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J. Biol. Chem., Vol. 279, Issue 42, 43716-43724, October 15, 2004

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Characterization of Acid-sensing Ion Channels in Dorsal Horn Neurons of Rat Spinal Cord^*

Long-Jun Wu, Bo Duan, Yi-De Mei, Jun Gao, Jian-Guo Chen¶, Min Zhuo||, Lin Xu**, Mian Wu, and Tian-Le Xu

From the Institute of Neuroscience, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, School of Life Sciences, University of Science and Technology of China, Hefei 230027, ^¶Department of Pharmacology, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China, ^||Department of Physiology, University of Toronto, Toronto, Ontario M5S 1A1, Canada, and ^**Laboratory of Learning and Memory, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China

Acid-sensing ion channels (ASICs) are ligand-gated cation channels activated by extracellular protons. In periphery, they contribute to sensory transmission, including that of nociception and pain. Here we characterized ASIC-like currents in dorsal horn neurons of the rat spinal cord and their functional modulation in pathological conditions. Reverse transcriptase-nested PCR and Western blotting showed that three ASIC isoforms, ASIC1a, ASIC2a, and ASIC2b, are expressed at a high level in dorsal horn neurons. Electrophysiological and pharmacological properties of the proton-gated currents suggest that homomeric ASIC1a and/or heteromeric ASIC1a + 2b channels are responsible for the proton-induced currents in the majority of dorsal horn neurons. Acidification-induced action potentials in these neurons were compatible in a pH-dependent manner with the pH dependence of ASIC-like current. Furthermore, peripheral complete Freund's adjuvant-induced inflammation resulted in increased expression of both ASIC1a and ASIC2a in dorsal horn. These results support the idea that the ASICs of dorsal horn neurons participate in central sensory transmission/modulation under physiological conditions and may play important roles in inflammation-related persistent pain.

Received for publication, March 31, 2004 , and in revised form, August 2, 2004.

^* This study was supported by the National Basic Research Program of China (G1999054000), the National Natural Science Foundation of China (30125015, 30321002, 30170247, 30228020), and the Knowledge Innovation Project from the Chinese Academy of Sciences (KSCX 2-SW-217, KSCX 2-2-04) (to T.-L. X.) 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.

The on-line version of this article (available at http://www.jbc.org) contains a supplemental figure.

To whom correspondence should be addressed: Institute of Neuroscience, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, 320 Yue-yang Road, Shanghai 200031, China. Tel.: 86-21-5492-1751; Fax: 86-21-5492-1735; E-mail: tlxu{at}ion.ac.cn.

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