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Circulation Research. 2001;88:947-953
Published online before print April 27, 2001, doi: 10.1161/hh0901.089987
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(Circulation Research. 2001;88:947.)
© 2001 American Heart Association, Inc.

Integrative Physiology

Role of NADPH Oxidase in the Vascular Hypertrophic and Oxidative Stress Response to Angiotensin II in Mice

Hui Di Wang, Shanqin Xu, Douglas G. Johns, Yue Du, Mark T. Quinn, Antonio J. Cayatte, Richard A. Cohen

From the Vascular Biology Unit (H.D.W., S.X., D.G.J., Y.D., A.J.C., R.A.C.), Whitaker Cardiovascular Institute, Department of Medicine, Boston University Medical Center, Boston, Mass, and Department of Veterinary Biology (M.T.Q.), Montana State University, Bozeman, Mont.

Correspondence to Richard A. Cohen, MD, Vascular Biology Unit, X708, Boston University School of Medicine, 650 Albany St, Boston, MA 02118. E-mail racohen{at}medicine.bu.edu

Abstract—Oxygen-derived free radicals are involved in the vascular response to angiotensin II (Ang II), but the role of NADPH oxidase, its subunit proteins, and their vascular localization remain controversial. Our purpose was to address the role of NADPH oxidase in the blood pressure (BP), aortic hypertrophic, and oxidant responses to Ang II by taking advantage of knockout (KO) mice that are genetically deficient in gp91phox, an NADPH oxidase subunit protein. The baseline BP was significantly lower in KO mice than in wild-type (WT) (92±2 [KO] versus 101±1 [WT] mm Hg, P<0.01), but infusion of Ang II for 6 days caused similar increases in BP in the 2 strains (33±4 [KO] versus 38±2 [WT] mm Hg, P>0.4). Ang II increased aortic superoxide anion production 2-fold in the aorta of WT mice but did not do so in KO mice. Aortic medial area increased in WT (0.12±0.02 to 0.17±0.02 mm2, P<0.05), but did not do so in KO mice (0.10±0.01 to 0.11±0.01 mm2, P>0.05). Histochemistry and polymerase chain reaction demonstrated gp91phox localized in endothelium and adventitia of WT mice. Levels of reactive oxidant species as indicated by 3-nitrotyrosine immunoreactivity increased in these regions in WT but not in KO mouse aorta in response to Ang II. These results indicate an essential role in vivo of gp91phox and NADPH oxidase–derived superoxide anion in the regulation of basal BP and a pressure-independent vascular hypertrophic and oxidant stress response to Ang II.


Key Words: angiotensin II • superoxide anion • 3-nitrotyrosine • gp91phox • NADPH oxidase




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 Am. J. Physiol. Heart Circ. Physiol.Home page
W. Guo, T. Adachi, R. Matsui, S. Xu, B. Jiang, M.-H. Zou, M. Kirber, W. Lieberthal, and R. A. Cohen
Quantitative assessment of tyrosine nitration of manganese superoxide dismutase in angiotensin II-infused rat kidney
Am J Physiol Heart Circ Physiol, October 1, 2003; 285(4): H1396 - H1403.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
B. Lassegue and R. E. Clempus
Vascular NAD(P)H oxidases: specific features, expression, and regulation
Am J Physiol Regulatory Integrative Comp Physiol, August 1, 2003; 285(2): R277 - R297.
[Abstract] [Full Text] [PDF]

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 HypertensionHome page
J. R. Privratsky, L. E. Wold, J. R. Sowers, M. T. Quinn, and J. Ren
AT1 Blockade Prevents Glucose-Induced Cardiac Dysfunction in Ventricular Myocytes: Role of the AT1 Receptor and NADPH Oxidase
Hypertension, August 1, 2003; 42(2): 206 - 212.
[Abstract] [Full Text] [PDF]

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 J Am Coll CardiolHome page
C. Heymes, J. K. Bendall, P. Ratajczak, A. C. Cave, J.-L. Samuel, G. Hasenfuss, and A. M. Shah
Increased myocardial NADPH oxidase activity in human heart failure
J. Am. Coll. Cardiol., June 18, 2003; 41(12): 2164 - 2171.
[Abstract] [Full Text] [PDF]

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 Arterioscler. Thromb. Vasc. Bio.Home page
M. E. Cifuentes and P. J. Pagano
c-Src and Smooth Muscle NAD(P)H Oxidase: Assembling a Path to Hypertrophy
Arterioscler. Thromb. Vasc. Biol., June 1, 2003; 23(6): 919 - 921.
[Full Text] [PDF]

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 Arterioscler. Thromb. Vasc. Bio.Home page
J. Liu, F. Yang, X.-P. Yang, M. Jankowski, and P. J. Pagano
NAD(P)H Oxidase Mediates Angiotensin II-Induced Vascular Macrophage Infiltration and Medial Hypertrophy
Arterioscler. Thromb. Vasc. Biol., May 1, 2003; 23(5): 776 - 782.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Heart Circ. Physiol.Home page
C. Rugale, S. Delbosc, J.-P. Cristol, A. Mimran, and B. Jover
Sodium restriction prevents cardiac hypertrophy and oxidative stress in angiotensin II hypertension
Am J Physiol Heart Circ Physiol, May 1, 2003; 284(5): H1744 - H1750.
[Abstract] [Full Text] [PDF]

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 Circ. Res.Home page
R. P. Brandes
A Radical Adventure: The Quest for Specific Functions and Inhibitors of Vascular NAPDH Oxidases
Circ. Res., April 4, 2003; 92(6): 583 - 585.
[Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
A. Avogaro, E. Pagnin, and L. Calo
Monocyte NADPH Oxidase Subunit p22phox and Inducible Hemeoxygenase-1 Gene Expressions Are Increased in Type II Diabetic Patients: Relationship with Oxidative Stress
J. Clin. Endocrinol. Metab., April 1, 2003; 88(4): 1753 - 1759.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
J.-M. Li and A. M. Shah
Mechanism of Endothelial Cell NADPH Oxidase Activation by Angiotensin II. ROLE OF THE p47phox SUBUNIT
J. Biol. Chem., March 28, 2003; 278(14): 12094 - 12100.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
U. Laufs, O. Adam, K. Strehlow, S. Wassmann, C. Konkol, K. Laufs, W. Schmidt, M. Bohm, and G. Nickenig
Down-regulation of Rac-1 GTPase by Estrogen
J. Biol. Chem., February 14, 2003; 278(8): 5956 - 5962.
[Abstract] [Full Text] [PDF]

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 Pharmacol. Rev.Home page
I. V. Turko and F. Murad
Protein Nitration in Cardiovascular Diseases
Pharmacol. Rev., December 1, 2002; 54(4): 619 - 634.
[Abstract] [Full Text] [PDF]

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 Arterioscler. Thromb. Vasc. Bio.Home page
F. E. Rey and P. J. Pagano
The Reactive Adventitia: Fibroblast Oxidase in Vascular Function
Arterioscler. Thromb. Vasc. Biol., December 1, 2002; 22(12): 1962 - 1971.
[Abstract] [Full Text] [PDF]

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 Arterioscler. Thromb. Vasc. Bio.Home page
N. Kalinina, A. Agrotis, E. Tararak, Y. Antropova, P. Kanellakis, O. Ilyinskaya, M. T. Quinn, V. Smirnov, and A. Bobik
Cytochrome b558-Dependent NAD(P)H Oxidase-Phox Units in Smooth Muscle and Macrophages of Atherosclerotic Lesions
Arterioscler. Thromb. Vasc. Biol., December 1, 2002; 22(12): 2037 - 2043.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
D. M. Tham, B. Martin-McNulty, Y.-X. Wang, V. Da Cunha, D. W. Wilson, C. N. Athanassious, A. F. Powers, M. E. Sullivan, and J. C. Rutledge
Angiotensin II injures the arterial wall causing increased aortic stiffening in apolipoprotein E-deficient mice
Am J Physiol Regulatory Integrative Comp Physiol, December 1, 2002; 283(6): R1442 - R1449.
[Abstract] [Full Text] [PDF]

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 CirculationHome page
F. E. Rey, X.-C. Li, O. A. Carretero, J. L. Garvin, and P. J. Pagano
Perivascular Superoxide Anion Contributes to Impairment of Endothelium-Dependent Relaxation: Role of gp91phox
Circulation, November 5, 2002; 106(19): 2497 - 2502.
[Abstract] [Full Text] [PDF]

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 Arterioscler. Thromb. Vasc. Bio.Home page
U. Rueckschloss, M. T. Quinn, J. Holtz, and H. Morawietz
Dose-Dependent Regulation of NAD(P)H Oxidase Expression by Angiotensin II in Human Endothelial Cells: Protective Effect of Angiotensin II Type 1 Receptor Blockade in Patients With Coronary Artery Disease
Arterioscler. Thromb. Vasc. Biol., November 1, 2002; 22(11): 1845 - 1851.
[Abstract] [Full Text] [PDF]

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 HypertensionHome page
S. Delbosc, J.-P. Cristol, B. Descomps, A. Mimran, and B. Jover
Simvastatin Prevents Angiotensin II-Induced Cardiac Alteration and Oxidative Stress
Hypertension, August 1, 2002; 40(2): 142 - 147.
[Abstract] [Full Text] [PDF]

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 Circ. Res.Home page
C. Vecchione and R. P. Brandes
Withdrawal of 3-Hydroxy-3-Methylglutaryl Coenzyme A Reductase Inhibitors Elicits Oxidative Stress and Induces Endothelial Dysfunction in Mice
Circ. Res., July 26, 2002; 91(2): 173 - 179.
[Abstract] [Full Text] [PDF]

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 Circ. Res.Home page
R. M. Touyz, X. Chen, F. Tabet, G. Yao, G. He, M. T. Quinn, P. J. Pagano, and E. L. Schiffrin
Expression of a Functionally Active gp91phox-Containing Neutrophil-Type NAD(P)H Oxidase in Smooth Muscle Cells From Human Resistance Arteries: Regulation by Angiotensin II
Circ. Res., June 14, 2002; 90(11): 1205 - 1213.
[Abstract] [Full Text] [PDF]

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 Circ. Res.Home page
T. Adachi, R. Matsui, S. Xu, M. Kirber, H. L. Lazar, V. S. Sharov, C. Schoneich, and R. A. Cohen
Antioxidant Improves Smooth Muscle Sarco/Endoplasmic Reticulum Ca2+-ATPase Function and Lowers Tyrosine Nitration in Hypercholesterolemia and Improves Nitric Oxide-Induced Relaxation
Circ. Res., May 31, 2002; 90(10): 1114 - 1121.
[Abstract] [Full Text] [PDF]

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 J. Leukoc. Biol.Home page
K. A. Gauss, P. L. Mascolo, D. W. Siemsen, L. K. Nelson, P. L. Bunger, P. J. Pagano, and M. T. Quinn
Cloning and sequencing of rabbit leukocyte NADPH oxidase genes reveals a unique p67phox homolog
J. Leukoc. Biol., February 1, 2002; 71(2): 319 - 328.
[Abstract] [Full Text] [PDF]

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 Eur Heart J SupplHome page
R. Ferrari, G. Guardigli, G. Cicchitelli, M. Valgimigli, E. Merli, O. Soukhomorskaia, and C. Ceconi
Angiotensin II overproduction: enemy of the vessel wall
Eur. Heart J. Suppl., February 1, 2002; 4(suppl_A): A26 - A30.
[Abstract] [PDF]

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 CirculationHome page
J. K. Bendall, A. C. Cave, C. Heymes, N. Gall, and A. M. Shah
Pivotal Role of a gp91phox-Containing NADPH Oxidase in Angiotensin II-Induced Cardiac Hypertrophy in Mice
Circulation, January 22, 2002; 105(3): 293 - 296.
[Abstract] [Full Text] [PDF]

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 HypertensionHome page
M. Ruiz-Ortega, O. Lorenzo, M. Ruperez, V. Esteban, Y. Suzuki, S. Mezzano, J.J. Plaza, and J. Egido
Role of the Renin-Angiotensin System in Vascular Diseases: Expanding the Field
Hypertension, December 1, 2001; 38(6): 1382 - 1387.
[Abstract] [Full Text] [PDF]

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 Arterioscler. Thromb. Vasc. Bio.Home page
A. J. Cayatte, A. Rupin, J. Oliver-Krasinski, K. Maitland, P. Sansilvestri-Morel, M.-F. Boussard, M. Wierzbicki, T. J. Verbeuren, and R. A. Cohen
S17834, a New Inhibitor of Cell Adhesion and Atherosclerosis That Targets NADPH Oxidase
Arterioscler. Thromb. Vasc. Biol., October 1, 2001; 21(10): 1577 - 1584.
[Abstract] [Full Text] [PDF]

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 Circ. Res.Home page
K. Irani
Angiotensin II-Stimulated Vascular Remodeling : The Search for the Culprit Oxidase
Circ. Res., May 11, 2001; 88(9): 858 - 860.
[Full Text] [PDF]

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 Am. J. Physiol. Heart Circ. Physiol.Home page
H. D. Wang, D. G. Johns, S. Xu, and R. A. Cohen
Role of superoxide anion in regulating pressor and vascular hypertrophic response to angiotensin II
Am J Physiol Heart Circ Physiol, May 1, 2002; 282(5): H1697 - H1702.
[Abstract] [Full Text] [PDF]

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 CirculationHome page
D. Sorescu, D. Weiss, B. Lassegue, R. E. Clempus, K. Szocs, G. P. Sorescu, L. Valppu, M. T. Quinn, J. D. Lambeth, J. D. Vega, et al.
Superoxide Production and Expression of Nox Family Proteins in Human Atherosclerosis
Circulation, March 26, 2002; 105(12): 1429 - 1435.
[Abstract] [Full Text] [PDF]


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