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Originally published In Press as doi:10.1074/jbc.M109439200 on December 3, 2001

J. Biol. Chem., Vol. 277, Issue 7, 4945-4950, February 15, 2002
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Diversity of Neuron-specific K+-Clminus Cotransporter Expression and Inhibitory Postsynaptic Potential Depression in Rat Motoneurons*

Tsuyoshi UenoDagger , Akihito Okabe§, Norio AkaikeDagger , Atsuo Fukuda§, and Junichi NabekuraDagger

From the Dagger  Department of Cellular and System Physiology, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka 812-8582, Japan and § Department of Physiology, Hamamatsu University School of Medicine, 20-1 Handayama 1-chome, Hamamatsu, Shizuoka 431-3192, Japan

Motoneurons receive a robust recurrent synaptic inhibition by gamma -aminobutyric acid and glycine, which activate Cl- channels. Thus, Cl- homeostasis determines the efficacy of synaptic inhibition in the motoneurons. In situ hybridization reveals that the neuronal K+-Cl- cotransporter isoform 2 (KCC2), a major mechanism in maintaining a low Cl- concentration in neurons, is abundantly expressed in the facial, hypoglossal (XII), and spinal motoneurons innervating striated muscle, whereas the dorsal vagal motoneurons (DMVs) controlling smooth muscle exhibited little expression of KCC2. This raises a general interest in the correlation between KCC2 expression and inhibitory postsynaptic potential (IPSP) performance in the native circuits. Intracellular and whole-cell patch recordings revealed that an activity-dependent depression of IPSPs and positive shift of IPSP reversal potentials were more prominent in the DMV than in the XII. Cl- influx through Cl- channels was extruded more potently in the XII than in the DMV, suggesting that differences in Cl- extrusion account for these dynamic differences of IPSP. Cl- extrusion was inhibited by either furosemide or an increase in extracellular potassium concentrations. Thus, the rigid maintenance of IPSP and rapid Cl- extrusion in the XII reflects an intense expression of KCC2. KCC2 expression may strongly influence the IPSP depression and functional properties of the motoneurons innervating striated muscles.

* This work was supported by Grants-in-aid for Scientific Research 13210108 on Advanced Brain Research and 13035036 on Integrated Brain Research (to J. N.) from the Ministry of Education, Science and Culture, Japan.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.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBankTM/EBI Data Bank with accession number(s) U55816.

To whom correspondence should be addressed. Tel.: 81-92- 642-6090; Fax: 81-92-642-6094; E-mail: Nabekura@mailserver.med.kyushu-u.ac.jp.

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