Abstract
Heart failure (HF) is one of the major health and economic burdens worldwide, and its prevalence is continuously increasing. The study of HF requires reliable animal models to study the chronic changes and pharmacologic interventions in myocardial structure and function and to follow its progression toward HF. Indeed, during the past 40 years, basic and translational scientists have used small animal models to understand the pathophysiology of HF and find more efficient ways of preventing and managing patients suffering from congestive HF (CHF). Each species and each animal model has advantages and disadvantages, and the choice of one model over another should take them into account for a good experimental design. The aim of this review is to describe and highlight the advantages and drawbacks of some commonly used HF rodents models, including both non-genetically and genetically engineered models, with a specific subchapter concerning diastolic HF models.
Similar content being viewed by others
References
Abbate A, Scarpa S, Santini D, Palleiro J, Vasaturo F, Miller J, Morales C, Vetrovec GW, Baldi A (2006) Myocardial expression of survivin, an apoptosis inhibitor, in aging and heart failure. An experimental study in the spontaneously hypertensive rat. Int J Cardiol 111:371–376. doi:10.1016/j.ijcard.2005.07.061
Akhter SA, Luttrell LM, Rockman HA, Iaccarino G, Lefkowitz RJ, Koch WJ (1998) Targeting the receptor-Gq interface to inhibit in vivo pressure overload myocardial hypertrophy. Science 280:574–577
Akhter SA, Milano CA, Shotwell KF, Cho MC, Rockman HA, Lefkowitz RJ, Koch WJ (1997) Transgenic mice with cardiac overexpression of alpha1B-adrenergic receptors. In vivo alpha1-adrenergic receptor-mediated regulation of beta-adrenergic signaling. J Biol Chem 272:21253–21259
An D, Rodrigues B (2006) Role of changes in cardiac metabolism in development of diabetic cardiomyopathy. Am J Physiol Heart Circ Physiol 291:H1489–1506. doi:10.1152/ajpheart.00278.2006
Anderson ME (2005) Calmodulin kinase signaling in heart: an intriguing candidate target for therapy of myocardial dysfunction and arrhythmias. Pharmacol Ther 106:39–55. doi:10.1016/j.pharmthera.2004.11.002
Antos CL, Frey N, Marx SO, Reiken S, Gaburjakova M, Richardson JA, Marks AR, Olson EN (2001) Dilated cardiomyopathy and sudden death resulting from constitutive activation of protein kinase a. Circ Res 89:997–1004
Arber S, Hunter JJ, Ross J Jr, Hongo M, Sansig G, Borg J, Perriard JC, Chien KR, Caroni P (1997) MLP-deficient mice exhibit a disruption of cardiac cytoarchitectural organization, dilated cardiomyopathy, and heart failure. Cell 88:393–403
Arnolda L, McGrath B, Cocks M, Sumithran E, Johnston C (1985) Adriamycin cardiomyopathy in the rabbit: an animal model of low output cardiac failure with activation of vasoconstrictor mechanisms. Cardiovasc Res 19:378–382
Baker DL, Hashimoto K, Grupp IL, Ji Y, Reed T, Loukianov E, Grupp G, Bhagwhat A, Hoit B, Walsh R, Marban E, Periasamy M (1998) Targeted overexpression of the sarcoplasmic reticulum Ca2+-ATPase increases cardiac contractility in transgenic mouse hearts. Circ Res 83:1205–1214
Bayat H, Swaney JS, Ander AN, Dalton N, Kennedy BP, Hammond HK, Roth DM (2002) Progressive heart failure after myocardial infarction in mice. Basic Res Cardiol 97:206–213
Berg RG, Leenen FH, de Jong W (1979) Plasma renin activity and sodium, potassium and water excretion during reversal of hypertension in the one-clip two-kidney hypertensive rat. Clin Sci (Lond) 57:47–52
Bialik GM, Abassi ZA, Hammel I, Winaver J, Lewinson D (2001) Evaluation of atrial natriuretic peptide and brain natriuretic peptide in atrial granules of rats with experimental congestive heart failure. J Histochem Cytochem 49:1293–1300
Bing OH, Brooks WW, Robinson KG, Slawsky MT, Hayes JA, Litwin SE, Sen S, Conrad CH (1995) The spontaneously hypertensive rat as a model of the transition from compensated left ventricular hypertrophy to failure. J Mol Cell Cardiol 27:383–396
Bittner HB, Chen EP, Milano CA, Lefkowitz RJ, Van Trigt P (1997) Functional analysis of myocardial performance in murine hearts overexpressing the human beta 2-adrenergic receptor. J Mol Cell Cardiol 29:961–967. doi:10.1006/jmcc.1996.0339
Boluyt MO, O’Neill L, Meredith AL, Bing OH, Brooks WW, Conrad CH, Crow MT, Lakatta EG (1994) Alterations in cardiac gene expression during the transition from stable hypertrophy to heart failure. Marked upregulation of genes encoding extracellular matrix components. Circ Res 75:23–32
Boluyt MO, Robinson KG, Meredith AL, Sen S, Lakatta EG, Crow MT, Brooks WW, Conrad CH, Bing OH (2005) Heart failure after long-term supravalvular aortic constriction in rats. Am J Hypertens 18:202–212. doi:10.1016/j.amjhyper.2004.08.034
Bond RA, Leff P, Johnson TD, Milano CA, Rockman HA, McMinn TR, Apparsundaram S, Hyek MF, Kenakin TP, Allen LF et al (1995) Physiological effects of inverse agonists in transgenic mice with myocardial overexpression of the beta 2-adrenoceptor. Nature 374:272–276. doi:10.1038/374272a0
Boudina S, Abel ED (2007) Diabetic cardiomyopathy revisited. Circulation 115:3213–3223. doi:10.1161/CIRCULATIONAHA.106.679597
Boudina S, Sena S, Theobald H, Sheng X, Wright JJ, Hu XX, Aziz S, Johnson JI, Bugger H, Zaha VG, Abel ED (2007) Mitochondrial energetics in the heart in obesity-related diabetes: direct evidence for increased uncoupled respiration and activation of uncoupling proteins. Diabetes 56:2457–2466. doi:10.2337/db07-0481
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 (2003) Melusin, a muscle-specific integrin beta1-interacting protein, is required to prevent cardiac failure in response to chronic pressure overload. Nat Med 9:68–75. doi:10.1038/nm805nm805
Bras-Silva C, Fontes-Sousa AP, Moura C, Areias JC, Leite-Moreira AF (2006) Impaired response to ET(B) receptor stimulation in heart failure: functional evidence of endocardial endothelial dysfunction? Exp Biol Med (Maywood) 231:893–898
Bras-Silva C, Leite-Moreira AF (2008) Myocardial effects of endothelin-1. Rev Port Cardiol 27:925–951
Braun A, Trigatti BL, Post MJ, Sato K, Simons M, Edelberg JM, Rosenberg RD, Schrenzel M, Krieger M (2002) Loss of SR-BI expression leads to the early onset of occlusive atherosclerotic coronary artery disease, spontaneous myocardial infarctions, severe cardiac dysfunction, and premature death in apolipoprotein E-deficient mice. Circ Res 90:270–276
Braunschweig F, Cowie MR, Auricchio A (2011) What are the costs of heart failure? Europace 13(Suppl 2):ii13–17. doi:10.1093/europace/eur081
Brede M, Wiesmann F, Jahns R, Hadamek K, Arnolt C, Neubauer S, Lohse MJ, Hein L (2002) Feedback inhibition of catecholamine release by two different alpha2-adrenoceptor subtypes prevents progression of heart failure. Circulation 106:2491–2496
Brenner DA, Apstein CS, Saupe KW (2001) Exercise training attenuates age-associated diastolic dysfunction in rats. Circulation 104:221–226
Bristow MR, Thompson PD, Martin RP, Mason JW, Billingham ME, Harrison DC (1978) Early anthracycline cardiotoxicity. Am J Med 65:823–832
Brower GL, Levick SP, Janicki JS (2007) Inhibition of matrix metalloproteinase activity by ACE inhibitors prevents left ventricular remodeling in a rat model of heart failure. Am J Physiol Heart Circ Physiol 292:H3057–3064. doi:10.1152/ajpheart.00447.2006
Brown L, Ooi SY, Lau K, Sernia C (2000) Cardiac and vascular responses in deoxycorticosterone acetate-salt hypertensive rats. Clin Exp Pharmacol Physiol 27:263–269
Buermans HP, Redout EM, Schiel AE, Musters RJ, Zuidwijk M, Eijk PP, van Hardeveld C, Kasanmoentalib S, Visser FC, Ylstra B, Simonides WS (2005) Microarray analysis reveals pivotal divergent mRNA expression profiles early in the development of either compensated ventricular hypertrophy or heart failure. Physiol Genomics 21:314–323. doi:10.1152/physiolgenomics.00185.2004
Bugger H, Abel ED (2008) Molecular mechanisms for myocardial mitochondrial dysfunction in the metabolic syndrome. Clin Sci (Lond) 114:195–210. doi:10.1042/CS20070166
Burke SL, Evans RG, Head GA (2011) Effects of chronic sympatho-inhibition on renal excretory function in renovascular hypertension. J Hypertens 29:945–952. doi:10.1097/HJH.0b013e3283449529
Calderone A, de Champlain J, Rouleau JL (1991) Adriamycin-induced changes to the myocardial beta-adrenergic system in the rabbit. J Mol Cell Cardiol 23:333–342
Cantor EJ, Babick AP, Vasanji Z, Dhalla NS, Netticadan T (2005) A comparative serial echocardiographic analysis of cardiac structure and function in rats subjected to pressure or volume overload. J Mol Cell Cardiol 38:777–786. doi:10.1016/j.yjmcc.2005.02.012
Carvalho KA, Guarita-Souza LC, Hansen P, Rebelatto CL, Senegaglia AC, Miyague N, Olandoski M, Francisco JC, Furuta M, Gremski W (2006) Cell transplantation after the coculture of skeletal myoblasts and mesenchymal stem cells in the regeneration of the myocardium scar: an experimental study in rats. Transplant Proc 38:1596–1602. doi:10.1016/j.transproceed.2006.03.023
Cavallero S, Gonzalez GE, Puyo AM, Roson MI, Perez S, Morales C, Hertig CM, Gelpi RJ, Fernandez BE (2007) Atrial natriuretic peptide behaviour and myocyte hypertrophic profile in combined pressure and volume-induced cardiac hypertrophy. J Hypertens 25:1940–1950. doi:10.1097/HJH.0b013e3282435b1e00004872-200709000-00026
Chekanov VS (1999) A stable model of chronic bilateral ventricular insufficiency (dilated cardiomyopathy) induced by arteriovenous anastomosis and doxorubicin administration in sheep. J Thorac Cardiovasc Surg 117:198–199
Chen H, Charlat O, Tartaglia LA, Woolf EA, Weng X, Ellis SJ, Lakey ND, Culpepper J, Moore KJ, Breitbart RE, Duyk GM, Tepper RI, Morgenstern JP (1996) Evidence that the diabetes gene encodes the leptin receptor: identification of a mutation in the leptin receptor gene in db/db mice. Cell 84:491–495
Chen J, Chien KR (1999) Complexity in simplicity: monogenic disorders and complex cardiomyopathies. J Clin Invest 103:1483–1485. doi:10.1172/JCI7297
Chen Y, Daosukho C, Opii WO, Turner DM, Pierce WM, Klein JB, Vore M, Butterfield DA, St Clair DK (2006) Redox proteomic identification of oxidized cardiac proteins in adriamycin-treated mice. Free Radic Biol Med 41:1470–1477. doi:10.1016/j.freeradbiomed.2006.08.006
Chua SC Jr, Chung WK, Wu-Peng XS, Zhang Y, Liu SM, Tartaglia L, Leibel RL (1996) Phenotypes of mouse diabetes and rat fatty due to mutations in the OB (leptin) receptor. Science 271:994–996
Cohn JN (2002) Sympathetic nervous system in heart failure. Circulation 106:2417–2418
Colbert MC, Hall DG, Kimball TR, Witt SA, Lorenz JN, Kirby ML, Hewett TE, Klevitsky R, Robbins J (1997) Cardiac compartment-specific overexpression of a modified retinoic acid receptor produces dilated cardiomyopathy and congestive heart failure in transgenic mice. J Clin Invest 100:1958–1968. doi:10.1172/JCI119727
Coral-Vazquez R, Cohn RD, Moore SA, Hill JA, Weiss RM, Davisson RL, Straub V, Barresi R, Bansal D, Hrstka RF, Williamson R, Campbell KP (1999) Disruption of the sarcoglycan-sarcospan complex in vascular smooth muscle: a novel mechanism for cardiomyopathy and muscular dystrophy. Cell 98:465–474
Creemers EE, Davis JN, Parkhurst AM, Leenders P, Dowdy KB, Hapke E, Hauet AM, Escobar PG, Cleutjens JP, Smits JF, Daemen MJ, Zile MR, Spinale FG (2003) Deficiency of TIMP-1 exacerbates LV remodeling after myocardial infarction in mice. Am J Physiol Heart Circ Physiol 284:H364–371. doi:10.1152/ajpheart.00511.2002
Cunha-Neto E, Dzau VJ, Allen PD, Stamatiou D, Benvenutti L, Higuchi ML, Koyama NS, Silva JS, Kalil J, Liew CC (2005) Cardiac gene expression profiling provides evidence for cytokinopathy as a molecular mechanism in Chagas’ disease cardiomyopathy. Am J Pathol 167:305–313. doi:10.1016/S0002-9440(10)62976-8
D’Angelo DD, Sakata Y, Lorenz JN, Boivin GP, Walsh RA, Liggett SB, Dorn GW 2nd (1997) Transgenic Galphaq overexpression induces cardiac contractile failure in mice. Proc Natl Acad Sci USA 94:8121–8126
Dahl LK, Heine M, Tassinari L (1962) Role of genetic factors in susceptibility to experimental hypertension due to chronic excess salt ingestion. Nature 194:480–482
Dash R, Kadambi V, Schmidt AG, Tepe NM, Biniakiewicz D, Gerst MJ, Canning AM, Abraham WT, Hoit BD, Liggett SB, Lorenz JN, Dorn GW 2nd, Kranias EG (2001) Interactions between phospholamban and beta-adrenergic drive may lead to cardiomyopathy and early mortality. Circulation 103:889–896
De Angelis A, Piegari E, Cappetta D, Marino L, Filippelli A, Berrino L, Ferreira-Martins J, Zheng H, Hosoda T, Rota M, Urbanek K, Kajstura J, Leri A, Rossi F, Anversa P (2010) Anthracycline cardiomyopathy is mediated by depletion of the cardiac stem cell pool and is rescued by restoration of progenitor cell function. Circulation 121:276–292. doi:10.1161/CIRCULATIONAHA.109.895771
Delgado RM 3rd, Nawar MA, Zewail AM, Kar B, Vaughn WK, Wu KK, Aleksic N, Sivasubramanian N, McKay K, Mann DL, Willerson JT (2004) Cyclooxygenase-2 inhibitor treatment improves left ventricular function and mortality in a murine model of doxorubicin-induced heart failure. Circulation 109:1428–1433. doi:10.1161/01.CIR.0000121354.34067.48
Devi S, Kennedy RH, Joseph L, Shekhawat NS, Melchert RB, Joseph J (2006) Effect of long-term hyperhomocysteinemia on myocardial structure and function in hypertensive rats. Cardiovasc Pathol 15:75–82. doi:10.1016/j.carpath.2005.11.001
Dickstein K, Cohen-Solal A, Filippatos G, McMurray JJ, Ponikowski P, Poole-Wilson PA, Stromberg A, van Veldhuisen DJ, Atar D, Hoes AW, Keren A, Mebazaa A, Nieminen M, Priori SG, Swedberg K (2008) ESC guidelines for the diagnosis and treatment of acute and chronic heart failure 2008: the Task Force for the diagnosis and treatment of acute and chronic heart failure 2008 of the European Society of Cardiology. Developed in collaboration with the Heart Failure Association of the ESC (HFA) and endorsed by the European Society of Intensive Care Medicine (ESICM). Eur J Heart Fail 10:933–989. doi:10.1016/j.ejheart.2008.08.005
Dodd DA, Atkinson JB, Olson RD, Buck S, Cusack BJ, Fleischer S, Boucek RJ Jr (1993) Doxorubicin cardiomyopathy is associated with a decrease in calcium release channel of the sarcoplasmic reticulum in a chronic rabbit model. J Clin Invest 91:1697–1705. doi:10.1172/JCI116379
Doi R, Masuyama T, Yamamoto K, Doi Y, Mano T, Sakata Y, Ono K, Kuzuya T, Hirota S, Koyama T, Miwa T, Hori M (2000) Development of different phenotypes of hypertensive heart failure: systolic versus diastolic failure in Dahl salt-sensitive rats. J Hypertens 18:111–120
Drolet MC, Lachance D, Plante E, Roussel E, Couet J, Arsenault M (2006) Gender-related differences in left ventricular remodeling in chronic severe aortic valve regurgitation in rats. J Heart Valve Dis 15:345–351
Du XJ, Autelitano DJ, Dilley RJ, Wang B, Dart AM, Woodcock EA (2000) beta(2)-adrenergic receptor overexpression exacerbates development of heart failure after aortic stenosis. Circulation 101:71–77
Du XJ, Gao XM, Wang B, Jennings GL, Woodcock EA, Dart AM (2000) Age-dependent cardiomyopathy and heart failure phenotype in mice overexpressing beta(2)-adrenergic receptors in the heart. Cardiovasc Res 48:448–454
Du XJ, Vincan E, Woodcock DM, Milano CA, Dart AM, Woodcock EA (1996) Response to cardiac sympathetic activation in transgenic mice overexpressing beta 2-adrenergic receptor. Am J Physiol 271:H630–H636
Dubi S, Arbel Y (2010) Large animal models for diastolic dysfunction and diastolic heart failure-a review of the literature. Cardiovasc Pathol 19:147–152. doi:10.1016/j.carpath.2008.12.008
Ducharme A, Frantz S, Aikawa M, Rabkin E, Lindsey M, Rohde LE, Schoen FJ, Kelly RA, Werb Z, Libby P, Lee RT (2000) Targeted deletion of matrix metalloproteinase-9 attenuates left ventricular enlargement and collagen accumulation after experimental myocardial infarction. J Clin Invest 106:55–62. doi:10.1172/JCI8768
El-Demerdash E, Awad AS, Taha RM, El-Hady AM, Sayed-Ahmed MM (2005) Probucol attenuates oxidative stress and energy decline in isoproterenol-induced heart failure in rat. Pharmacol Res 51:311–318. doi:10.1016/j.phrs.2004.10.002
Engelhardt S, Boknik P, Keller U, Neumann J, Lohse MJ, Hein L (2001) Early impairment of calcium handling and altered expression of junctin in hearts of mice overexpressing the beta1-adrenergic receptor. FASEB J 15:2718–2720. doi:10.1096/fj.01-0107fje
Engelhardt S, Hein L, Dyachenkow V, Kranias EG, Isenberg G, Lohse MJ (2004) Altered calcium handling is critically involved in the cardiotoxic effects of chronic beta-adrenergic stimulation. Circulation 109:1154–1160. doi:10.1161/01.CIR.0000117254.68497.39
Engelhardt S, Hein L, Wiesmann F, Lohse MJ (1999) Progressive hypertrophy and heart failure in beta1-adrenergic receptor transgenic mice. Proc Natl Acad Sci USA 96:7059–7064
Escobales N, Crespo MJ (2008) Early pathophysiological alterations in experimental cardiomyopathy: the Syrian cardiomyopathic hamster. P R Health Sci J 27:307–314
Esposito G, Rapacciuolo A, Naga Prasad SV, Takaoka H, Thomas SA, Koch WJ, Rockman HA (2002) Genetic alterations that inhibit in vivo pressure-overload hypertrophy prevent cardiac dysfunction despite increased wall stress. Circulation 105:85–92
Fairweather D, Kaya Z, Shellam GR, Lawson CM, Rose NR (2001) From infection to autoimmunity. J Autoimmun 16:175–186. doi:10.1006/jaut.2000.0492
Falcao-Pires I, Palladini G, Goncalves N, van der Velden J, Moreira-Goncalves D, Miranda-Silva D, Salinaro F, Paulus WJ, Niessen HW, Perlini S, Leite-Moreira AF (2011) Distinct mechanisms for diastolic dysfunction in diabetes mellitus and chronic pressure-overload. Basic Res Cardiol 106:801–814. doi:10.1007/s00395-011-0184-x
Feldman AM, Weinberg EO, Ray PE, Lorell BH (1993) Selective changes in cardiac gene expression during compensated hypertrophy and the transition to cardiac decompensation in rats with chronic aortic banding. Circ Res 73:184–192
Finck BN, Lehman JJ, Leone TC, Welch MJ, Bennett MJ, Kovacs A, Han X, Gross RW, Kozak R, Lopaschuk GD, Kelly DP (2002) The cardiac phenotype induced by PPARalpha overexpression mimics that caused by diabetes mellitus. J Clin Invest 109:121–130. doi:10.1172/JCI14080
Francis GS, Tang WH (2003) Pathophysiology of congestive heart failure. Rev Cardiovasc Med 4(Suppl 2):S14–S20
Freeman RH, Davis JO, Watkins BE, Stephens GA, DeForrest JM (1979) Effects of continuous converting enzyme blockade on renovascular hypertension in the rat. Am J Physiol 236:F21–F24
Fu M, Matoba M, Liang QM, Sjogren KG, Hjalmarson A (1994) Properties of G-protein modulated receptor-adenylyl cyclase system in myocardium of spontaneously hypertensive rats treated with adriamycin. Int J Cardiol 44:9–18
Fujihira S, Yamamoto T, Matsumoto M, Yoshizawa K, Oishi Y, Fujii T, Noguchi H, Mori H (1993) The high incidence of atrial thrombosis in mice given doxorubicin. Toxicol Pathol 21:362–368
Gao XM, Dart AM, Dewar E, Jennings G, Du XJ (2000) Serial echocardiographic assessment of left ventricular dimensions and function after myocardial infarction in mice. Cardiovasc Res 45:330–338
Garcia R, Diebold S (1990) Simple, rapid, and effective method of producing aortocaval shunts in the rat. Cardiovasc Res 24:430–432
Gaudin PB, Hruban RH, Beschorner WE, Kasper EK, Olson JL, Baughman KL, Hutchins GM (1993) Myocarditis associated with doxorubicin cardiotoxicity. Am J Clin Pathol 100:158–163
Gehrmann J, Frantz S, Maguire CT, Vargas M, Ducharme A, Wakimoto H, Lee RT, Berul CI (2001) Electrophysiological characterization of murine myocardial ischemia and infarction. Basic Res Cardiol 96:237–250
Georgakopoulos D, Mitzner WA, Chen CH, Byrne BJ, Millar HD, Hare JM, Kass DA (1998) In vivo murine left ventricular pressure-volume relations by miniaturized conductance micromanometry. Am J Physiol 274:H1416–H1422
Goldblatt H, Lynch J, Hanzal RF, Summerville WW (1934) Studies on Experimental Hypertension : I. The production of persistent elevation of systolic blood pressure by means of renal ischemia. J Exp Med 59:347–379
Gomez AM, Valdivia HH, Cheng H, Lederer MR, Santana LF, Cannell MB, McCune SA, Altschuld RA, Lederer WJ (1997) Defective excitation-contraction coupling in experimental cardiac hypertrophy and heart failure. Science 276:800–806
Goser S, Andrassy M, Buss SJ, Leuschner F, Volz CH, Ottl R, Zittrich S, Blaudeck N, Hardt SE, Pfitzer G, Rose NR, Katus HA, Kaya Z (2006) Cardiac troponin I but not cardiac troponin T induces severe autoimmune inflammation in the myocardium. Circulation 114:1693–1702. doi:10.1161/CIRCULATIONAHA.106.635664
Goto Y, Suzuki K, Ono T, Sasaki M, Toyota T (1988) Development of diabetes in the non-obese NIDDM rat (GK rat). Adv Exp Med Biol 246:29–31
Gould KE, Taffet GE, Michael LH, Christie RM, Konkol DL, Pocius JS, Zachariah JP, Chaupin DF, Daniel SL, Sandusky GE Jr, Hartley CJ, Entman ML (2002) Heart failure and greater infarct expansion in middle-aged mice: a relevant model for postinfarction failure. Am J Physiol Heart Circ Physiol 282:H615–H621. doi:10.1152/ajpheart.00206.2001
Grady RM, Teng H, Nichol MC, Cunningham JC, Wilkinson RS, Sanes JR (1997) Skeletal and cardiac myopathies in mice lacking utrophin and dystrophin: a model for Duchenne muscular dystrophy. Cell 90:729–738
Greer JJ, Ware DP, Lefer DJ (2006) Myocardial infarction and heart failure in the db/db diabetic mouse. Am J Physiol Heart Circ Physiol 290:H146–153. doi:10.1152/ajpheart.00583.2005
Grimm D, Elsner D, Schunkert H, Pfeifer M, Griese D, Bruckschlegel G, Muders F, Riegger GA, Kromer EP (1998) Development of heart failure following isoproterenol administration in the rat: role of the renin-angiotensin system. Cardiovasc Res 37:91–100
Grobe JL, Mecca AP, Mao H, Katovich MJ (2006) Chronic angiotensin-(1–7) prevents cardiac fibrosis in DOCA-salt model of hypertension. Am J Physiol Heart Circ Physiol 290:H2417–2423. doi:10.1152/ajpheart.01170.2005
Gruver CL, DeMayo F, Goldstein MA, Means AR (1993) Targeted developmental overexpression of calmodulin induces proliferative and hypertrophic growth of cardiomyocytes in transgenic mice. Endocrinology 133:376–388
Haghighi K, Schmidt AG, Hoit BD, Brittsan AG, Yatani A, Lester JW, Zhai J, Kimura Y, Dorn GW 2nd, MacLennan DH, Kranias EG (2001) Superinhibition of sarcoplasmic reticulum function by phospholamban induces cardiac contractile failure. J Biol Chem 276:24145–24152. doi:10.1074/jbc.M102403200
Halapas A, Papalois A, Stauropoulou A, Philippou A, Pissimissis N, Chatzigeorgiou A, Kamper E, Koutsilieris M (2008) In vivo models for heart failure research. In Vivo 22:767–780
Halapas A, Pissimissis N, Lembessis P, Rizos I, Rigopoulos AG, Kremastinos DT, Koutsilieris M (2008) Molecular diagnosis of the viral component in cardiomyopathies: pathophysiological, clinical and therapeutic implications. Expert Opin Ther Targets 12:821–836. doi:10.1517/14728222.12.7.821
Hara M, Ono K, Hwang MW, Iwasaki A, Okada M, Nakatani K, Sasayama S, Matsumori A (2002) Evidence for a role of mast cells in the evolution to congestive heart failure. J Exp Med 195:375–381
Harding VB, Jones LR, Lefkowitz RJ, Koch WJ, Rockman HA (2001) Cardiac beta ARK1 inhibition prolongs survival and augments beta blocker therapy in a mouse model of severe heart failure. Proc Natl Acad Sci USA 98:5809–5814. doi:10.1073/pnas.091102398
Hayashidani S, Tsutsui H, Ikeuchi M, Shiomi T, Matsusaka H, Kubota T, Imanaka-Yoshida K, Itoh T, Takeshita A (2003) Targeted deletion of MMP-2 attenuates early LV rupture and late remodeling after experimental myocardial infarction. Am J Physiol Heart Circ Physiol 285:H1229–1235. doi:10.1152/ajpheart.00207.2003
He H, Giordano FJ, Hilal-Dandan R, Choi DJ, Rockman HA, McDonough PM, Bluhm WF, Meyer M, Sayen MR, Swanson E, Dillmann WH (1997) Overexpression of the rat sarcoplasmic reticulum Ca2+ATPase gene in the heart of transgenic mice accelerates calcium transients and cardiac relaxation. J Clin Invest 100:380–389. doi:10.1172/JCI119544
Herman EH, Ferrans VJ (1998) Preclinical animal models of cardiac protection from anthracycline-induced cardiotoxicity. Semin Oncol 25:15–21
Hessel MH, Steendijk P, den Adel B, Schutte CI, van der Laarse A (2006) Characterization of right ventricular function after monocrotaline-induced pulmonary hypertension in the intact rat. Am J Physiol Heart Circ Physiol 291:H2424–2430. doi:10.1152/ajpheart.00369.2006
Heyen JR, Blasi ER, Nikula K, Rocha R, Daust HA, Frierdich G, Van Vleet JF, De Ciechi P, McMahon EG, Rudolph AE (2002) Structural, functional, and molecular characterization of the SHHF model of heart failure. Am J Physiol Heart Circ Physiol 283:H1775–H1784. doi:10.1152/ajpheart.00305.2002
Heymans S, Hirsch E, Anker SD, Aukrust P, Balligand JL, Cohen-Tervaert JW, Drexler H, Filippatos G, Felix SB, Gullestad L, Hilfiker-Kleiner D, Janssens S, Latini R, Neubauer G, Paulus WJ, Pieske B, Ponikowski P, Schroen B, Schultheiss HP, Tschope C, Van Bilsen M, Zannad F, McMurray J, Shah AM (2009) Inflammation as a therapeutic target in heart failure? A scientific statement from the Translational Research Committee of the Heart Failure Association of the European Society of Cardiology. Eur J Heart Fail 11:119–129. doi:10.1093/eurjhf/hfn043
Heymans S, Pauschinger M, De Palma A, Kallwellis-Opara A, Rutschow S, Swinnen M, Vanhoutte D, Gao F, Torpai R, Baker AH, Padalko E, Neyts J, Schultheiss HP, Van de Werf F, Carmeliet P, Pinto YM (2006) Inhibition of urokinase-type plasminogen activator or matrix metalloproteinases prevents cardiac injury and dysfunction during viral myocarditis. Circulation 114:565–573. doi:10.1161/CIRCULATIONAHA.105.591032
Hibbs RG, Ferrans VJ, Walsh JJ, Burch GE (1965) Electron microscopic observations on lysosomes and related cytoplasmic components of normal and pathological cardiac muscle. Anat Rec 153:173–185
Hirono S, Islam MO, Nakazawa M, Yoshida Y, Kodama M, Shibata A, Izumi T, Imai S (1997) Expression of inducible nitric oxide synthase in rat experimental autoimmune myocarditis with special reference to changes in cardiac hemodynamics. Circ Res 80:11–20
Hirota H, Chen J, Betz UA, Rajewsky K, Gu Y, Ross J Jr, Muller W, Chien KR (1999) Loss of a gp130 cardiac muscle cell survival pathway is a critical event in the onset of heart failure during biomechanical stress. Cell 97:189–198
Hirota H, Yoshida K, Kishimoto T, Taga T (1995) Continuous activation of gp130, a signal-transducing receptor component for interleukin 6-related cytokines, causes myocardial hypertrophy in mice. Proc Natl Acad Sci USA 92:4862–4866
Holycross BJ, Summers BM, Dunn RB, McCune SA (1997) Plasma renin activity in heart failure-prone SHHF/Mcc-facp rats. Am J Physiol 273:H228–H233
Homburger F (1979) Myopathy of hamster dystrophy: history and morphologic aspects. Ann N Y Acad Sci 317:1–17
Homburger F, Baker JR, Nixon CW, Wilgram G (1962) New hereditary disease of Syrian hamsters. Primary, generalized polymyopathy and cardiac necrosis. Arch Intern Med 110:660–662
Homburger F, Nixon CW, Eppenberger M, Baker JR (1966) Hereditary myopathy in the Syrian hamster: studies on pathogenesis. Ann N Y Acad Sci 138:14–27
Hu P, Zhang D, Swenson L, Chakrabarti G, Abel ED, Litwin SE (2003) Minimally invasive aortic banding in mice: effects of altered cardiomyocyte insulin signaling during pressure overload. Am J Physiol Heart Circ Physiol 285:H1261–1269. doi:10.1152/ajpheart.00108.2003
Huang WY, Aramburu J, Douglas PS, Izumo S (2000) Transgenic expression of green fluorescence protein can cause dilated cardiomyopathy. Nat Med 6:482–483. doi:10.1038/74914
Hunter EG, Hughes V, White J (1984) Cardiomyopathic hamsters, CHF 146 and CHF 147: a preliminary study. Can J Physiol Pharmacol 62:1423–1428
Hunter JJ, Tanaka N, Rockman HA, Ross J Jr, Chien KR (1995) Ventricular expression of a MLC-2v-ras fusion gene induces cardiac hypertrophy and selective diastolic dysfunction in transgenic mice. J Biol Chem 270:23173–23178
Hwang GS, Oh KS, Koo HN, Seo HW, You KH, Lee BH (2006) Effects of KR-31378, a novel ATP-sensitive potassium channel activator, on hypertrophy of H9c2 cells and on cardiac dysfunction in rats with congestive heart failure. Eur J Pharmacol 540:131–138. doi:10.1016/j.ejphar.2006.04.031
Ichihara S, Obata K, Yamada Y, Nagata K, Noda A, Ichihara G, Yamada A, Kato T, Izawa H, Murohara T, Yokota M (2006) Attenuation of cardiac dysfunction by a PPAR-alpha agonist is associated with down-regulation of redox-regulated transcription factors. J Mol Cell Cardiol 41:318–329. doi:10.1016/j.yjmcc.2006.05.013
Ikegami T, Suzuki Y, Shimizu T, Isono K, Koseki H, Shirasawa T (2002) Model mice for tissue-specific deletion of the manganese superoxide dismutase (MnSOD) gene. Biochem Biophys Res Commun 296:729–736
Ingalls AM, Dickie MM, Snell GD (1950) Obese, a new mutation in the house mouse. J Hered 41:317–318
Inoko M, Kihara Y, Morii I, Fujiwara H, Sasayama S (1994) Transition from compensatory hypertrophy to dilated, failing left ventricles in Dahl salt-sensitive rats. Am J Physiol 267:H2471–H2482
Intengan HD, Park JB, Schiffrin EL (1999) Blood pressure and small arteries in DOCA-salt-treated genetically AVP-deficient rats: role of endothelin. Hypertension 34:907–913
Ishibashi S, Goldstein JL, Brown MS, Herz J, Burns DK (1994) Massive xanthomatosis and atherosclerosis in cholesterol-fed low density lipoprotein receptor-negative mice. J Clin Invest 93:1885–1893. doi:10.1172/JCI117179
Ito H, Torii M, Suzuki T (1995) Decreased superoxide dismutase activity and increased superoxide anion production in cardiac hypertrophy of spontaneously hypertensive rats. Clin Exp Hypertens 17:803–816
Ito K, Yan X, Feng X, Manning WJ, Dillmann WH, Lorell BH (2001) Transgenic expression of sarcoplasmic reticulum Ca(2+) ATPase modifies the transition from hypertrophy to early heart failure. Circ Res 89:422–429
Iwase M, Bishop SP, Uechi M, Vatner DE, Shannon RP, Kudej RK, Wight DC, Wagner TE, Ishikawa Y, Homcy CJ, Vatner SF (1996) Adverse effects of chronic endogenous sympathetic drive induced by cardiac GS alpha overexpression. Circ Res 78:517–524
Janssen SW, Martens GJ, Sweep CG, Ross HA, Hermus AR (1999) In Zucker diabetic fatty rats plasma leptin levels are correlated with plasma insulin levels rather than with body weight. Horm Metab Res 31:610–615. doi:10.1055/s-2007-978806
Jasmin G, Eu HY (1979) Cardiomyopathy of hamster dystrophy. Ann N Y Acad Sci 317:46–58
Jeong D, Cha H, Kim E, Kang M, Yang DK, Kim JM, Yoon PO, Oh JG, Bernecker OY, Sakata S, Le TT, Cui L, Lee YH, Kim do H, Woo SH, Liao R, Hajjar RJ, Park WJ (2006) PICOT inhibits cardiac hypertrophy and enhances ventricular function and cardiomyocyte contractility. Circ Res 99:307–314. doi:10.1161/01.RES.0000234780.06115.2c
Jones LR, Suzuki YJ, Wang W, Kobayashi YM, Ramesh V, Franzini-Armstrong C, Cleemann L, Morad M (1998) Regulation of Ca2+ signaling in transgenic mouse cardiac myocytes overexpressing calsequestrin. J Clin Invest 101:1385–1393. doi:10.1172/JCI1362
Joseph J, Joseph L, Shekhawat NS, Devi S, Wang J, Melchert RB, Hauer-Jensen M, Kennedy RH (2003) Hyperhomocysteinemia leads to pathological ventricular hypertrophy in normotensive rats. Am J Physiol Heart Circ Physiol 285:H679–686. doi:10.1152/ajpheart.00145.2003
Joseph J, Washington A, Joseph L, Koehler L, Fink LM, Hauer-Jensen M, Kennedy RH (2002) Hyperhomocysteinemia leads to adverse cardiac remodeling in hypertensive rats. Am J Physiol Heart Circ Physiol 283:H2567–2574. doi:10.1152/ajpheart.00475.2002
Junhong W, Jing Y, Jizheng M, Shushu Z, Xiangjian C, Hengfang W, Di Y, Jinan Z (2008) Proteomic analysis of left ventricular diastolic dysfunction hearts in renovascular hypertensive rats. Int J Cardiol 127:198–207. doi:10.1016/j.ijcard.2007.07.003
Katholi RE, Naftilan AJ, Oparil S (1980) Importance of renal sympathetic tone in the development of DOCA-salt hypertension in the rat. Hypertension 2:266–273
Kawano K, Hirashima T, Mori S, Saitoh Y, Kurosumi M, Natori T (1992) Spontaneous long-term hyperglycemic rat with diabetic complications—Otsuka Long-Evans Tokushima Fatty (Oletf) strain. Diabetes 41:1422–1428
Kawase Y, Ly HQ, Prunier F, Lebeche D, Shi Y, Jin H, Hadri L, Yoneyama R, Hoshino K, Takewa Y, Sakata S, Peluso R, Zsebo K, Gwathmey JK, Tardif JC, Tanguay JF, Hajjar RJ (2008) Reversal of cardiac dysfunction after long-term expression of SERCA2a by gene transfer in a pre-clinical model of heart failure. J Am Coll Cardiol 51:1112–1119. doi:10.1016/j.jacc.2007.12.014
Kay JM, Smith P, Heath D (1969) Electron microscopy of Crotalaria pulmonary hypertension. Thorax 24:511–526
Kazumi T, Odaka H, Hozumi T, Ishida Y, Amano N, Yoshino G (1997) Effects of dietary fructose or glucose on triglyceride production and lipogenic enzyme activities in the liver of Wistar fatty rats, an animal model of NIDDM. Endocr J 44:239–245
Kim S, Yoshiyama M, Izumi Y, Kawano H, Kimoto M, Zhan Y, Iwao H (2001) Effects of combination of ACE inhibitor and angiotensin receptor blocker on cardiac remodeling, cardiac function, and survival in rat heart failure. Circulation 103:148–154
Kiss E, Ball NA, Kranias EG, Walsh RA (1995) Differential changes in cardiac phospholamban and sarcoplasmic reticular Ca(2+)-ATPase protein levels. Effects on Ca2+ transport and mechanics in compensated pressure-overload hypertrophy and congestive heart failure. Circ Res 77:759–764
Klotz S, Hay I, Zhang G, Maurer M, Wang J, Burkhoff D (2006) Development of heart failure in chronic hypertensive Dahl rats: focus on heart failure with preserved ejection fraction. Hypertension 47:901–911. doi:10.1161/01.HYP.0000215579.81408.8e
Koch WJ, Rockman HA, Samama P, Hamilton RA, Bond RA, Milano CA, Lefkowitz RJ (1995) Cardiac function in mice overexpressing the beta-adrenergic receptor kinase or a beta ARK inhibitor. Science 268:1350–1353
Konduracka E, Gackowski A, Rostoff P, Galicka-Latala D, Frasik W, Piwowarska W (2007) Diabetes-specific cardiomyopathy in type 1 diabetes mellitus: no evidence for its occurrence in the era of intensive insulin therapy. Eur Heart J 28:2465–2471. doi:10.1093/eurheartj/ehm361
Krzeminski TF, Nozynski JK, Grzyb J, Porc M (2008) Wide-spread myocardial remodeling after acute myocardial infarction in rat. Features for heart failure progression. Vascul Pharmacol 48:100–108. doi:10.1016/j.vph.2008.01.002
Kubota T, McTiernan CF, Frye CS, Slawson SE, Lemster BH, Koretsky AP, Demetris AJ, Feldman AM (1997) Dilated cardiomyopathy in transgenic mice with cardiac-specific overexpression of tumor necrosis factor-alpha. Circ Res 81:627–635
Kuhlmann MT, Kirchhof P, Klocke R, Hasib L, Stypmann J, Fabritz L, Stelljes M, Tian W, Zwiener M, Mueller M, Kienast J, Breithardt G, Nikol S (2006) G-CSF/SCF reduces inducible arrhythmias in the infarcted heart potentially via increased connexin43 expression and arteriogenesis. J Exp Med 203:87–97. doi:10.1084/jem.20051151
Kumar A, Crawford K, Close L, Madison M, Lorenz J, Doetschman T, Pawlowski S, Duffy J, Neumann J, Robbins J, Boivin GP, O’Toole BA, Lessard JL (1997) Rescue of cardiac alpha-actin-deficient mice by enteric smooth muscle gamma-actin. Proc Natl Acad Sci USA 94:4406–4411
Kurrelmeyer KM, Michael LH, Baumgarten G, Taffet GE, Peschon JJ, Sivasubramanian N, Entman ML, Mann DL (2000) Endogenous tumor necrosis factor protects the adult cardiac myocyte against ischemic-induced apoptosis in a murine model of acute myocardial infarction. Proc Natl Acad Sci U S A 97:5456–5461. doi:10.1073/pnas.070036297
Kuwajima I, Kardon MB, Pegram BL, Sesoko S, Frohlich ED (1982) Regression of left ventricular hypertrophy in two-kidney, one clip Goldblatt hypertension. Hypertension 4:113–118
Langenickel T, Pagel I, Hohnel K, Dietz R, Willenbrock R (2000) Differential regulation of cardiac ANP and BNP mRNA in different stages of experimental heart failure. Am J Physiol Heart Circ Physiol 278:H1500–H1506
Lebrecht D, Kokkori A, Ketelsen UP, Setzer B, Walker UA (2005) Tissue-specific mtDNA lesions and radical-associated mitochondrial dysfunction in human hearts exposed to doxorubicin. J Pathol 207:436–444. doi:10.1002/path.1863
Leenen FH, de Jong W (1975) Plasma renin and sodium balance during development of moderate and severe renal hypertension in rats. Circ Res 36:179–186
Lefrak EA, Pitha J, Rosenheim S, Gottlieb JA (1973) A clinicopathologic analysis of adriamycin cardiotoxicity. Cancer 32:302–314
Leite-Moreira AF (2006) Current perspectives in diastolic dysfunction and diastolic heart failure. Heart 92:712–718. doi:10.1136/hrt.2005.062950
Li JM, Yao ZF, Zou YZ, Ge JB, Guan AL, Wu J, Mi SL, Liang YY, Ma Z (2011) The therapeutic potential of G-CSF in pressure overload induced ventricular reconstruction and heart failure in mice. Mol Biol Rep doi:10.1007/s11033-011-0703-8
Li L, Chu Y, Fink GD, Engelhardt JF, Heistad DD, Chen AF (2003) Endothelin-1 stimulates arterial VCAM-1 expression via NADPH oxidase-derived superoxide in mineralocorticoid hypertension. Hypertension 42:997–1003. doi:10.1161/01.HYP.0000095980.43859.59
Li Y, Takemura G, Kosai K, Takahashi T, Okada H, Miyata S, Yuge K, Nagano S, Esaki M, Khai NC, Goto K, Mikami A, Maruyama R, Minatoguchi S, Fujiwara T, Fujiwara H (2004) Critical roles for the Fas/Fas ligand system in postinfarction ventricular remodeling and heart failure. Circ Res 95:627–636. doi:10.1161/01.RES.0000141528.54850.bd
Li YY, Feldman AM (2001) Matrix metalloproteinases in the progression of heart failure: potential therapeutic implications. Drugs 61:1239–1252
Li Z, Bing OH, Long X, Robinson KG, Lakatta EG (1997) Increased cardiomyocyte apoptosis during the transition to heart failure in the spontaneously hypertensive rat. Am J Physiol 272:H2313–H2319
Li Z, Tran TT, Ma JY, O’Young G, Kapoun AM, Chakravarty S, Dugar S, Schreiner G, Protter AA (2004) p38 alpha mitogen-activated protein kinase inhibition improves cardiac function and reduces myocardial damage in isoproterenol-induced acute myocardial injury in rats. J Cardiovasc Pharmacol 44:486–492.
Liggett SB, Tepe NM, Lorenz JN, Canning AM, Jantz TD, Mitarai S, Yatani A, Dorn GW 2nd (2000) Early and delayed consequences of beta(2)-adrenergic receptor overexpression in mouse hearts: critical role for expression level. Circulation 101:1707–1714
Lim CC, Zuppinger C, Guo X, Kuster GM, Helmes M, Eppenberger HM, Suter TM, Liao R, Sawyer DB (2004) Anthracyclines induce calpain-dependent titin proteolysis and necrosis in cardiomyocytes. J Biol Chem 279:8290–8299. doi:10.1074/jbc.M308033200
Ling H, Zhang T, Pereira L, Means CK, Cheng H, Gu Y, Dalton ND, Peterson KL, Chen J, Bers D, Heller Brown J (2009) Requirement for Ca2+/calmodulin-dependent kinase II in the transition from pressure overload-induced cardiac hypertrophy to heart failure in mice. J Clin Invest 119:1230–1240. doi:10.1172/JCI38022
Litwin SE, Katz SE, Weinberg EO, Lorell BH, Aurigemma GP, Douglas PS (1995) Serial echocardiographic-Doppler assessment of left ventricular geometry and function in rats with pressure-overload hypertrophy. Chronic angiotensin-converting enzyme inhibition attenuates the transition to heart failure. Circulation 91:2642–2654
Liu P, Penninger J, Aitken K, Sole M, Mak T (1995) The role of transgenic knockout models in defining the pathogenesis of viral heart disease. Eur Heart J 16 Suppl O:25–27
Liu YH, Yang XP, Nass O, Sabbah HN, Peterson E, Carretero OA (1997) Chronic heart failure induced by coronary artery ligation in Lewis inbred rats. Am J Physiol 272:H722–H727
Liu Z, Hilbelink DR, Crockett WB, Gerdes AM (1991) Regional changes in hemodynamics and cardiac myocyte size in rats with aortocaval fistulas. 1. Developing and established hypertrophy. Circ Res 69:52–58
Lloyd-Jones D, Adams RJ, Brown TM, Carnethon M, Dai S, De Simone G, Ferguson TB, Ford E, Furie K, Gillespie C, Go A, Greenlund K, Haase N, Hailpern S, Ho PM, Howard V, Kissela B, Kittner S, Lackland D, Lisabeth L, Marelli A, McDermott MM, Meigs J, Mozaffarian D, Mussolino M, Nichol G, Roger VL, Rosamond W, Sacco R, Sorlie P, Thom T, Wasserthiel-Smoller S, Wong ND, Wylie-Rosett J (2010) Heart disease and stroke statistics–2010 update: a report from the American Heart Association. Circulation 121:e46–e215. doi:10.1161/CIRCULATIONAHA.109.192667
London B, Baker LC, Lee JS, Shusterman V, Choi BR, Kubota T, McTiernan CF, Feldman AM, Salama G (2003) Calcium-dependent arrhythmias in transgenic mice with heart failure. Am J Physiol Heart Circ Physiol 284:H431–441. doi:10.1152/ajpheart.00431.2002
Lou H, Danelisen I, Singal PK (2004) Cytokines are not upregulated in adriamycin-induced cardiomyopathy and heart failure. J Mol Cell Cardiol 36:683–690. doi:10.1016/j.yjmcc.2004.03.004
Luo J, Fujikura K, Homma S, Konofagou EE (2007) Myocardial elastography at both high temporal and spatial resolution for the detection of infarcts. Ultrasound Med Biol 33:1206–1223. doi:10.1016/j.ultrasmedbio.2007.01.019
Luo W, Grupp IL, Harrer J, Ponniah S, Grupp G, Duffy JJ, Doetschman T, Kranias EG (1994) Targeted ablation of the phospholamban gene is associated with markedly enhanced myocardial contractility and loss of beta-agonist stimulation. Circ Res 75:401–409
Lygate CA, Schneider JE, Hulbert K, ten Hove M, Sebag-Montefiore LM, Cassidy PJ, Clarke K, Neubauer S (2006) Serial high resolution 3D-MRI after aortic banding in mice: band internalization is a source of variability in the hypertrophic response. Basic Res Cardiol 101:8–16. doi:10.1007/s00395-005-0546-3
MacLennan DH, Kranias EG (2003) Phospholamban: a crucial regulator of cardiac contractility. Nat Rev Mol Cell Biol 4:566–577. doi:10.1038/nrm1151
Maier LS, Wahl-Schott C, Horn W, Weichert S, Pagel C, Wagner S, Dybkova N, Muller OJ, Nabauer M, Franz WM, Pieske B (2005) Increased SR Ca2+ cycling contributes to improved contractile performance in SERCA2a-overexpressing transgenic rats. Cardiovasc Res 67:636–646. doi:10.1016/j.cardiores.2005.05.006
Mann DL (2002) Inflammatory mediators and the failing heart: past, present, and the foreseeable future. Circ Res 91:988–998
Manning RD Jr, Meng S, Tian N (2003) Renal and vascular oxidative stress and salt-sensitivity of arterial pressure. Acta Physiol Scand 179:243–250
Marian AJ, Roberts R (2001) The molecular genetic basis for hypertrophic cardiomyopathy. J Mol Cell Cardiol 33:655–670. doi:10.1006/jmcc.2001.1340
Matsumori A, Kawai C (1982) An experimental model for congestive heart failure after encephalomyocarditis virus myocarditis in mice. Circulation 65:1230–1235
Matsumori A, Sasayama S (1995) Immunomodulating agents for the management of heart failure with myocarditis and cardiomyopathy–lessons from animal experiments. Eur Heart J 16 Suppl O:140–143
Matsumura Y, Hashimoto N, Taira S, Kuro T, Kitano R, Ohkita M, Opgenorth TJ, Takaoka M (1999) Different contributions of endothelin-A and endothelin-B receptors in the pathogenesis of deoxycorticosterone acetate-salt-induced hypertension in rats. Hypertension 33:759–765
McCully JD, Jandreski MA, Liew J, Sole MJ, Liew CC (1987) Construction of cosmid genomic libraries for the normal and myopathic Syrian hamsters. Biochem Cell Biol 65:997–1000
McMurray J, Pfeffer MA (2002) New therapeutic options in congestive heart failure: Part I. Circulation 105:2099–2106
McMurray J, Pfeffer MA (2002) New therapeutic options in congestive heart failure: Part II. Circulation 105:2223–2228
Mende U, Kagen A, Cohen A, Aramburu J, Schoen FJ, Neer EJ (1998) Transient cardiac expression of constitutively active Galphaq leads to hypertrophy and dilated cardiomyopathy by calcineurin-dependent and independent pathways. Proc Natl Acad Sci USA 95:13893–13898
Mendez GF, Cowie MR (2001) The epidemiological features of heart failure in developing countries: a review of the literature. Int J Cardiol 80:213–219
Menna P, Recalcati S, Cairo G, Minotti G (2007) An introduction to the metabolic determinants of anthracycline cardiotoxicity. Cardiovasc Toxicol 7:80–85. doi:10.1007/s12012-007-0011-7
Mering JV MO (1889) Diabetes mellitus nach Pankreasextirpation. Centralblatt fu¨ r klinische Medicin, Leipzig10:383
Michael LH, Entman ML, Hartley CJ, Youker KA, Zhu J, Hall SR, Hawkins HK, Berens K, Ballantyne CM (1995) Myocardial ischemia and reperfusion: a murine model. Am J Physiol 269:H2147–H2154
Michael O’Donnell J, Narayan P, Bailey MQ, Abduljalil AM, Altschuld RA, McCune SA, Robitaille PM (1998) 31P-NMR analysis of congestive heart failure in the SHHF/Mcc-facp rat heart. J Mol Cell Cardiol 30:235–241. doi:10.1006/jmcc.1997.0587
Mihm MJ, Yu F, Weinstein DM, Reiser PJ, Bauer JA (2002) Intracellular distribution of peroxynitrite during doxorubicin cardiomyopathy: evidence for selective impairment of myofibrillar creatine kinase. Br J Pharmacol 135:581–588. doi:10.1038/sj.bjp.0704495
Milano CA, Allen LF, Dolber PC, Johnson TD, Rockman HA, Bond RA, Lefkowitz RJ (1995) Marked enhancement in myocardial function resulting from overexpression of a human beta-adrenergic receptor gene. J Thorac Cardiovasc Surg 109:236–241
Milano CA, Dolber PC, Rockman HA, Bond RA, Venable ME, Allen LF, Lefkowitz RJ (1994) Myocardial expression of a constitutively active alpha 1B-adrenergic receptor in transgenic mice induces cardiac hypertrophy. Proc Natl Acad Sci USA 91:10109–10113
Milner DJ, Weitzer G, Tran D, Bradley A, Capetanaki Y (1996) Disruption of muscle architecture and myocardial degeneration in mice lacking desmin. J Cell Biol 134:1255–1270
Minamisawa S, Hoshijima M, Chu G, Ward CA, Frank K, Gu Y, Martone ME, Wang Y, Ross J Jr, Kranias EG, Giles WR, Chien KR (1999) Chronic phospholamban-sarcoplasmic reticulum calcium ATPase interaction is the critical calcium cycling defect in dilated cardiomyopathy. Cell 99:313–322
Mitchell GF, Pfeffer JM, Pfeffer MA (1997) The transition to failure in the spontaneously hypertensive rat. Am J Hypertens 10:120S–126S
Moens AL, Champion HC, Claeys MJ, Tavazzi B, Kaminski PM, Wolin MS, Borgonjon DJ, Van Nassauw L, Haile A, Zviman M, Bedja D, Wuyts FL, Elsaesser RS, Cos P, Gabrielson KL, Lazzarino G, Paolocci N, Timmermans JP, Vrints CJ, Kass DA (2008) High-dose folic acid pretreatment blunts cardiac dysfunction during ischemia coupled to maintenance of high-energy phosphates and reduces postreperfusion injury. Circulation 117:1810–1819. doi:10.1161/CIRCULATIONAHA.107.725481
Moens AL, Ketner EA, Takimoto E, Schmidt TS, O’Neill CA, Wolin MS, Alp NJ, Channon KM, Kass DA (2011) Bi-modal dose-dependent cardiac response to tetrahydrobiopterin in pressure-overload induced hypertrophy and heart failure. J Mol Cell Cardiol. doi:10.1016/j.yjmcc.2011.05.017
Moens AL, Leyton-Mange JS, Niu X, Yang R, Cingolani O, Arkenbout EK, Champion HC, Bedja D, Gabrielson KL, Chen J, Xia Y, Hale AB, Channon KM, Halushka MK, Barker N, Wuyts FL, Kaminski PM, Wolin MS, Kass DA, Barouch LA (2009) Adverse ventricular remodeling and exacerbated NOS uncoupling from pressure-overload in mice lacking the beta3-adrenoreceptor. J Mol Cell Cardiol 47:576–585. doi:10.1016/j.yjmcc.2009.06.005
Mohammed SF, Storlie JR, Oehler EA, Bowen LA, Korinek J, Lam CS, Simari RD, Burnett JC Jr, Redfield MM (2011) Variable phenotype in murine transverse aortic constriction. Cardiovasc Pathol. doi:10.1016/j.carpath.2011.05.002
Mohapatra B, Jimenez S, Lin JH, Bowles KR, Coveler KJ, Marx JG, Chrisco MA, Murphy RT, Lurie PR, Schwartz RJ, Elliott PM, Vatta M, McKenna W, Towbin JA, Bowles NE (2003) Mutations in the muscle LIM protein and alpha-actinin-2 genes in dilated cardiomyopathy and endocardial fibroelastosis. Mol Genet Metab 80:207–215
Molina EJ, Gupta D, Palma J, Torres D, Gaughan JP, Houser S, Macha M (2009) Novel experimental model of pressure overload hypertrophy in rats. J Surg Res 153:287–294. doi:10.1016/j.jss.2008.03.043
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
Molkentin JD, Robbins J (2009) With great power comes great responsibility: using mouse genetics to study cardiac hypertrophy and failure. J Mol Cell Cardiol 46:130–136. doi:10.1016/j.yjmcc.2008.09.002
Monnet E, Chachques JC (2005) Animal models of heart failure: what is new? Ann Thorac Surg 79:1445–1453. doi:10.1016/j.athoracsur.2004.04.002
Moreau P, Schiffrin EL (2003) Role of endothelins in animal models of hypertension: focus on cardiovascular protection. Can J Physiol Pharmacol 81:511–521. doi:10.1139/y03-015
Movsesian MA, Kukreja RC (2011) Phosphodiesterase inhibition in heart failure. Handb Exp Pharmacol 237–249 doi:10.1007/978-3-642-17969-3_10
Muller FU, Kirchhefer U, Begrow F, Reinke U, Neumann J, Schmitz W (2002) Junctional sarcoplasmic reticulum transmembrane proteins in the heart. Basic Res Cardiol 97(Suppl 1):I52–I55
Murakami K, Mizushige K, Noma T, Tsuji T, Kimura S, Kohno M (2002) Perindopril effect on uncoupling protein and energy metabolism in failing rat hearts. Hypertension 40:251–255
Murata T, Yamawaki H, Yoshimoto R, Hori M, Sato K, Ozaki H, Karaki H (2001) Chronic effect of doxorubicin on vascular endothelium assessed by organ culture study. Life Sci 69:2685–2695
Muth JN, Bodi I, Lewis W, Varadi G, Schwartz A (2001) A Ca(2+)-dependent transgenic model of cardiac hypertrophy: a role for protein kinase Calpha. Circulation 103:140–147
Nagano M, Kato M, Nagai M, Yang J (1991) Protective effect of ACE- and kininase-inhibitor on the onset of cardiomyopathy. Basic Res Cardiol 86(Suppl 3):187–195
Nagatsu M, Zile MR, Tsutsui H, Schmid PG, DeFreyte G, Cooper Gt, Carabello BA (1994) Native beta-adrenergic support for left ventricular dysfunction in experimental mitral regurgitation normalizes indexes of pump and contractile function. Circulation 89:818–826
Nigro V, Okazaki Y, Belsito A, Piluso G, Matsuda Y, Politano L, Nigro G, Ventura C, Abbondanza C, Molinari AM, Acampora D, Nishimura M, Hayashizaki Y, Puca GA (1997) Identification of the Syrian hamster cardiomyopathy gene. Hum Mol Genet 6:601–607
Nishio R, Sasayama S, Matsumori A (2002) Left ventricular pressure-volume relationship in a murine model of congestive heart failure due to acute viral myocarditis. J Am Coll Cardiol 40:1506–1514
O’Donnell SM, Hansberger MW, Connolly JL, Chappell JD, Watson MJ, Pierce JM, Wetzel JD, Han W, Barton ES, Forrest JC, Valyi-Nagy T, Yull FE, Blackwell TS, Rottman JN, Sherry B, Dermody TS (2005) Organ-specific roles for transcription factor NF-kappaB in reovirus-induced apoptosis and disease. J Clin Invest 115:2341–2350. doi:10.1172/JCI22428
Ogata T, Miyauchi T, Sakai S, Takanashi M, Irukayama-Tomobe Y, Yamaguchi I (2004) Myocardial fibrosis and diastolic dysfunction in deoxycorticosterone acetate-salt hypertensive rats is ameliorated by the peroxisome proliferator-activated receptor-alpha activator fenofibrate, partly by suppressing inflammatory responses associated with the nuclear factor-kappa-B pathway. J Am Coll Cardiol 43:1481–1488. doi:10.1016/j.jacc.2003.11.043
Oudit GY, Crackower MA, Eriksson U, Sarao R, Kozieradzki I, Sasaki T, Irie-Sasaki J, Gidrewicz D, Rybin VO, Wada T, Steinberg SF, Backx PH, Penninger JM (2003) Phosphoinositide 3-kinase gamma-deficient mice are protected from isoproterenol-induced heart failure. Circulation 108:2147–2152. doi:10.1161/01.CIR.0000091403.62293.2B
Ozek C, Zhang F, Lineaweaver WC, Chin BT, Eiman T, Newlin L, Buncke HJ (1998) A new heart failure model in rat by an end-to-side femoral vessel anastomosis. Cardiovasc Res 37:236–238
Pacher P, Nagayama T, Mukhopadhyay P, Batkai S, Kass DA (2008) Measurement of cardiac function using pressure-volume conductance catheter technique in mice and rats. Nat Protoc 3:1422–1434. doi:10.1038/nprot.2008.138
Padmanabhan M, Prince PS (2006) Preventive effect of S-allylcysteine on lipid peroxides and antioxidants in normal and isoproterenol-induced cardiotoxicity in rats: a histopathological study. Toxicology 224:128–137. doi:10.1016/j.tox.2006.04.039
Padmanabhan M, Rajadurai M, Prince PS (2008) Preventive effect of S-allylcysteine on membrane-bound enzymes and glycoproteins in normal and isoproterenol-induced cardiac toxicity in male Wistar rats. Basic Clin Pharmacol Toxicol 103:507–513. doi:10.1111/j.1742-7843.2008.00244.x
Paradis P, Dali-Youcef N, Paradis FW, Thibault G, Nemer M (2000) Overexpression of angiotensin II type I receptor in cardiomyocytes induces cardiac hypertrophy and remodeling. Proc Natl Acad Sci USA 97:931–936
Park SC, Liu-Stratton Y, Medeiros LC, McCune SA, Radin MJ (2004) Effect of male sex and obesity on platelet arachidonic acid in spontaneous hypertensive heart failure rats. Exp Biol Med (Maywood) 229:657–664
Patten RD, Hall-Porter MR (2009) Small animal models of heart failure: development of novel therapies, past and present. Circ Heart Fail 2:138–144. doi:10.1161/CIRCHEARTFAILURE.108.839761
Peng X, Chen B, Lim CC, Sawyer DB (2005) The cardiotoxicology of anthracycline chemotherapeutics: translating molecular mechanism into preventative medicine. Mol Interv 5:163–171. doi:10.1124/mi.5.3.6
Periasamy M, Reed TD, Liu LH, Ji Y, Loukianov E, Paul RJ, Nieman ML, Riddle T, Duffy JJ, Doetschman T, Lorenz JN, Shull GE (1999) Impaired cardiac performance in heterozygous mice with a null mutation in the sarco(endo)plasmic reticulum Ca2+-ATPase isoform 2 (SERCA2) gene. J Biol Chem 274:2556–2562
Pfeffer JM, Pfeffer MA, Fishbein MC, Frohlich ED (1979) Cardiac function and morphology with aging in the spontaneously hypertensive rat. Am J Physiol 237:H461–H468
Pfeffer JM, Pfeffer MA, Mirsky I, Braunwald E (1982) Regression of left ventricular hypertrophy and prevention of left ventricular dysfunction by captopril in the spontaneously hypertensive rat. Proc Natl Acad Sci USA 79:3310–3314
Pfeffer MA, Pfeffer JM, Fishbein MC, Fletcher PJ, Spadaro J, Kloner RA, Braunwald E (1979) Myocardial infarct size and ventricular function in rats. Circ Res 44:503–512
Pleger ST, Remppis A, Heidt B, Volkers M, Chuprun JK, Kuhn M, Zhou RH, Gao E, Szabo G, Weichenhan D, Muller OJ, Eckhart AD, Katus HA, Koch WJ, Most P (2005) S100A1 gene therapy preserves in vivo cardiac function after myocardial infarction. Mol Ther 12:1120–1129. doi:10.1016/j.ymthe.2005.08.002
Plestina R, Stoner HB (1972) Pulmonary oedema in rats given monocrotaline pyrrole. J Pathol 106:235–249. doi:10.1002/path.1711060405
Porter CB, Walsh RA, Badke FR, O’Rourke RA (1983) Differential effects of diltiazem and nitroprusside on left ventricular function in experimental chronic volume overload. Circulation 68:685–692
Rakieten N, Rakieten ML, Nadkarni MV (1963) Studies on the diabetogenic action of streptozotocin (NSC-37917). Cancer Chemother Rep 29:91–98
Redfern CH, Degtyarev MY, Kwa AT, Salomonis N, Cotte N, Nanevicz T, Fidelman N, Desai K, Vranizan K, Lee EK, Coward P, Shah N, Warrington JA, Fishman GI, Bernstein D, Baker AJ, Conklin BR (2000) Conditional expression of a Gi-coupled receptor causes ventricular conduction delay and a lethal cardiomyopathy. Proc Natl Acad Sci USA 97:4826–4831
Redfield MM (2000) Epidemiology and pathophysiology of heart failure. Curr Cardiol Rep 2:179–180
Reed AL, Tanaka A, Sorescu D, Liu H, Jeong EM, Sturdy M, Walp ER, Dudley SC Jr, Sutliff RL (2011) Diastolic dysfunction is associated with cardiac fibrosis in the senescence-accelerated mouse. Am J Physiol Heart Circ Physiol 301:H824–831. doi:10.1152/ajpheart.00407.2010
Rerup CC (1970) Drugs producing diabetes through damage of the insulin secreting cells. Pharmacol Rev 22:485–518
Rizzi E, Castro MM, Prado CM, Silva CA, Fazan R Jr, Rossi MA, Tanus-Santos JE, Gerlach RF (2010) Matrix metalloproteinase inhibition improves cardiac dysfunction and remodeling in 2-kidney, 1-clip hypertension. J Card Fail 16:599–608. doi:10.1016/j.cardfail.2010.02.005
Rockman HA, Chien KR, Choi DJ, Iaccarino G, Hunter JJ, Ross J Jr, Lefkowitz RJ, Koch WJ (1998) Expression of a beta-adrenergic receptor kinase 1 inhibitor prevents the development of myocardial failure in gene-targeted mice. Proc Natl Acad Sci USA 95:7000–7005
Rockman HA, Ross RS, Harris AN, Knowlton KU, Steinhelper ME, Field LJ, Ross J Jr, Chien KR (1991) Segregation of atrial-specific and inducible expression of an atrial natriuretic factor transgene in an in vivo murine model of cardiac hypertrophy. Proc Natl Acad Sci USA 88:8277–8281
Rockman HA, Wachhorst SP, Mao L, Ross J Jr (1994) ANG II receptor blockade prevents ventricular hypertrophy and ANF gene expression with pressure overload in mice. Am J Physiol 266:H2468–H2475
Rodriguez-Iturbe B, Quiroz Y, Kim CH, Vaziri ND (2005) Hypertension induced by aortic coarctation above the renal arteries is associated with immune cell infiltration of the kidneys. Am J Hypertens 18:1449–1456. doi:10.1016/j.amjhyper.2005.05.034
Rohrer DK, Chruscinski A, Schauble EH, Bernstein D, Kobilka BK (1999) Cardiovascular and metabolic alterations in mice lacking both beta1- and beta2-adrenergic receptors. J Biol Chem 274:16701–16708
Ruiz-Hurtado G, Fernandez-Velasco M, Mourelle M, Delgado C (2007) LA419, a novel nitric oxide donor, prevents pathological cardiac remodeling in pressure-overloaded rats via endothelial nitric oxide synthase pathway regulation. Hypertension 50:1049–1056. doi:10.1161/HYPERTENSIONAHA.107.093666
Ruiz P, Witt H (2006) Microarray analysis to evaluate different animal models for human heart failure. J Mol Cell Cardiol 40:13–15. doi:10.1016/j.yjmcc.2005.09.010
Ryu JH, Kim IK, Cho SW, Cho MC, Hwang KK, Piao H, Piao S, Lim SH, Hong YS, Choi CY, Yoo KJ, Kim BS (2005) Implantation of bone marrow mononuclear cells using injectable fibrin matrix enhances neovascularization in infarcted myocardium. Biomaterials 26:319–326. doi:10.1016/j.biomaterials.2004.02.058
Sah VP, Minamisawa S, Tam SP, Wu TH, Dorn GW 2nd, Ross J Jr, Chien KR, Brown JH (1999) Cardiac-specific overexpression of RhoA results in sinus and atrioventricular nodal dysfunction and contractile failure. J Clin Invest 103:1627–1634. doi:10.1172/JCI6842
Sakamoto A (2004) Electrical and ionic abnormalities in the heart of cardiomyopathic hamsters: in quest of a new paradigm for cardiac failure and lethal arrhythmia. Mol Cell Biochem 259:183–187
Sakamoto A, Abe M, Masaki T (1999) Delineation of genomic deletion in cardiomyopathic hamster. FEBS Lett 447:124–128
Sakamoto A, Ono K, Abe M, Jasmin G, Eki T, Murakami Y, Masaki T, Toyo-oka T, Hanaoka F (1997) Both hypertrophic and dilated cardiomyopathies are caused by mutation of the same gene, delta-sarcoglycan, in hamster: an animal model of disrupted dystrophin-associated glycoprotein complex. Proc Natl Acad Sci USA 94:13873–13878
Sanbe A, Gulick J, Hanks MC, Liang Q, Osinska H, Robbins J (2003) Reengineering inducible cardiac-specific transgenesis with an attenuated myosin heavy chain promoter. Circ Res 92:609–616. doi:10.1161/01.RES.0000065442.64694.9F
Sato Y, Ferguson DG, Sako H, Dorn GW 2nd, Kadambi VJ, Yatani A, Hoit BD, Walsh RA, Kranias EG (1998) Cardiac-specific overexpression of mouse cardiac calsequestrin is associated with depressed cardiovascular function and hypertrophy in transgenic mice. J Biol Chem 273:28470–28477
Sato Y, Kiriazis H, Yatani A, Schmidt AG, Hahn H, Ferguson DG, Sako H, Mitarai S, Honda R, Mesnard-Rouiller L, Frank KF, Beyermann B, Wu G, Fujimori K, Dorn GW 2nd, Kranias EG (2001) Rescue of contractile parameters and myocyte hypertrophy in calsequestrin overexpressing myocardium by phospholamban ablation. J Biol Chem 276:9392–9399. doi:10.1074/jbc.M006889200
Satoh S, Ueda Y, Suematsu N, Oyama J, Kadokami T, Sugano M, Yoshikawa Y, Makino N (2003) Beneficial effects of angiotensin-converting enzyme inhibition on sarcoplasmic reticulum function in the failing heart of the Dahl rat. Circ J 67:705–711
Sawyer DB, Fukazawa R, Arstall MA, Kelly RA (1999) Daunorubicin-induced apoptosis in rat cardiac myocytes is inhibited by dexrazoxane. Circ Res 84:257–265
Sawyer DB, Peng X, Chen B, Pentassuglia L, Lim CC (2010) Mechanisms of anthracycline cardiac injury: can we identify strategies for cardioprotection? Prog Cardiovasc Dis 53:105–113. doi:10.1016/j.pcad.2010.06.007
Scheuermann-Freestone M, Freestone NS, Langenickel T, Hohnel K, Dietz R, Willenbrock R (2001) A new model of congestive heart failure in the mouse due to chronic volume overload. Eur J Heart Fail 3:535–543
Schiffrin EL (2000) Endothelin: role in experimental hypertension. J Cardiovasc Pharmacol 35:S33–S35
Schiffrin EL (2001) Role of endothelin-1 in hypertension and vascular disease. Am J Hypertens 14:83S–89S. doi:S089570610102074X
Schlenker EH, Kost CK Jr, Likness MM (2004) Effects of long-term captopril and l-arginine treatment on ventilation and blood pressure in obese male SHHF rats. J Appl Physiol 97:1032–1039. doi:10.1152/japplphysiol.00255.2004
Schmidt-Supprian M, Rajewsky K (2007) Vagaries of conditional gene targeting. Nat Immunol 8:665–668. doi:10.1038/ni0707-665
Schmitt JP, Kamisago M, Asahi M, Li GH, Ahmad F, Mende U, Kranias EG, MacLennan DH, Seidman JG, Seidman CE (2003) Dilated cardiomyopathy and heart failure caused by a mutation in phospholamban. Science 299:1410–1413. doi:10.1126/science.1081578299/5611/1410
Schoental R, Head MA (1955) Pathological changes in rats as a result of treatment with monocrotaline. Br J Cancer 9:229–237
Schunkert H, Dzau VJ, Tang SS, Hirsch AT, Apstein CS, Lorell BH (1990) Increased rat cardiac angiotensin converting enzyme activity and mRNA expression in pressure overload left ventricular hypertrophy. Effects on coronary resistance, contractility, and relaxation. J Clin Invest 86:1913–1920. doi:10.1172/JCI114924
Schwarz B, Percy E, Gao XM, Dart AM, Richardt G, Du XJ (2003) Altered calcium transient and development of hypertrophy in beta2-adrenoceptor overexpressing mice with and without pressure overload. Eur J Heart Fail 5:131–136.
Schwinger RH, Bohm M, Erdmann E (1990) Evidence against spare or uncoupled beta-adrenoceptors in the human heart. Am Heart J 119:899–904
Schwinger RH, Bohm M, Schmidt U, Karczewski P, Bavendiek U, Flesch M, Krause EG, Erdmann E (1995) Unchanged protein levels of SERCA II and phospholamban but reduced Ca2+ uptake and Ca(2+)-ATPase activity of cardiac sarcoplasmic reticulum from dilated cardiomyopathy patients compared with patients with nonfailing hearts. Circulation 92:3220–3228
Seidman JG, Seidman C (2001) The genetic basis for cardiomyopathy: from mutation identification to mechanistic paradigms. Cell 104:557–567
Selye H (1942) Production of nephrosclerosis by overdosage with desoxycorticosterone acetate. Can Med Assoc J 47:515–519
Shai SY, Harpf AE, Babbitt CJ, Jordan MC, Fishbein MC, Chen J, Omura M, Leil TA, Becker KD, Jiang M, Smith DJ, Cherry SR, Loftus JC, Ross RS (2002) Cardiac myocyte-specific excision of the beta1 integrin gene results in myocardial fibrosis and cardiac failure. Circ Res 90:458–464
Shen FM, Xie HH, Ling G, Xu LP, Su DF (2005) Synergistic effects of atenolol and amlodipine for lowering and stabilizing blood pressure in 2K1C renovascular hypertensive rats. Acta Pharmacol Sin 26:1303–1308. doi:10.1111/j.1745-7254.2005.00185.x
Shimizu T, Nojiri H, Kawakami S, Uchiyama S, Shirasawa T (2010) Model mice for tissue-specific deletion of the manganese superoxide dismutase gene. Geriatr Gerontol Int 10(Suppl 1):S70–79. doi:10.1111/j.1447-0594.2010.00604.x
Shusterman V, Usiene I, Harrigal C, Lee JS, Kubota T, Feldman AM, London B (2002) Strain-specific patterns of autonomic nervous system activity and heart failure susceptibility in mice. Am J Physiol Heart Circ Physiol 282:H2076–H2083. doi:10.1152/ajpheart.00917.2001
Sicard P, Oudot A, Guilland JC, Moreau D, Vergely C, Rochette L (2006) Dissociation between vascular oxidative stress and cardiovascular function in Wistar Kyoto and spontaneously hypertensive rats. Vascul Pharmacol 45:112–121. doi:10.1016/j.vph.2006.04.001
Silberman GA, Fan TH, Liu H, Jiao Z, Xiao HD, Lovelock JD, Boulden BM, Widder J, Fredd S, Bernstein KE, Wolska BM, Dikalov S, Harrison DG, Dudley SC Jr (2010) Uncoupled cardiac nitric oxide synthase mediates diastolic dysfunction. Circulation 121:519–528. doi:10.1161/CIRCULATIONAHA.109.883777
Silver DP, Livingston DM (2001) Self-excising retroviral vectors encoding the Cre recombinase overcome Cre-mediated cellular toxicity. Mol Cell 8:233–243
Simunek T, Sterba M, Popelova O, Adamcova M, Hrdina R, Gersl V (2009) Anthracycline-induced cardiotoxicity: overview of studies examining the roles of oxidative stress and free cellular iron. Pharmacol Rep 61:154–171
Sohal DS, Nghiem M, Crackower MA, Witt SA, Kimball TR, Tymitz KM, Penninger JM, Molkentin JD (2001) Temporally regulated and tissue-specific gene manipulations in the adult and embryonic heart using a tamoxifen-inducible Cre protein. Circ Res 89:20–25
Stansfield WE, Rojas M, Corn D, Willis M, Patterson C, Smyth SS, Selzman CH (2007) Characterization of a model to independently study regression of ventricular hypertrophy. J Surg Res 142:387–393. doi:10.1016/j.jss.2007.01.037
Stock JH, Reller MD, Sharma S, Pavcnik D, Shiota T, Sahn DJ (1997) Transballoon intravascular ultrasound imaging during balloon angioplasty in animal models with coarctation and branch pulmonary stenosis. Circulation 95:2354–2357
Sun ZJ, Zhang ZE (2005) Historic perspectives and recent advances in major animal models of hypertension. Acta Pharmacol Sin 26:295–301. doi:10.1111/j.1745-7254.2005.00054.x
Surwit RS, Feinglos MN, Rodin J, Sutherland A, Petro AE, Opara EC, Kuhn CM, Rebuffe-Scrive M (1995) Differential effects of fat and sucrose on the development of obesity and diabetes in C57BL/6J and A/J mice. Metabolism 44:645–651
Sussman MA, Welch S, Walker A, Klevitsky R, Hewett TE, Price RL, Schaefer E, Yager K (2000) Altered focal adhesion regulation correlates with cardiomyopathy in mice expressing constitutively active rac1. J Clin Invest 105:875–886. doi:10.1172/JCI8497
Suzuki M, Carlson KM, Marchuk DA, Rockman HA (2002) Genetic modifier loci affecting survival and cardiac function in murine dilated cardiomyopathy. Circulation 105:1824–1829
Szenczi O, Kemecsei P, Holthuijsen MF, van Riel NA, van der Vusse GJ, Pacher P, Szabo C, Kollai M, Ligeti L, Ivanics T (2005) Poly(ADP-ribose) polymerase regulates myocardial calcium handling in doxorubicin-induced heart failure. Biochem Pharmacol 69:725–732. doi:10.1016/j.bcp.2004.11.023
Takahashi S, Denvir MA, Harder L, Miller DJ, Cobbe SM, Kawakami M, MacFarlane NG, Okabe E (1998) Effects of in vitro and in vivo exposure to doxorubicin (adriamycin) on caffeine-induced Ca2+ release from sarcoplasmic reticulum and contractile protein function in ‘chemically-skinned’ rabbit ventricular trabeculae. Jpn J Pharmacol 76:405–413
Takeishi Y, Ping P, Bolli R, Kirkpatrick DL, Hoit BD, Walsh RA (2000) Transgenic overexpression of constitutively active protein kinase C epsilon causes concentric cardiac hypertrophy. Circ Res 86:1218–1223
Takemura G, Fujiwara H (2007) Doxorubicin-induced cardiomyopathy from the cardiotoxic mechanisms to management. Prog Cardiovasc Dis 49:330–352. doi:10.1016/j.pcad.2006.10.002
Takemura G, Miyata S, Kawase Y, Okada H, Maruyama R, Fujiwara H (2006) Autophagic degeneration and death of cardiomyocytes in heart failure. Autophagy 2:212–214
Takenaka H, Kihara Y, Iwanaga Y, Onozawa Y, Toyokuni S, Kita T (2006) Angiotensin II, oxidative stress, and extracellular matrix degradation during transition to LV failure in rats with hypertension. J Mol Cell Cardiol 41:989–997. doi:10.1016/j.yjmcc.2006.07.019
Takimoto E, Champion HC, Li M, Belardi D, Ren S, Rodriguez ER, Bedja D, Gabrielson KL, Wang Y, Kass DA (2005) Chronic inhibition of cyclic GMP phosphodiesterase 5A prevents and reverses cardiac hypertrophy. Nat Med 11:214–222. doi:10.1038/nm1175
Taniyama Y, Walsh K (2002) Elevated myocardial Akt signaling ameliorates doxorubicin-induced congestive heart failure and promotes heart growth. J Mol Cell Cardiol 34:1241–1247
Teerlink JR, Pfeffer JM, Pfeffer MA (1994) Progressive ventricular remodeling in response to diffuse isoproterenol-induced myocardial necrosis in rats. Circ Res 75:105–113
Terrand J, Xu B, Morrissy S, Dinh TN, Williams S, Chen QM (2011) p21(WAF1/Cip1/Sdi1) knockout mice respond to doxorubicin with reduced cardiotoxicity. Toxicol Appl Pharmacol. doi:10.1016/j.taap.2011.08.024
Toischer K, Rokita AG, Unsold B, Zhu W, Kararigas G, Sossalla S, Reuter SP, Becker A, Teucher N, Seidler T, Grebe C, Preuss L, Gupta SN, Schmidt K, Lehnart SE, Kruger M, Linke WA, Backs J, Regitz-Zagrosek V, Schafer K, Field LJ, Maier LS, Hasenfuss G (2010) Differential cardiac remodeling in preload versus afterload. Circulation 122:993–1003. doi:10.1161/CIRCULATIONAHA.110.943431
Tomlinson KC, Gardiner SM, Hebden RA, Bennett T (1992) Functional consequences of streptozotocin-induced diabetes mellitus, with particular reference to the cardiovascular system. Pharmacol Rev 44:103–150
Towbin JA, Bowles NE (2002) The failing heart. Nature 415:227–233. doi:10.1038/415227a
Tsuji T, Del Monte F, Yoshikawa Y, Abe T, Shimizu J, Nakajima-Takenaka C, Taniguchi S, Hajjar RJ, Takaki M (2009) Rescue of Ca2+ overload-induced left ventricular dysfunction by targeted ablation of phospholamban. Am J Physiol Heart Circ Physiol 296:H310–317. doi:10.1152/ajpheart.00975.2008
Ungerer M, Parruti G, Bohm M, Puzicha M, DeBlasi A, Erdmann E, Lohse MJ (1994) Expression of beta-arrestins and beta-adrenergic receptor kinases in the failing human heart. Circ Res 74:206–213
Usui S, Yao A, Hatano M, Kohmoto O, Takahashi T, Nagai R, Kinugawa K (2006) Upregulated neurohumoral factors are associated with left ventricular remodeling and poor prognosis in rats with monocrotaline-induced pulmonary arterial hypertension. Circ J 70:1208–1215
Van den Berg DT, de Kloet ER, de Jong W (1994) Central effects of mineralocorticoid antagonist RU-28318 on blood pressure of DOCA-salt hypertensive rats. Am J Physiol 267:E927–E933
Van den Bergh A, Flameng W, Herijgers P (2006) Type II diabetic mice exhibit contractile dysfunction but maintain cardiac output by favourable loading conditions. Eur J Heart Fail 8:777–783. doi:10.1016/j.ejheart.2006.03.001
van den Meiracker AH (2002) Endothelins and venous tone in DOCA-salt hypertension. J Hypertens 20:587–589
Vicart P, Caron A, Guicheney P, Li Z, Prevost MC, Faure A, Chateau D, Chapon F, Tome F, Dupret JM, Paulin D, Fardeau M (1998) A missense mutation in the alphaB-crystallin chaperone gene causes a desmin-related myopathy. Nat Genet 20:92–95. doi:10.1038/1765
Wakasaki H, Koya D, Schoen FJ, Jirousek MR, Ways DK, Hoit BD, Walsh RA, King GL (1997) Targeted overexpression of protein kinase C beta2 isoform in myocardium causes cardiomyopathy. Proc Natl Acad Sci USA 94:9320–9325
Wakisaka Y, Niwano S, Niwano H, Saito J, Yoshida T, Hirasawa S, Kawada H, Izumi T (2004) Structural and electrical ventricular remodeling in rat acute myocarditis and subsequent heart failure. Cardiovasc Res 63:689–699. doi:10.1016/j.cardiores.2004.04.020
Wang QD, Bohlooly YM, Sjoquist PO (2004) Murine models for the study of congestive heart failure: Implications for understanding molecular mechanisms and for drug discovery. J Pharmacol Toxicol Methods 50:163–174. doi:10.1016/j.vascn.2004.05.005
Wang X, Ren B, Liu S, Sentex E, Tappia PS, Dhalla NS (2003) Characterization of cardiac hypertrophy and heart failure due to volume overload in the rat. J Appl Physiol 94:752–763. doi:10.1152/japplphysiol.00248.200294/2/752
Wang X, Sentex E, Saini HK, Chapman D, Dhalla NS (2005) Upregulation of beta-adrenergic receptors in heart failure due to volume overload. Am J Physiol Heart Circ Physiol 289:H151–159. doi:10.1152/ajpheart.00066.2005
Weinberg EO, Schoen FJ, George D, Kagaya Y, Douglas PS, Litwin SE, Schunkert H, Benedict CR, Lorell BH (1994) Angiotensin-converting enzyme inhibition prolongs survival and modifies the transition to heart failure in rats with pressure overload hypertrophy due to ascending aortic stenosis. Circulation 90:1410–1422
Werchan PM, Summer WR, Gerdes AM, McDonough KH (1989) Right ventricular performance after monocrotaline-induced pulmonary hypertension. Am J Physiol 256:H1328–H1336
West MB, Rokosh G, Obal D, Velayutham M, Xuan YT, Hill BG, Keith RJ, Schrader J, Guo Y, Conklin DJ, Prabhu SD, Zweier JL, Bolli R, Bhatnagar A (2008) Cardiac myocyte-specific expression of inducible nitric oxide synthase protects against ischemia/reperfusion injury by preventing mitochondrial permeability transition. Circulation 118:1970–1978. doi:10.1161/CIRCULATIONAHA.108.791533
Wettschureck N, Rutten H, Zywietz A, Gehring D, Wilkie TM, Chen J, Chien KR, Offermanns S (2001) Absence of pressure overload induced myocardial hypertrophy after conditional inactivation of Galphaq/Galpha11 in cardiomyocytes. Nat Med 7:1236–1240. doi:10.1038/nm1101-1236
Wilson KM, Sumners C, Hathaway S, Fregly MJ (1986) Mineralocorticoids modulate central angiotensin II receptors in rats. Brain Res 382:87–96
Wood P, Piran S, Liu PP (2011) Diastolic heart failure: progress, treatment challenges, and prevention. Can J Cardiol 27:302–310. doi:10.1016/j.cjca.2011.02.008
Wu JC, Nasseri BA, Bloch KD, Picard MH, Scherrer-Crosbie M (2003) Influence of sex on ventricular remodeling after myocardial infarction in mice. J Am Soc Echocardiogr 16:1158–1162. doi:10.1067/S0894-7317(03)00648-5
Xiao CY, Chen M, Zsengeller Z, Li H, Kiss L, Kollai M, Szabo C (2005) Poly(ADP-Ribose) polymerase promotes cardiac remodeling, contractile failure, and translocation of apoptosis-inducing factor in a murine experimental model of aortic banding and heart failure. J Pharmacol Exp Ther 312:891–898. doi:10.1124/jpet.104.077164
Xin HB, Senbonmatsu T, Cheng DS, Wang YX, Copello JA, Ji GJ, Collier ML, Deng KY, Jeyakumar LH, Magnuson MA, Inagami T, Kotlikoff MI, Fleischer S (2002) Oestrogen protects FKBP12.6 null mice from cardiac hypertrophy. Nature 416:334–338. doi:10.1038/416334a
Yamada T, Matsumori A, Wang WZ, Ohashi N, Shiota K, Sasayama S (1999) Apoptosis in congestive heart failure induced by viral myocarditis in mice. Heart Vessels 14:29–37
Yamori Y (1991) Overview: studies on spontaneous hypertension-development from animal models toward man. Clin Exp Hypertens A 13:631–644
Yang S, Su L, Wang Z, Liu Z, Kang Y, Lei J (2011) Comparative study on repairing rabbit radius segmental defects with two different proportions of chitosan combined with allogeneic morselized bone. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi 25:877–883
Yano M, Kobayashi S, Kohno M, Doi M, Tokuhisa T, Okuda S, Suetsugu M, Hisaoka T, Obayashi M, Ohkusa T, Matsuzaki M (2003) FKBP12.6-mediated stabilization of calcium-release channel (ryanodine receptor) as a novel therapeutic strategy against heart failure. Circulation 107:477–484
Yoo B, Lemaire A, Mangmool S, Wolf MJ, Curcio A, Mao L, Rockman HA (2009) Beta1-adrenergic receptors stimulate cardiac contractility and CaMKII activation in vivo and enhance cardiac dysfunction following myocardial infarction. Am J Physiol Heart Circ Physiol 297:H1377–1386. doi:10.1152/ajpheart.00504.2009
Yoshida M, Ohkusa T, Nakashima T, Takanari H, Yano M, Takemura G, Honjo H, Kodama I, Mizukami Y, Matsuzaki M (2011) Alterations in adhesion junction precede gap junction remodelling during the development of heart failure in cardiomyopathic hamsters. Cardiovasc Res 92:95–105. doi:10.1093/cvr/cvr182
Zbinden G, Bagdon RE (1963) Isoproterenol-induced heart necrosis, an experimental model for the study of Angina Pectoris and Myocardial Infarct. Rev Can Biol 22:257–263
Zbinden G, Moe RA (1969) Pharmacological studies on heart muscle lesions induced by isoproterenol. Ann N Y Acad Sci 156:294–308
Zhou YY, Song LS, Lakatta EG, Xiao RP, Cheng H (1999) Constitutive beta2-adrenergic signalling enhances sarcoplasmic reticulum Ca2+ cycling to augment contraction in mouse heart. J Physiol 521(Pt 2):351–361
Zile MR, Brutsaert DL (2002) New concepts in diastolic dysfunction and diastolic heart failure: Part I: diagnosis, prognosis, and measurements of diastolic function. Circulation 105:1387–1393
Zisa D, Shabbir A, Mastri M, Suzuki G, Lee T (2009) Intramuscular VEGF repairs the failing heart: role of host-derived growth factors and mobilization of progenitor cells. Am J Physiol Regul Integr Comp Physiol 297:R1503–1515. doi:10.1152/ajpregu.00227.2009
Acknowledgments
This work was supported by a grant from the European Commission (FP7-Health-2010; MEDIA-261409). Inês Falcão-Pires, Ana Luisa Pires and Carmen Brás-Silva are supported by an individual grants from Portuguese Foundation for Science and Technology (SFRH/BPD/66176/2009, SFRH/BD/19544/2004 as well as Ciência 2008 and PTDC/SAU-FCT/100442/2008, COMPETE, FEDER, respectively).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Gomes, A.C., Falcão-Pires, I., Pires, A.L. et al. Rodent models of heart failure: an updated review. Heart Fail Rev 18, 219–249 (2013). https://doi.org/10.1007/s10741-012-9305-3
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10741-012-9305-3