Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons.
C. elegans OSM-9 is a TRPV channel protein involved in sensory transduction and adaptation. Here, we show that distinct sensory functions arise from different combinations of OSM-9 and related OCR TRPV proteins. Both OSM-9 and OCR-2 are essential for several forms of sensory transduction, including olfaction, osmosensation, mechanosensation, and chemosensation. In neurons that express both OSM-9 and OCR-2, tagged OCR-2 and OSM-9 proteins reside in sensory cilia and promote each other's localization to cilia. In neurons that express only OSM-9, tagged OSM-9 protein resides in the cell body and acts in sensory adaptation rather than sensory transduction. Thus, alternative combinations of TRPV proteins may direct different functions in distinct subcellular locations. Animals expressing the mammalian TRPV1 (VR1) channel in ASH nociceptor neurons avoid the TRPV1 ligand capsaicin, allowing selective, drug-inducible activation of a specific behavior.
Tobin
David M
DM
Howard Hughes Medical Institute, Program in Developmental Biology, Program in Genetics, Program in Neuroscience, Department of Anatomy, Department of Biochemistry and Biophysics, The University of California, San Francisco, San Francisco, CA 94143, USA.
Madsen
David M
DM
Kahn-Kirby
Amanda
A
Peckol
Erin L
EL
Moulder
Gary
G
Barstead
Robert
R
Maricq
Andres V
AV
Bargmann
Cornelia I
CI
D000595:Amino Acid Sequence / Q000235:genetics; D000818:Animals; D001483:Base Sequence / Q000235:genetics; D001522:Behavior, Animal / Q000187:drug effects / Q000502:physiology; D017173:Caenorhabditis elegans / Q000166:cytology / Q000378:metabolism*; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000302:isolation & purification* / Q000378:metabolism; D002211:Capsaicin / Q000494:pharmacology; D002451:Cell Compartmentation / Q000235:genetics; D002462:Cell Membrane / Q000187:drug effects / Q000378:metabolism* / Q000648:ultrastructure; D005786:Gene Expression Regulation / Q000502:physiology; D007473:Ion Channels / Q000235:genetics / Q000302:isolation & purification* / Q000378:metabolism* / Q000648:ultrastructure; D008969:Molecular Sequence Data; D009154:Mutation / Q000235:genetics; D009419:Nerve Tissue Proteins / Q000235:genetics / Q000302:isolation & purification* / Q000378:metabolism* / Q000648:ultrastructure; D009420:Nervous System / Q000166:cytology / Q000187:drug effects / Q000378:metabolism*; D009475:Neurons, Afferent / Q000166:cytology / Q000187:drug effects / Q000378:metabolism*; D010146:Pain / Q000235:genetics / Q000378:metabolism / Q000503:physiopathology; D010802:Phylogeny; D011955:Receptors, Drug / Q000187:drug effects / Q000378:metabolism / Q000648:ultrastructure; D012677:Sensation / Q000187:drug effects / Q000235:genetics*; D015398:Signal Transduction / Q000235:genetics; D050916:TRPV Cation Channels; D050051:Transient Receptor Potential Channels
D029742:Caenorhabditis elegans Proteins; D007473:Ion Channels; D009419:Nerve Tissue Proteins; C464589:OCR-1 protein, C elegans; C464590:OCR-2 protein, C elegans; C108820:OSM-9 protein, C elegans; D011955:Receptors, Drug; D050916:TRPV Cation Channels; D050051:Transient Receptor Potential Channels; D002211:Capsaicin