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Published 5 August 2002. doi:10.1083/jcb.200204142
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© The Rockefeller University Press, 0021-9525/2002/8/435 $5.00
The Journal of Cell Biology, Volume 158, Number 3, August 5, 2002 435-444

Report

 Cell cycle– and swelling-induced activation of a Caenorhabditis elegans ClC channel is mediated by CeGLC-7{alpha}/ß phosphatases

Eric Rutledge1, Jerod Denton1 and Kevin Strange1,2,3

1 Department of Anesthesiology, Vanderbilt University Medical Center, Nashville, TN 37232
2 Department of Molecular Physiology, Vanderbilt University Medical Center, Nashville, TN 37232
3 Department of Biophysics and Pharmacology, Vanderbilt University Medical Center, Nashville, TN 37232

Address correspondence to Dr. Kevin Strange, Vanderbilt University Medical Center, T-4202 Medical Center North, Nashville, TN 37232-2520. Tel.: (615) 343-7425. Fax: (615) 343-3916. E-mail: kevin.strange{at}mcmail.vanderbilt.edu

ClC voltage-gated anion channels have been identified in bacteria, yeast, plants, and animals. The biophysical and structural properties of ClCs have been studied extensively, but relatively little is known about their precise physiological functions. Furthermore, virtually nothing is known about the signaling pathways and molecular mechanisms that regulate channel activity. The nematode Caenorhabditis elegans provides significant experimental advantages for characterizing ion channel function and regulation. We have shown previously that the ClC Cl- channel homologue CLH-3 is expressed in C. elegans oocytes, and that it is activated during meiotic maturation and by cell swelling. We demonstrate here that depletion of intracellular ATP or removal of Mg2+, experimental maneuvers that inhibit kinase function, constitutively activate CLH-3. Maturation- and swelling-induced channel activation are inhibited by type 1 serine/threonine phosphatase inhibitors. RNA interference studies demonstrated that the type 1 protein phosphatases CeGLC-7{alpha} and ß, both of which play essential regulatory roles in mitotic and meiotic cell cycle events, mediate CLH-3 activation. We have suggested previously that CLH-3 and mammalian ClC-2 are orthologues that play important roles in heterologous cell–cell interactions, intercellular communication, and regulation of cell cycle–dependent physiological processes. Consistent with this hypothesis, we show that heterologously expressed rat ClC-2 is also activated by serine/threonine dephosphorylation, suggesting that the two channels have common regulatory mechanisms.

Key Words: chloride channel; meiosis; cell volume; oocyte; phosphorylation


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