Inhibition of hypertrophy, per se, may not be a good therapeutic strategy in ventricular pressure overload: Other approaches could be more beneficial

Circulation

Volumn 131, Issue 16, 2015, Pages 1448-1457

  Crozatier, Bertrand ^a   Ventura Clapier, Renée ^a  

^a UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN RECEPTOR; CALCINEURIN; GLYCOPROTEIN GP 130; HISTONE DEACETYLASE; P21 ACTIVATED KINASE 1; STRESS ACTIVATED PROTEIN KINASE; CALCINEURIN INHIBITOR; HISTONE DEACETYLASE INHIBITOR;

AORTA STENOSIS; ARTICLE; CARDIOVASCULAR RISK; CELL STRUCTURE; ENERGY TRANSFER; EVOLUTION; HEART FUNCTION; HEART MUSCLE FIBROSIS; HEART MUSCLE PERFUSION; HEART VENTRICLE HYPERTROPHY; HEART VENTRICLE OVERLOAD; INOTROPISM; LONG TERM SURVIVAL; NONHUMAN; PATHOLOGY; PHYSIOLOGICAL PROCESS; PREVENTION; PRIORITY JOURNAL; RISK BENEFIT ANALYSIS; SEX RATIO; WALL STRESS; ANIMAL; AORTA VALVE STENOSIS; COMPLICATION; CORONARY ARTERY BLOOD FLOW; DRUG EFFECTS; FEMALE; FIBROSIS; HEART CONTRACTION; HEART MUSCLE CELL; HEART VENTRICLE REMODELING; HUMAN; HYPERTROPHY, LEFT VENTRICULAR; MALE; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); PATHOPHYSIOLOGY; PHYSIOLOGY; SEX DIFFERENCE; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIUM;

ANIMALS; AORTIC VALVE STENOSIS; CALCINEURIN INHIBITORS; CORONARY CIRCULATION; ENDOTHELIUM, VASCULAR; FEMALE; FIBROSIS; HISTONE DEACETYLASE INHIBITORS; HUMANS; HYPERTROPHY, LEFT VENTRICULAR; MALE; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; NEOVASCULARIZATION, PATHOLOGIC; SEX FACTORS; SIGNAL TRANSDUCTION; VENTRICULAR REMODELING;

EID: 84929378032     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.114.013895     Document Type: Article

References (75)

1. Frey N, Katus HA, Olson EN, Hill JA. Hypertrophy of the heart: a new therapeutic target? Circulation. 2004;109:1580-1589.
2. Meerson FZ. The myocardium in hyperfunction, hypertrophy and heart failure. Circ Res. 1969;25:163.
3. Sasayama S, Ross J Jr, Franklin D, Bloor CM, Bishop S, Dilley RB. Adaptations of the left ventricle to chronic pressure overload. Circ Res. 1976;38:172-178.
4. Alpert NR, Mulieri LA. Heat, mechanics, and myosin ATPase in normal and hypertrophied heart muscle. Fed Proc. 1982;41:192-198.
5. Lompre AM, Schwartz K, d'Albis A, Lacombe G, Van Thiem N, Swynghedauw B. Myosin isoenzyme redistribution in chronic heart overload. Nature. 1979;282:105-107.
6. Swynghedauw B. Molecular mechanisms of myocardial remodeling. Physiol Rev. 1999;79:215-262.
7. Gwathmey JK, Morgan JP. Altered calcium handling in experimental pressure-overload hypertrophy in the ferret. Circ Res. 1985;57:836-843.
8. Limas CJ, Spier SS, Kahlon J. Enhanced calcium transport by sarcoplasmic reticulum in mild cardiac hypertrophy. J Mol Cell Cardiol. 1980;12:1103-1116.
9. Ingwall J. Is cardiac failure a consequence of decreased energy reserve? Circulation. 1993;87:VII 58-62.
10. Tagawa H, Koide M, Sato H, Zile MR, Carabello BA, Cooper G 4th. Cytoskeletal role in the transition from compensated to decompensated hypertrophy during adult canine left ventricular pressure overloading. Circ Res. 1998;82:751-761.
11. Levy D, Garrison RJ, Savage DD, Kannel WB, Castelli WP. Prognostic implications of echocardiographically determined left-ventricular mass in the Framingham-Heart-Study. New Eng J Med. 1990;322:1561-1566.
12. Akhter SA, Luttrell LM, Rockman HA, Iaccarino G, Lefkowitz RJ, Koch WJ. Targeting the receptor-Gq interface to inhibit in vivo pressure overload myocardial hypertrophy. Science. 1998;280:574-577.
13. Sussman MA, Lim HW, Gude N, Taigen T, Olson EN, Robbins J, Colbert MC, Gualberto A, Wieczorek DF, Molkentin JD. Prevention of cardiac hypertrophy in mice by calcineurin inhibition. Science. 1998;281:1690-1693.
14. Wilkins BJ, Dai YS, Bueno OF, Parsons SA, Xu J, Plank DM, Jones F, Kimball TR, Molkentin JD. Calcineurin/NFAT coupling participates in pathological, but not physiological, cardiac hypertrophy. Circ Res. 2004;94:110-118. doi: 10.1161/01.RES.0000109415.17511.18.
15. Grossman W. Cardiac hypertrophy: useful adaptation or pathologic process? Am J Med. 1980;69:576-584.
16. Mann DL, Barger PM, Burkhoff D. Myocardial recovery and the failing heart myth, magic, or molecular target? J Am Coll Cardiol. 2012;60:2465-2472.
17. Bernardo BC, Weeks KL, Pretorius L, McMullen JR. Molecular distinction between physiological and pathological cardiac hypertrophy: experimental findings and therapeutic strategies. Pharmacol Ther. 2010;128:191-227. doi: 10.1016/j.pharmthera.2010.04.005.
18. McMullen JR, Shioi T, Zhang L, Tarnavski O, Sherwood MC, Kang PM, Izumo S. Phosphoinositide 3-kinase(p110 α) plays a critical role for the induction of physiological, but not pathological, cardiac hypertrophy. Proc Natl Acad Sci U S A. 2003;100:12355-12360.
19. DeBosch B, Treskov I, Lupu TS, Weinheimer C, Kovacs A, Courtois M, Muslin AJ. Akt1 is required for physiological cardiac growth. Circulation. 2006;113:2097-2104. doi: 10.1161/CIRCULATIONAHA.105.595231.
20. Uozumi H, Hiroi Y, Zou Y, Takimoto E, Toko H, Niu P, Shimoyama M, Yazaki Y, Nagai R, Komuro I. gp130 plays a critical role in pressure overload-induced cardiac hypertrophy. J Biol Chem. 2001;276:23115-23119. doi: 10.1074/jbc.M100814200.
21. Shimoyama M, Hayashi D, Takimoto E, Zou Y, Oka T, Uozumi H, Kudoh S, Shibasaki F, Yazaki Y, Nagai R, Komuro I. Calcineurin plays a critical role in pressure overload-induced cardiac hypertrophy. Circulation. 1999;100:2449-2454.
22. Zou Y, Hiroi Y, Uozumi H, Takimoto E, Toko H, Zhu W, Kudoh S, Mizukami M, Shimoyama M, Shibasaki F, Nagai R, Yazaki Y, Komuro I. Calcineurin plays a critical role in the development of pressure overload-induced cardiac hypertrophy. Circulation. 2001;104:97-101.
23. Hill JA, Karimi M, Kutschke W, Davisson RL, Zimmerman K, Wang Z, Kerber RE, Weiss RM. Cardiac hypertrophy is not a required compensatory response to short-term pressure overload. Circulation. 2000;101:2863-2869.
24. Hill JA, Rothermel B, Yoo KD, Cabuay B, Demetroulis E, Weiss RM, Kutschke W, Bassel-Duby R, Williams RS. Targeted inhibition of calcineurin in pressure-overload cardiac hypertrophy: preservation of systolic function. J Biol Chem. 2002;277:10251-10255.
25. Choukroun G, Hajjar R, Fry S, del Monte F, Haq S, Guerrero JL, Picard M, Rosenzweig A, Force T. Regulation of cardiac hypertrophy in vivo by the stress-activated protein kinases/c-Jun NH2-terminal kinases. J Clin Invest. 1999;104:391-398.
26. Senbonmatsu T, Ichihara S, Price E Jr, Gaffney FA, Inagami T. Evidence for angiotensin II type 2 receptor-mediated cardiac myocyte enlargement during in vivo pressure overload. J Clin Invest. 2000;106:R25-R29. doi: 10.1172/JCI10037.
27. Esposito G, Rapacciuolo A, Naga Prasad SV, Takaoka H, Thomas SA, Koch WJ, Rockman HA. Genetic alterations that inhibit in vivo pressure-overload hypertrophy prevent cardiac dysfunction despite increased wall stress. Circulation. 2002;105:85-92.
28. Kong Y, Tannous P, Lu G, Berenji K, Rothermel BA, Olson EN, Hill JA. Suppression of class I and II histone deacetylases blunts pressure-overload cardiac hypertrophy. Circulation. 2006;113:2579-2588. doi: 10.1161/CIRCULATIONAHA.106.625467.
29. Giampietri C, Petrungaro S, Musumeci M, Coluccia P, Antonangeli F, De Cesaris P, Filippini A, Marano G, Ziparo E. c-Flip overexpression reduces cardiac hypertrophy in response to pressure overload. J Hypertens. 2008;26:1008-1016. doi: 10.1097/HJH.0b013e3282f6a179.
30. Liu W, Zi M, Naumann R, Ulm S, Jin JW, Taglieri DM, Prehar S, Gui JH, Tsui H, Xiao RP, Neyses L, Solaro RJ, Ke YB, Cartwright EJ, Lei M, Wang X. Pak1 as a novel therapeutic target for antihypertrophic treatment in the heart. Circulation. 2011;124:2702-U289.
31. Völkers M, Toko H, Doroudgar S, Din S, Quijada P, Joyo AY, Ornelas L, Joyo E, Thuerauf DJ, Konstandin MH, Gude N, Glembotski CC, Sussman MA. Pathological hypertrophy amelioration by PRAS40-mediated inhibition of mTORC1. Proc Natl Acad Sci U S A. 2013;110:12661-12666. doi: 10.1073/pnas.1301455110.
32. Martins PAD, Salic K, Gladka MM, Armand AS, Leptidis S, el Azzouzit H, Hansen A, Coenen-de Roo CJ, Bierhuizen MF, van der Nagel R, van Kuik J, de Weger R, de Bruin A, Condorelli G, Arbones ML, Eschenhagen T, De Windt LJ. MicroRNA-199b targets the nuclear kinase Dyrk1a in an auto-amplification loop promoting calcineurin/NFAT signalling. Nat Cell Biol. 2010;12:1220-U231.
33. Ucar A, Gupta SK, Fiedler J, Erikci E, Kardasinski M, Batkai S, Dangwal S, Kumarswamy R, Bang C, Holzmann A, Remke J, Caprio M, Jentzsch C, Engelhardt S, Geisendorf S, Glas C, Hofmann TG, Nessling M, Richter K, Schiffer M, Carrier L, Napp LC, Bauersachs J, Chowdhury K, Thum T. The miRNA-212/132 family regulates both cardiac hypertrophy and cardiomyocyte autophagy. Nat Commun. 2012;3:1078. doi: 10.1038/ncomms2090.
34. Karakikes I, Chaanine AH, Kang S, Mukete BN, Jeong D, Zhang S, Hajjar RJ, Lebeche D. Therapeutic cardiac-targeted delivery of miR-1 reverses pressure overload-induced cardiac hypertrophy and attenuates pathological remodeling. J Am Heart Assoc. 2013;2:e000078. doi: 10.1161/JAHA.113.000078.
35. Muraski JA, Fischer KM, Wu W, Cottage CT, Quijada P, Mason M, Din S, Gude N, Alvarez R Jr, Rota M, Kajstura J, Wang Z, Schaefer E, Chen X, MacDonnel S, Magnuson N, Houser SR, Anversa P, Sussman MA. Pim-1 kinase antagonizes aspects of myocardial hypertrophy and compensation to pathological pressure overload. Proc Natl Acad Sci U S A. 2008;105:13889-13894. doi: 10.1073/pnas.0709135105.
36. Gelpi RJ, Gao S, Zhai P, Yan L, Hong C, Danridge LM, Ge H, Maejima Y, Donato M, Yokota M, Molkentin JD, Vatner DE, Vatner SF, Sadoshima J. Genetic inhibition of calcineurin induces diastolic dysfunction in mice with chronic pressure overload. Am J Physiol Heart Circ Physiol. 2009;297:H1814-H1819. doi: 10.1152/ajpheart.00449.2009.
37. Rothermel BA, Berenji K, Tannous P, Kutschke W, Dey A, Nolan B, Yoo KD, Demetroulis E, Gimbel M, Cabuay B, Karimi M, Hill JA. Differential activation of stress-response signaling in load-induced cardiac hypertrophy and failure. Physiol Genomics. 2005;23:18-27. doi: 10.1152/physiolgenomics.00061.2005.
38. Meguro T, Hong C, Asai K, Takagi G, McKinsey TA, Olson EN, Vatner SF. Cyclosporine attenuates pressure-overload hypertrophy in mice while enhancing susceptibility to decompensation and heart failure. Circ Res. 1999;84:735-740.
39. Brancaccio M, Fratta L, Notte A, Hirsch E, Poulet R, Guazzone S, De Acetis M, Vecchione C, Marino G, Altruda F, Silengo L, Tarone G, Lembo G. Melusin, a muscle-specific integrin β(1)-interacting protein, is required to prevent cardiac failure in response to chronic pressure overload. Nat Med. 2003;9:68-75.
40. Rogers JH, Tamirisa P, Kovacs A, Weinheimer C, Courtois M, Blumer KJ, Kelly DP, Muslin AJ. RGS4 causes increased mortality and reduced cardiac hypertrophy in response to pressure overload. J Clin Invest. 1999;104:567-576. doi: 10.1172/JCI6713.
41. Ichihara S, Senbonmatsu T, Price E Jr, Ichiki T, Gaffney FA, Inagami T. Angiotensin II type 2 receptor is essential for left ventricular hypertrophy and cardiac fibrosis in chronic angiotensin II-induced hypertension. Circulation. 2001;104:346-351.
42. Ichihara S, Senbonmatsu T, Price E Jr, Ichiki T, Gaffney FA, Inagami T. Targeted deletion of angiotensin II type 2 receptor caused cardiac rupture after acute myocardial infarction. Circulation. 2002;106:2244-2249.
43. Takeda N, Manabe I, Uchino Y, Eguchi K, Matsumoto S, Nishimura S, Shindo T, Sano M, Otsu K, Snider P, Conway SJ, Nagai R. Cardiac fibroblasts are essential for the adaptive response of the murine heart to pressure overload. J Clin Invest. 2010;120:254-265. doi: 10.1172/JCI40295.
44. Perrino C, Naga Prasad SV, Mao L, Noma T, Yan Z, Kim HS, Smithies O, Rockman HA. Intermittent pressure overload triggers hypertrophy-independent cardiac dysfunction and vascular rarefaction. J Clin Invest. 2006;116:1547-1560. doi: 10.1172/JCI25397.
45. Crozatier B, Caillet D, Bical O. Left ventricular adaptation to sustained pressure overload in the conscious dog. Circ Res. 1984;54:21-29.
46. Packer M, Carver JR, Rodeheffer RJ, Ivanhoe RJ, Dibianco R, Zeldis SM, Hendrix GH, Bommer WJ, Elkayam U, Kukin ML, Mallis GI, Sollano JA, Shannon J, Tandon PK, Demets DL. Effect of oral milrinone on mortality in severe chronic heart-failure. New Eng J Med. 1991;325:1468-1475.
47. Cohn JN, Goldstein SO, Greenberg BH, Lorell BH, Bourge RC, Jaski BE, Gottlieb SO, McGrew F, DeMets DL, White BG. A dose-dependent increase in mortality with vesnarinone among patients with severe heart failure. New Eng J Med. 1998;339:1810-1816.
48. Douglas PS, Katz SE, Weinberg EO, Chen MH, Bishop SP, Lorell BH. Hypertrophic remodeling: gender differences in the early response to left ventricular pressure overload. J Am Coll Cardiol. 1998;32:1118-1125.
49. Loyer X, Oliviero P, Damy T, Robidel E, Marotte F, Heymes C, Samuel JL. Effects of sex differences on constitutive nitric oxide synthase expression and activity in response to pressure overload in rats. Am J Physiol Heart Circ Physiol. 2007;293:H2650-H2658. doi: 10.1152/ajpheart.00883.2007.
50. Levy D, Larson MG, Vasan RS, Kannel WB, Ho KK. The progression from hypertension to congestive heart failure. JAMA. 1996;275:1557-1562.
51. Bui AL, Horwich TB, Fonarow GC. Epidemiology and risk profile of heart failure. Nat Rev Cardiol. 2011;8:30-41. doi: 10.1038/nrcardio.2010.165.
52. Sorgato A, Faggiano P, Aurigemma GP, Rusconi C, Gaasch WH. Ventricular arrhythmias in adult aortic stenosis: prevalence, mechanisms, and clinical relevance. Chest. 1998;113:482-491.
53. Alyono D, Anderson RW, Parrish DG, Dai XZ, Bache RJ. Alterations of myocardial blood flow associated with experimental canine left ventricular hypertrophy secondary to valvular aortic stenosis. Circ Res. 1986;58:47-57.
54. Hittinger L, Patrick T, Ihara T, Hasebe N, Shen YT, Kalthof B, Shannon RP, Vatner SF. Exercise induces cardiac dysfunction in both moderate, compensated and severe hypertrophy. Circulation. 1994;89:2219-2231.
55. Hittinger L, Mirsky I, Shen YT, Patrick TA, Bishop SP, Vatner SF. Hemodynamic mechanisms responsible for reduced subendocardial coronary reserve in dogs with severe left ventricular hypertrophy. Circulation. 1995;92:978-986.
56. Hittinger L, Shannon RP, Bishop SP, Gelpi RJ, Vatner SF. Subendomyocardial exhaustion of blood flow reserve and increased fibrosis in conscious dogs with heart failure. Circ Res. 1989;65:971-980.
57. Anversa P, Capasso JM, Ricci R, Sonnenblick EH, Olivetti G. Morphometric analysis of coronary capillaries during physiologic myocardial growth and induced cardiac hypertrophy: a review. Int J Microcirc Clin Exp. 1989;8:353-363.
58. Camici PG, Crea F. Coronary microvascular dysfunction. N Engl J Med. 2007;356:830-840. doi: 10.1056/NEJMra061889.
59. Shiojima I, Sato K, Izumiya Y, Schiekofer S, Ito M, Liao R, Colucci WS, Walsh K. Disruption of coordinated cardiac hypertrophy and angiogenesis contributes to the transition to heart failure. J Clin Invest. 2005;115:2108-2118. doi: 10.1172/JCI24682.
60. Jiang Y, Reynolds C, Xiao C, Feng W, Zhou Z, Rodriguez W, Tyagi SC, Eaton JW, Saari JT, Kang YJ. Dietary copper supplementation reverses hypertrophic cardiomyopathy induced by chronic pressure overload in mice. J Exp Med. 2007;204:657-666. doi: 10.1084/jem.20061943.
61. Konstandin MH, Völkers M, Collins B, Quijada P, Quintana M, De La Torre A, Ormachea L, Din S, Gude N, Toko H, Sussman MA. Fibronectin contributes to pathological cardiac hypertrophy but not physiological growth. Basic Res Cardiol. 2013;108:375. doi: 10.1007/s00395-013-0375-8.
62. Creemers EE, Pinto YM. Molecular mechanisms that control interstitial fibrosis in the pressure-overloaded heart. Cardiovasc Res. 2011;89:265-272. doi: 10.1093/cvr/cvq308.
63. Derumeaux G, Mulder P, Richard V, Chagraoui A, Nafeh C, Bauer F, Henry JP, Thuillez C. Tissue Doppler imaging differentiates physiological from pathological pressure-overload left ventricular hypertrophy in rats. Circulation. 2002;105:1602-1608.
64. Lund O, Erlandsen M. Changes in left ventricular function and mass during serial investigations after valve replacement for aortic stenosis. J Heart Valve Dis. 2000;9:583-593.
65. Weidemann F, Herrmann S, Störk S, Niemann M, Frantz S, Lange V, Beer M, Gattenlöhner S, Voelker W, Ertl G, Strotmann JM. Impact of myocardial fibrosis in patients with symptomatic severe aortic stenosis. Circulation. 2009;120:577-584. doi: 10.1161/CIRCULATIONAHA.108.847772.
66. Lindsay MM, Dunn FG. Biochemical evidence of myocardial fibrosis in veteran endurance athletes. Br J Sports Med. 2007;41:447-452. doi: 10.1136/bjsm.2006.031534.
67. Saks VA, Kaambre T, Sikk P, Eimre M, Orlova E, Paju K, Piirsoo A, Appaix F, Kay L, Regitz-Zagrosek V, Fleck E, Seppet E. Intracellular energetic units in red muscle cells. Biochem J. 2001;356(pt 2):643-657.
68. Ventura-Clapier R, Garnier A, Veksler V, Joubert F. Bioenergetics of the failing heart. Biochim Biophys Acta. 2011;1813:1360-1372. doi: 10.1016/j.bbamcr.2010.09.006.
69. Wilding JR, Joubert F, de Araujo C, Fortin D, Novotova M, Veksler V, Ventura-Clapier R. Altered energy transfer from mitochondria to sarcoplasmic reticulum after cytoarchitectural perturbations in mice hearts. J Physiol. 2006;575(pt 1):191-200. doi: 10.1113/jphysiol.2006.114116.
70. Joubert F, Wilding JR, Fortin D, Domergue-Dupont V, Novotova M, Ventura-Clapier R, Veksler V. Local energetic regulation of sarcoplasmic and myosin ATPase is differently impaired in rats with heart failure. J Physiol. 2008;586(pt 21):5181-5192. doi: 10.1113/jphysiol.2008.157677.
71. Sabbah HN, Sharov V, Riddle JM, Kono T, Lesch M, Goldstein S. Mitochondrial abnormalities in myocardium of dogs with chronic heart failure. J Mol Cell Cardiol. 1992;24:1333-1347.
72. Kuwahara F, Kai H, Tokuda K, Takeya M, Takeshita A, Egashira K, Imaizumi T. Hypertensive myocardial fibrosis and diastolic dysfunction: another model of inflammation? Hypertension. 2004;43:739-745.
73. Liu YY, Cai WF, Yang HZ, Cui B, Chen ZR, Liu HZ, Yan J, Jin W, Yan HM, Xin BM, Yuan B, Hua F, Hu ZW. Bacillus Calmette-Guérin and TLR4 agonist prevent cardiovascular hypertrophy and fibrosis by regulating immune microenvironment. J Immunol. 2008;180:7349-7357.
74. Cai WF, Zhang XW, Yan HM, Ma YG, Wang XX, Yan J, Xin BM, Lv XX, Wang QQ, Wang ZY, Yang HZ, Hu ZW. Intracellular or extracellular heat shock protein 70 differentially regulates cardiac remodelling in pressure overload mice. Cardiovasc Res. 2010;88:140-149. doi: 10.1093/cvr/cvq182.
75. Fischer KM, Cottage CT, Konstandin MH, Völkers M, Khan M, Sussman MA. Pim-1 kinase inhibits pathological injury by promoting cardioprotective signaling. J Mol Cell Cardiol. 2011;51:554-558. doi: 10.1016/j.yjmcc.2011.01.004.