OSM-9, A Novel Protein with Structural Similarity to Channels, Is Required for Olfaction, Mechanosensation, and Olfactory Adaptation inCaenorhabditis elegans

Abstract

Although cyclic nucleotide-gated channels mediate sensory transduction in olfaction and vision, other forms of sensory transduction are independent of these channels. Caenorhabditis elegans cyclic nucleotide-gated channel mutants respond normally to some olfactory stimuli and to osmotic stimuli, suggesting that these chemosensory responses use an alternative sensory transduction pathway. One gene that may act in this pathway is osm-9, which is required for each of these responses as well as a mechanosensory response to nose touch. osm-9 encodes a protein with ankyrin repeats and multiple predicted transmembrane domains that has limited similarity to the Drosophila phototransduction channels transient receptor potential (TRP) and TRP-like (TRPL). The sequence of OSM-9 and other TRP-like genes reveals a previously unsuspected diversity of mammalian and invertebrate genes in this family. osm-9 is required for the activity of the predicted G-proteincoupled odorant receptor ODR-10, which acts in the AWA olfactory neurons; its similarity to other G-protein-regulated transduction channels suggests that OSM-9 is involved in AWA signaling. osm-9::GFP fusion genes are expressed in a subset of chemosensory, mechanosensory, and osmosensory neurons. osm-9 also affects olfactory adaptation within neurons that require the cyclic nucleotide-gated channel for olfaction; in these neurons, the gene has a regulatory function and not a primary role in sensory transduction.Key words: olfaction; C. elegans; mechanosensation; sensory transduction; signaling pathways; olfactory adaptation; TRP channels Sensory neurons transduce environmental stimuli via the activation of channels that differ by organism and by sensory system. One important class of sensory channels includes cAMP-and cGM P-gated channels. In the vertebrate visual system, photoactivation of the G-protein-coupled receptor rhodopsin results in closure of cGM P-gated channels (Stryer, 1991). Olfactory transduction in vertebrates also begins with the activation of Gprotein-coupled receptors and is mediated by opening of cAM P-gated channels (Reed, 1992). Mice mutant for the olfactory cyclic nucleotide-gated channel fail to generate electrical responses to all tested odorants, although the olfactory neurons are present and have normal passive membrane properties (Brunet et al., 1996). C yclic nucleotide-gated channels have also been implicated in chemosensation in the nematode Caenorhabditis elegans. C. elegans senses a large number of volatile attractants with two pairs of olfactory neurons designated AWA and AWC (Bargmann et al., 1993). AWC olfactory responses may be mediated by a putative cyclic nucleotide-gated channel encoded by the tax-2 and tax-4 genes (Coburn and Bargmann, 1996;Komatsu et al., 1996). The TAX-2/TAX-4 channel also participates in chemotaxis to water-soluble attractants (Dusenbery et al., 1975) and in thermotaxis (Mori and Ohshima, 1995). TAX-2 and TAX-4 gene fusions are expressed in the sensory neurons that mediate these responses.By contrast, sensory tr...

Physiological and molecular mechanisms of salt and water homeostasis in the nematodeCaenorhabditis elegans

“…OSM-9 was the first member of the transient receptor potential-vanilloid (TRPV) subfamily of cation channels to be identified (21); OCR-2 is also a TRPV subfamily member (116). TRP channels are a large group of transmembrane proteins that function in sensory signal transduction, epithelial transport, and Ca 2ϩ signaling (90).…”

Touch sensitivity in Caenorhabditis elegans

“…Two TRPV proteins, OSM-9 and OCR-2, are required for nose touch; they are coexpressed and possibly interact in the ASH neurons [19,85]. OSM-9 is also expressed in the FLP and OLQ neurons.…”

Generation and modulation of chemosensory behaviors in C. elegans

“…Thus, in the absence of TAX-2/4 function, these neurons fail to respond to any odorants. However, in a subset of additional neuron types, primary chemosensory signal transduction is likely mediated via the OSM-9 and OCR-2 TRPV channels, which may be gated by polyunsaturated fatty acids (PUFAs) or their derivatives [63,113,144] (Fig. 2b).…”