Circulation Research. 2001;88:888-894
Published online before print April 27, 2001, doi: 10.1161/hh0901.090299
Published online before print April 27, 2001, doi: 10.1161/hh0901.090299
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© 2001 American Heart Association, Inc.
Molecular Medicine |
Novel gp91phox Homologues in Vascular Smooth Muscle Cells
nox1 Mediates Angiotensin II–Induced Superoxide Formation and Redox-Sensitive Signaling Pathways
From the Department of Medicine, Division of Cardiology (B.L., D.S., K.S., Q.Q.Y., M.A., Y.Z., S.L.G., K.K.G.) and Department of Biochemistry (J.D.L.), Emory University, Atlanta, Ga.
Correspondence to Bernard Lassègue, Emory University, Division of Cardiology, 1639 Pierce Dr, 319 WMB, Atlanta, GA 30322. E-mail medbpl{at}emory.edu
Abstract—Emerging evidence indicates that reactive oxygen species are important regulators of vascular function. Although NAD(P)H oxidases have been implicated as major sources of superoxide in the vessel wall, the molecular identity of these proteins remains unclear. We recently cloned nox1 (formerly mox-1), a member of a new family of gp91phox homologues, and showed that it is expressed in proliferating vascular smooth muscle cells (VSMCs). In this study, we examined the expression of three nox family members, nox1, nox4, and gp91phox, in VSMCs, their regulation by angiotensin II (Ang II), and their role in redox-sensitive signaling. We found that both nox1 and nox4 are expressed to a much higher degree than gp91phox in VSMCs. Although serum, platelet-derived growth factor (PDGF), and Ang II downregulated nox4, they markedly upregulated nox1, suggesting that this enzyme may account for the delayed phase of superoxide production in these cells. Furthermore, an adenovirus expressing antisense nox1 mRNA completely inhibited the early phase of superoxide production induced by Ang II or PDGF and significantly decreased activation of the redox-sensitive signaling molecules p38 mitogen-activated protein kinase and Akt by Ang II. In contrast, redox-independent pathways induced by PDGF or Ang II were unaffected. These data support a role for nox1 in redox signaling in VSMCs and provide insight into the molecular identity of the VSMC NAD(P)H oxidase and its potentially critical role in vascular disease.
Key Words: nox1 • nox4 • superoxide • angiotensin II • vascular smooth muscle
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|
|
|
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|
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|
|
|
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|
|
|
|
|
|
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|
|
|
|
 |
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
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|
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|
|
|
|
|
|
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|
|
|
|
 |
|
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|
|
|
|
|
|
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|
|
|
|
 |
|
 A. N. Lyle and K. K. Griendling Modulation of vascular smooth muscle signaling by reactive oxygen species. Physiology, August 1, 2006; 21: 269 - 280. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. E. Murdoch, M. Zhang, A. C. Cave, and A. M. Shah NADPH oxidase-dependent redox signalling in cardiac hypertrophy, remodelling and failure Cardiovasc Res, July 15, 2006; 71(2): 208 - 215. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. E. Clempus and K. K. Griendling Reactive oxygen species signaling in vascular smooth muscle cells Cardiovasc Res, July 15, 2006; 71(2): 216 - 225. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. M. Paravicini and R. M. Touyz Redox signaling in hypertension Cardiovasc Res, July 15, 2006; 71(2): 247 - 258. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. ten Freyhaus, M. Huntgeburth, K. Wingler, J. Schnitker, A. T. Baumer, M. Vantler, M. M. Bekhite, M. Wartenberg, H. Sauer, and S. Rosenkranz Novel Nox inhibitor VAS2870 attenuates PDGF-dependent smooth muscle cell chemotaxis, but not proliferation Cardiovasc Res, July 15, 2006; 71(2): 331 - 341. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Li, K. Witte, M. August, I. Brausch, U. Godtel-Armbrust, A. Habermeier, E. I. Closs, M. Oelze, T. Munzel, and U. Forstermann Reversal of Endothelial Nitric Oxide Synthase Uncoupling and Up-Regulation of Endothelial Nitric Oxide Synthase Expression Lowers Blood Pressure in Hypertensive Rats J. Am. Coll. Cardiol., June 20, 2006; 47(12): 2536 - 2544. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
 |
|
 D. Feliers, Y. Gorin, G. Ghosh-Choudhury, H. E. Abboud, and B. S. Kasinath Angiotensin II stimulation of VEGF mRNA translation requires production of reactive oxygen species Am J Physiol Renal Physiol, April 1, 2006; 290(4): F927 - F936. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
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|
|
|
|
|
|
P. L. Hordijk Regulation of NADPH Oxidases: The Role of Rac Proteins Circ. Res., March 3, 2006; 98(4): 453 - 462. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. Ueyama, M. Geiszt, and T. L. Leto Involvement of rac1 in activation of multicomponent nox1- and nox3-based NADPH oxidases. Mol. Cell. Biol., March 1, 2006; 26(6): 2160 - 2174. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
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|
|
|
|
|
|
X. Dai, X. Cao, and D. L. Kreulen Superoxide anion is elevated in sympathetic neurons in DOCA-salt hypertension via activation of NADPH oxidase Am J Physiol Heart Circ Physiol, March 1, 2006; 290(3): H1019 - H1026. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
X.-Y. Yi, V. X. Li, F. Zhang, F. Yi, D. R. Matson, M. T. Jiang, and P.-L. Li Characteristics and actions of NAD(P)H oxidase on the sarcoplasmic reticulum of coronary artery smooth muscle Am J Physiol Heart Circ Physiol, March 1, 2006; 290(3): H1136 - H1144. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
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|
|
|
 |
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|
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