Effects of Angiotensin 1-7 and Mas Receptor Agonist on Renal System in a Rat Model of Heart Failure
Abstract
:1. Introduction
2. Results
2.1. Acute Protocols
2.1.1. Effects of Ang 1-7 and AVE 0991 on Urine Flow and Na Excretion
2.1.2. Effects of Ang 1-7 and AVE 0991 on Kidney Function
2.1.3. Effects of Ang 1-7 and AVE0991 on MAP
2.1.4. Effects of Ang 1-7 and AVE 0991 on Urinary cGMP
2.2. Chronic Protocols
2.2.1. Kidney Function and Kidney Weight
Effects of Ang 1-7 and AVE 0991 on UF, UNaV and UKV in CHF Rats and Sham Controls
Effect of Ang 1-7 and AVE 0991 on Kidney Weight and Serum Creatinine (sCr)
2.2.2. Cardiac Parameters
Effect of Ang 1-7 and AVE 0991 on Cardiac Remodeling
Effect of Ang 1-7 and AVE 0991 on Plasma BNP
2.2.3. Effect of Ang 1-7 and AVE 0991 on RAAS Status
3. Discussion
3.1. Acute Protocol
3.2. Chronic Protocol
4. Materials and Methods
4.1. The Experimental Model
4.2. Acute Studies
4.3. Chronic Studies
4.4. Physiological and Chemical Analyzes
4.5. Statistical Analysis
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
References
- Roger, V.L. Epidemiology of heart failure. Circ. Res. 2013, 113, 646–659. [Google Scholar] [CrossRef] [PubMed]
- Kehat, I.; Molkentin, J.D. Molecular pathways underlying cardiac remodeling during pathophysiological stimulation. Circulation 2010, 122, 2727–2735. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Takimoto, E.; Kass, D.A. Role of oxidative stress in cardiac hypertrophy and remodeling. Hypertension 2007, 49, 241–248. [Google Scholar] [CrossRef] [PubMed]
- Dzau, V.J. Renal and circulatory mechanisms in congestive heart failure. Kidney Int. 1987, 31, 1402–1415. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schrier, R.W.; Gurevich, A.K.; Cadnapaphornchai, M.A. Pathogenesis and management of sodium and water retention in cardiac failure and cirrhosis. Semin. Nephrol. 2001, 21, 157–172. [Google Scholar] [CrossRef]
- Hillege, H.L.; Girbes, A.R.; de Kam, P.J.; Boomsma, F.; de Zeeuw, D.; Charlesworth, A.; Hampton, J.R.; van Veldhuisen, D.J. Renal function, neurohormonal activation, and survival in patients with chronic heart failure. Circulation 2000, 102, 203–210. [Google Scholar] [CrossRef] [Green Version]
- Metra, M.; Cotter, G.; Gheorghiade, M.; Dei Cas, L.; Voors, A.A. The role of the kidney in heart failure. Eur. Heart J. 2012, 33, 2135–2142. [Google Scholar] [CrossRef] [Green Version]
- Winaver, J.; Hoffman, A.; Burnett, J.C., Jr.; Haramati, A. Hormonal determinants of sodium excretion in rats with experimental high-output heart failure. Am. J. Physiol. 1988, 254 Pt 2, R776–R784. [Google Scholar] [CrossRef]
- Pieruzzi, F.; Abassi, Z.A.; Keiser, H.R. Expression of renin-angiotensin system components in the heart, kidneys, and lungs of rats with experimental heart failure. Circulation 1995, 92, 3105–3112. [Google Scholar] [CrossRef]
- Abassi, Z.; Gurbanov, K.; Rubinstein, I.; Better, O.S.; Hoffman, A.; Winaver, J. Regulation of intrarenal blood flow in experimental heart failure: Role of endothelin and nitric oxide. Am. J. Physiol. 1998, 274, F766–F774. [Google Scholar] [CrossRef]
- Abassi, Z.A.; Brodsky, S.; Karram, T.; Dobkin, I.; Winaver, J.; Hoffman, A. Temporal changes in natriuretic and antinatriuretic systems after closure of a large arteriovenous fistula. Cardiovasc. Res. 2001, 51, 567–576. [Google Scholar] [CrossRef] [Green Version]
- Kalra, P.R.; Anker, S.D.; Coats, A.J. Water and sodium regulation in chronic heart failure: The role of natriuretic peptides and vasopressin. Cardiovasc. Res. 2001, 51, 495–509. [Google Scholar] [CrossRef] [Green Version]
- Tsuruda, T.; Boerrigter, G.; Huntley, B.K.; Noser, J.A.; Cataliotti, A.; Costello-Boerrigter, L.C.; Chen, H.H.; Burnett, J.C., Jr. Brain natriuretic Peptide is produced in cardiac fibroblasts and induces matrix metalloproteinases. Circ. Res. 2002, 91, 1127–1134. [Google Scholar] [CrossRef]
- Woodard, G.E.; Rosado, J.A. Recent advances in natriuretic peptide research. J. Cell. Mol. Med. 2007, 11, 1263–1271. [Google Scholar] [CrossRef] [Green Version]
- Packer, M. The neurohormonal hypothesis: A theory to explain the mechanism of disease progression in heart failure. J. Am. Coll. Cardiol. 1992, 20, 248–254. [Google Scholar] [CrossRef] [Green Version]
- Schroten, N.F.; Gaillard, C.A.J.M.; van Veldhuisen, D.J.; Szymanski, M.K.; Village, H.L.; de Boer, R.A. New roles for renin and prorenin in heart failure and cardiorenal crosstalk. Heart Fail. Rev. 2012, 17, 191–201. [Google Scholar] [CrossRef] [Green Version]
- Francis, G.S.; Benedict, C.; Johnstone, D.E.; Kirlin, P.C.; Nicklas, J.; Liang, C.S.; Kubo, S.H.; Rudin-Toretsky, E.; Yusuf, S. Comparison of Neuroendocrine Activation in Patients with Left-Ventricular Dysfunction with and without Congestive-Heart-Failure—A Substudy of the Studies of Left-Ventricular Dysfunction (Solvd). Circulation 1990, 82, 1724–1729. [Google Scholar] [CrossRef] [Green Version]
- Schrier, R.W.; Abraham, W.T. Hormones and hemodynamics in heart failure. N. Engl. J. Med. 1999, 341, 577–585. [Google Scholar] [CrossRef]
- Katz, A.M. Heart failure: A hemodynamic disorder complicated by maladaptive proliferative responses. J. Cell. Mol. Med. 2003, 7, 1–10. [Google Scholar] [CrossRef] [Green Version]
- Jessup, M.; Brozena, S. Heart failure. N. Engl. J. Med. 2003, 348, 2007–2018. [Google Scholar] [CrossRef]
- Steckelings, U.M.; Paulis, L.; Unger, T.; Bader, M. Emerging drugs which target the renin-angiotensin-aldosterone system. Expert Opin. Emerg. Drugs 2011, 16, 619–630. [Google Scholar] [CrossRef] [PubMed]
- Carey, R.M. Newly discovered components and actions of the renin-angiotensin system. Hypertension 2013, 62, 818–822. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fyhrquist, F.; Saijonmaa, O. Renin-angiotensin system revisited. J. Intern. Med. 2008, 264, 224–236. [Google Scholar] [CrossRef] [PubMed]
- Fraga-Silva, R.A.; Costa-Fraga, F.P.; Murça, T.M.; Moraes, P.L.; Lima, A.M.; Lautner, R.Q.; Castro, C.H.; Soares, C.-M.A.; Borges, C.L.; Nadu, A.P.; et al. Angiotensin-converting enzyme 2 activation improves endothelial function. Hypertension 2013, 61, 1233–1238. [Google Scholar] [CrossRef]
- Dilauro, M.; Burns, K.D. Angiotensin-(1-7) and its effects in the kidney. Sci. World J. 2009, 9, 522–535. [Google Scholar] [CrossRef] [Green Version]
- Ferreira, J.C.B.; Bacurau, A.V.; Evangelista, F.S.; Coelho, M.A.; Oliveira, E.M.; Casarini, D.E.; Krieger, J.E.; Brum, P.C. The role of local and systemic renin angiotensin system activation in a genetic model of sympathetic hyperactivity-induced heart failure in mice. Am. J. Physiol. Integr. Comp. Physiol. 2008, 294, R26–R32. [Google Scholar] [CrossRef]
- Ferreira, A.J.; Jacoby, B.A.; Araújo, C.A.A.; Macedo, F.A.F.F.; Silva, G.A.B.; Almeida, A.P.; Caliari, M.V.; Santos, R.A.S. The nonpeptide angiotensin-(1-7) receptor Mas agonist AVE-0991 attenuates heart failure induced by myocardial infarction. Am. J. Physiol. Heart Circ. Physiol. 2007, 292, H1113–H1119. [Google Scholar] [CrossRef] [Green Version]
- Santos, R.A.; Ferreira, A.J. Pharmacological effects of AVE 0991, a nonpeptide angiotensin-(1-7) receptor agonist. Cardiovasc. Drug Rev. 2006, 24, 239–246. [Google Scholar] [CrossRef]
- Abassi, Z.; Goltsman, I.; Karram, T.; Winaver, J.; Hoffman, A. Aortocaval fistula in rat: A unique model of volume-overload congestive heart failure and cardiac hypertrophy. J. Biomed. Biotechnol. 2011, 2011, 729497. [Google Scholar] [CrossRef] [Green Version]
- Igase, M.; Yokoyama, H.; Ferrario, C.M. Attenuation of hypertension-mediated glomerulosclerosis in conjunction with increased angiotensin (1-7). Ther. Adv. Cardiovasc. Dis. 2011, 5, 297–304. [Google Scholar] [CrossRef] [Green Version]
- Verano-Braga, T.; Schwämmle, V.; Sylvester, M.; Passos-Silva, D.G.; Peluso, A.A.B.; Etelvino, G.M.; Santos, R.A.S.; Roepstorff, P. Time-Resolved Quantitative Phosphoproteomics: New Insights into Angiotensin-(1-7) Signaling Networks in Human Endothelial Cells. J. Proteome Res. 2012, 11, 3370–3381. [Google Scholar] [CrossRef]
- Johnson, J.A.; West, J.; Maynard, K.B.; Hemnes, A.R. ACE2 improves right ventricular function in a pressure overload model. PLoS ONE 2011, 6, e20828. [Google Scholar] [CrossRef] [Green Version]
- Chappell, M.C.; Modrall, J.G.; Diz, D.I.; Ferrario, C.M. Novel aspects of the renal renin-angiotensin system: Angiotensin-(1-7), ACE2 and blood pressure regulation. Kidney Blood Press. Regul. 2004, 143, 77–89. [Google Scholar]
- Vallon, V. Tubuloglomerular feedback and the control of glomerular filtration rate. News Physiol. Sci. 2003, 18, 169–174. [Google Scholar] [CrossRef] [Green Version]
- van der Wouden, E.A.; Ochodnický, P.; van Dokkum, R.P.; Rocks, A.; Deelman, L.E.; de Zeeuw, D.; Henning, R.H. The role of angiotensin(1-7) in renal vasculature of the rat. J. Hypertens. 2006, 24, 1971–1978. [Google Scholar] [CrossRef]
- DelliPizzi, A.M.; Hilchey, S.D.; Bell-Quilley, C.P. Natriuretic action of angiotensin(1-7). Br. J. Pharmacol. 1994, 111, 1–3. [Google Scholar] [CrossRef]
- Handa, R.K.; Ferrario, C.M.; Strandhoy, J.W. Renal actions of angiotensin-(1-7): In vivo and in vitro studies. Am. J. Physiol. -Ren. Physiol. 1996, 270, F141–F147. [Google Scholar] [CrossRef]
- Supaporn, T.; Sandberg, S.M.; Borgeson, D.D.; Heublein, D.M.; Luchner, A.; Wei, C.M.; Dousa, T.P.; Burnett, J.C., Jr. Blunted cGMP response to agonists and enhanced glomerular cyclic 3′,5′-nucleotide phosphodiesterase activities in experimental congestive heart failure. Kidney Int. 1996, 50, 1718–1725. [Google Scholar] [CrossRef] [Green Version]
- Carrithers, S.L.; Eber, S.L.; Forte, L.R.; Greenberg, R.N. Increased urinary excretion of uroguanylin in patients with congestive heart failure. Am. J. Physiol. Heart Circ. Physiol. 2000, 278, H538–H547. [Google Scholar] [CrossRef] [Green Version]
- Gomes, E.R.M.; Lara, A.A.; Almeida, P.W.M.; Guimarães, D.; Resende, R.R.; Campagnole-Santos, M.J.; Bader, M.; Santos, R.A.S.; Guatimosim, S. Angiotensin-(1-7) Prevents Cardiomyocyte Pathological Remodeling Through a Nitric Oxide/Guanosine 3′,5′-Cyclic Monophosphate-Dependent Pathway. Hypertension 2010, 55, 153–160. [Google Scholar] [CrossRef] [Green Version]
- Nakamoto, H.; Ferrario, C.M.; Fuller, S.B.; Robaczewski, D.L.; Winicov, E.; Dean, R.H. Angiotensin-(1-7) and Nitric-Oxide Interaction in Renovascular Hypertension. Hypertension 1995, 25, 796–802. [Google Scholar] [CrossRef] [PubMed]
- Wiemer, G.; Dobrucki, L.W.; Louka, F.R.; Malinski, T.; Heitsch, H. AVE 0991, a nonpeptide mimic of the effects of angiotensin-(1-7) on the endothelium. Hypertension 2002, 40, 847–852. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Raffai, G.; Durand, M.J.; Lombard, J.H. Acute and chronic angiotensin-(1-7) restores vasodilation and reduces oxidative stress in mesenteric arteries of salt-fed rats. Am. J. Physiol. Heart Circ. Physiol. 2011, 301, H1341–H1352. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Walters, P.E.; Gaspari, T.A.; Widdop, R.E. Angiotensin-(1-7) acts as a vasodepressor agent via angiotensin II type 2 receptors in conscious rats. Hypertension 2005, 45, 960–966. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wu, J.-G.; Tang, H.; Liu, Z.-J.; Ma, Z.-F.; Tang, A.-L.; Zhang, X.-J.; Gao, X.-R.; Ma, H. Angiotensin-(1-7) inhibits vascular remodelling in rat jugular vein grafts via reduced ERK1/2 and p38 MAPK activity. J. Int. Med. Res. 2011, 39, 2158–2168. [Google Scholar] [CrossRef] [PubMed]
- Goltsman, I.; Wang, X.; Lavallie, E.R.; Diblasio-Smith, E.A.; Ovcharenko, E.; Hoffman, A.; Abassi, Z.; Feuerstein, G.Z.; Winaver, J. Effects of chronic rosiglitazone treatment on renal handling of salt and water in rats with volume-overload congestive heart failure. Circ. Heart Fail. 2011, 4, 345–354. [Google Scholar] [CrossRef] [Green Version]
- Abassi, Z.A.; Gurbanov, K.; Mulroney, S.E.; Potlog, C.; Opgenorth, T.J.; Hoffman, A.; Haramati, A.; Winaver, J. Impaired nitric oxide-mediated renal vasodilation in rats with experimental heart failure: Role of angiotensin II. Circulation 1997, 96, 3655–3664. [Google Scholar] [CrossRef]
- Hong, N.J.; Garvin, J.L. Angiotensin II Type 2 Receptor-Mediated Inhibition of NaCl Absorption Is Blunted in Thick Ascending Limbs from Dahl Salt-Sensitive Rats. Hypertension 2012, 60, 765–769. [Google Scholar] [CrossRef] [Green Version]
- Torp, M.; Brønd, L.; Nielsen, J.B.; Nielsen, S.; Christensen, S.; Jonassen, T.E.N. Effects of renal denervation on the NKCC2 cotransporter in the thick ascending limb of the loop of Henle in rats with congestive heart failure. Acta Physiol. 2012, 204, 451–459. [Google Scholar] [CrossRef]
- Stegbauer, J.; Potthoff, S.A.; Quack, I.; Mergia, E.; Clasen, T.; Friedrich, S.; Vonend, O.; Woznowski, M.; Königshausen, E.; Sellin, L.; et al. Chronic treatment with angiotensin-(1-7) improves renal endothelial dysfunction in apolipoproteinE-deficient mice. Br. J. Pharmacol. 2011, 163, 974–983. [Google Scholar] [CrossRef] [Green Version]
- Gawrys, O.; Husková, Z.; Škaroupková, P.; Honetschlägerová, Z.; Vaňourková, Z.; Kikerlová, S.; Melenovský, V.; Bačová, B.S.; Sykora, M.; Táborský, M.; et al. The treatment with sGC stimulator improves survival of hypertensive rats in response to volume-overload induced by aorto-caval fistula. Naunyn-Schmiedeberg’s Arch. Pharmacol. 2023. [Google Scholar] [CrossRef]
- Armstrong, P.W.; Pieske, B.; Anstrom, K.J.; Ezekowitz, J.; Hernandez, A.F.; Butler, J.; Lam, C.S.P.; Ponikowski, P.; Voors, A.A.; Jia, G.; et al. Vericiguat in Patients with Heart Failure and Reduced Ejection Fraction. N. Engl. J. Med. 2020, 382, 1883–1893. [Google Scholar] [CrossRef]
- Byku, M.; Macarthur, H.; Westfall, T.C. Inhibitory effects of angiotensin-(1-7) on the nerve stimulation-induced release of norepinephrine and neuropeptide Y from the mesenteric arterial bed. Am. J. Physiol. Heart Circ. Physiol. 2010, 298, H457–H465. [Google Scholar] [CrossRef] [Green Version]
- Poletti, R.; Vergaro, G.; Zyw, L.; Prontera, C.; Passino, C.; Emdin, M. Prognostic value of plasma renin activity in heart failure patients with chronic kidney disease. Int. J. Cardiol. 2013, 167, 711–715. [Google Scholar] [CrossRef]
- Rezk, B.M.; Yoshida, T.; Semprun-Prieto, L.; Higashi, Y.; Sukhanov, S.; Delafontaine, P. Angiotensin II infusion induces marked diaphragmatic skeletal muscle atrophy. PLoS ONE 2012, 7, e30276. [Google Scholar] [CrossRef]
- Yu, L.; Yuan, K.; Phuong, H.-T.A.; Park, B.M.; Kim, S.H. Angiotensin-(1-5), an active mediator of renin-angiotensin system, stimulates ANP secretion via Mas receptor. Peptides 2016, 86, 33–41. [Google Scholar] [CrossRef]
- Patel, V.B.; Bodiga, S.; Fan, D.; Das, S.K.; Wang, Z.; Wang, W.; Basu, R.; Zhong, J.-C.; Kassiri, Z.; Oudit, G.Y. Cardioprotective effects mediated by angiotensin II type 1 receptor blockade and enhancing angiotensin 1-7 in experimental heart failure in angiotensin-converting enzyme 2-null mice. Hypertension 2012, 59, 1195–1203. [Google Scholar] [CrossRef] [Green Version]
- Grobe, J.L.; Mecca, A.P.; Lingis, M.; Shenoy, V.; Bolton, T.A.; Machado, J.M.; Speth, R.C.; Raizada, M.K.; Katovich, M.J. Prevention of angiotensin II-induced cardiac remodeling by angiotensin-(1-7). Am. J. Physiol. Heart Circ. Physiol. 2007, 292, H736–H742. [Google Scholar] [CrossRef] [Green Version]
- Ferreira, A.J.; Oliveira, T.L.; Castro, M.-C.M.; Almeida, A.P.; Castro, C.H.; Caliari, M.V.; Gava, E.; Kitten, G.T.; Santos, R.A.S. Isoproterenol-induced impairment of heart function and remodeling are attenuated by the nonpeptide angiotensin-(1-7) analogue AVE 0991. Life Sci. 2007, 81, 916–923. [Google Scholar] [CrossRef]
- Flores-Munoz, M.; Godinho, B.M.D.C.; Almalik, A.; Nicklin, S.A. Adenoviral delivery of angiotensin-(1-7) or angiotensin-(1-9) inhibits cardiomyocyte hypertrophy via the mas or angiotensin type 2 receptor. PLoS ONE 2012, 7, e45564. [Google Scholar] [CrossRef]
- de Almeida, P.W.M.; de Freitas Lima, R.; de Morais Gomes, E.R.; Rocha-Resende, C.; Roman-Campos, D.; Gondim, A.N.S.; Gavioli, M.; Lara, A.; Parreira, A.; de Azevedo Nunes, S.L.; et al. Functional Cross-Talk Between Aldosterone and Angiotensin-(1-7) in Ventricular Myocytes. Hypertension 2013, 61, 425–430. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Luchner, A.; Stevens, T.L.; Borgeson, D.D.; Redfield, M.M.; Bailey, J.E.; Sandberg, S.M.; Heublein, D.M.; Burnett, J.C., Jr. Angiotensin II in the evolution of experimental heart failure. Hypertension 1996, 28, 472–477. [Google Scholar] [CrossRef] [PubMed]
- Stumpe, K.O.; Sölle, H.; Klein, H.; Krück, F.; Ressel, C. Mechanism of sodium and water retention in rats with experimental heart failure. Kidney Int. 1973, 4, 309–317. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Cohen-Segev, R.; Nativ, O.; Kinaneh, S.; Aronson, D.; Kabala, A.; Hamoud, S.; Karram, T.; Abassi, Z. Effects of Angiotensin 1-7 and Mas Receptor Agonist on Renal System in a Rat Model of Heart Failure. Int. J. Mol. Sci. 2023, 24, 11470. https://doi.org/10.3390/ijms241411470
Cohen-Segev R, Nativ O, Kinaneh S, Aronson D, Kabala A, Hamoud S, Karram T, Abassi Z. Effects of Angiotensin 1-7 and Mas Receptor Agonist on Renal System in a Rat Model of Heart Failure. International Journal of Molecular Sciences. 2023; 24(14):11470. https://doi.org/10.3390/ijms241411470
Chicago/Turabian StyleCohen-Segev, Ravit, Omri Nativ, Safa Kinaneh, Doron Aronson, Aviva Kabala, Shadi Hamoud, Tony Karram, and Zaid Abassi. 2023. "Effects of Angiotensin 1-7 and Mas Receptor Agonist on Renal System in a Rat Model of Heart Failure" International Journal of Molecular Sciences 24, no. 14: 11470. https://doi.org/10.3390/ijms241411470