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J. Biol. Chem., Vol. 281, Issue 30, 20825-20833, July 28, 2006

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CIB1, a Ubiquitously Expressed Ca²⁺-binding Protein Ligand of the InsP₃ Receptor Ca²⁺ Release Channel^*

Carl White, Jun Yang, Mervyn J. Monteiro, and J. Kevin Foskett^¶1

From the Departments of Physiology and ^¶Cell and Developmental Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104 and University of Maryland Biotechnology Institute and Medical Biotechnology Center, University of Maryland, Baltimore, Maryland 21201

A family of Ca²⁺-binding proteins (CaBPs) was shown to bind to the inositol 1,4,5-trisphosphate receptor (InsP₃R) Ca²⁺ release channel and gate it in the absence of InsP₃, establishing them as protein ligands (Yang, J., McBride, S., Mak, D.-O. D., Vardi, N., Palczewski, K., Haeseleer, F., and Foskett, J. K. (2002) Proc. Natl. Acad. Sci. U. S. A. 99, 7711–7716). However, the neuronally restricted expression of CaBP and its inhibition of InsP₃R-mediated Ca²⁺ signaling when overexpressed (Kasri, N. N., Holmes, A. M., Bultynck, G., Parys, J. B., Bootman, M. D., Rietdorf, K., Missiaen, L., McDonald, F., De Smedt, H., Conway, S. J., Holmes, A. B., Berridge, M. J., and Roderick, H. L. (2004) EMBO J. 23, 312–321; Haynes, L. P., Tepikin, A. V., and Burgoyne, R. D. (2004) J. Biol. Chem. 279, 547–555) have raised questions regarding the functional implications of this regulation. We have discovered the Ca²⁺-binding protein CIB1 (calmyrin) as a ubiquitously expressed ligand of the InsP₃R. CIB1 binds to all mammalian InsP₃R isoforms in a Ca²⁺-sensitive manner dependent on its two functional EF-hands and activates InsP₃R channel gating in the absence of InsP₃. In contrast, overexpression of CIB1 or CaBP1 attenuated InsP₃R-dependent Ca²⁺ signaling, and in vitro pre-exposure to CIB1 reduced the number of channels available for subsequent stimulation by InsP₃. These results establish CIB1 as a ubiquitously expressed activating and inhibiting protein ligand of the InsP₃R.

Received for publication, March 7, 2006 , and in revised form, May 23, 2006.

^* This work was supported by Grant R01-GM056328 from the National Institutes of Health (to J. K. F.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains two supplemental figures.

¹ To whom correspondence should be addressed: Dept. of Physiology, University of Pennsylvania, B39 Anatomy-Chemistry Bldg., 414 Guardian Dr., Philadelphia, PA 19104-6085; Tel.: 215-898-1354; Fax: 215-573-6808; E-mail: foskett{at}mail.med.upenn.edu.

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