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J. Biol. Chem., Vol. 276, Issue 22, 18888-18896, June 1, 2001
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From the Department of Biochemistry and Molecular Biology,
University of Maryland School of Medicine, Baltimore, Maryland 21201, § Department of Biological Chemistry, Johns Hopkins
University School of Medicine, Baltimore, Maryland 21205, and
¶ Department of Molecular Genetics, Kansai Medical University,
Moriguchi 570-8506, Japan
The mechanism for coupling
between Ca2+ stores and store-operated channels
(SOCs) is an important but unresolved question. Although SOCs have not
been molecularly identified, transient receptor potential (TRP)
channels share a number of operational parameters with SOCs. The
question of whether activation of SOCs and TRP channels is mediated by
the inositol 1,4,5-trisphosphate receptor (InsP3R) was
examined using the permeant InsP3R antagonist,
2-aminoethoxydiphenyl borate (2-APB) in both mammalian and invertebrate
systems. In HEK293 cells stably transfected with human TRPC3 channels,
the actions of 2-APB to block carbachol-induced
InsP3R-mediated store release and carbachol-induced
Sr2+ entry through TRPC3 channels were both reversed at
high agonist levels, suggesting InsP3Rs mediate TRPC3
activation. However, electroretinogram recordings of the light-induced
current in Drosophila revealed that the TRP
channel-mediated responses in wild-type as well as trp and
trpl mutant flies were all inhibited by 2-APB. This action
of 2-APB is likely InsP3R-independent since
InsP3Rs are dispensable for the light response. We used
triple InsP3R knockout DT40 chicken B-cells to further
assess the role of InsP3Rs in SOC activation.
45Ca2+ flux analysis revealed that although
DT40 wild-type cells retained normal InsP3Rs mediating
2-APB-sensitive Ca2+ release, the
DT40InsP3R-k/o cells were devoid of functional
InsP3Rs. Using intact cells, all parameters of
Ca2+ store function and SOC activation were identical in
DT40wt and DT40InsP3R-k/o cells. Moreover, in both cell
lines SOC activation was completely blocked by 2-APB, and the kinetics
of action of 2-APB on SOCs (time dependence and IC50) were
identical. The results indicate that (a) the action of
2-APB on Ca2+ entry is not mediated by the
InsP3R and (b) the effects of 2-APB provide
evidence for an important similarity in the function of invertebrate TRP channels, mammalian TRP channels, and mammalian store-operated channels.
Assessment of the Role of the Inositol 1,4,5-Trisphosphate
Receptor in the Activation of Transient Receptor Potential Channels and
Store-operated Ca2+ Entry Channels*
,,
*
This work was supported by National Institutes of Health
(NIH) Grant HL55426 (to D. L. G.), a fellowship from the American Heart Association, Maryland Affiliate (to H-T. M.), a fellowship from
the Interdisciplinary Muscle Training Program (to R. L. P.), and NIH
Grant EY10852 (to C. M.).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.
The contribution of these two authors was equal.
To whom correspondence should be addressed: Dept. of
Biochemistry and Molecular Biology, University of Maryland School of Medicine, 108 North Greene St., Baltimore, MD
21201. Tel.: 410-706-2593 (office) and 410-706-7247 (laboratory); Fax:
410-706-6676; E-mail: dgill@umaryland.edu.
Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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