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Vol. 52, Issue 3, 415-472, September 2000

International Union of Pharmacology. XXIII. The Angiotensin II Receptors

M. de Gasparo1, K. J. Catt, T. Inagami, J. W. Wright and Th. Unger

Novartis Pharma AG, Metabolic & Cardiovascular Diseases, Basel, Switzerland (M.d.G.); Endocrinology and Reproduction Research Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland (K.J.C.); Department of Biochemistry, Vanderbilt University, School of Medicine, Nashville, Tennessee (T.I.); Department of Psychology, Washington State University, Pullman, Washington (J.W.W.); Institute of Pharmacology, Christian-Albrechts-University of Kiel Hospitalstrasse 4, Kiel, Germany (Th.U.)

I. Introduction
    A. Historical Background
    B. International Union of Pharmacology Committee on Receptor Nomenclature and Drug Classification Criteria for Classification
    C. Current Nomenclature
    D. Structural Analysis
II. The Type 1 (AT1) Angiotensin Receptor
    A. Angiotensin II Receptors: Early Studies
    B. Cloned AT1 Receptors
    C. Genomic Organization of Rat AT1A and AT1B Receptor Genes
    D. Expression and Regulation of Rat AT1A and AT1B Receptor
    E. The Human AT1 Receptor
        1. AT1 Receptor Gene Polymorphisms and Cardiovascular Disease.
    F. The Amphibian AT1 Receptor
    G. The AT1 Receptor Null Mouse
    H. Structural Basis of Ligand Binding to the AT1 Receptor
        1. Determinants of Ang II Bioactivity.
        2. Agonist Binding Site of the AT1 Receptor.
        3. Antagonist Binding of the AT1 Receptor.
I. AT1 Receptor Signaling Mechanisms
        1. AT1 Receptor Activation and Signal Transduction.
        2. AT1 Receptor and Tyrosine Phosphorylation.
        3. AT1 Receptor-Activated Growth Responses.
        4. Transactivation of Growth Factor Signaling by the AT1 Receptor,
        5. Other AT1 Receptor-Mediated Signaling Pathways.
    J. Receptor Activation and Endocytosis
    K. AT1 Receptor Function in Selected Tissues
        1. The AT1 Receptor and the Brain.
        2. Ang II-Induced Neuronal Signaling Pathways.
        3. Role of Ang III in the Brain.
        4. The AT1 Receptor and the Pituitary Gland.
        5. The AT1 Receptor and the Heart.
III. The Type 2 (AT2) Angiotensin Receptor
    A. Cloning, Purification, and Properties of the AT2 Receptor
    B. Regulation of the AT2 Receptor
    C. AT2 Receptor Diversity
    D. Targeted AT2 Receptor Gene Overexpression and Deletion
        1. Behavioral Changes in AT2 Receptor Null Mice.
    E. Signaling Mechanisms of the AT2 Receptor
        1. Dephosphorylation and Inactivation of the Mitogen-Activated Protein Kinases ERK1 and ERK2.
        2. Activation of Phospholipase A2 and Prostacyclin Generation.
    F. Tissue Distribution of the AT2 Receptor
        1. Brain.
        2. Heart.
        3. Kidney.
        4. Vasculature.
        5. Pancreas, Lung, Thymus, and Other Tissues.
        6. Cells in Primary Culture and Cell Lines Expressing the AT2 Receptor.
    G. Pathophysiological Aspects of AT2 Receptor Activation
        1. The AT2 Receptor Can Induce Apoptosis.
        2. Effects on Vascular Tone.
        3. Vascular Hypertrophy and Fibrosis and the AT2 Receptor.
        4. Renal Tubular Function.
        5. Neuronal Cell Differentiation and Nerve Regeneration.
    H. Summary
IV. The AT4 Receptor
    A. Signaling Mechanisms
    B. Tissue Distribution of the AT4 Receptor
        1. Brain.
        2. Peripheral Tissue.
    C. Development of Agonists and Antagonists
        1. Binding Requirements of AT4 Receptor.
        2. Antagonists of the AT4 Receptor.
    D. Physiology Associated with the AT4 Receptor
        1. Regulation of Blood Flow.
        2. Cardiac Hypertrophy.
        3. Renal Tubular Reabsorption.
        4. Electrophysiological Analysis.
        5. Role of Ang IV in Learning and Memory.
    E. Summary
V. General Conclusions
References

The cardiovascular and other actions of angiotensin II (Ang II) are mediated by AT1 and AT2 receptors, which are seven transmembrane glycoproteins with 30% sequence similarity. Most species express a single autosomal AT1 gene, but two related AT1A and AT1B receptor genes are expressed in rodents. AT1 receptors are predominantly coupled to Gq/11, and signal through phospholipases A, C, D, inositol phosphates, calcium channels, and a variety of serine/threonine and tyrosine kinases. Many AT1-induced growth responses are mediated by transactivation of growth factor receptors. The receptor binding sites for agonist and nonpeptide antagonist ligands have been defined. The latter compounds are as effective as angiotensin converting enzyme inhibitors in cardiovascular diseases but are better tolerated. The AT2 receptor is expressed at high density during fetal development. It is much less abundant in adult tissues and is up-regulated in pathological conditions. Its signaling pathways include serine and tyrosine phosphatases, phospholipase A2, nitric oxide, and cyclic guanosine monophosphate. The AT2 receptor counteracts several of the growth responses initiated by the AT1 and growth factor receptors. The AT4 receptor specifically binds Ang IV (Ang 3-8), and is located in brain and kidney. Its signaling mechanisms are unknown, but it influences local blood flow and is associated with cognitive processes and sensory and motor functions. Although AT1 receptors mediate most of the known actions of Ang II, the AT2 receptor contributes to the regulation of blood pressure and renal function. The development of specific nonpeptide receptor antagonists has led to major advances in the physiology, pharmacology, and therapy of the renin-angiotensin system.

1 Address for correspondence: Marc de Gasparo, Novartis Pharma AG, Metabolic & Cardiovascular Diseases, WKL 121-210, P.O. Box 4200, Basel, Switzerland. E-mail: marc.de_gasparo{at}pharma.Novartis.com and m.de_gasparo{at}bluewin.ch (after October 1, 2000)

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Copyright © 2000 by The American Society for Pharmacology and Experimental Therapeutics


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X. C. Li and J. L. Zhuo
In vivo regulation of AT1a receptor-mediated intracellular uptake of [125I]Val5-ANG II in the kidneys and adrenals of AT1a receptor-deficient mice
Am J Physiol Renal Physiol, February 1, 2008; 294(2): F293 - F302.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Renal Physiol.Home page
R. M. Ortiz
Delineating the contributions of AT1a and AT1b receptor-mediated uptake of ANG II in kidneys and adrenals
Am J Physiol Renal Physiol, February 1, 2008; 294(2): F291 - F292.
[Full Text] [PDF]

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 Cardiovasc ResHome page
Q. Zhang, F. He, R. Kuruba, X. Gao, A. Wilson, J. Li, T. R. Billiar, B. R. Pitt, W. Xie, and S. Li
FXR-mediated regulation of angiotensin type 2 receptor expression in vascular smooth muscle cells
Cardiovasc Res, February 1, 2008; 77(3): 560 - 569.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
H. Choi, T. L. Leto, L. Hunyady, K. J. Catt, Y. S. Bae, and S. G. Rhee
Mechanism of Angiotensin II-induced Superoxide Production in Cells Reconstituted with Angiotensin Type 1 Receptor and the Components of NADPH Oxidase
J. Biol. Chem., January 4, 2008; 283(1): 255 - 267.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
S.-i. Miura, Y. Kiya, T. Kanazawa, S. Imaizumi, M. Fujino, Y. Matsuo, S. S. Karnik, and K. Saku
Differential Bonding Interactions of Inverse Agonists of Angiotensin II Type 1 Receptor in Stabilizing the Inactive State
Mol. Endocrinol., January 1, 2008; 22(1): 139 - 146.
[Abstract] [Full Text] [PDF]

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 Arterioscler. Thromb. Vasc. Bio.Home page
M. Mogi, M. Iwai, and M. Horiuchi
Emerging Concepts of Regulation of Angiotensin II Receptors: New Players and Targets for Traditional Receptors
Arterioscler Thromb Vasc Biol, December 1, 2007; 27(12): 2532 - 2539.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
E. Mendez-Bolaina, J. Sanchez-Gonzalez, I. Ramirez-Sanchez, E. Ocharan-Hernandez, M. Nunez-Sanchez, E. Meaney-Mendiolea, A. Meaney, J. Asbun-Bojalil, A. Miliar-Garcia, I. Olivares-Corichi, et al.
Effect of caveolin-1 scaffolding peptide and 17 -estradiol on intracellular Ca2+ kinetics evoked by angiotensin II in human vascular smooth muscle cells
Am J Physiol Cell Physiol, December 1, 2007; 293(6): C1953 - C1961.
[Abstract] [Full Text] [PDF]

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 Cardiovasc ResHome page
L.-J. Min, M. Mogi, J. Iwanami, J.-M. Li, A. Sakata, T. Fujita, K. Tsukuda, M. Iwai, and M. Horiuchi
Cross-talk between aldosterone and angiotensin II in vascular smooth muscle cell senescence
Cardiovasc Res, December 1, 2007; 76(3): 506 - 516.
[Abstract] [Full Text] [PDF]

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 Nephrol Dial TransplantHome page
J. Li, Y. Doerffel, B. Hocher, and T. Unger
Inflammation in the genesis of hypertension and its complications the role of angiotensin II
Nephrol. Dial. Transplant., November 1, 2007; 22(11): 3107 - 3109.
[Full Text] [PDF]

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 Am. J. Physiol. Heart Circ. Physiol.Home page
D. M. Harris, H. I. Cohn, S. Pesant, R.-H. Zhou, and A. D. Eckhart
Vascular smooth muscle Gq signaling is involved in high blood pressure in both induced renal and genetic vascular smooth muscle-derived models of hypertension
Am J Physiol Heart Circ Physiol, November 1, 2007; 293(5): H3072 - H3079.
[Abstract] [Full Text] [PDF]

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 J. Pharmacol. Exp. Ther.Home page
A. E. Linder, K. M. Thakali, J. M. Thompson, S. W. Watts, R. C. Webb, and R. Leite
Methyl-beta-cyclodextrin Prevents Angiotensin II-Induced Tachyphylactic Contractile Responses in Rat Aorta
J. Pharmacol. Exp. Ther., October 1, 2007; 323(1): 78 - 84.
[Abstract] [Full Text] [PDF]

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 IOVSHome page
N. Nagai, K. Izumi-Nagai, Y. Oike, T. Koto, S. Satofuka, Y. Ozawa, K. Yamashiro, M. Inoue, K. Tsubota, K. Umezawa, et al.
Suppression of Diabetes-Induced Retinal Inflammation by Blocking the Angiotensin II Type 1 Receptor or Its Downstream Nuclear Factor-{kappa}B Pathway
Invest. Ophthalmol. Vis. Sci., September 1, 2007; 48(9): 4342 - 4350.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
M. M. Martin, J. A. Buckenberger, J. Jiang, G. E. Malana, D. L. Knoell, D. S. Feldman, and T. S. Elton
TGF-beta1 stimulates human AT1 receptor expression in lung fibroblasts by cross talk between the Smad, p38 MAPK, JNK, and PI3K signaling pathways
Am J Physiol Lung Cell Mol Physiol, September 1, 2007; 293(3): L790 - L799.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
K. Wosik, R. Cayrol, A. Dodelet-Devillers, F. Berthelet, M. Bernard, R. Moumdjian, A. Bouthillier, T. L. Reudelhuber, and A. Prat
Angiotensin II Controls Occludin Function and Is Required for Blood Brain Barrier Maintenance: Relevance to Multiple Sclerosis
J. Neurosci., August 22, 2007; 27(34): 9032 - 9042.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
M. M. Martin, J. A. Buckenberger, J. Jiang, G. E. Malana, G. J. Nuovo, M. Chotani, D. S. Feldman, T. D. Schmittgen, and T. S. Elton
The Human Angiotensin II Type 1 Receptor +1166 A/C Polymorphism Attenuates MicroRNA-155 Binding
J. Biol. Chem., August 17, 2007; 282(33): 24262 - 24269.
[Abstract] [Full Text] [PDF]

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 J. Physiol.Home page
M. S. Carneiro-Ramos, G. P. Diniz, J. Almeida, R. L. P. Vieira, S. V. B. Pinheiro, R. A. Santos, and M. L. M. Barreto-Chaves
Cardiac angiotensin II type I and type II receptors are increased in rats submitted to experimental hypothyroidism
J. Physiol., August 15, 2007; 583(1): 213 - 223.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Renal Physiol.Home page
X. C. Li, L. G. Navar, Y. Shao, and J. L. Zhuo
Genetic deletion of AT1a receptors attenuates intracellular accumulation of ANG II in the kidney of AT1a receptor-deficient mice
Am J Physiol Renal Physiol, August 1, 2007; 293(2): F586 - F593.
[Abstract] [Full Text] [PDF]

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 IOVSHome page
P. deS. Senanayake, J. Drazba, K. Shadrach, A. Milsted, E. Rungger-Brandle, K. Nishiyama, S.-I. Miura, S. Karnik, J. E. Sears, and J. G. Hollyfield
Angiotensin II and Its Receptor Subtypes in the Human Retina
Invest. Ophthalmol. Vis. Sci., July 1, 2007; 48(7): 3301 - 3311.
[Abstract] [Full Text] [PDF]

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 Mol. Pharmacol.Home page
S. S. Martin, B. J. Holleran, E. Escher, G. Guillemette, and R. Leduc
Activation of the Angiotensin II Type 1 Receptor Leads to Movement of the Sixth Transmembrane Domain: Analysis by the Substituted Cysteine Accessibility Method
Mol. Pharmacol., July 1, 2007; 72(1): 182 - 190.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
X. C. Li and J. L. Zhuo
Selective knockdown of AT1 receptors by RNA interference inhibits Val5-ANG II endocytosis and NHE-3 expression in immortalized rabbit proximal tubule cells
Am J Physiol Cell Physiol, July 1, 2007; 293(1): C367 - C378.
[Abstract] [Full Text] [PDF]

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 J. Physiol.Home page
T. Slowinski, P. Kalk, M. Christian, F. Schmager, K. Relle, M. Godes, H. Funke-Kaiser, H.-H. Neumayer, C. Bauer, F. Theuring, et al.
Cell-type specific interaction of endothelin and the nitric oxide system: pattern of prepro-ET-1 expression in kidneys of L-NAME treated prepro-ET-1 promoter-lacZ-transgenic mice
J. Physiol., June 15, 2007; 581(3): 1173 - 1181.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
J. Li, X. Zhao, X. Li, K. M. Lerea, and S. C. Olson
Angiotensin II type 2 receptor-dependent increases in nitric oxide synthase expression in the pulmonary endothelium is mediated via a G{alpha}i3/Ras/Raf/MAPK pathway
Am J Physiol Cell Physiol, June 1, 2007; 292(6): C2185 - C2196.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Heart Circ. Physiol.Home page
M. Yusof, K. Kamada, F. Spencer Gaskin, and R. J. Korthuis
Angiotensin II mediates postischemic leukocyte-endothelial interactions: role of calcitonin gene-related peptide
Am J Physiol Heart Circ Physiol, June 1, 2007; 292(6): H3032 - H3037.
[Abstract] [Full Text] [PDF]

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 Am. J. Pathol.Home page
K. Suzuki, G. D. Han, N. Miyauchi, T. Hashimoto, T. Nakatsue, Y. Fujioka, H. Koike, F. Shimizu, and H. Kawachi
Angiotensin II Type 1 and Type 2 Receptors Play Opposite Roles in Regulating the Barrier Function of Kidney Glomerular Capillary Wall
Am. J. Pathol., June 1, 2007; 170(6): 1841 - 1853.
[Abstract] [Full Text] [PDF]

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 HypertensionHome page
X. Yu, K. Murao, H. Imachi, W.-M. Cao, J. Li, K. Matsumoto, T. Nishiuchi, R. A.M. Ahmed, N. C.W. Wong, H. Kosaka, et al.
Regulation of Scavenger Receptor Class BI Gene Expression by Angiotensin II in Vascular Endothelial Cells
Hypertension, June 1, 2007; 49(6): 1378 - 1384.
[Abstract] [Full Text] [PDF]

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 HypertensionHome page
R. J. Kokje, W. L. Wilson, T. E. Brown, V. T. Karamyan, J. W. Wright, and R. C. Speth
Central Pressor Actions of Aminopeptidase-Resistant Angiotensin II Analogs: Challenging the Angiotensin III Hypothesis
Hypertension, June 1, 2007; 49(6): 1328 - 1335.
[Abstract] [Full Text] [PDF]

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 IOVSHome page
N. Nagai, Y. Oike, K. Izumi-Nagai, T. Koto, S. Satofuka, H. Shinoda, K. Noda, Y. Ozawa, M. Inoue, K. Tsubota, et al.
Suppression of Choroidal Neovascularization by Inhibiting Angiotensin-Converting Enzyme: Minimal Role of Bradykinin
Invest. Ophthalmol. Vis. Sci., May 1, 2007; 48(5): 2321 - 2326.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
G. Chipitsyna, Q. Gong, C. F. Gray, Y. Haroon, E. Kamer, and H. A. Arafat
Induction of Monocyte Chemoattractant Protein-1 Expression by Angiotensin II in the Pancreatic Islets and {beta}-Cells
Endocrinology, May 1, 2007; 148(5): 2198 - 2208.
[Abstract] [Full Text] [PDF]

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 Exp PhysiolHome page
D. Daniels, D. K. Yee, and S. J. Fluharty
Hydromineral Neuroendocrinology: Angiotensin II receptor signalling
Exp Physiol, May 1, 2007; 92(3): 523 - 527.
[Abstract] [Full Text] [PDF]

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 HypertensionHome page
T. S. Elton and M. M. Martin
Angiotensin II Type 1 Receptor Gene Regulation: Transcriptional and Posttranscriptional Mechanisms
Hypertension, May 1, 2007; 49(5): 953 - 961.
[Full Text] [PDF]

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 HypertensionHome page
V. C. Munk, L. Sanchez de Miguel, M. Petrimpol, N. Butz, A. Banfi, U. Eriksson, L. Hein, R. Humar, and E. J. Battegay
Angiotensin II Induces Angiogenesis in the Hypoxic Adult Mouse Heart In Vitro Through an AT2-B2 Receptor Pathway
Hypertension, May 1, 2007; 49(5): 1178 - 1185.
[Abstract] [Full Text] [PDF]

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 Physiol. Rev.Home page
L. Oliveira, C. M. Costa-Neto, C. R. Nakaie, S. Schreier, S. I. Shimuta, and A. C. M. Paiva
The Angiotensin II AT1 Receptor Structure-Activity Correlations in the Light of Rhodopsin Structure
Physiol Rev, April 1, 2007; 87(2): 565 - 592.
[Abstract] [Full Text] [PDF]

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 J. Physiol.Home page
P. S. Leung
The physiology of a local renin-angiotensin system in the pancreas
J. Physiol., April 1, 2007; 580(1): 31 - 37.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
J. L. Cook, S. J. Mills, R. T. Naquin, J. Alam, and R. N. Re
Cleavage of the angiotensin II type 1 receptor and nuclear accumulation of the cytoplasmic carboxy-terminal fragment
Am J Physiol Cell Physiol, April 1, 2007; 292(4): C1313 - C1322.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
T. A. Morinelli, J. R. Raymond, A. Baldys, Q. Yang, M.-h. Lee, L. Luttrell, and M. E. Ullian
Identification of a putative nuclear localization sequence within ANG II AT1A receptor associated with nuclear activation
Am J Physiol Cell Physiol, April 1, 2007; 292(4): C1398 - C1408.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Heart Circ. Physiol.Home page
A. H. Siddiqui and T. Hussain
Enhanced AT1 receptor-mediated vasocontractile response to ANG II in endothelium-denuded aorta of obese Zucker rats
Am J Physiol Heart Circ Physiol, April 1, 2007; 292(4): H1722 - H1727.
[Abstract] [Full Text] [PDF]

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 Circ. Res.Home page
A. M. Nuyt and M. Szyf
Developmental Programming Through Epigenetic Changes
Circ. Res., March 2, 2007; 100(4): 452 - 455.
[Full Text] [PDF]

Home page
 Journal of Renin-Angiotensin-Aldosterone SystemHome page
J. L Zhuo and X. C Li
Review: Novel roles of intracrine angiotensin II and signalling mechanisms in kidney cells
Journal of Renin-Angiotensin-Aldosterone System, March 1, 2007; 8(1): 23 - 33.
[Abstract] [PDF]

Home page
 Arterioscler. Thromb. Vasc. Bio.Home page
V. Jankowski, R. Vanholder, M. van der Giet, M. Tolle, S. Karadogan, J. Gobom, J. Furkert, A. Oksche, E. Krause, T. N. Anh Tran, et al.
Mass-Spectrometric Identification of a Novel Angiotensin Peptide in Human Plasma
Arterioscler Thromb Vasc Biol, February 1, 2007; 27(2): 297 - 302.
[Abstract] [Full Text] [PDF]


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