Angiotensin II‐induced increase in myocardial distensibility and its modulation by the endocardial endothelium in the rabbit heart

As recently demonstrated, angiotensin II (Ang II) induces an increase in myocardial distensibility. Although endothelin‐1 and the endocardial endothelium (EE) also modulate myocardial diastolic properties, their interaction with Ang II at this level has not yet been investigated. Increasing concentrations of Ang II (from 10−8 to 10−5m) were studied in rabbit right papillary muscles in the following conditions: (1) baseline; (2) after selective removal of EE with Triton X‐100; and (3) with intact EE in presence of a non‐selective endothelin receptor antagonist (PD‐145065), a selective endothelin type A receptor antagonist (BQ‐123), an inhibitor of nitric oxide synthesis (NG‐nitro‐l‐arginine (l‐NA) or an inhibitor of the NAD(P)H oxidase (apocynin). At baseline, Ang II induced a concentration‐dependent positive inotropic effect and an increase in passive muscle length (L) up to 1.020 ± 0.004L/Lmax. After restoring muscle length to maximal physiological length (Lmax), passive tension decreased by 46.1 ± 4.0%. When the EE was removed, the effect on myocardial distensibility was abolished. With intact EE in presence of PD‐145065, BQ‐123 or l‐NA, the effects of Ang II on myocardial distensibility were attenuated, with a maximal increase in passive muscle length of 1.0087 ± 0.0012, 1.0068 ± 0.0022 and 1.0066 ± 0.0020L/Lmax and a decrease in resting tension of 22.6 ± 3.6, 16.1 ± 6.0 and 20.4 ± 5.6%, respectively. In the presence of apocynin, the effect on myocardial distensibility was abolished. In conclusion, the Ang II‐dependent acute increase in myocardial distensibility is abolished by the selective removal of the EE and attenuated in the presence of endothelin‐1 receptor antagonists, an inhibitor of nitric oxide synthesis or an inhibitor of NAD(P)H oxidase.

[1]  A. Leite-Moreira,et al.  Acute neurohumoral modulation of diastolic function , 2009, Peptides.

[2]  K. Schlüter,et al.  Angiotensin II: a hormone involved in and contributing to pro-hypertrophic cardiac networks and target of anti-hypertrophic cross-talks. , 2008, Pharmacology & therapeutics.

[3]  A. Leite-Moreira,et al.  Negative inotropic effect of selective AT2 receptor stimulation and its modulation by the endocardial endothelium. , 2008, European journal of pharmacology.

[4]  N. Toda,et al.  Interaction of Endothelial Nitric Oxide and Angiotensin in the Circulation , 2007, Pharmacological Reviews.

[5]  S. Eguchi,et al.  Activation of endothelial nitric oxide synthase by the angiotensin II type 1 receptor. , 2006, Endocrinology.

[6]  A. Leite-Moreira,et al.  Endothelin ETA receptors and endothelium partially mediate the positive inotropic and lusitropic effects of angiotensin II. , 2006, European journal of pharmacology.

[7]  Martin Paul,et al.  Physiology of local renin-angiotensin systems. , 2006, Physiological reviews.

[8]  A. Leite-Moreira,et al.  Angiotensin II acutely decreases myocardial stiffness: a novel AT1, PKC and Na+/H+ exchanger‐mediated effect , 2006, British journal of pharmacology.

[9]  A. Leite-Moreira,et al.  Obligatory role of the endocardial endothelium in the increase of myocardial distensibility induced by endothelin-1. , 2005, Experimental biology and medicine.

[10]  A. Leite-Moreira,et al.  Inotropic effects of ETB receptor stimulation and their modulation by endocardial endothelium, NO, and prostaglandins. , 2004, American Journal of Physiology. Heart and Circulatory Physiology.

[11]  D. Kass,et al.  What Mechanisms Underlie Diastolic Dysfunction in Heart Failure? , 2004, Circulation research.

[12]  A. Haase,et al.  Cardiac Hypertrophy Is Associated With Decreased eNOS Expression in Angiotensin AT2 Receptor–Deficient Mice , 2003, Hypertension.

[13]  R. Carey,et al.  Newly recognized components of the renin-angiotensin system: potential roles in cardiovascular and renal regulation. , 2003, Endocrine reviews.

[14]  A. Leite-Moreira,et al.  ET-1 increases distensibility of acutely loaded myocardium: a novel ETA and Na+/H+ exchanger-mediated effect. , 2003, American journal of physiology. Heart and circulatory physiology.

[15]  H. Matsubara,et al.  Cardiac Angiotensin II Type 2 Receptor Activates the Kinin/NO System and Inhibits Fibrosis , 2003, Hypertension.

[16]  A. Shah,et al.  Role of cyclic GMP‐dependent protein kinase in the contractile response to exogenous nitric oxide in rat cardiac myocytes , 2002, The Journal of physiology.

[17]  U. Walter,et al.  Effects of Angiotensin II Infusion on the Expression and Function of NAD(P)H Oxidase and Components of Nitric Oxide/cGMP Signaling , 2002, Circulation research.

[18]  C. Baylis,et al.  Endothelin Mediates Some of the Renal Actions of Acutely Administered Angiotensin II , 2001, Hypertension.

[19]  S. Vanni,et al.  Cardiac Angiotensin II Formation in the Clinical Course of Heart Failure and Its Relationship With Left Ventricular Function , 2001, Circulation research.

[20]  P. Vallance,et al.  Positive inotropic effects of NO donors in isolated guinea-pig and human cardiomyocytes independent of NO species and cyclic nucleotides. , 2000, Cardiovascular research.

[21]  E. Schiffrin,et al.  Signal transduction mechanisms mediating the physiological and pathophysiological actions of angiotensin II in vascular smooth muscle cells. , 2000, Pharmacological reviews.

[22]  K. Catt,et al.  International union of pharmacology. XXIII. The angiotensin II receptors. , 2000, Pharmacological reviews.

[23]  A. Shah,et al.  Paracrine and autocrine effects of nitric oxide on myocardial function. , 2000, Pharmacology & therapeutics.

[24]  Shokei Kim,et al.  Molecular and cellular mechanisms of angiotensin II-mediated cardiovascular and renal diseases. , 2000, Pharmacological reviews.

[25]  M. Zile,et al.  Angiotensin-converting enzyme and matrix metalloproteinase inhibition with developing heart failure: comparative effects on left ventricular function and geometry. , 1999, The Journal of pharmacology and experimental therapeutics.

[26]  K. Baker,et al.  The cardiac renin-angiotensin system: conceptual, or a regulator of cardiac function? , 1999, Circulation research.

[27]  H. Drexler,et al.  The renin-angiotensin system and experimental heart failure. , 1999, Cardiovascular research.

[28]  J. Bronzwaer,et al.  Endomyocardial nitric oxide synthase and left ventricular preload reserve in dilated cardiomyopathy. , 1999, Circulation.

[29]  E. Lakatta,et al.  Activation of distinct cAMP-dependent and cGMP-dependent pathways by nitric oxide in cardiac myocytes. , 1999, Circulation research.

[30]  A. Pessina,et al.  Interactions between endothelin-1 and the renin-angiotensin-aldosterone system. , 1999, Cardiovascular research.

[31]  T. Lüscher,et al.  Angiotensin II increases tissue endothelin and induces vascular hypertrophy: reversal by ET(A)-receptor antagonist. , 1997, Circulation.

[32]  W. Paulus,et al.  Myocardial contractile response to nitric oxide and cGMP. , 1996, Circulation.

[33]  O. Carretero,et al.  Myocardial contractility is modulated by angiotensin II via nitric oxide. , 1996, Hypertension.

[34]  C. Szabó,et al.  Selective pharmacological inhibition of distinct nitric oxide synthase isoforms. , 1996, Biochemical pharmacology.

[35]  P. Mulrow,et al.  The adrenal renin-angiotensin system: a local hormonal regulator of aldosterone production. , 1996, Journal of hypertension.

[36]  K. Weber,et al.  Structural remodelling of the heart by fibrous tissue: role of circulating hormones and locally produced peptides. , 1995, European heart journal.

[37]  U. Ikeda,et al.  Angiotensin II augments cytokine-stimulated nitric oxide synthesis in rat cardiac myocytes. , 1995, Circulation.

[38]  X. Xu,et al.  Coronary kinin generation mediates nitric oxide release after angiotensin receptor stimulation. , 1995, Hypertension.

[39]  Shokei Kim,et al.  Angiotensin II induces cardiac phenotypic modulation and remodeling in vivo in rats. , 1995, Hypertension.

[40]  G. D. De Keulenaer,et al.  Endothelin-mediated positive inotropic effect induced by reactive oxygen species in isolated cardiac muscle. , 1995, Circulation research.

[41]  T. Gillebert,et al.  Preload, length-tension relation, and isometric relaxation in cardiac muscle. , 1994, The American journal of physiology.

[42]  M. Lewis,et al.  Modulation of myocardial relaxation by basal release of endothelin from endocardial endothelium. , 1994, Cardiovascular research.

[43]  G. McClellan,et al.  Endothelial cell storage and release of endothelin as a cardioregulatory mechanism. , 1994, Circulation research.

[44]  W. Paulus,et al.  Acute effects of nitric oxide on left ventricular relaxation and diastolic distensibility in humans. Assessment by bicoronary sodium nitroprusside infusion. , 1994, Circulation.

[45]  E. Lakatta,et al.  8-bromo-cGMP reduces the myofilament response to Ca2+ in intact cardiac myocytes. , 1994, Circulation research.

[46]  A Mebazaa,et al.  Paracrine effects of endocardial endothelial cells on myocyte contraction mediated via endothelin. , 1993, The American journal of physiology.

[47]  A. Nogami,et al.  Endothelin-1 is an autocrine/paracrine factor in the mechanism of angiotensin II-induced hypertrophy in cultured rat cardiomyocytes. , 1993, The Journal of clinical investigation.

[48]  Y. Hirata,et al.  Induction of Endothelin‐1 Gene by Angiotensin and Vasopressin in Endothelial Cells , 1992, Hypertension.

[49]  Vicotor J Dzau,et al.  Circulating versus local renin‐angiotensin system in cardiovascular homeostasis , 1988, Circulation.

[50]  D. Brutsaert,et al.  Effects of Damaging the Endocardial Surface on the Mechanical Performance of Isolated Cardiac Muscle , 1988, Circulation research.

[51]  V. Dzau,et al.  Endothelial renin-angiotensin pathway: evidence for intracellular synthesis and secretion of angiotensins. , 1987, Circulation research.

[52]  R. Richard,et al.  The myocardial intracellular renin-angiotensin system , 1987 .

[53]  V. Dzau.  Vascular wall renin-angiotensin pathway in control of the circulation. A hypothesis. , 1984, The American journal of medicine.

[54]  J. Fallon,et al.  Renin synthesis by canine aortic smooth muscle cells in culture. , 1982, Life sciences.

[55]  R. Carey,et al.  Role of the intrarenal renin-angiotensin system in the control of renal function. , 1981, Circulation research.

[56]  R. Carey,et al.  Effect of Intrarenal Angiotensin II Blockade on Renal Function in Conscious Dogs , 1977, Circulation research.

[57]  J. Areias,et al.  Nitric oxide and prostaglandins - important players in endothelin-1 induced myocardial distensibility. , 2008, Physiological research.

[58]  W. Arendshorst,et al.  Superoxide mediates acute renal vasoconstriction produced by angiotensin II and catecholamines by a mechanism independent of nitric oxide. , 2007, American journal of physiology. Heart and circulatory physiology.

[59]  D. Brutsaert,et al.  Cardiac endothelial-myocardial signaling: its role in cardiac growth, contractile performance, and rhythmicity. , 2003, Physiological reviews.

[60]  U. Walter,et al.  Effects of Angiotensin II Infusion on the Expression and Function of NAD(P)H Oxidase , 2002 .

[61]  J. Michel,et al.  Angiotensin II stimulates the production of NO and peroxynitrite in endothelial cells. , 1998, American journal of physiology. Cell physiology.

[62]  A. Mimran,et al.  Prevention of the cardiovascular and renal effects of angiotensin II by endothelin blockade. , 1998, Hypertension.

[63]  G. Kojda,et al.  Low increase in cGMP induced by organic nitrates and nitrovasodilators improves contractile response of rat ventricular myocytes. , 1996, Circulation research.

[64]  R. Re,et al.  Evidence for the existence of renin in the heart. , 1987, Circulation.

[65]  R. Re.  The myocardial intracellular renin-angiotensin system. , 1987, The American journal of cardiology.

[66]  R. Carey,et al.  Control of renal function by intrarenal angiotensin II. , 1983, Endocrinology.