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MBC in Press, published online ahead of print June 11, 2004
Mol. Biol. Cell 10.1091/mbc.E04-03-0198

A more recent version of this article appeared on August 1, 2004
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Submitted on March 10, 2004
Revised on May 24, 2004
Accepted on May 30, 2004

IP3 Signaling Regulates Rhythmic Contractile Activity of Myoepithelial Sheath Cells in C. elegans

Xiaoyan Yin*, Nicholas J. D. Gower{dagger}, Howard A. Baylis{dagger}, and Kevin Strange*{ddagger}

*Departments of Molecular Physiology and Biophysics, and Pharmacology, Vanderbilt University Medical Center, Nashville, Tennessee 37232; {dagger}Department of Zoology, University of Cambridge, Cambridge, United Kingdom CB2 3EJ

Monitoring Editor: Susan Strome

Intercellular communication between germ cells and neighboring somatic cells is essential for reproduction. C. elegans oocytes are surrounded by and coupled via gap junctions to smooth muscle-like myoepithelial sheath cells. Rhythmic sheath cell contraction drives ovulation and is triggered by a factor secreted from oocytes undergoing meiotic maturation. We demonstrate for the first time that signaling through the EGF-like ligand LIN-3 and the LET-23 tyrosine kinase receptor induces ovulatory contractions of sheath cells. Reduction-of-function mutations in the IP3 receptor gene itr-1 and knockdown of itr-1 expression by RNA interference (RNAi) inhibit sheath contractile activity. itr-1 gain-of-function mutations increase the rate and force of basal contractions and induce tonic sheath contraction during ovulation. Sheath contractile activity is disrupted by RNAi of plc-3, one of six phospholipase C-encoding genes in the C. elegans genome. PLC-3 is a PLC-{gamma} homolog and is expressed in contractile sheath cells of the proximal gonad. Maintenance of sheath contractile activity requires plasma membrane Ca2+ entry. We conclude that IP3 generated by LET-23 mediated activation of PLC-{gamma} induces repetitive intracellular Ca2+ release that drives rhythmic sheath cell contraction. Calcium entry may function to trigger Ca2+ release via IP3 receptors and/or refill intracellular Ca2+ stores.

{ddagger}Corresponding author. E-mail: kevin.strange{at}vanderbilt.edu




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