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Vol. 15, Issue 8, 3938-3949, August 2004

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Inositol 1,4,5-Trisphosphate Signaling Regulates Rhythmic Contractile Activity of Myoepithelial Sheath Cells in Caenorhabditis elegans

Xiaoyan Yin ^*, Nicholas J.D. Gower , Howard A. Baylis , and Kevin Strange ^* 

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

Submitted March 10, 2004; Revised May 24, 2004; Accepted May 30, 2004
Monitoring Editor: Susan Strome

Intercellular communication between germ cells and neighboring somatic cells is essential for reproduction. Caenorhabditis 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 epidermal growth factor-like ligand LIN-3 and the LET-23 tyrosine kinase receptor induces ovulatory contractions of sheath cells. Reduction-of-function mutations in the inositol 1,4,5-trisphosphate (IP₃) receptor gene itr-1 and knockdown of itr-1 expression by RNA interference 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- 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- 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.

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

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