Function of a STIM1 homologue in C. elegans: evidence that store-operated Ca2+ entry is not essential for oscillatory Ca2+ signaling and ER Ca2+ homeostasis

J Gen Physiol. 2006 Oct;128(4):443-59. doi: 10.1085/jgp.200609611. Epub 2006 Sep 11.

Abstract

1,4,5-trisphosphate (IP(3))-dependent Ca(2+) signaling regulates gonad function, fertility, and rhythmic posterior body wall muscle contraction (pBoc) required for defecation in Caenorhabditis elegans. Store-operated Ca(2+) entry (SOCE) is activated during endoplasmic reticulum (ER) Ca(2+) store depletion and is believed to be an essential and ubiquitous component of Ca(2+) signaling pathways. SOCE is thought to function to refill Ca(2+) stores and modulate Ca(2+) signals. Recently, stromal interaction molecule 1 (STIM1) was identified as a putative ER Ca(2+) sensor that regulates SOCE. We cloned a full-length C. elegans stim-1 cDNA that encodes a 530-amino acid protein with approximately 21% sequence identity to human STIM1. Green fluorescent protein (GFP)-tagged STIM-1 is expressed in the intestine, gonad sheath cells, and spermatheca. Knockdown of stim-1 expression by RNA interference (RNAi) causes sterility due to loss of sheath cell and spermatheca contractile activity required for ovulation. Transgenic worms expressing a STIM-1 EF-hand mutant that constitutively activates SOCE in Drosophila and mammalian cells are sterile and exhibit severe pBoc arrhythmia. stim-1 RNAi dramatically reduces STIM-1GFP expression, suppresses the EF-hand mutation-induced pBoc arrhythmia, and inhibits intestinal store-operated Ca(2+) (SOC) channels. However, stim-1 RNAi surprisingly has no effect on pBoc rhythm, which is controlled by intestinal oscillatory Ca(2+) signaling, in wild type and IP(3) signaling mutant worms, and has no effect on intestinal Ca(2+) oscillations and waves. Depletion of intestinal Ca(2+) stores by RNAi knockdown of the ER Ca(2+) pump triggers the ER unfolded protein response (UPR). In contrast, stim-1 RNAi fails to induce the UPR. Our studies provide the first detailed characterization of STIM-1 function in an intact animal and suggest that SOCE is not essential for certain oscillatory Ca(2+) signaling processes and for maintenance of store Ca(2+) levels in C. elegans. These findings raise interesting and important questions regarding the function of SOCE and SOC channels under normal and pathophysiological conditions.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Animals, Genetically Modified
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / physiology*
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / physiology*
  • Calcium / metabolism*
  • Calcium Channels / genetics
  • Calcium Channels / physiology
  • Calcium Signaling / physiology*
  • Cloning, Molecular
  • Defecation / genetics
  • Defecation / physiology
  • Electrophysiology
  • Endoplasmic Reticulum / metabolism*
  • Female
  • Fertility / genetics
  • Fertility / physiology
  • Homeostasis / physiology
  • Inositol 1,4,5-Trisphosphate Receptors / genetics
  • Inositol 1,4,5-Trisphosphate Receptors / physiology
  • Intestinal Mucosa / metabolism
  • Membrane Proteins / physiology*
  • Molecular Sequence Data
  • Muscle Contraction / genetics
  • Muscle Contraction / physiology
  • Mutation / genetics
  • Ovulation / genetics
  • Ovulation / physiology
  • RNA Interference / physiology
  • Sequence Homology, Amino Acid
  • Stromal Interaction Molecule 1

Substances

  • Caenorhabditis elegans Proteins
  • Calcium Channels
  • Inositol 1,4,5-Trisphosphate Receptors
  • Membrane Proteins
  • Stromal Interaction Molecule 1
  • stim-1 protein, C elegans
  • Calcium

Associated data

  • GENBANK/DQ812088