Eccentric and concentric cardiac hypertrophy induced by exercise training: MicroRNAs and molecular determinants

Brazilian Journal of Medical and Biological Research

Volumn 44, Issue 9, 2011, Pages 836-847

  Fernandes, T ^a   Soci, U P R ^a   Oliveira, E M ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Akt; AT1 receptor; Cardiac hypertrophy; Exercise training; MicroRNAs; Renin angiotensin system

Indexed keywords

ACTIN; ALDOSTERONE; ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN 1 RECEPTOR ANTAGONIST; ANGIOTENSIN II; ATRIAL NATRIURETIC FACTOR; ISOPRENALINE; LOSARTAN; MICRORNA; MYOSIN HEAVY CHAIN BETA;

CONCENTRIC MUSCLE CONTRACTION; DISEASE MARKER; ECCENTRIC MUSCLE CONTRACTION; EXERCISE; HEART VENTRICLE HYPERTROPHY; HUMAN; MOLECULAR MECHANICS; NONHUMAN; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; SARCOMERE;

EID: 80053331731     PISSN: 0100879X     EISSN: 1414431X     Source Type: Journal    
DOI: 10.1590/S0100-879X2011007500112     Document Type: Review

References (60)

1. Pluim BM, Zwinderman AH, van der Laarse A, van der Wall EE. The athlete's heart. A meta-analysis of cardiac structure and function. Circulation 2000; 101: 336-344.
2. Dorn GW. The fuzzy logic of physiological cardiac hypertrophy. Hypertension 2007; 49: 962-970.
3. Steding K, Engblom H, Buhre T, Carlsson M, Mosen H, Wohlfart B, et al. Relation between cardiac dimensions and peak oxygen uptake. J Cardiovasc Magn Reson 2010; 12: 8.
4. Longhurst JC, Kelly AR, Gonyea WJ, Mitchell JH. Echocardiographic left ventricular masses in distance runners and weight lifters. J Appl Physiol 1980; 48: 154-162.
5. Grossman W, Jones D, McLaurin LP. Wall stress and patterns of hypertrophy in the human left ventricle. J Clin Invest 1975; 56: 56-64.
6. MacDougall JD, Tuxen D, Sale DG, Moroz JR, Sutton JR. Arterial blood pressure response to heavy resistance exercise. J Appl Physiol 1985; 58: 785-790.
7. MacDougall JD, McKelvie RS, Moroz DE, Sale DG, McCartney N, Buick F. Factors affecting blood pressure during heavy weight lifting and static contractions. J Appl Physiol 1992; 73: 1590-1597.
8. Zamo FS, Lacchini S, Mostarda C, Chiavegatto S, Silva IC, Oliveira EM, et al. Hemodynamic, morphometric and autonomic patterns in hypertensive rats-Renin-Angiotensin system modulation. Clinics 2010; 65: 85-92.
9. Lal A, Veinot JP, Ganten D, Leenen FH. Prevention of cardiac remodeling after myocardial infarction in transgenic rats deficient in brain angiotensinogen. J Mol Cell Cardiol 2005; 39: 521-529.
10. Pereira MG, Ferreira JC, Bueno CR Jr, Mattos KC, Rosa KT, Irigoyen MC, et al. Exercise training reduces cardiac angiotensin II levels and prevents cardiac dysfunction in a genetic model of sympathetic hyperactivity-induced heart failure in mice. Eur J Appl Physiol 2009; 105: 843-850.
11. Riebe D, Fernhall B, Thompson PD. The blood pressure response to exercise in anabolic steroid users. Med Sci Sports Exerc 1992; 24: 633-637.
12. do Carmo EC, Fernandes T, Koike D, da Silva NDJ, Mattos KC, Rosa KT, et al. Anabolic Steroid Associated To Physical Training Induces Deleterious Cardiac Effects. Med Sci Sports Exerc 2011 [Epub ahead of print].
13. Barauna VG, Batista ML Jr, Costa Rosa LF, Casarini DE, Krieger JE, Oliveira EM. Cardiovascular adaptations in rats submitted to a resistance-training model. Clin Exp Pharmacol Physiol 2005; 32: 249-254.
14. Barauna VG, Rosa KT, Irigoyen MC, de Oliveira EM. Effects of resistance training on ventricular function and hypertrophy in a rat model. Clin Med Res 2007; 5: 114-120.
15. Tamaki T, Uchiyama S, Nakano S. A weight-lifting exercise model for inducing hypertrophy in the hindlimb muscles of rats. Med Sci Sports Exerc 1992; 24: 881-886.
16. de Cassia Cypriano Ervati Pinter R, Padilha AS, de Oliveira EM, Vassallo DV, de Fucio Lizardo JH. Cardiovascular adaptive responses in rats submitted to moderate resistance training. Eur J Appl Physiol 2008; 103: 605-613.
17. Barauna VG, Magalhaes FC, Krieger JE, Oliveira EM. AT1 receptor participates in the cardiac hypertrophy induced by resistance training in rats. Am J Physiol Regul Integr Comp Physiol 2008; 295: R381-R387.
18. Izumo S, Nadal-Ginard B, Mahdavi V. Protooncogene induction and reprogramming of cardiac gene expression produced by pressure overload. Proc Natl Acad Sci U S A 1988; 85: 339-343.
19. Oliveira EM, Sasaki MS, Cerencio M, Barauna VG, Krieger JE. Local renin-angiotensin system regulates left ventricular hypertrophy induced by swimming training independent of circulating renin: a pharmacological study. J Renin Angiotensin Aldosterone Syst 2009; 10: 15-23.
20. Soci UP, Fernandes T, Hashimoto NY, Mota GF, Amadeu MA, Rosa KT, et al. MicroRNAs 29 are involved in the improvement of ventricular compliance promoted by aerobic exercise training in rats. Physiol Genomics 2011; 43: 665-673.
21. Rafalski K, Abdourahman A, Edwards JG. Early adaptations to training: upregulation of alpha-myosin heavy chain gene expression. Med Sci Sports Exerc 2007; 39: 75-82.
22. Medeiros A, Oliveira EM, Gianolla R, Casarini DE, Negrao CE, Brum PC. Swimming training increases cardiac vagal activity and induces cardiac hypertrophy in rats. Braz J Med Biol Res 2004; 37: 1909-1917.
23. Claessens C, Claessens P, Bloemen H, Claessens M, Verbanck M, Fagard R, et al. Structural heart adaptations in triathletes. Acta Cardiol 1999; 54: 317-325.
24. Wang Y, Wisloff U, Kemi OJ. Animal models in the study of exercise-induced cardiac hypertrophy. Physiol Res 2010; 59: 633-644.
25. Evangelista FS, Krieger JE. Small gene effect and exercise training-induced cardiac hypertrophy in mice: an Ace gene dosage study. Physiol Genomics 2006; 27: 231-236.
26. Dostal DE. The cardiac renin-angiotensin system: novel signaling mechanisms related to cardiac growth and function. Regul Pept 2000; 91: 1-11.
27. Wagenaar LJ, Voors AA, Buikema H, van Gilst WH. Angiotensin receptors in the cardiovascular system. Can J Cardiol 2002; 18: 1331-1339.
28. Sadoshima J, Xu Y, Slayter HS, Izumo S. Autocrine release of angiotensin II mediates stretch-induced hypertrophy of cardiac myocytes in vitro. Cell 1993; 75: 977-984.
29. Sadoshima J, Izumo S. Molecular characterization of angiotensin II-induced hypertrophy of cardiac myocytes and hyperplasia of cardiac fibroblasts. Critical role of the AT1 receptor subtype. Circ Res 1993; 73: 413-423.
30. Reudelhuber TL, Bernstein KE, Delafontaine P. Is angiotensin II a direct mediator of left ventricular hypertrophy? Time for another look. Hypertension 2007; 49: 1196-1201.
31. van Kats JP, Methot D, Paradis P, Silversides DW, Reudelhuber TL. Use of a biological peptide pump to study chronic peptide hormone action in transgenic mice. Direct and indirect effects of angiotensin II on the heart. J Biol Chem 2001; 276: 44012-44017.
32. Xiao HD, Fuchs S, Bernstein EA, Li P, Campbell DJ, Bernstein KE. Mice expressing ACE only in the heart show that increased cardiac angiotensin II is not associated with cardiac hypertrophy. Am J Physiol Heart Circ Physiol 2008; 294: H659-H667.
33. Zhai P, Yamamoto M, Galeotti J, Liu J, Masurekar M, Thaisz J, et al. Cardiac-specific overexpression of AT1 receptor mutant lacking G alpha q/G alpha i coupling causes hypertrophy and bradycardia in transgenic mice. J Clin Invest 2005; 115: 3045-3056.
34. Zou Y, Akazawa H, Qin Y, Sano M, Takano H, Minamino T, et al. Mechanical stress activates angiotensin II type 1 receptor without the involvement of angiotensin II. Nat Cell Biol 2004; 6: 499-506.
35. Yasuda N, Miura S, Akazawa H, Tanaka T, Qin Y, Kiya Y, et al. Conformational switch of angiotensin II type 1 receptor underlying mechanical stress-induced activation. EMBO Rep 2008; 9: 179-186.
36. Shikata C, Takeda A, Takeda N. Effect of an ACE inhibitor and an AT1 receptor antagonist on cardiac hypertrophy. Mol Cell Biochem 2003; 248: 197-202.
37. Varo N, Iraburu MJ, Varela M, Lopez B, Etayo JC, Diez J. Chronic AT(1) blockade stimulates extracellular collagen type I degradation and reverses myocardial fibrosis in spontaneously hypertensive rats. Hypertension 2000; 35: 1197-1202.
38. Crackower MA, Sarao R, Oudit GY, Yagil C, Kozieradzki I, Scanga SE, et al. Angiotensin-converting enzyme 2 is an essential regulator of heart function. Nature 2002; 417: 822-828.
39. Mercure C, Yogi A, Callera GE, Aranha AB, Bader M, Ferreira AJ, et al. Angiotensin(1-7) blunts hypertensive cardiac remodeling by a direct effect on the heart. Circ Res 2008; 103: 1319-1326.
40. Keidar S, Kaplan M, Gamliel-Lazarovich A. ACE2 of the heart: From angiotensin I to angiotensin (1-7). Cardiovasc Res 2007; 73: 463-469.
41. Fernandes T, Hashimoto NY, Magalhaes FC, Fernandes FB, Casarini DE, Carmona AK, et al. 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 2011; 58: 182-189.
42. Geenen DL, Malhotra A, Buttrick PM. Angiotensin receptor 1 blockade does not prevent physiological cardiac hypertrophy in the adult rat. J Appl Physiol 1996; 81: 816-821.
43. Zhai P, Galeotti J, Liu J, Holle E, Yu X, Wagner T, et al. An angiotensin II type 1 receptor mutant lacking epidermal growth factor receptor transactivation does not induce angiotensin II-mediated cardiac hypertrophy. Circ Res 2006; 99: 528-536.
44. DeBosch B, Treskov I, Lupu TS, Weinheimer C, Kovacs A, Courtois M, et al. Akt1 is required for physiological cardiac growth. Circulation 2006; 113: 2097-2104.
45. Kemi OJ, Ceci M, Wisloff U, Grimaldi S, Gallo P, Smith GL, et al. Activation or inactivation of cardiac Akt/mTOR signaling diverges physiological from pathological hypertrophy. J Cell Physiol 2008; 214: 316-321.
46. Melo SFS, Amadeu MA, Fernandes T, Carmo EC, Magalhaes FC, Barreti DLM, et al. A session of strength exercise induced cardiac hypertrophy by AT1 receptor-Akt-mTOR signaling pathway. FASEB J 2010; 24: 622.1 (Abstract).
47. Nagoshi T, Matsui T, Aoyama T, Leri A, Anversa P, Li L, et al. PI3K rescues the detrimental effects of chronic Akt activation in the heart during ischemia/reperfusion injury. J Clin Invest 2006; 115: 2128-2138.
48. Ohtani K, Dimmeler S. Control of cardiovascular differentiation by microRNAs. Basic Res Cardiol 2011; 106: 5-11.
49. Ghildiyal M, Zamore PD. Small silencing RNAs: an expanding universe. Nat Rev Genet 2009; 10: 94-108.
50. Care A, Catalucci D, Felicetti F, Bonci D, Addario A, Gallo P, et al. MicroRNA-133 controls cardiac hypertrophy. Nat Med 2007; 13: 613-618.
51. Rao PK, Toyama Y, Chiang HR, Gupta S, Bauer M, Medvid R, et al. Loss of cardiac microRNA-mediated regulation leads to dilated cardiomyopathy and heart failure. Circ Res 2009; 105: 585-594.
52. Lin Z, Murtaza I, Wang K, Jiao J, Gao J, Li PF. miR-23a functions downstream of NFATc3 to regulate cardiac hypertrophy. Proc Natl Acad Sci U S A 2009; 106: 12103-12108.
53. van Rooij E, Sutherland LB, Thatcher JE, DiMaio JM, Naseem RH, Marshall WS, et al. Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis. Proc Natl Acad Sci U S A 2008; 105: 13027-13032.
54. Sayed D, Abdellatif M. AKT-ing via microRNA. Cell Cycle 2010; 9: 3213-3217.
55. Thum T, Gross C, Fiedler J, Fischer T, Kissler S, Bussen M, et al. MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature 2008; 456: 980-984.
56. Small EM, Olson EN. Pervasive roles of microRNAs in cardiovascular biology. Nature 2011; 469: 336-342.
57. van Rooij E, Sutherland LB, Liu N, Williams AH, McAnally J, Gerard RD, et al. A signature pattern of stress-responsive microRNAs that can evoke cardiac hypertrophy and heart failure. Proc Natl Acad Sci U S A 2006; 103: 18255-18260.
58. van Rooij E, Quiat D, Johnson BA, Sutherland LB, Qi X, Richardson JA, et al. A family of microRNAs encoded by myosin genes governs myosin expression and muscle performance. Dev Cell 2009; 17: 662-673.
59. Boettger T, Beetz N, Kostin S, Schneider J, Kruger M, Hein L, et al. Acquisition of the contractile phenotype by murine arterial smooth muscle cells depends on the Mir143/145 gene cluster. J Clin Invest 2009; 119: 2634-2647.
60. Elton TS, Sansom SE, Martin MM. Cardiovascular disease, single nucleotide polymorphisms; and the renin angiotensin system: Is there a MicroRNA connection? Int J Hypertens 2010; doi: 10.4061/2010/281692.