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J. Biol. Chem., Vol. 278, Issue 35, 33492-33500, August 29, 2003

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RhoA Interaction with Inositol 1,4,5-Trisphosphate Receptor and Transient Receptor Potential Channel-1 Regulates Ca²⁺ Entry

ROLE IN SIGNALING INCREASED ENDOTHELIAL PERMEABILITY^*

Dolly Mehta , Gias U. Ahmmed, Biman C. Paria, Michael Holinstat, Tatyana Voyno-Yasenetskaya, Chinnaswamy Tiruppathi, Richard D. Minshall and Asrar B. Malik

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

We tested the hypothesis that RhoA, a monomeric GTP-binding protein, induces association of inositol trisphosphate receptor (IP₃R) with transient receptor potential channel (TRPC1), and thereby activates store depletion-induced Ca²⁺ entry in endothelial cells. We showed that RhoA upon activation with thrombin associated with both IP₃R and TRPC1. Thrombin also induced translocation of a complex consisting of Rho, IP₃R, and TRPC1 to the plasma membrane. IP₃R and TRPC1 translocation and association required Rho activation because the response was not seen in C3 transferase (C3)-treated cells. Rho function inhibition using Rho dominant-negative mutant or C3 dampened Ca²⁺ entry regardless of whether Ca²⁺ stores were emptied by thrombin, thapsigargin, or inositol trisphosphate. Rho-induced association of IP₃R with TRPC1 was dependent on actin filament polymerization because latrunculin (which inhibits actin polymerization) prevented both the association and Ca²⁺ entry. We also showed that thrombin produced a sustained Rho-dependent increase in cytosolic Ca²⁺ concentration [Ca²⁺]_i in endothelial cells overexpressing TRPC1. We further showed that Rho-activated Ca²⁺ entry via TRPC1 is important in the mechanism of the thrombin-induced increase in endothelial permeability. In summary, Rho activation signals interaction of IP₃R with TRPC1 at the plasma membrane of endothelial cells, and triggers Ca²⁺ entry following store depletion and the resultant increase in endothelial permeability.

Received for publication, March 7, 2003 , and in revised form, May 2, 2003.

^* This work was supported by National Institutes of Health Grants HL45638 and HL71794. 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, The University of Illinois, College of Medicine, 835 S. Wolcott Ave., Chicago, IL 60612. Tel.: 312-355-0236; Fax: 312-996-1225; E-mail: dmehta{at}uic.edu.

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