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The Journal of Neuroscience, January 26, 2005, 25(4):1015-1023; doi:10.1523/JNEUROSCI.3107-04.2005

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Cellular/Molecular
Polymodal Sensory Function of the Caenorhabditis elegans OCR-2 Channel Arises from Distinct Intrinsic Determinants within the Protein and Is Selectively Conserved in Mammalian TRPV Proteins

Irina Sokolchik,¹ Takahiro Tanabe,¹ Pierre F. Baldi,^2,3,4 and Ji Ying Sze¹

¹Department of Anatomy and Neurobiology, ²School of Information and Computer Science, ³Department of Biological Chemistry, and ⁴Institute for Genomics and Bioinformatics, University of California, Irvine, California 92697

Caenorhabditis elegans OCR-2 (OSM-9 and capsaicin receptor-related) is a TRPV (vanilloid subfamily of transient receptor potential channel) protein that regulates serotonin (5-HT) biosynthesis in chemosensory neurons and also mediates olfactory and osmotic sensation. Here, we identify the molecular basis for the polymodal function of OCR-2 in its native cellular environment. We show that OCR-2 function in 5-HT production and osmotic sensing is governed by its N-terminal region upstream of the ankyrin repeats domain, but the diacetyl sensitivity is mediated by independent mechanisms. The ocr-2(yz5) mutation results in a glycine-to-glutamate substitution (G36E) within the N-terminal region. The G36E substitution causes dramatic downregulation of 5-HT synthesis in the ADF neurons, eliminates osmosensation mediated by the ASH neurons, but does not affect the response to the odorant diacetyl mediated by the AWA neurons. Conversely, wild-type sequence of the N-terminal segment confers osmotic sensitivity and upregulation of 5-HT production to a normally insensitive C. elegans homolog, OCR-4, but this chimeric channel does not respond to diacetyl stimuli. Furthermore, expression of either the mouse or human TRPV2 gene under the ocr-2 promoter can substantially restore 5-HT biosynthesis in ocr-2-null mutants but cannot improve the deficits in osmotic or olfactory sensation, suggesting that TRPV2 can substitute for the role of OCR-2 only in serotonergic neurons. Thus, different sensory functions of OCR-2 arise from separable intrinsic determinants, and specific functional properties of TRPV channel proteins may be selectively conserved across phyla.

Key words: TRPV channel; sensory modality; serotonin; behavior; C. elegans; gene expression

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Received July 29, 2004; revised November 23, 2004; accepted December 7, 2004.

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