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J. Biol. Chem., Vol. 280, Issue 29, 27013-27021, July 22, 2005

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acr-16 Encodes an Essential Subunit of the Levamisole-resistant Nicotinic Receptor at the Caenorhabditis elegans Neuromuscular Junction^*

Denis Touroutine, Rebecca M. Fox¶, Stephen E. Von Stetina¶, Anna Burdina, David M. Miller, III¶||, and Janet E. Richmond**

From the Department of Biology, University of Illinois, Chicago, Illinois 60607 and the ^¶Department of Cell and Developmental Biology, Vanderbilt University, Nashville, Tennessee 37232-8240

The Caenorhabditis elegans neuromuscular junction (NMJ) contains three pharmacologically distinct ionotropic receptors: -aminobutyric acid receptors, levamisole-sensitive nicotinic receptors, and levamisole-insensitive nicotinic receptors. The subunit compositions of the -aminobutyric acid- and levamisole-sensitive receptors have been elucidated, but the levamisole-insensitive acetylcholine receptor is uncharacterized. To determine which of the 40 putative nicotinic receptor subunit genes in the C. elegans genome encodes the levamisole-resistant receptor, we utilized MAPCeL, a microarray profiling strategy. Of seven nicotinic receptor subunit transcripts found to be enriched in muscle, five encode the levamisole receptor subunits, leaving two candidates for the levamisole-insensitive receptor: acr-8 and acr-16. Electrophysiological analysis of the acr-16 deletion mutant showed that the levamisole-insensitive muscle acetylcholine current was eliminated, whereas deletion of acr-8 had no effect. These data suggest that ACR-16, like its closest vertebrate homolog, the nicotinic receptor 7-subunit, may form homomeric receptors in vivo. Genetic ablation of both the levamisole-sensitive receptor and acr-16 abolished all cholinergic synaptic currents at the NMJ and severely impaired C. elegans locomotion. Therefore, ACR-16-containing receptors account for all non-levamisole-sensitive nicotinic synaptic signaling at the C. elegans NMJ. The determination of subunit composition for all three C. elegans body wall muscle ionotropic receptors provides a critical foundation for future research at this tractable model synapse.

Received for publication, March 15, 2005 , and in revised form, May 18, 2005.

^* This work was supported by National Institutes of Health Grants R01 NS26115 and P01 DK58212 (to D. M. M.), F31 NS046923 (to R. M. F.), F31 NS043068 (to S. E. V.), R01 NS41477 (to J. E. R.), P30 CA68485, P60 DK20593, P30 DK58404, HD15052, P30 EY08126, and Grant 1 P01 HL6744-01. Additional support for microarray experiments was provided by DK58749 (to A. L. George). 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.

Both authors contributed equally to this work.

|| To whom correspondence concerning the microarray profiling should be addressed. Tel.: 615-343-3447; E-mail: david.miller{at}vanderbilt.edu. ^** To whom all other correspondence should be addressed: Dept. of Biology, Bldg. SEL, Rm. 4311, University of Illinois, 840 W. Taylor St., Chicago, IL 60607. Tel.: 312-413-2513; Fax: 312-996-2805; E-mail: jer{at}uic.edu.

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