Article  PubMed  CAS  Google Scholar 

  113. Baggish AL, Park J, Min PK et al (2014) Rapid upregulation and clearance of distinct circulating microRNAs after prolonged aerobic exercise. J Appl Physiol (1985) 116(5):522–531

    Article  CAS  Google Scholar 

  114. Arem H, Moore SC, Patel A et al (2015) Leisure time physical activity and mortality: a detailed pooled analysis of the dose-response relationship. JAMA Intern Med 175(6):959–967

    Article  PubMed  PubMed Central  Google Scholar 

  115. Ai J, Zhang R, Li Y et al (2010) Circulating microRNA-1 as a potential novel biomarker for acute myocardial infarction. Biochem Biophys Res Commun 391(1):73–77

    Article  CAS  PubMed  Google Scholar 

  116. Mooren FC, Viereck J, Kruger K et al (2014) Circulating microRNAs as potential biomarkers of aerobic exercise capacity. Am J Physiol Heart Circ Physiol 306(4):H557–H563

    Article  CAS  PubMed  Google Scholar 

  117. Hartmann D, Fiedler J, Sonnenschein K et al (2016) MicroRNA-based therapy of GATA2-deficient vascular disease. Circulation 134(24):1973–1990

    Article  CAS  PubMed  Google Scholar 

  118. Li K, Ching D, Luk FS et al (2015) Apolipoprotein E enhances microRNA-146a in monocytes and macrophages to suppress nuclear factor-kappaB-driven inflammation and atherosclerosis. Circ Res 117(1):e1–e11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Nielsen S, Akerstrom T, Rinnov A et al (2014) The miRNA plasma signature in response to acute aerobic exercise and endurance training. PLoS One 9(2):e87308

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  120. Sawada S, Kon M, Wada S et al (2013) Profiling of circulating microRNAs after a bout of acute resistance exercise in humans. PLoS One 8(7):e70823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Aoi W, Ichikawa H, Mune K et al (2013) Muscle-enriched microRNA miR-486 decreases in circulation in response to exercise in young men. Front Physiol 4:80

    Article  PubMed  PubMed Central  Google Scholar 

  122. Davis BN, Hilyard AC, Lagna G et al (2008) SMAD proteins control DROSHA-mediated microRNA maturation. Nature 454(7200):56–61

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Hansen TB, Jensen TI, Clausen BH et al (2013) Natural RNA circles function as efficient microRNA sponges. Nature 495(7441):384–388

    Article  CAS  PubMed  Google Scholar 

  124. Lerchenmuller C, Rosenzweig A (2014) Mechanisms of exercise-induced cardiac growth. Drug Discov Today 19(7):1003–1009

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the grants from National Natural Science Foundation of China (81570362, 91639101 and 81200169 to JJ Xiao and 81400647 to Y Bei), and the development fund for Shanghai talents (to JJ Xiao), Innovation Program of Shanghai Municipal Education Commission (2017-01-07-00-09-E00042), the grant from Science and Technology Commission of Shanghai Municipality (17010500100).

Competing Financial Interests

The authors declare no competing financial interests.

Author information

Author notes

  1. Yihua Bei and Lichan Tao contributed equally to this work.

Authors and Affiliations

  1. Cardiac Regeneration and Ageing Lab, School of Life Science, Shanghai University, Shanghai, 200444, China

    Yihua Bei & Junjie Xiao

  2. Department of Cardiology, The Third Affiliated Hospital of Soochow University, Changzhou, 213003, China

    Lichan Tao

  3. Victor Babes National Institute of Pathology, Bucharest, 050096, Romania

    Dragos Cretoiu & Sanda Maria Cretoiu

  4. Division of Cellular and Molecular Biology and Histology, Carol Davila University of Medicine and Pharmacy, Bucharest, 050474, Romania

    Dragos Cretoiu & Sanda Maria Cretoiu

Authors
  1. Yihua Bei
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lichan Tao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dragos Cretoiu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sanda Maria Cretoiu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Junjie Xiao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Junjie Xiao .

Editor information

Editors and Affiliations

  1. Cardiac Regeneration and Ageing Lab, School of Life Science, Shanghai University, Shanghai, China

    Junjie Xiao

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Bei, Y., Tao, L., Cretoiu, D., Cretoiu, S.M., Xiao, J. (2017). MicroRNAs Mediate Beneficial Effects of Exercise in Heart. In: Xiao, J. (eds) Exercise for Cardiovascular Disease Prevention and Treatment. Advances in Experimental Medicine and Biology, vol 1000. Springer, Singapore. https://doi.org/10.1007/978-981-10-4304-8_15

Download citation

Publish with us

Policies and ethics

Search

Navigation