Cardiac anti-remodelling effect of aerobic training is associated with a reduction in the calcineurin/NFAT signalling pathway in heart failure mice

Journal of Physiology

Volumn 587, Issue 15, 2009, Pages 3899-3910

  Oliveira, R S F ^a   Ferreira, J C B ^a   Gomes, E R M ^b   Paixao N A ^a   Rolim, N P L ^a   Medeiros, A ^a   Guatimosim, S ^b   Brum, P C ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA 2A ADRENERGIC RECEPTOR; ALPHA 2C ADRENERGIC RECEPTOR; CALCINEURIN; CALCINEURIN B; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CYCLOSPORIN; HISTONE DEACETYLASE; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN KINASE B; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR NFATC3; UNCLASSIFIED DRUG; MYOSIN HEAVY CHAIN BETA;

AEROBIC EXERCISE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME ACTIVATION; EXERCISE TOLERANCE; EXPERIMENTAL MOUSE; HEART DILATATION; HEART DISEASE; HEART FAILURE; HEART FUNCTION; HEART VENTRICLE FUNCTION; HEART VENTRICLE HYPERTROPHY; HEART VENTRICLE REMODELING; HEART WEIGHT; HYPERACTIVITY; MALE; MOUSE; NONHUMAN; NUCLEIC ACID TRANSPORT; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SYMPATHETIC FUNCTION; ANTI CARDIAC REMODELLING EFFECT; BETA MHC GENE; CARDIOMYOCYTE WIDTH; CELLULAR PARAMETERS; EXERCISE; EXERCISE INTENSITY; EXERCISE INTOLERANCE; GENE EXPRESSION; HEART LEFT VENTRICLE HYPERTROPHY; HEART LEFT VENTRICLE SIZE; HEART MUSCLE CELL; LEFT VENTRICULAR END DIASTOLIC DIMENSION; PROTEIN LOCALIZATION; SYMPATHETIC HYPERACTIVITY; SYMPATHETIC TONE; THERAPY EFFECT; TREATMENT DURATION;

ANIMALS; CALCINEURIN; CARDIOMEGALY; CARRIER PROTEINS; CYCLOSPORINE; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; EXERCISE TOLERANCE; HEART FAILURE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCYTES, CARDIAC; NFATC TRANSCRIPTION FACTORS; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PHYSICAL CONDITIONING, ANIMAL; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, ADRENERGIC, ALPHA-2; SIGNAL TRANSDUCTION; VENTRICULAR REMODELING;

EID: 68149168072     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2009.173948     Document Type: Article

References (50)

1. Atherton PJ, Babraj J, Smith K, Singh J, Rennie MJ & Wackerhage H (2005). Selective activation of AMPKPGC-1α or PKB-TSC2-mTOR signalling can explain specific adaptive responses to endurance or resistance training-like electrical muscle stimulation. FASEB J 19, 786-788.
2. Balke CW & Shorofsky SR (1998). Alterations in calcium handling in cardiac hypertrophy and heart failure. Cardiovasc Res 37, 290-299.
3. Barki-Harrington L, Perrino C & Rockman HA (2004). Network integration of the adrenergic system in cardiac hypertrophy. Cardiovasc Res 63, 391-402.
4. Bartholomeu JB, Vanzelli AS, Rolim NP, Ferreira JC, Bechara LR, Tanaka LY, Rosa KT, Alves MM, Medeiros A, Mattos KC, Coelho MA, Irigoyen MC, Krieger EM, Krieger JE, Negrao CE, Ramires PR, Guatimosim S & Brum PC (2008). Intracellular mechanisms of specific β-adrenoceptor antagonists involved in improved cardiac function and survival in a genetic model of heart failure. J Mol Cell Cardiol 45, 240-249.
5. Bourajjaj M, Armand AS, da Costa Martins PA, Weijts B, Van Der Nagel R, Heeneman S, Wehrens XH & De Windt LJ (2008). NFATc2 is a necessary mediator of calcineurin-dependent cardiac hypertrophy and heart failure. J Biol Chem 283, 22295-22305.
6. Brum PC, Kosek J, Patterson A, Bernstein D & Kobilka B (2002). Abnormal cardiac function associated with sympathetic nervous system hyperactivity in mice. Am J Physiol Heart Circ Physiol 283, H1838-1845.
7. Bueno OF, Wilkins BJ, Tymitz KM, Glascock BJ, Kimball TF, Lorenz JN & Molkentin JD (2002). Impaired cardiac hypertrophic response in calcineurin Aβ-deficient mice. Proc Natl Acad Sci U S A 99, 4586-4591.
8. Bustamante JO, Ruknudin A & Sachs F (1991). Stretch-activated channels in heart cells: Relevance to cardiac hypertrophy. J Cardiovasc Pharmacol 17(Suppl 2), S110-113.
9. Condorelli G, Drusco A, Stassi G, Bellacosa A, Roncarati R, Iaccarino G, Russo MA, Gu Y, Dalton N, Chung C, Latronico MV, Napoli C, Sadoshima J, Croce CM & Ross J Jr (2002). Akt induces enhanced myocardial contractility and cell size in vivo in transgenic mice. Proc Natl Acad Sci U S A 99, 12333-12338.
10. DeBosch B, Treskov I, Lupu TS, Weinheimer C, Kovacs A, Courtois M & Muslin AJ (2006). Akt1 is required for physiological cardiac growth. Circulation 113, 2097-2104.
11. Diedrichs H, Chi M, Boelck B, Mehlhorn U & Schwinger RH (2004). Increased regulatory activity of the calcineurin/NFAT pathway in human heart failure. Eur J Heart Fail 6, 3-9.
12. Ferreira JC, Bacurau AV, Evangelista FS, Coelho MA, Oliveira EM, Casarini DE, Krieger JE & Brum PC (2008). The role of local and systemic renin angiotensin system activation in a genetic model of sympathetic hyperactivity-induced heart failure in mice. Am J Physiol Regul Integr Comp Physiol 294, R26-32.
13. Ferreira JC, Rolim NP, Bartholomeu JB, Gobatto CA, Kokubun E & Brum PC (2007). Maximal lactate steady state in running mice: Effect of exercise training. Clin Exp Pharmacol Physiol 34, 760-765.
14. Fraga R, Franco FG, Roveda F, de Matos LN, Braga AM, Rondon MU, Rotta DR, Brum PC, Barretto AC, Middlekauff HR & Negrao CE (2007). Exercise training reduces sympathetic nerve activity in heart failure patients treated with carvedilol. Eur J Heart Fail 9, 630-636.
15. Frey N & Olson EN (2003). Cardiac hypertrophy: The good, the bad, and the ugly. Annu Rev Physiol 65, 45-79.
16. 2+ regulates cardiomyocyte function. Cell Calcium 44, 230-242.
17. 2+ current. Am J Physiol Cell Physiol 280, C1327-1339.
18. Gwathmey JK, Copelas L, MacKinnon R, Schoen FJ, Feldman MD, Grossman W & Morgan JP (1987). Abnormal intracellular calcium handling in myocardium from patients with end-stage heart failure. Circ Res 61, 70-76.
19. Ho KK, Pinsky JL, Kannel WB & Levy D (1993). The epidemiology of heart failure: The Framingham Study. J Am Coll Cardiol 22, 6A-13A.
20. Jonsdottir S, Andersen KK, Sigurosson AF & Sigurosson SB (2006). The effect of physical training in chronic heart failure. Eur J Heart Fail 8, 97-101.
21. 2+ ATPase function is increased by aerobic interval training. Eur J Cardiovasc Prev Rehabil 15, 145-148.
22. Kemi OJ, Ceci M, Wisloff U, Grimaldi S, Gallo P, Smith GL, Condorelli G & Ellingsen O (2008b). Activation or inactivation of cardiac Akt/ mTOR signalling diverges physiological from pathological hypertrophy. J Cell Physiol 214, 316-321.
23. Konhilas JP, Watson PA, Maass A, Boucek DM, Horn T, Stauffer BL, Luckey SW, Rosenberg P & Leinwand LA (2006). Exercise can prevent and reverse the severity of hypertrophic cardiomyopathy. Circ Res 98, 540-548.
24. Levy D, Garrison RJ, Savage DD, Kannel WB & Castelli WP (1990). Prognostic implications of echocardiographically determined left ventricular mass in the Framingham Heart Study. N Engl J Med 322, 1561-1566.
25. Lim HW, De Windt LJ, Steinberg L, Taigen T, Witt SA, Kimball TR & Molkentin JD (2000). Calcineurin expression, activation, and function in cardiac pressure-overload hypertrophy. Circulation 101, 2431-2437.
26. Lorell BH & Carabello BA (2000). Left ventricular hypertrophy: pathogenesis, detection, and prognosis. Circulation 102, 470-479.
27. Lu L, Mei DF, Gu AG, Wang S, Lentzner B, Gutstein DE, Zwas D, Homma S, Yi GH & Wang J (2002). Exercise training normalizes altered calcium-handling proteins during development of heart failure. J Appl Physiol 92, 1524-1530.
28. MacDonnell SM, Kubo H, Harris DM, Chen X, Berretta R, Barbe MF, Kolwicz S, Reger PO, Eckhart A, Renna BF, Koch WJ, Houser SR & Libonati JR (2007). Calcineurin inhibition normalizes β-adrenergic responsiveness in the spontaneously hypertensive rat. Am J Physiol Heart Circ Physiol 293, H3122-3129.
29. Maier LS (2009). Role of CaMKII for signalling and regulation in the heart. Front Biosci 14, 486-496.
30. McMullen JR, Amirahmadi F, Woodcock EA, Schinke-Braun M, Bouwman RD, Hewitt KA, Mollica JP, Zhang L, Zhang Y, Shioi T, Buerger A, Izumo S, Jay PY & Jennings GL (2007). Protective effects of exercise and phosphoinositide 3-kinase(p110α) signalling in dilated and hypertrophic cardiomyopathy. Proc Natl Acad Sci U S A 104, 612-617.
31. McMullen JR, Shioi T, Zhang L, Tarnavski O, Sherwood MC, Kang PM & Izumo S (2003). Phosphoinositide 3-kinase(p110α) plays a critical role for the induction of physiological, but not pathological, cardiac hypertrophy. Proc Natl Acad Sci U S A 100, 12355-12360.
32. Medeiros A, Rolim NP, Oliveira RS, Rosa KT, Mattos KC, Casarini DE, Irigoyen MC, Krieger EM, Krieger JE, Negrao CE & Brum PC (2008). Exercise training delays cardiac dysfunction and prevents calcium handling abnormalities in sympathetic hyperactivity-induced heart failure mice. J Appl Physiol 104, 103-109.
33. Meguro T, Hong C, Asai K, Takagi G, McKinsey TA, Olson EN & Vatner SF (1999). Cyclosporine attenuates pressure overload hypertrophy in mice while enhancing susceptibility to decompensation and heart failure. Circ Res 84, 735-740.
34. Molkentin JD (2000). Calcineurin and beyond: Cardiac hypertrophic signalling. Circ Res 87, 731-738.
35. Molkentin JD, Lu JR, Antos CL, Markham B, Richardson J, Robbins J, Grant SR & Olson EN (1998). A calcineurin dependent transcriptional pathway for cardiac hypertrophy. Cell 93, 215-228.
36. Munch G, Bolck B, Karczewski P & Schwinger RH (2002). Evidence for calcineurin-mediated regulation of SERCA 2a activity in human myocardium. J Mol Cell Cardiol 34, 321-334.
37. Nader GA & Esser KA (2001). Intracellular signalling specificity in skeletal muscle in response to different modes of exercise. J Appl Physiol 90, 1936-1942.
38. Naylor LH, George K, O'Driscoll G & Green DJ (2008). The athlete's heart: A contemporary appraisal of the 'Morganroth hypothesis'. Sports Med 38, 69-90.
39. Pereira MG, Ferreira JC, Bueno CR Jr, Mattos KC, Rosa KT, Irigoyen MC, Oliveira EM, Krieger JE & Brum PC (2009). 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.
40. 2+ handling protein expression in heart failure. Physiol Genomics 29, 246-252.
41. Rossman EI, Petre RE, Chaudhary KW, Piacentino V 3rd, Janssen PM, Gaughan JP, Houser SR & Margulies KB (2004). Abnormal frequency-dependent responses represent the pathophysiologic signature of contractile failure in human myocardium. J Mol Cell Cardiol 36, 33-42.
42. Roveda F, Middlekauff HR, Rondon MU, Reis SF, Souza M, Nastari L, Barretto AC, Krieger EM & Negrao CE (2003). The effects of exercise training on sympathetic neural activation in advanced heart failure: A randomized controlled trial. J Am Coll Cardiol 42, 854-860.
43. 2+ in cardiac myocytes. Biophys J 95, 4597-4612.
44. 2+- ATPase activity of cardiac sarcoplasmic reticulum from dilated cardiomyopathy patients compared with patients with nonfailing hearts. Circulation 92, 3220-3228.
45. 2+ handling in perfused hypertrophic hearts from Dahl salt-sensitive rats. Hypertens Res 26, 643-653.
46. 2+-calmodulin targets. J Biol Chem 283, 31531-31540.
47. Sussman MA, Lim HW, Gude N, Taigen T, Olson EN, Robbins J, Colbert MC, Gualberto A, Wieczorek DF & Molkentin JD (1998). Prevention of cardiac hypertrophy in mice by calcineurin inhibition. Science 281, 1690-1693.
48. Wilkins BJ, Dai YS, Bueno OF, Parsons SA, Xu J, Plank DM, Jones F, Kimball TR & Molkentin JD (2004). Calcineurin/NFAT coupling participates in pathological, but not physiological, cardiac hypertrophy. Circ Res 94, 110-118.
49. Wilkins BJ, De Windt LJ, Bueno OF, Braz JC, Glascock BJ, Kimball TF & Molkentin JD (2002). Targeted disruption of NFATc3, but not NFATc4, reveals an intrinsic defect in calcineurin-mediated cardiac hypertrophic growth. Mol Cell Biol 22, 7603-7613.
50. Wisloff U, Stoylen A, Loennechen JP, Bruvold M, Rognmo O, Haram PM, Tjonna AE, Helgerud J, Slordahl SA, Lee SJ, Videm V, Bye A, Smith GL, Najjar SM, Ellingsen O & Skjaerpe T (2007). Superior cardiovascular effect of aerobic interval training versus moderate continuous training in heart failure patients: A randomized study. Circulation 115, 3086-3094.