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J Biol Chem, Vol. 274, Issue 32, 22231-22237, August 6, 1999

ATP Regulation of Type 1 Inositol 1,4,5-Trisphosphate Receptor Channel Gating by Allosteric Tuning of Ca2+ Activation

Don-On Daniel MakDagger , Sean McBrideDagger , and J. Kevin FoskettDagger §

From the Dagger  Department of Physiology and § Institute for Human Gene Therapy, University of Pennsylvania, Philadelphia, Pennsylvania 19104-6100

Inositol 1,4,5-trisphosphate (InsP3) mobilizes intracellular Ca2+ by binding to its receptor (InsP3R), an endoplasmic reticulum-localized Ca2+ release channel. Patch clamp electrophysiology of Xenopus oocyte nuclei was used to study the effects of cytoplasmic ATP concentration on the cytoplasmic Ca2+ ([Ca2+]i) dependence of single type 1 InsP3R channels in native endoplasmic reticulum membrane. Cytoplasmic ATP free-acid ([ATP]i), but not the MgATP complex, activated gating of the InsP3-liganded InsP3R, by stabilizing open channel state(s) and destabilizing the closed state(s). Activation was associated with a reduction of the half-maximal activating [Ca2+]i from 500 ± 50 nM in 0 [ATP]i to 29 ± 4 nM in 9.5 mM [ATP]i, with apparent ATP affinity = 0.27 ± 0.04 mM, similar to in vivo concentrations. In contrast, ATP was without effect on maximum open probability or the Hill coefficient for Ca2+ activation. Thus, ATP enhances gating of the InsP3R by allosteric regulation of the Ca2+ sensitivity of the Ca2+ activation sites of the channel. By regulating the Ca2+-induced Ca2+ release properties of the InsP3R, ATP may play an important role in shaping cytoplasmic Ca2+ signals, possibly linking cell metabolic state to important Ca2+-dependent processes.

Copyright © 1999 by The American Society for Biochemistry and Molecular Biology, Inc.
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