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PNAS 100 (14): 8258-8263

Copyright © 2003 by the National Academy of Sciences.

BIOLOGICAL SCIENCES / CELL BIOLOGY

Angiotensin-(1–7) is an endogenous ligand for the G protein-coupled receptor Mas

Robson A. S. Santos*, Ana C. Simoes e Silva*, Christine Maric{dagger}, Denise M. R. Silva*, Raquel Pillar Machado*, Insa de Buhr{ddagger}, Silvia Heringer-Walther{ddagger}, Sergio Veloso B. Pinheiro*, Myriam Teresa Lopes*, Michael Bader§, Elizabeth P. Mendes*, Virgina Soares Lemos*, Maria Jose Campagnole-Santos*, Heinz-Peter Schultheiss{ddagger}, Robert Speth ,||, and Thomas Walther {ddagger},**

*Department of Physiology and Biophysics, Federal University of Minas Gerais, Belo Horizonte, 31270, Minas Gerais, Brazil; {dagger}Department of Medicine, Georgetown University, Washington, DC 20057; {ddagger}Department of Cardiology and Pneumology, University Hospital Benjamin Franklin, Free University, 12200 Berlin, Germany; §Max Delbrück Center, 13125 Berlin, Germany; and Department of Veterinary and Comparative Anatomy, Pharmacology, and Physiology, Washington State University, Pullman, WA 99164-6520

Accepted for publication May 13, 2003.

Received for publication July 30, 2002.

Abstract: The renin–angiotensin system plays a critical role in blood pressure control and body fluid and electrolyte homeostasis. Besides angiotensin (Ang) II, other Ang peptides, such as Ang III [Ang-(2–8)], Ang IV [Ang-(3–8)], and Ang-(1–7) may also have important biological activities. Ang-(1–7) has become an angiotensin of interest in the past few years, because its cardiovascular and baroreflex actions counteract those of Ang II. Unique angiotensin-binding sites specific for this heptapeptide and studies with a selective Ang-(1–7) antagonist indicated the existence of a distinct Ang-(1–7) receptor. We demonstrate that genetic deletion of the G protein-coupled receptor encoded by the Mas protooncogene abolishes the binding of Ang-(1–7) to mouse kidneys. Accordingly, Mas-deficient mice completely lack the antidiuretic action of Ang-(1–7) after an acute water load. Ang-(1–7) binds to Mas-transfected cells and elicits arachidonic acid release. Furthermore, Mas-deficient aortas lose their Ang-(1–7)-induced relaxation response. Collectively, these findings identify Mas as a functional receptor for Ang-(1–7) and provide a clear molecular basis for the physiological actions of this biologically active peptide.

Key Words: binding • Mas protooncogene • renin angiotensin system

** To whom correspondence should be addressed at: Benjamin Franklin Medical Center, Department of Cardiology and Pneumology, Free University of Berlin, Hindenburgdamm 30, 12200 Berlin, Germany. E-mail: thomas.walther{at}ukbf.fu-berlin.de.

|| Present address: Department of Pharmacology, School of Pharmacy, University of Mississippi, University, MS 38677-1848.

Edited by Richard P. Lifton, Yale University School of Medicine, New Haven, CT

This paper was submitted directly (Track II) to the PNAS office.

Abbreviations: Ang, angiotensin; AVP, arginine-vasopressin; AA, arachidonic acid; CHO, Chinese hamster ovary.

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Inhibitory effects of angiotensin-(1-7) on the nerve stimulation-induced release of norepinephrine and neuropeptide Y from the mesenteric arterial bed.
M. Byku, H. Macarthur, and T. C. Westfall (2010)
Am J Physiol Heart Circ Physiol 298, H457-H465
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Therapeutic Implications of the Vasoprotective Axis of the Renin-Angiotensin System in Cardiovascular Diseases.
A. J. Ferreira, R. A.S. Santos, C. N. Bradford, A. P. Mecca, C. Sumners, M. J. Katovich, and M. K. Raizada (2010)
Hypertension 55, 207-213
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Effects of Angiotensin Metabolites in the Coronary Vascular Bed of the Spontaneously Hypertensive Rat: Loss of Angiotensin II Type 2 Receptor-Mediated Vasodilation.
E. Moltzer, A. V. A. Verkuil, R. van Veghel, A. H. J. Danser, and J. H. M. van Esch (2010)
Hypertension 55, 516-522
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New Physiological Concepts of the Renin-Angiotensin System From the Investigation of Precursors and Products of Angiotensin I Metabolism.
C. M. Ferrario (2010)
Hypertension 55, 445-452
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Targeting the Degradation of Angiotensin II With Recombinant Angiotensin-Converting Enzyme 2: Prevention of Angiotensin II-Dependent Hypertension.
J. Wysocki, M. Ye, E. Rodriguez, F. R. Gonzalez-Pacheco, C. Barrios, K. Evora, M. Schuster, H. Loibner, K. B. Brosnihan, C. M. Ferrario, et al. (2010)
Hypertension 55, 90-98
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Angiotensin II reduces membranous angiotensin-converting enzyme 2 in pressurized human aortic endothelial cells.
K. Iizuka, A. Kusunoki, T. Machida, and M. Hirafuji (2009)
Journal of Renin-Angiotensin-Aldosterone System 10, 210-215
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Gonadotropin Stimulation Increases the Expression of Angiotensin-(1--7) and Mas Receptor in the Rat Ovary.
V. M. Pereira, F. M. Reis, R. A. S. Santos, G. D. Cassali, S. H. S. Santos, K. Honorato-Sampaio, and A. M. dos Reis (2009)
Reproductive Sciences 16, 1165-1174
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Phase I and Pharmacokinetic Study of Angiotensin-(1-7), an Endogenous Antiangiogenic Hormone.
W. J. Petty, A. A. Miller, T. P. McCoy, P. E. Gallagher, E. A. Tallant, and F. M. Torti (2009)
Clin. Cancer Res. 15, 7398-7404
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Angiotensin-(1-7) activates a tyrosine phosphatase and inhibits glucose-induced signalling in proximal tubular cells.
E. Gava, A. Samad-Zadeh, J. Zimpelmann, N. Bahramifarid, G. T. Kitten, R. A. Santos, R. M. Touyz, and K. D. Burns (2009)
Nephrol. Dial. Transplant. 24, 1766-1773
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Angiotensin-(1-7) inhibits tumor angiogenesis in human lung cancer xenografts with a reduction in vascular endothelial growth factor.
D. R. Soto-Pantoja, J. Menon, P. E. Gallagher, and E. A. Tallant (2009)
Mol. Cancer Ther. 8, 1676-1683
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Apelin decreases myocardial injury and improves right ventricular function in monocrotaline-induced pulmonary hypertension.
I. Falcao-Pires, N. Goncalves, T. Henriques-Coelho, D. Moreira-Goncalves, R. Roncon-Albuquerque Jr., and A. F. Leite-Moreira (2009)
Am J Physiol Heart Circ Physiol 296, H2007-H2014
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Angiotensin I Is Largely Converted to Angiotensin (1-7) and Angiotensin (2-10) by Isolated Rat Glomeruli.
J. C. Q. Velez, K. J. Ryan, C. E. Harbeson, A. M. Bland, M. N. Budisavljevic, J. M. Arthur, W. R. Fitzgibbon, J. R. Raymond, and M. G. Janech (2009)
Hypertension 53, 790-797
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Differential regulation of angiotensin-(1-12) in plasma and cardiac tissue in response to bilateral nephrectomy.
C. M. Ferrario, J. Varagic, J. Habibi, S. Nagata, J. Kato, M. C. Chappell, A. J. Trask, K. Kitamura, A. Whaley-Connell, and J. R. Sowers (2009)
Am J Physiol Heart Circ Physiol 296, H1184-H1192
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Angiotensin-(1-7) with Thioether Bridge: An Angiotensin-Converting Enzyme-Resistant, Potent Angiotensin-(1-7) Analog.
L. D. Kluskens, S. A. Nelemans, R. Rink, L. de Vries, A. Meter-Arkema, Y. Wang, T. Walther, A. Kuipers, G. N. Moll, and M. Haas (2009)
J. Pharmacol. Exp. Ther. 328, 849-854
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The Vasoactive Peptide Angiotensin-(1--7), Its Receptor Mas and the Angiotensin-converting Enzyme Type 2 are Expressed in the Human Endometrium.
J. Vaz-Silva, M.M. Carneiro, M.C. Ferreira, S.V.B. Pinheiro, D.A. Silva, A.L. Silva Filho, C.A. Witz, A.M. Reis, R.A. Santos, and F.M. Reis (2009)
Reproductive Sciences 16, 247-256
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Gender differences in the effects of antenatal betamethasone exposure on renal function in adult sheep.
L. Tang, L. C. Carey, J. Bi, N. Valego, X. Sun, P. Deibel, J. Perrott, J. P. Figueroa, M. C. Chappell, and J. C. Rose (2009)
Am J Physiol Regulatory Integrative Comp Physiol 296, R309-R317
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Angiotensin-(1-7) activates growth-stimulatory pathways in human mesangial cells.
J. Zimpelmann and K. D. Burns (2009)
Am J Physiol Renal Physiol 296, F337-F346
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Angiotensin II Type 1 Receptor-Mediated Reduction of Angiotensin-Converting Enzyme 2 Activity in the Brain Impairs Baroreflex Function in Hypertensive Mice.
H. Xia, Y. Feng, T. D. Obr, P. J. Hickman, and E. Lazartigues (2009)
Hypertension 53, 210-216
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Discovery and Validation of Novel Peptide Agonists for G-protein-coupled Receptors.
R. Shemesh, A. Toporik, Z. Levine, I. Hecht, G. Rotman, A. Wool, D. Dahary, E. Gofer, Y. Kliger, M. A. Soffer, et al. (2008)
J. Biol. Chem. 283, 34643-34649
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Renin-angiotensin system-related highlights from the High Blood Pressure Research Conference annual meeting.
F. C Luft (2008)
Journal of Renin-Angiotensin-Aldosterone System 9, 242-247
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Transgenic Angiotensin-Converting Enzyme 2 Overexpression in Vessels of SHRSP Rats Reduces Blood Pressure and Improves Endothelial Function.
B. Rentzsch, M. Todiras, R. Iliescu, E. Popova, L. A. Campos, M. L. Oliveira, O. C. Baltatu, R. A. Santos, and M. Bader (2008)
Hypertension 52, 967-973
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