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Originally published In Press as doi:10.1074/jbc.M110054200 on November 29, 2001

J. Biol. Chem., Vol. 277, Issue 5, 3404-3411, February 1, 2002
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Role of Neutrophil NADPH Oxidase in the Mechanism of Tumor Necrosis Factor-alpha -induced NF-kappa B Activation and Intercellular Adhesion Molecule-1 Expression in Endothelial Cells*

Jie FanDagger , Randall S. Frey, Arshad Rahman, and Asrar B. Malik

From the Department of Pharmacology, University of Illinois College of Medicine, Chicago, Illinois 60612

In this study, we explored a novel function of polymorphonuclear neutrophils (PMN) NAD(P)H oxidase in the mechanism of tumor necrosis factor-alpha (TNFalpha )-induced NF-kappa B activation and intercellular adhesion molecule-1 (ICAM-1) expression in endothelial cells. Studies were made in mice lacking the p47phox subunit of NAD(P)H oxidase as well as in cultured mouse lung vascular endothelial cells (MLVEC) from these mice. In response to TNFalpha challenge, NF-kappa B activation and ICAM-1 expression were significantly attenuated in lungs of p47phox-/- mice as compared with wild-type (WT) mice. The attenuated NF-kappa B activation in p47phox-/- mice was secondary to inhibition of NIK activity and subsequent Ikappa Balpha degradation. Induction of neutropenia using anti-PMN serum prevented the initial TNFalpha -induced NF-kappa B activation and ICAM-1 expression in WT mice, indicating the involvement of PMN NAD(P)H oxidase in signaling these responses. Moreover, the responses were restored upon repletion with PMN obtained from WT mice but not with PMN from p47phox-/- mice. These findings were recapitulated in MLVEC co-cultured with PMN, suggesting that NF-kappa B activation and resultant ICAM-1 expression in endothelial cells occurred secondary to oxidants generated by the PMN NAD(P)H oxidase complex. The functional relevance of the PMN NAD(P)H oxidase in mediating TNFalpha -induced ICAM-1-dependent endothelial adhesivity was evident by markedly reduced adhesion of p47phox-/- PMN in co-culture experiments. Thus, oxidant signaling by the PMN NAD(P)H oxidase complex is an important determinant of TNFalpha -induced NF-kappa B activation and ICAM-1 expression in endothelial cells.

* This work was supported by National Institutes of Health Grants T32 HL07829, HL45638, HL60678, and HL27016.The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Dagger To whom correspondence should be addressed: Dept. of Pharmacology, University of Illinois College of Medicine, 835 South Wolcott Ave., Rm. E425 (M/C 868), Chicago, IL 60612. Tel.: 312-996-1666; Fax: 312-413-0222; E-mail: jiefan@uic.edu.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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