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J. Biol. Chem., Vol. 276, Issue 23, 20093-20100, June 8, 2001
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From the Department of Neurobiology, Pharmacology and Physiology,
§ IBD Research Center and Department of Medicine, The
University of Chicago, Chicago, Illinois 60637 and the
¶ Department of Molecular & Cellular Physiology, University of
Cincinnati, Cincinnati, Ohio 45267
The multifunctional
calcium/calmodulin-dependent protein kinase II, CaMKII, has
been shown to regulate chloride movement and cellular function in both
excitable and non-excitable cells. We show that the plasma membrane
expression of a member of the ClC family of Cl This work is dedicated to the fond memory of Wellesley Anne Johnson. The nucleotide sequence(s) reported in this paper has been submitted to the GenBankTM/EMBL Data Bank with accession number(s) AF172729.
Regulation of Human CLC-3 Channels by Multifunctional
Ca2+/Calmodulin-dependent Protein Kinase*
,,
channels, human CLC-3 (hCLC-3), a 90-kDa protein, is regulated by
CaMKII. We cloned the full-length hCLC-3 gene from
the human colonic tumor cell line T84, previously shown to express a
CaMKII-activated Cl conductance (ICl,CaMKII),
and transfected this gene into the mammalian epithelial cell line tsA,
which lacks endogenous expression of ICl,CaMKII. Biotinylation experiments demonstrated plasma membrane expression of
hCLC-3 in the stably transfected cells. In whole cell patch clamp
experiments, autonomously active CaMKII was introduced into tsA cells
stably transfected with hCLC-3 via the patch pipette. Cells
transfected with the hCLC-3 gene showed a 22-fold increase in current density over cells expressing the vector alone.
Kinase-dependent current expression was abolished in the
presence of the autocamtide-2-related inhibitory peptide, a
specific inhibitor of CaMKII. A mutation of glycine 280 to glutamic
acid in the conserved motif in the putative pore region of the channel
changed anion selectivity from I > Cl to Cl > I. These results
indicate that hCLC-3 encodes a Cl channel
that is regulated by CaMKII-dependent phosphorylation.
*
This work was supported by National Institutes of Health
Grant GM36823 and a grant from the Cystic Fibrosis Foundation
(Nelson96PO) (to D. J. N.), National Institutes of Health
Grant DK46433 (to M. A. K.), National Institutes of Health
Digestive Disease Core Grant DK-42086 and The Caroline Halfter Spahn
Trust.The costs of publication of this
article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement" in
accordance with 18 U.S.C. Section
1734 solely to indicate this fact.
Contributed equally to the results of this work.
To whom correspondence should be addressed: Dept. of
Neurobiology, Pharmacology, and Physiology, the University of Chicago, 947 E. 58th St., MC 0926, Chicago, IL 60637. Tel.:
773-702-0126; Fax: 773-702-4066; E-mail:
dnelson@drugs.bsd.uchicago.edu.
Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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