CLH-3, ClC-2 anion channel ortholog activated during meiotic maturation in C. elegans oocytes

Eric Rutledge, Laura Bianchi, Michael Christensen, Christoph Boehmer, Rebecca Morrison, Adam Broslat, Andrew M. Beld, Alfred L. George, David Greenstein, Kevin Strange*

*Corresponding author for this work

Research output: Contribution to journalArticle

58 Scopus citations

Abstract

Background: ClC anion channels are ubiquitous and have been identified in organisms as diverse as bacteria and humans. Despite their widespread expression and likely physiological importance, the function and regulation of most ClCs are obscure. The nematode Caenorhabditis elegans offers significant experimental advantages for defining ClC biology. These advantages include a fully sequenced genome, cellular and molecular manipulability, and genetic tractability. Results: We show by patch clamp electrophysiology that C. elegans oocytes express a hyperpolarization- and swelling-activated Cl- current with biophysical characteristics strongly resembling those of mammalian ClC-2. Double-stranded RNA-mediated gene interference (RNAi) and single-oocyte RT-PCR demonstrated that the channel is encoded by clh-3, one of six C. elegans ClC genes. CLH-3 is inactive in immature oocytes but can be triggered by cell swelling. However, CLH-3 plays no apparent role in oocyte volume homeostasis. The physiological signal for channel activation is the induction of oocyte meiotic maturation. During meiotic maturation, the contractile activity of gonadal sheath cells, which surround oocytes and are coupled to them via gap junctions, increases dramatically. These ovulatory sheath cell contractions are initiated prematurely in animals in which CLH-3 expression is disrupted by RNAi. Conclusions: The inwardly rectifying Cl- current in C. elegans oocytes is due to the activity of a CIC channel encoded by clh-3. Functional and structural similarities suggest that CLH-3 and mammalian ClC-2 are orthologs. CLH-3 is activated during oocyte meiotic maturation and functions in part to modulate ovulatory contractions of gap junction-coupled gonadal sheath cells.

Original languageEnglish (US)
Pages (from-to)161-170
Number of pages10
JournalCurrent Biology
Volume11
Issue number3
DOIs
StatePublished - Feb 6 2001

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

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    Rutledge, E., Bianchi, L., Christensen, M., Boehmer, C., Morrison, R., Broslat, A., Beld, A. M., George, A. L., Greenstein, D., & Strange, K. (2001). CLH-3, ClC-2 anion channel ortholog activated during meiotic maturation in C. elegans oocytes. Current Biology, 11(3), 161-170. https://doi.org/10.1016/S0960-9822(01)00051-3