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J. Biol. Chem., Vol. 278, Issue 39, 37195-37203, September 26, 2003

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Tumor Necrosis Factor- Induces Nuclear Factor-B-dependent TRPC1 Expression in Endothelial Cells^*

Biman C. Paria , Asrar B. Malik , Angela M. Kwiatek , Arshad Rahman , Michael J. May , Sankar Ghosh  and Chinnaswamy Tiruppathi  ¶

From the Department of Pharmacology, College of Medicine, University of Illinois, Chicago, Illinois 60612 and Section of Immunology and Department of Molecular Biophysics and Biochemistry, Howard Hughes Medical Institute, Yale University School of Medicine, New Haven, Connecticut 06520

We investigated the role of tumor necrosis factor- (TNF-) in activating the store-operated Ca²⁺ channels in endothelial cells via the expression of transient receptor potential channel (TRPC) isoforms. We observed that TNF- exposure of human umbilical vein endothelial cells resulted in TRPC1 mRNA and protein expression, whereas it had no effect on TRPC3, TRPC4, or TRPC5 expression. The TRPC1 expression was associated with increased Ca²⁺ influx after intracellular Ca²⁺ store depletion with either thrombin or thapsigargin. We cloned the 5'-regulatory region of the human TRPC1 (hTRPC1) gene which contained a TATA box and CCAAT sequence close to the transcription initiation site. We also identified four nuclear factor-B (NF-B)-binding sites in the 5'-regulatory region. To address the contribution of NF-B in the mechanism of TRPC1 expression, we determined the effects of TNF- on expression of the reporter luciferase after transfection of hTRPC1 promoter-luciferase (hTRPC1-Pro-Luc) construct in the human dermal microvascular endothelial cell line. Reporter activity increased >4-fold at 4 h after TNF- challenge. TNF--induced increase in reporter activity was markedly reduced by co-expression of either kinase-defective IKK kinase mutant or non-phosphorylatable IB mutant. Treatment with NEMO-binding domain peptide, which prevents NF-B activation by selectively inhibiting IKK interaction with IKK complex, also blocked the TNF--induced TRPC1 expression. Thus, TNF- induces TRPC1 expression through an NF-B-dependent pathway in endothelial cells, which can trigger augmented Ca²⁺ entry following Ca²⁺ store depletion. The augmented Ca²⁺ entry secondary to TRPC1 expression may be an important mechanism of endothelial injury induced by TNF-.

Received for publication, April 24, 2003 , and in revised form, July 1, 2003.

^* This work was supported by National Institutes of Health Grants GM-58531, HL45638, and T32-HL-07829. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

^¶ To whom correspondence should be addressed: Dept. of Pharmacology (M/C868), College of Medicine, University of Illinois, 835 S. Wolcott Ave., Chicago, IL 60612. Tel.: 312-355-0249; Fax: 312-413-0222; E-mail: tiruc{at}uic.edu.

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