title: Inositol 1,4,5-trisphosphate signaling regulates rhythmic contractile activity of myoepithelial sheath cells in Caenorhabditis elegans.
abstract: 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 (IP(3)) 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-gamma homolog and is expressed in contractile sheath cells of the proximal gonad. Maintenance of sheath contractile activity requires plasma membrane Ca(2+) entry. We conclude that IP(3) generated by LET-23 mediated activation of PLC-gamma induces repetitive intracellular Ca(2+) release that drives rhythmic sheath cell contraction. Calcium entry may function to trigger Ca(2+) release via IP(3) receptors and/or refill intracellular Ca(2+) stores.
authors.affiliation: Department of Anesthesiology, Vanderbilt University Medical Center, Nashville, Tennessee 37232, USA.
authors.forename: Xiaoyan
authors.initials: X
authors.lastname: Yin
authors.forename: Nicholas J D
authors.initials: NJ
authors.lastname: Gower
authors.forename: Howard A
authors.initials: HA
authors.lastname: Baylis
authors.forename: Kevin
authors.initials: K
authors.lastname: Strange
mesh_terms: D000818:Animals; D017173:Caenorhabditis elegans / Q000502:physiology*; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000502:physiology; D002118:Calcium / Q000378:metabolism; D015220:Calcium Channels / Q000235:genetics / Q000502:physiology; D002450:Cell Communication / Q000502:physiology; D004815:Epidermal Growth Factor / Q000235:genetics / Q000502:physiology; D004847:Epithelial Cells / Q000737:chemistry / Q000502:physiology*; D066246:ErbB Receptors / Q000235:genetics / Q000502:physiology; D005260:Female; D015544:Inositol 1,4,5-Trisphosphate / Q000096:biosynthesis / Q000378:metabolism*; D053496:Inositol 1,4,5-Trisphosphate Receptors; D008297:Male; D009130:Muscle, Smooth / Q000166:cytology* / Q000502:physiology; D009154:Mutation / Q000235:genetics; D009865:Oocytes / Q000502:physiology; D010060:Ovulation / Q000502:physiology*; D051966:Phospholipase C gamma; D034622:RNA Interference; D018160:Receptors, Cytoplasmic and Nuclear / Q000235:genetics / Q000502:physiology; D013094:Spermatozoa / Q000502:physiology; D010738:Type C Phospholipases / Q000032:analysis / Q000235:genetics / Q000502:physiology
chemical_list: D029742:Caenorhabditis elegans Proteins; D015220:Calcium Channels; D053496:Inositol 1,4,5-Trisphosphate Receptors; D018160:Receptors, Cytoplasmic and Nuclear; C075912:Lin-3 protein, C elegans; D004815:Epidermal Growth Factor; D015544:Inositol 1,4,5-Trisphosphate; D066246:ErbB Receptors; C085873:let-23 protein, C elegans; D010738:Type C Phospholipases; D051966:Phospholipase C gamma; D002118:Calcium