Caenorhabditis elegans TRPV ion channel regulates 5HT biosynthesis in chemosensory neurons

Shenyuan Zhang, Irina Sokolchik, Gabriela Blanco, and Ji Ying Sze^*

Department of Anatomy and Neurobiology, College of Medicine, University of California Irvine, Irvine, CA 92697-4040, USA

^* Author for correspondence (e-mail: jsze{at}uci.edu)

Abstract: Serotonin (5HT) is a pivotal signaling molecule that modulates behavioral and endocrine responses to diverse chemical and physical stimuli. We report cell-specific regulation of 5HT biosynthesis by transient receptor potential V (TRPV) ion channels in C. elegans. Mutations in the TRPV genes osm-9 or ocr-2 dramatically downregulate the expression of the gene encoding the 5HT synthesis enzyme tryptophan hydroxylase (tph-1) in the serotonergic chemosensory neurons ADF, but neither the mutation nor the double mutation of both channel genes affects other types of serotonergic neurons. The TRPV genes are expressed in the ADF neurons but not in other serotonergic neurons, and act cell-autonomously to regulate a neuron-specific transcription program. Whereas in olfactory neurons OSM-9 and OCR-2 function is dependent on ODR-3 G, the activity of ODR-3 or two other G proteins expressed in the ADF neurons is not required for upregulating tph-1 expression, thus the TRPV ion channels in different neurons may be regulated by different mechanisms. A gain-of-function mutation in CaMKII UNC-43 partially suppresses the downregulation of tph-1 in the TRPV mutants, thus CaMKII may be an effector of the TRPV signaling. Mutations in the TRPV genes cause worms developmentally arrest at the Dauer stage. This developmental defect is due in part to reduced 5HT inputs into daf-2/insulin neuroendocrine signaling.

Key Words: C. elegans • Transcription • Serotonin biosynthesis • TRPV ion channels • Metabolic control

A Neuronal Signaling Pathway of CaMKII and Gq{alpha} Regulates Experience-Dependent Transcription of tph-1.

Y. Qin, X. Zhang, and Y. Zhang (2013)
J. Neurosci. 33, 925-935
 |  Abstract »  |  Full Text »  |  PDF »

Caenorhabditis elegans TRPV Channels Function in a Modality-Specific Pathway to Regulate Response to Aberrant Sensory Signaling.

M. J. Ezak, E. Hong, A. Chaparro-Garcia, and D. M. Ferkey (2010)
Genetics 185, 233-244
 |  Abstract »  |  Full Text »  |  PDF »

Intraflagellar Transport/Hedgehog-Related Signaling Components Couple Sensory Cilium Morphology and Serotonin Biosynthesis in Caenorhabditis elegans.

M. Moussaif and J. Y. Sze (2009)
J. Neurosci. 29, 4065-4075
 |  Abstract »  |  Full Text »  |  PDF »

C. elegans dauer formation and the molecular basis of plasticity.

N. Fielenbach and A. Antebi (2008)
Genes & Dev. 22, 2149-2165
 |  Abstract »  |  Full Text »  |  PDF »

Regulation of Serotonin Biosynthesis by the G Proteins G{alpha}o and G{alpha}q Controls Serotonin Signaling in Caenorhabditis elegans.

J. E. Tanis, J. J. Moresco, R. A. Lindquist, and M. R. Koelle (2008)
Genetics 178, 157-169
 |  Abstract »  |  Full Text »  |  PDF »

Transient receptor potential vanilloid channels functioning in transduction of osmotic stimuli.

W. Liedtke (2006)
J. Endocrinol. 191, 515-523
 |  Abstract »  |  Full Text »  |  PDF »

Differential contributions of Caenorhabditis elegans histone deacetylases to huntingtin polyglutamine toxicity..

E. A. Bates, M. Victor, A. K. Jones, Y. Shi, and A. C. Hart (2006)
J. Neurosci. 26, 2830-2838
 |  Abstract »  |  Full Text »  |  PDF »

TRPV4 plays an evolutionary conserved role in the transduction of osmotic and mechanical stimuli in live animals.

W. Liedtke (2005)
J. Physiol. 567, 53-58
 |  Abstract »  |  Full Text »  |  PDF »