Sarcolemmal activities of Na+-Ca2+ exchange and N+-K+ ATPase as well protein content and mRNA levels of N+-K+ ATPase in control and MI animals with or without ENP and LOS treatments for 4 weeks starting at 3 weeks after induction of MI
Parameters
Control
MI
MI + ENP
MI + LOS
A. SL activities
Na+-Ca2+ exchange activity (nmol Ca2+ mg/2s)
8.2 ± 0.51
3.8 ± 0.26*
7.4 ± 0.45†
7.0 ± 0.21†
Na+-K+-ATPase activity (μmol Pi/mg per h)
22.1 ± 0.82
12.9 ± 0.64*
18.3 ± 0.59†
18.6 ± 0.84†
B. Na+-K+-ATPase isoform protein content (% of control)
α2
100
79.6 ± 3.4*
89.9 ± 1.6†
92.9 ± 2.5†
α3
100
134.0 ± 5.2*
114.7 ± 4.2†
113.6 ± 5.5†
β2
100
73.6 ± 3.1*
98.6 ± 8.5†
99.2 ± 8.5†
β3
100
66.8 ± 1.6*
81.1 ± 4.5†
90.3 ± 6.7†
C. Na+-K+-ATPase isoform mRNA level (% of control)
α1
100
107.5 ± 2.5
110.2 ± 4.8
112.2 ± 4.5
α2
100
72.9 ± 2.1*
86.3 ± 3.6†
85.5 ± 4.5†
α3
100
170.5 ± 9.5*
116.2 ± 4.8†
115.3 ± 14.8†
β1
100
110.7 ± 7.2
120.5 ± 6.5
120.2 ± 7.5
Values are mean ± SE of 6 animals in each group. Data are based on the analysis of the information in our papers Shao et al. Am J Physiol Heart Circ Physiol. 2005;288:H2637–46 [116] and Guo et al. Can J Physiol Pharmacol. 2008;86:139–47 [131]. *P < 0.05 compared with control; †P < 0.05 compared with MI group
Declarations
Acknowledgments
The infrastructure support for this project was provided by the St. Boniface Hospital Research Foundation, Winnipeg, Canada. Thanks are also due to Ms. Andrea Opsima for typing this manuscript.
Author contributions
SKB searched the literature, analyzed the data and wrote the first draft; AKS analyzed the data and wrote the manuscript; NSD conceived, designed and edited the article. All authors have read and agreed to the published version of the manuscript.
Benjamin EJ, Muntner P, Alonso A, Bittencourt MS, Callaway CW, Carson AP, et al.; American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee.Heart disease and stroke statistics-2019 update: a report from the American Heart Association. Circulation. 2019;139:e56–528. [DOI] [PubMed]
Lippi G, Sanchis-Gomar F, . Global epidemiology and future trends of heart failure. AME Med J. 2020;5:15. [DOI]
Packer M, . Neurohormonal interactions and adaptations in congestive heart failure. Circulation. 1988;77:721–30. [DOI] [PubMed]
Ferrario CM, Strawn WB, . Role of the renin-angiotensin-aldosterone system and proinflammatory mediators in cardiovascular disease. Am J Cardiol. 2006;98:121–8. [DOI] [PubMed]
Cohn JN, Ferrari R, Sharpe N, . Cardiac remodeling-concepts and clinical implications: a consensus paper from an international forum on cardiac remodeling. J Am Coll Cardiol. 2000;35:569–82. [DOI]
Dhalla NS, Afzal N, Beamish RE, Naimark B, Takeda N, Nagano M, . Pathophysiology of cardiac dysfunction in congestive heart failure. Can J Cardiol. 1993;9:873–87. [PubMed]
Gajarsa JJ, Kloner RA, . Left ventricular remodeling in the post-infarction heart: a review of cellular, molecular mechanisms, and therapeutic modalities. Heart Fail Rev. 2011;16:13–21. [DOI] [PubMed]
Azevedo PS, Polegato BF, Minicucci MF, Paiva SA, Zornoff LA, . Cardiac remodeling: concepts, clinical impact, pathophysiological mechanisms and pharmacologic treatment. Arq Bras Cardiol. 2016;106:62–9. [DOI] [PubMed] [PMC]
Oldfield CJ, Duhamel TA, Dhalla NS, . Mechanisms for the transition from physiological to pathological cardiac hypertrophy. Can J Physiol Pharmacol. 2020;98:74–84. [DOI] [PubMed]
Dhalla NS, Saini HK, Tappia PS, Sethi R, Mengi SA, Gupta SK, . Potential role and mechanisms of subcellular remodeling in cardiac dysfunction due to ischemic heart disease. J Cardiovasc Med (Hagerstown). 2007;8:238–50. [DOI] [PubMed]
Dhalla NS, Dent MR, Tappia PS, Sethi R, Barta J, Goyal RK, . Subcellular remodeling as a viable target for the treatment of congestive heart failure. J Cardiovasc Pharmacol Ther. 2006;11:31–45. [DOI] [PubMed]
Duhamel TA, Dhalla NS, . New insights into the causes of heart failure. Drug Discov Today Dis Mech. 2007;4:175–84. [DOI]
Babick AP, Dhalla NS, . Role of subcellular remodeling in cardiac dysfunction due to congestive heart failure. Med Princ Pract. 2007;16:81–9. [DOI] [PubMed]
Dhalla NS, Rangi S, Babick AP, Zieroth S, Elimban V, . Cardiac remodeling and subcellular defects in heart failure due to myocardial infarction and aging. Heart Fail Rev. 2012;17:671–81. [DOI] [PubMed]
Dhalla NS, Shah AK, Tappia PS, . Role of oxidative stress in metabolic and subcellular abnormalities in diabetic cardiomyopathy. Int J Mol Sci. 2020;21:2413. [DOI] [PubMed] [PMC]
Machackova J, Barta J, Dhalla NS, . Myofibrillar remodelling in cardiac hypertrophy, heart failure and cardiomyopathies. Can J Cardiol. 2006;22:953–68. [DOI]
Deschamps AM, Spinale FG, . Pathways of matrix metalloproteinase induction in heart failure: bioactive molecules and transcriptional regulation. Cardiovasc Res. 2006;69:666–76. [DOI] [PubMed]
Hasenfuss G, . Alterations of calcium-regulatory proteins in heart failure. Cardiovasc Res. 1998;37:279–89. [DOI]
Morano I, Hädicke K, Haase H, Böhm M, Erdmann E, Schaub MC, . Changes in essential myosin light chain isoform expression provide a molecular basis for isometric force regulation in the failing human heart. J Mol Cell Cardiol. 1997;29:1177–87. [DOI] [PubMed]
Hasenfuss G, . Animal models of human cardiovascular disease, heart failure and hypertrophy. Cardiovasc Res. 1998;39:60–76. [DOI]
Prestle J, Quinn FR, Smith GL, . Ca2+ -handling proteins and heart failure: novel molecular targets?Curr Med Chem. 2003;10:967–81. [DOI] [PubMed]
Nehme A, Zouein FA, Zayeri ZD, Zibara K, . An update on the tissue renin angiotensin system and its role in physiology and pathology. J Cardiovasc Dev Dis. 2019;6:14. [DOI] [PubMed] [PMC]
Bader M, . Tissue renin-angiotensin-aldosterone systems: targets for pharmacological therapy. Annu Rev Pharmacol Toxicol. 2010;50:439–65. [DOI] [PubMed]
Nehme A, Zibara K, . Efficiency and specificity of RAAS inhibitors in cardiovascular diseases: how to achieve better end-organ protection?Hypertens Res. 2017;40:903–9. [DOI] [PubMed]
Emdin M, Fatini C, Mirizzi G, Poletti R, Borrelli C, Prontera C, et al. Biomarkers of activation of renin-angiotensin-aldosterone system in heart failure: how useful, how feasible?Clin Chim Acta. 2015;443:85–93. [DOI] [PubMed]
Vergaro G, Emdin M, Iervasi A, Zyw L, Gabutti A, Poletti R, et al. Prognostic value of plasma renin activity in heart failure. Am J Cardiol. 2011;108:246–51. [DOI] [PubMed]
Emdin CA, Callender T, Cao J, McMurray JJ, Rahimi K, . Meta-analysis of large-scale randomized trials to determine the effectiveness of inhibition of the renin-angiotensin aldosterone system in heart failure. Am J Cardiol. 2015;116:155–61. [DOI] [PubMed]
Mehta PK, Griendling KK, . Angiotensin II cell signaling: physiological and pathological effects in the cardiovascular system. Am J Physiol Cell Physiol. 2007;292:C82–97. [DOI] [PubMed]
Flather MD, Yusuf S, Køber L, Pfeffer M, Hall A, Murray G, et al. Long-term ACE-inhibitor therapy in patients with heart failure or left-ventricular dysfunction: a systematic overview of data from individual patients. Lancet. 2000;355:1575–81. [DOI]
McMurray JJ, Pfeffer MA, Swedberg K, Dzau VJ, . Which inhibitor of the renin-angiotensin system should be used in chronic heart failure and acute myocardial infarction?Circulation. 2004;110:3281–8. [DOI] [PubMed]
Francis GS, Cohn JN, Johnson G, Rector TS, Goldman S, Simon A, . Plasma norepinephrine, plasma renin activity, and congestive heart failure. Relations to survival and the effects of therapy in V-HeFT II. The V-HeFT VA Cooperative Studies Group. Circulation. 1993;87:VI40–8. [PubMed]
Singh KD, Karnik SS, . Angiotensin type 1 receptor blockers in heart failure. Curr Drug Targets. 2020;21:125–31. [DOI] [PubMed] [PMC]
Dzau VJ, . Implications of local angiotensin production in cardiovascular physiology and pharmacology. Am J Cardiol. 1987;59:A59–65. [DOI]
Hartupee J, Mann DL, . Neurohormonal activation in heart failure with reduced ejection fraction. Nat Rev Cardiol. 2017;14:30–8. [DOI] [PubMed] [PMC]
Tham YK, Bernardo BC, Ooi JY, Weeks KL, McMullen JR, . Pathophysiology of cardiac hypertrophy and heart failure: signaling pathways and novel therapeutic targets. Arch Toxicol. 2015;89:1401–38. [DOI] [PubMed]
Dhalla NS, Shao Q, Panagia V, . Remodeling of cardiac membranes during the development of congestive heart failure. Heart Fail Rev. 1998;2:261–72. [DOI]
Guo X, Saini HK, Wang J, Gupta SK, Goyal RK, Dhalla NS, . Prevention of remodeling in congestive heart failure due to myocardial infarction by blockade of the renin-angiotensin system. Expert Rev Cardiovasc Ther. 2005;3:717–32. [DOI] [PubMed]
Shao Q, Takeda N, Temsah R, Dhalla KS, Dhalla NS, . Prevention of hemodynamic changes due to myocardial infarction by early treatment of rats with imidapril. Cardiovasc Pathobiol. 1996;1:180–6.
Hsieh CC, Li CY, Hsu CH, Chen HL, Chen YH, Liu YP, et al. Mitochondrial protection by simvastatin against angiotensin II-mediated heart failure. Br J Pharmacol. 2019; 176:3791–804. [DOI] [PubMed] [PMC]
Wang X, Yuan B, Dong W, Yang B, Yang Y, Lin X, et al. Humid heat exposure induced oxidative stress and apoptosis in cardiomyocytes through the angiotensin II signaling pathway. Heart Vessels. 2015;30:396–405. [DOI] [PubMed]
Zhou B, Tian R, . Mitochondrial dysfunction in pathophysiology of heart failure. J Clin Invest. 2018;128:3716–26. [DOI] [PubMed] [PMC]
Higuchi S, Ohtsu H, Suzuki H, Shirai H, Frank GD, Eguchi S, . Angiotensin II signal transduction through the AT1 receptor: novel insights into mechanisms and pathophysiology. Clin Sci (Lond). 2007;112:417–28. [DOI] [PubMed]
Touyz RM, Schiffrin EL, . Signal transduction mechanisms mediating the physiological and pathophysiological actions of angiotensin II in vascular smooth muscle cells. Pharmacol Rev. 2000;52:639–72. [PubMed]
Kumar R, Boim MA, . Diversity of pathways for intracellular angiotensin II synthesis. Curr Opin Nephrol Hypertens. 2009;18:33–9. [DOI] [PubMed]
Doggrell SA, Wanstall JC, . Cardiac chymase: pathophysiology role and therapeutic potential of chymase inhibitors. Can J Physiol Pharmacol. 2005;83:123–30. [DOI] [PubMed]
Patel VB, Zhong JC, Grant MB, Oudit GY, . Role of the ACE2/angiotensin 1-7 axis of the renin-angiotensin system in heart failure. Circ Res. 2016;118:1313–26. [DOI] [PubMed] [PMC]
Dorsainval W, . ACE2/Ang1-7 Mas axis: the counter-regulator of the classical renin angiotensin system. Mako: NSU Undergrad Stud J. 2020;2020:Article 2.
Dang Z, Su S, Jin G, Nan X, Ma L, Li Z, et al. Tsantan sumtang attenuated chronic hypoxia-induced right ventricular structure remodeling and fibrosis by equilibrating local ACE-Ang II- AT1R/ACE2-Ang1-7- Mas axis in rat. J Ethnopharmacol. 2020;250:112470. [DOI] [PubMed]
Sukumaran V, Veeraveedu PT, Gurusamy N, Yamaguchi K, Lakshmanan AP, Ma M, et al. Cardioprotective effects of telmisartan against heart failure in rats induced by experimental autoimmune myocarditis through the modulation of angiotensin-covering enzyme-2/angiotensin 1-7/mas receptor axis. Int J Biol Sci. 2011;7:1077–92. [DOI] [PubMed] [PMC]
Te Riet L, van Esch JH, Roks AJ, van den Meiracker AH, Danser AH, . Hypertension: renin-angiotensin- aldosterone system alterations. Circ Res. 2015;116:960–75. [DOI] [PubMed]
Vukelic S, Griendling KK, . Angiotensin II, from vasoconstrictor to growth factor: a paradigm shift. Circ Res. 2014;114:754–7. [DOI] [PubMed] [PMC]
Forrester SJ, Booz GW, Sigmund CD, Coffman TM, Kawai T, Rizzo V, et al. Angiotensin II signal transduction: an update on mechanisms of physiology and pathophysiology. Physiol Rev. 2018;98:1627–738. [DOI] [PubMed] [PMC]
Ferrario CM, Ahmad S, Nagata S, Simington SW, Varagic J, Kon N, et al. An evolving story of angiotensin- II-forming pathways in rodents and humans. Clin Sci (Lond). 2014;126:461–9. [DOI] [PubMed] [PMC]
Sepehrdad R, Frishman WH, Stier CT Jr, Sica DA, . Direct inhibition of renin as a cardiovascular pharmacotherapy: focus on aliskiren. Cardiol Rev. 2007;15:242–56. [DOI] [PubMed]
Seed A, Gardner R, McMurray J, Hillier C, Murdoch D, MacFadyen R, et al. Neurohumoral effects of the new orally active renin inhibitor, aliskiren, in chronic heart failure. Eur J Heart Fail. 2007;9:1120–7. [DOI] [PubMed]
Pitt B, Zannad F, Remme WJ, Cody R, Castaigne A, Perez A, et al. The effect of spironolactone on morbidity and mortality in patients with severe heart failure. N Engl J Med. 1999;341:709–17. [DOI] [PubMed]
Pitt B, Remme W, Zannad F, Neaton J, Martinez F, Roniker B, et al. Eplerenone, a selective aldosterone blocker, in patients with left ventricular dysfunction after myocardial infarction. N Engl J Med. 2003;348:1309–21. [DOI] [PubMed]
Chaudhry SI, Mattera JA, Curtis JP, Spertus JA, Herrin J, Lin Z, et al. Telemonitoring in patients with heart failure. N Engl J Med. 2010;363:2301–9. [DOI] [PubMed] [PMC]
Pelouch V, Dixon IM, Golfman L, Beamish RE, Dhalla NS, . Role of extracellular matrix proteins in heart function. Mol Cell Biochem. 1993;129:101–20. [DOI] [PubMed]
Dhalla NS, Wang X, Sethi R, Das PK, Beamish RE, . β-adrenergic linked signal transduction mechanisms in failing hearts. Heart Fail Rev. 1997;2:55–65. [DOI]
Panagia V, Pierce GN, Dhalla KS, Ganguly PK, Beamish RE, Dhalla NS, . Adaptive changes in subcellular calcium transport during catecholamine-induced cardiomyopathy. J Mol Cell Cardiol. 1985;17:411–20. [DOI]
Tappia P, Singal T, Dent M, Asemu G, Rabban M, Dhalla NS, . Phospholipid-mediated signaling in diseased myocardium. Future Lipidol. 2006;1:701–17. [DOI]
Singh RB, Dandekar SP, Elimban V, Gupta SK, Dhalla NS, . Role of proteases in the pathophysiology of cardiac disease. Mol Cell Biochem. 2004;263:241–56. [DOI] [PubMed]
Spinale FG, . Myocardial matrix remodeling and the matrix metalloproteinases: influence on cardiac form and function. Physiol Rev. 2007;87:1285–342. [DOI] [PubMed]
Rysä J, Leskinen H, Ilves M, Ruskoaho H, . Distinct upregulation of extracellular matrix genes in transition from hypertrophy to hypertensive heart failure. Hypertension. 2005;45:927–33. [DOI] [PubMed]
Li YY, McTiernan CF, Feldman AM, . Proinflammatory cytokines regulate tissue inhibitors of metalloproteinases and disintegrin metalloproteinase in cardiac cells. Cardiovasc Res. 1999;42:162–72. [DOI]
Weisser-Thomas J, Kubo H, Hefner CA, Gaughan JP, McGowan BS, Ross R, et al. The Na+/Ca2+ exchanger/ SR Ca2+ ATPase transport capacity regulates the contractility of normal and hypertrophied feline ventricular myocytes. J Card Fail. 2005;11:380–7. [DOI] [PubMed]
Camors E, Charue D, Trouvé P, Monceau V, Loyer X, Russo-Marie F, et al. Association of annexin A5 with Na+/Ca2+ exchanger and caveolin-3 in non-failing and failing human heart. J Mol Cell Cardiol. 2006;40:47–55. [DOI] [PubMed]
Tsutsui H, Ide T, Kinugawa S, . Mitochondrial oxidative stress, DNA damage, and heart failure. Antioxid Redox Signal. 2006;8:1737–44. [DOI] [PubMed]
Ishikawa K, Kimura S, Kobayashi A, Sato T, Matsumoto H, Ujiie Y, et al. Increased reactive oxygen species and anti-oxidative response in mitochondrial cardiomyopathy. Circ J. 2005;69:617–20. [DOI] [PubMed]
Javadov S, Karmazyn M, . Mitochondrial permeability transition pore opening as an endpoint to initiate cell death and as a putative target for cardioprotection. Cell Physiol Biochem. 2007;20:1–22. [DOI] [PubMed]
Matsushima S, Ide T, Yamato M, Matsusaka H, Hattori F, Ikeuchi M, et al. Overexpression of mitochondrial peroxiredoxin-3 prevents left ventricular remodeling and failure after myocardial infarction in mice. Circulation. 2006;113:1779–86. [DOI] [PubMed]
Dhalla NS, Wang X, Beamish RE, . Intracellular calcium handling in normal and failing hearts. Exp Clin Cardiol. 1996;1:7–20.
Davies CH, Harding SE, Poole-Wilson PA, . Cellular mechanisms of contractile dysfunction in human heart failure. Eur Heart J. 1996;17:189–98. [DOI] [PubMed]
O’Brien PJ, Ianuzzo CD, Moe GW, Stopps TP, Armstrong PW, . Rapid ventricular pacing of dogs to heart failure: biochemical and physiological studies. Can J Physiol Pharmacol. 1990;68:34–9. [DOI] [PubMed]
Pagani ED, Alousi AA, Grant AM, Older TM, Dziuban SW Jr, Allen PD, . Changes in myofibrillar content and Mg-ATPase activity in ventricular tissues from patients with heart failure caused by coronary artery disease, cardiomyopathy, or mitral valve insufficiency. Circ Res. 1988;63:380–5. [DOI] [PubMed]
Neagoe C, Kulke M, del Monte F, Gwathmey JK, de Tombe PP, Hajjar RJ, et al. Titin isoform switch in ischemic human heart disease. Circulation. 2002;106:1333–41. [DOI] [PubMed]
Huang X, Li J, Foster D, Lemanski SL, Dube DK, Zhang C, et al. Protein kinase C-mediated desmin phosphorylation is related to myofibril disarray in cardiomyopathic hamster heart. Exp Biol Med. 2002;227:1039–46. [DOI] [PubMed]
Mudd JO, Kass DA, . Tackling heart failure in the twenty-first century. Nature. 2008;451:919–28. [DOI] [PubMed]
Catterall WA, . Structure and regulation of voltage-gated Ca2+ channels. Annu Rev Cell Dev Biol. 2000;16:521–55. [DOI] [PubMed]
Meissner G, . Ryanodine receptor/ Ca2+ release channels and their regulation by endogenous effectors. Annu Rev Physiol. 1994;56:485–508. [DOI] [PubMed]
Wang J, Liu X, Ren B, Rupp H, Takeda N, Dhalla NS, . Modification of myosin gene expression by imidapril in failing heart due to myocardial infarction. J Mol Cell Cardiol. 2002;34:847–57. [DOI] [PubMed]
de Tombe PP, . Cardiac myofilaments: mechanics and regulation. J Biomech. 2003;36:721–30. [DOI]
Dhalla NS, Ziegelhoffer A, Harrow JA, . Regulatory role of membrane systems in heart function. Can J Physiol Pharmacol. 1977;55:1211–34. [DOI] [PubMed]
Egger M, Niggli E, . Regulatory function of Na-Ca exchange in the heart: milestones and outlook. J Membrane Biol. 1999;168:107–30. [DOI] [PubMed]
Ames MK, Atkins CE, Pitt B, . The renin-angiotensin-aldosterone system and its suppression. J Vet Intern Med. 2019;33:363–82. [DOI] [PubMed] [PMC]
Szczepanska-Sadowska E, Czarzasta K, Cudnoch-Jedrzejewska A, . Dysregulation of the renin-angiotensin system and the vasopressinergic system interactions in cardiovascular disorders. Curr Hypertens Rep. 2018;20:1–24. [DOI] [PubMed] [PMC]
Bakogiannis C, Theofilogiannakos E, Papadopoulos C, Lazaridis C, Bikakis I, Tzikas S, et al. A translational approach to the renin-angiotensin-aldosterone system in heart failure. Ann Res Hosp. 2019;3:11. [DOI]
Dasgupta C, Zhang L, . Angiotensin II receptors and drug discovery in cardiovascular disease. Drug Discov Today. 2011;16:22–34. [DOI] [PubMed] [PMC]
Jin M, Wilhelm MJ, Lang RE, Unger T, Lindpaintner K, Ganten D, . Endogenous tissue renin-angiotensin systems: from molecular biology to therapy. Am J Med. 1988;84:28–36. [DOI]
Sadoshima J, Xu Y, Slayter HS, Izumo S, . Autocrine release of angiotensin II mediates stretch-induced hypertrophy of cardiac myocytes in vitro. Cell. 1993;75:977–84. [DOI]
Griendling KK, Sorescu D, Ushio-Fukai M, . NAD(P)H oxidase: role in cardiovascular biology and disease. Circ Res. 2000;86:494–501. [DOI] [PubMed]
Hunyady L, Catt KJ, . Pleiotropic AT1 receptor signaling pathways mediating physiological and pathogenic actions of angiotensin II. Mol Endocrinol. 2006;20:953–70. [DOI] [PubMed]
Suzuki H, Motley ED, Frank GD, Utsunomiya H, Eguchi S, . Recent progress in signal transduction research of the angiotensin II type-1 receptor: protein kinases, vascular dysfunction and structural requirement. Curr Med Chem Cardiovasc Hematol Agents. 2005;3:305–22. [DOI] [PubMed]
Dhalla NS, Temsah RM, Netticadan T, . Role of oxidative stress in cardiovascular diseases. J Hypertens. 2000;18:655–73. [DOI] [PubMed]
Sethi R, Shao Q, Ren B, Saini HK, Takeda N, Dhalla NS, . Changes in β-adrenoceptors in heart failure due to myocardial infarction are attenuated by blockade of renin-angiotensin system. Moll Cell Biochem. 2004;263;11–20. [DOI]
SOLVD Investigators; Yusuf S, Pitt B, Davis CE, Hood WB Jr, Cohn JN, . Effect of enalapril on mortality and the development of heart failure in asymptomatic patients with reduced left ventricular ejection fractions. N Engl J Med. 1992;327:685–91. [DOI] [PubMed]
The Acute Infarction Ramipril Efficacy (AIRE) Study Investigators. Effect of ramipril on mortality and morbidity of survivors of acute myocardial infarction with clinical evidence of heart failure. Lancet. 1993;342:821–8. [DOI]
Pfeffer JM, Pfeffer MA, Braunwald E, . Hemodynamic benefits and prolonged survival with long-term captopril therapy in rats with myocardial infarction and heart failure. Circulation. 1987;75:I149–55. [PubMed]
Shao Q, Ren B, Saini HK, Netticadan T, Takeda N, Dhalla NS, . Sarcoplasmic reticulum Ca2+ -transport and gene expression in congestive heart failure are modified by imidapril treatment. Am J Physiol Heart Circ Physiol. 2005;288:H1674–82. [DOI] [PubMed]
Shao Q, Ren B, Zarain-Herzberg A, Ganguly PK, Dhalla NS, . Captopril treatment improves the sarcoplasmic reticular Ca2+ transport in heart failure due to myocardial infarction. J Mol Cell Cardiol. 1999;31:1663–72. [DOI] [PubMed]
Sanbe A, Tanonaka K, Kobayashi R, Takeo S, . Effects of long-term therapy with ACE inhibitors, captopril, enalapril and trandolapril, on myocardial energy metabolism in rats with heart failure following myocardial infarction. J Mol Cell Cardiol. 1995;27:2209–22. [DOI]
Shao Q, Ren B, Elimban V, Tappia PS, Takeda N, Dhalla NS, . Modification of sarcolemmal Na+-K+-ATPase and Na+/Ca2+ exchanger expression in heart failure by blockade of renin-angiotensin system. Am J Physiol Hear Circ Physiol. 2005;288:H2637–46. [DOI] [PubMed]
Semb SO, Lunde PK, Holt E, Tønnessen T, Christensen G, Sejersted OM, . Reduced myocardial Na+, K+- pump capacity in congestive heart failure following myocardial infarction in rats. J Mol Cell Cardiol. 1998;30:1311–28. [DOI] [PubMed]
Guo X, Chapman D, Dhalla NS, . Partial prevention of changes in SR gene expression in congestive heart failure due to myocardial infarction by enalapril or losartan. Mol Cell Biochem. 2003;254:163–72. [DOI] [PubMed]
Wang J, Guo X, Dhalla NS, . Modification of myosin protein and gene expression in failing hearts due to myocardial infarction by enalapril or losartan. Biochim Biophys Acta. 2004;1690:177–84. [DOI] [PubMed]
Dickstein K, Kjekshus J; Optimaal steering committee of the optimaal study group. Effects of losartan and captopril on mortality and morbidity in high-risk patients after acute myocardial infarction: the OPTIMAAL randomised trial. Lancet. 2002;360:P752–60. [DOI]
Yusuf S, Pfeffer MA, Swedberg K, Granger CB, Held P, McMurray JJ, et al. Effects of candesartan in patients with chronic heart failure and preserved left-ventricular ejection fraction: the CHARM-Preserved Trial. Lancet. 2003;362:777–81. [DOI]
Awwad ZM, El-Ganainy SO, ElMallah AI, Khattab MM, El-Khatib AS, . Telmisartan and captopril ameliorate pregabalin-induced heart failure in rats. Toxicology. 2019;428:152310. [DOI] [PubMed]
Dixon IM, Ju H, Jassal DS, Peterson DJ, . Effect of ramipril and losartan on collagen expression in right and left heart after myocardial infarction. Mol Cell Biochem. 1996;165:31–45. [DOI] [PubMed]
Shao Q, Saward L, Zahradka P, Dhalla NS, . Ca2+ mobilization in adult rat cardiomyocytes by angiotensin type 1 and 2 receptors. Biochem Pharmacol. 1998;55:1413–8. [DOI]
Sethi R, Shao Q, Takeda N, Dhalla NS, . Attenuation of changes in Gi-proteins and adenylyl cyclase in heart failure by an ACE inhibitor, imidapril. J Cell Mol Med. 2003;7:277–86. [DOI] [PubMed] [PMC]
Saini HK, Shao Q, Musat S, Takeda N, Tappia PS, Dhalla NS, . Imidapril treatment improves the attenuated inotropic and intracellular calcium responses to ATP in heart failure due to myocardial infarction. Br J Pharmacol. 2005;144:202–11. [DOI] [PubMed] [PMC]
Cahill TJ, Kharbanda RK, . Heart failure after myocardial infarction in the era of primary percutaneous coronary intervention: mechanisms, incidence and identification of patients at risk. World J Cardiol. 2017;9:407–15. [DOI] [PubMed] [PMC]
Sag CM, Wagner S, Maier LS, . Role of oxidants on calcium and sodium movement in healthy and diseased cardiac myocytes. Free Radic Biol Med. 2013;63:338–49. [DOI] [PubMed]
Dixon IM, Lee SL, Dhalla NS, . Nitrendipine binding in congestive heart failure due to myocardial infarction. Circ Res. 1990;66:782–8. [DOI] [PubMed]
Dixon IM, Hata T, Dhalla NS, . Sarcolemmal calcium transport in congestive heart failure due to myocardial infarction in rats. Am J Physiol. 1992;262:H1387–94. [DOI] [PubMed]
Guo X, Wang J, Elimban V, Dhalla NS, . Both enalapril and losartan attenuate sarcolemmal Na+-K+-ATPase remodeling in failing rat heart due to myocardial infarction. Can J Physiol Pharmacol. 2008;86:139–47. [DOI] [PubMed]
Yamaguchi F, Sanbe A, Takeo S, . Effects of long-term treatment with trandolapril on sarcoplasmic reticulum function of cardiac muscle in rats with chronic heart failure following myocardial infarction. Br J Pharmacol. 1998;123:326–34. [DOI] [PubMed] [PMC]
Yoshiyama M, Takeuchi K, Hanatani A, Shimada T, Takemoto Y, Shimizu N, et al. Effect of cilazapril on ventricular remodeling assessed by Doppler-echocardiographic assessment and cardiac gene expression. Cardiovasc Drugs Ther. 1998;12:57–70. [DOI] [PubMed]
Hosoya K, Ishimitsu T, . Protection of the cardiovascular system by imidapril, a versatile angiotensin- converting enzyme inhibitor. Cardiovasc Drug Rev. 2002;20:93–110. [DOI] [PubMed]
Tappia PS, Liu SY, Shatadal S, Takeda N, Dhalla NS, Panagia V, . Changes in sarcolemmal PLC isoenzymes in postinfarct congestive heart failure: partial correction by imidapril. Am J Physiol. 1999;277:H40–9. [DOI] [PubMed]
Wang J, Liu X, Sentex E, Takeda N, Dhalla NS, . Increased expression of protein kinase C isoforms in heart failure due to myocardial infarction. Am J Physiol Heart Circ Physiol. 2003;284:H2277–87. [DOI] [PubMed]
Yu CH, Panagia V, Tappia PS, Liu SY, Takeda N, Dhalla NS, . Alterations of sarcolemmal phospholipase D and phosphatidate phosphohydrolase in congestive heart failure. Biochim Biophys Acta. 2002;1584:65–72. [DOI]
Heyliger CE, Ganguly PK, Dhalla NS, . Sarcoplasmic reticular and mitochondrial calcium transport in cardiac hypertrophy. Can J Cardiol. 1985;1:401–8. [PubMed]
Heyliger CE, Takeo S, Dhalla NS, . Alterations in sarcolemmal Na+-[19, 94, 96, 97]Ca2+ exchange and ATP- dependent Ca2+ -binding in hypertrophied heart. Can J Cardiol. 1985;1:328–39. [PubMed]
Heyliger CE, Dhalla NS, . Sarcolemmal Ca2+ binding and Ca2+-ATPase activities in hypertrophied heart. J Appl Cardiol. 1986;1:447–67.
Ito Y, Suko J, Chidsey CA, . Intracellular calcium and myocardial contractility V. Calcium uptake of sarcoplasmic reticulum fractions in hypertrophied and failing rabbit hearts. J Mol Cell Cardiol. 1974;6:237–47. [DOI]
Lamers JM, Stinis JT, . Defective calcium pump in the sarcoplasmic reticulum of the hypertrophied rabbit heart. Life Sci. 1979;24:2313–9. [DOI]
Limas CJ, Spier SS, Kahlon J, . Enhanced calcium transport by sarcoplasmic reticulum in mild cardiac hypertrophy. J Mol Cell Cardiol. 1980;12:1103–16. [DOI]
Sordahl LA, McCollum WB, Wood WG, Schwartz A, . Mitochondria and sarcoplasmic reticulum function in cardiac hypertrophy and failure. Am J Physiol. 1973;224:497–502. [DOI] [PubMed]
Mercadier JJ, Lompré AM, Wisnewsky C, Samuel JL, Bercovici J, Swynghedauw B, et al. Myosin isoenzyme changes in several models of rat cardiac hypertrophy. Circ Res. 1981;49:525–32. [DOI] [PubMed]
Alpert NR, Mulieri LA, . Heat, mechanics, and myosin ATPase in normal and hypertrophied heart muscle. Feb Proc. 1982;41:192–8. [PubMed]
Rupp H, Elimban V, Dhalla NS, . Modification of subcellular organelles in pressure-overloaded heart by etomoxir, a carnitine palmitoyltransferase I inhibitor. FASEB J. 1992;6:2349–53. [DOI] [PubMed]
Zarain-Herzberg A, Rupp H, Elimban V, Dhalla NS, . Modification of sarcoplasmic reticulum gene expression in pressure overload cardiac hypertrophy by etomoxir. FASEB J. 1996;10:1303–9. [DOI] [PubMed]
Dhalla NS, Heyliger CE, Shah KR, Sethi R, Takeda N, Nagano M, . Remodeling of membrane systems during the development of cardiac hyertrophy due to pressure overload. Basic Res Cardiol. 1994:76:27–49.
Ju H, Scammell-La Fleur T, Dixon IM, . Altered mRNA abundance of calcium transport genes in cardiac myocytes induced by angiotensin II. J Mol Cell Cardiol. 1996;28:1119–28. [DOI] [PubMed]
Dunn FG, Oigman W, Ventura HO, Messerli FH, Kobrin I, Frohlich ED, . Enalapril improves systemic and renal hemodynamics and allows regression of left ventricular mass in essential hypertension. Am J Cardiol. 1984;53:105–8. [DOI]
Linz W, Schölkens BA, Ganten D, . Converting enzyme inhibition specifically prevents the development and induces regression of cardiac hypertrophy in rats. Clin Exp Hypertens A. 1989;11:1325–50. [DOI] [PubMed]
Liu X, Sentex E, Golfman L, Takeda S, Osada M, Dhalla NS, . Modification of cardiac subcellular remodeling due to pressure overload by captopril and losartan. Clin Exp Hypertens. 1999;21:145–56. [DOI] [PubMed]
Flesch M, Schiffer F, Zolk O, Pinto Y, Stasch JP, Knorr A, et al. Angiotensin receptor antagonism and angiotensin converting enzyme inhibition improve diastolic dysfunction and Ca2+ -ATPase expression in the sarcoplasmic reticulum in hypertensive cardiomyopathy. J Hypertens. 1997;15:1001–9. [DOI] [PubMed]
Schunkert H, Dzau VJ, Tang SS, Hirsch AT, Apstein CS, Lorell BH, . 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. 1990;86:1913–20. [DOI] [PubMed] [PMC]
Ferrario CM, Mullick AE, . Renin angiotensin aldosterone inhibition in the treatment of cardiovascular disease. Pharmacol Res. 2017;125:57–71. [DOI] [PubMed] [PMC]
Weir MR, Dzau VJ, . The renin-angiotensin-aldosterone system: a specific target for hypertension management. Am J Hypertens. 1999;12:205S–13S. [DOI]
Oparil S, Yarows SA, Patel S, Fang H, Zhang J, Satlin A, . Efficacy and safety of combined use of aliskiren and valsartan in patients with hypertension: a randomised, double-blind trial. Lancet. 2007;370:221–9. [DOI]
Wollert KC, Drexler H, . The renin-angiotensin system and experimental heart failure. Cardiovasc Res. 1999;43:838–49. [DOI]
Leenen FHH, Skarda V, Yuan B, White R, . Changes in cardiac Ang II postmyocardial infarction in rats: effects of nephrectomy and ACE inhibitors. Am J Physiol Circ Physiol. 1999;276:H317–25. [DOI] [PubMed]
Ruzicka M, Skarda V, Leenen FHH, . Effects of ACE inhibitors on circulating versus cardiac angiotensin II in volume overload induced cardiac hypertrophy in rats. Circulation. 1995;92:3568–73. [DOI] [PubMed]
Ruzicka M, Leenen FH, . Relevance of blockade of cardiac and circulatory angiotensin-converting enzyme for the prevention of volume overload-induced cardiac hypertrophy. Circulation. 1995;91:16–9. [DOI] [PubMed]
Hisamatsu Y, Ohkusa T, Kihara Y, Inoko M, Ueyama T, Yano M, et al. Early changes in the functions of cardiac sarcoplasmic reticulum in volume-overloaded cardiac hypertrophy in rats. J Mol Cell Cardiol. 1997;29:1097–109. [DOI] [PubMed]
Yoshida K, Yoshiyama M, Omura T, Nakamura Y, Kim S, Takeuchi K, et al. Activation of mitogen-activated protein kinases in the non-ischemic myocardium of an acute myocardial infarction in rats. Jpn Circ J. 2001;65:808–14. [DOI] [PubMed]
Bogoyevitch MA, Andersson MB, Gillespie-Brown J, Clerk A, Glennon PE, Fuller SJ, et al. Adrenergic receptor stimulation of the mitogen-activated protein kinase cascade and cardiac hypertrophy. Biochem J. 1996;314:115–21. [DOI] [PubMed] [PMC]
Shimizu N, Yoshiyama M, Omura T, Hanatani A, Kim S, Takeuchi K, et al. Activation of mitogen-activated protein kinases and activator protein-1 in myocardial infarction in rats. Cardiovasc Res. 1998;38:116–24. [DOI]
Kim S, Iwao H, . Activation of mitogen-activated protein kinases in cardiovascular hypertrophy and remodeling. Jpn J Pharmacol. 1999;80:97–102. [DOI] [PubMed]
Zhang W, Elimban V, Xu YJ, Zhang M, Nijjar MS, Dhalla NS, . Alterations of cardiac ERK1/2 expression and activity due to volume overload were attenuated by the blockade of RAS. J Cardiovasc Pharmacol Ther. 2010;15:84–92. [DOI] [PubMed]
Dhalla NS, Takeda N, Rodriguez-Leyva D, Elimban V, . Mechanisms of subcellular remodeling in heart failure due to diabetes. Heart Fail Rev. 2014;19:87–99. [DOI] [PubMed]
Stanley WC, Lopaschuk GD, McCormack JG, . Regulation of energy substrate metabolism in the diabetic heart. Cardiovasc Res. 1997;34:25–33. [DOI]
Pierce GN, Russell JC, . Regulation of intracellular Ca2+ in the heart during diabetes. Cardiovasc Res. 1997;34:41–7. [DOI]
Feuvray D, . The regulation of intracellular pH in the diabetic myocardium. Cardiovasc Res. 1997;34:48–54. [DOI]
Liu X, Suzuki H, Sethi R, Tappia PS, Takeda N, Dhalla NS, . Blockade of the renin-angiotensin system attenuates sarcolemma and sarcoplasmic reticulum remodeling in chronic diabetes. Ann N Y Acad Sci. 2006;1084:141–54. [DOI] [PubMed]
Machackova J, Liu X, Lukas A, Dhalla NS, . Renin-angiotensin blockade attenuates cardiac myofibrillar remodelling in chronic diabetes. Mol Cell Biochem. 2004;261:271–8. [DOI] [PubMed]
