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J. Biol. Chem., Vol. 280, Issue 8, 7301-7308, February 25, 2005

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Regulation of Intracellular Cl^- Concentration through Volume-regulated ClC-3 Chloride Channels in A10 Vascular Smooth Muscle Cells^*

Jia-Guo Zhou, Jing-Li Ren, Qin-ying Qiu, Hua He, and Yong-Yuan Guan

From the Department of Pharmacology, Zhongshan Medical College, Sun Yat-Sen University, Guangzhou, People's Republic of China 510089

We previously found that antisense oligonucleotide specific to ClC-3 (ClC-3 antisense) prevented rat aortic smooth muscle cell proliferation, which was related to cell volume regulation. In the present study, we further characterized the regulation of intracellular Cl^- concentrations ([Cl^-]_i) via volume-regulated ClC-3 Cl^- channels in an embryo rat aortic vascular smooth muscle cell line (A10 cell) and ClC-3 cDNA-transfected A10 cells (ClC-3-A10) using multiple approaches including [Cl^-]_i measurement, whole cell patch clamp, and application of ClC-3 antisense and intracellular dialysis of an anti-ClC-3 antibody. We found that hypotonic solution decreased [Cl^-]_i and evoked a native I_Cl.vol in A10 cells. The responses of [Cl^-]_i and I_Cl.vol to hypotonic challenge were enhanced by expression of ClC-3, and inhibited by ClC-3 antisense. The currents in A10 (I_Cl.vol) and in ClC-3-A10 cells (I_Cl.ClC-3) were remarkably inhibited by intracellular dialysis of anti-ClC-3 antibody. Reduction in [Cl^-]_i and activation of I_Cl.vol and I_Cl.ClC-3 in A10 and ClC-3-A10 cells, respectively, were significantly inhibited by activation of protein kinase C (PKC) by phorbol-12,13-dibutyrate (PDBu) and inhibition of tyrosine protein kinase by genistein. Sodium orthovanadate (vanadate), a protein-tyrosine phosphatase inhibitor, however, enhanced the cell swelling-induced reduction in [Cl^-]_i, accompanied by the activation of I_Cl.vol and I_Cl.ClC-3 in a voltage-independent manner. Our results suggest that the volume-regulated ClC-3 Cl^- channels play important role in the regulation of [Cl^-]_i and cell proliferation of vascular smooth muscle cells.

Received for publication, November 12, 2004 , and in revised form, December 8, 2004.

^* This work was supported by the National Natural Science Foundation of China (No. 30271503 and No. 30472021), by the Science Foundation of the Ministry of Education in China and by the China Medical Board (No. 00730). 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.

These authors contributed equally to this work.

To whom correspondence should be addressed: Dept. of Pharmacology, Zhongshan Medical College, Sun Yat-Sen University, 74 Zhongshan 2 Rd., Guangzhou, Guangdong, 510089, People's Republic of China. Tel.: 86-20-87331857; Fax: 86-20-87331209; E-mail: yyguan{at}gzsums.edu.cn.

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