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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,
Denise M. R. Silva*,
Raquel Pillar Machado*,
Insa de Buhr,
Silvia Heringer-Walther,
Sergio Veloso B. Pinheiro*,
Myriam Teresa Lopes*,
Michael Bader,
Elizabeth P. Mendes*,
Virgina Soares Lemos*,
Maria Jose Campagnole-Santos*,
Heinz-Peter Schultheiss,
Robert Speth ¶,||, and
Thomas Walther ,**
*Department of Physiology and Biophysics, Federal University of Minas Gerais, Belo Horizonte, 31270, Minas Gerais, Brazil; Department of Medicine, Georgetown University, Washington, DC 20057; 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 inblood pressure control and body fluid and electrolyte homeostasis.Besides angiotensin (Ang) II, other Ang peptides, such as AngIII [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 counteractthose of Ang II. Unique angiotensin-binding sites specificfor 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-coupledreceptor encoded by the Mas protooncogene abolishes the bindingof Ang-(1–7) to mouse kidneys. Accordingly, Mas-deficientmice completely lack the antidiuretic action of Ang-(1–7)after an acute water load. Ang-(1–7) binds to Mas-transfectedcells and elicits arachidonic acid release. Furthermore, Mas-deficientaortas lose their Ang-(1–7)-induced relaxation response.Collectively, these findings identify Mas as a functional receptorfor Ang-(1–7) and provide a clear molecular basis forthe physiological actions of this biologically active peptide.
Key Words: binding • Mas protooncogene • renin angiotensin system
** To whom correspondence should be addressed at: Benjamin FranklinMedical Center, Department of Cardiology and Pneumology, FreeUniversity 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.
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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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,
Denise M. R. Silva*,
Raquel Pillar Machado*,
Insa de Buhr
,
Silvia Heringer-Walther
,
Elizabeth P. Mendes*,
Virgina Soares Lemos*,
Maria Jose Campagnole-Santos*,
Heinz-Peter Schultheiss
