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PNAS 96 (26): 14955-14960

Copyright © 1999 by the National Academy of Sciences.


Modulation of Ca2+ entry by polypeptides of the inositol 1,4,5-trisphosphate receptor (IP3R) that bind transient receptor potential (TRP): Evidence for roles of TRP and IP3R in store depletion-activated Ca2+ entry

Guylain Boulay*,{dagger}, Darren M. Brown*,{dagger}, Ning Qin*,{dagger}, Meisheng Jiang*, Alexander Dietrich*, Michael Xi Zhu{ddagger}, Zhangguo Chen{ddagger}, Mariel Birnbaumer*,§, Katsuhiko Mikoshiba||, and Lutz Birnbaumer*,**,{ddagger}{ddagger}

Departments of *Anesthesiology, §Physiology, and **Biological Chemistry, and Molecular, Cell, and Developmental Biology, and Molecular Biology and Brain Research Institutes, University of California, Los Angeles, CA 90095; {ddagger}Department of Pharmacology and Neurobiotechnology Center, Ohio State University, Columbus, OH 43210; and ||Department of Molecular Neurobiology, Institute of Medical Science, University of Tokyo, 4-6-1 Shirokane dai, Minato-ku, Tokyo 108-8639, Japan

Contributed by Lutz Birnbaumer

Accepted for publication October 20, 1999.

Abstract: Homologues of Drosophilia transient receptor potential (TRP) have been proposed to be unitary subunits of plasma membrane ion channels that are activated as a consequence of active or passive depletion of Ca2+ stores. In agreement with this hypothesis, cells expressing TRPs display novel Ca2+-permeable cation channels that can be activated by the inositol 1,4,5-trisphosphate receptor (IP3R) protein. Expression of TRPs alters cells in many ways, including up-regulation of IP3Rs not coded for by TRP genes, and proof that TRP forms channels of these and other cells is still missing. Here, we document physical interaction of TRP and IP3R by coimmunoprecipitation and glutathione S-transferase-pulldown experiments and identify two regions of IP3R, F2q and F2g, that interact with one region of TRP, C7. These interacting regions were expressed in cells with an unmodified complement of TRPs and IP3Rs to study their effect on agonist- as well as store depletion-induced Ca2+ entry and to test for a role of their respective binding partners in Ca2+ entry. C7 and an F2q-containing fragment of IP3R decreased both forms of Ca2+ entry. In contrast, F2g enhanced the two forms of Ca2+ entry. We conclude that store depletion-activated Ca2+ entry occurs through channels that have TRPs as one of their normal structural components, and that these channels are directly activated by IP3Rs. IP3Rs, therefore, have the dual role of releasing Ca2+ from stores and activating Ca2+ influx in response to either increasing IP3 or decreasing luminal Ca2+.

{dagger} G.B., D.M.B., and N.Q. contributed equally to this work.

{ddagger}{ddagger} To whom reprint requests should be sent at the * address. E-mail: lutzb{at}

See commentary on page 14669.

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Involvement of TRPC in the abnormal calcium influx observed in dystrophic (mdx) mouse skeletal muscle fibers.
C. Vandebrouck, D. Martin, M. C.-V. Schoor, H. Debaix, and P. Gailly (2002)
J. Cell Biol. 158, 1089-1096
   Abstract »    Full Text »    PDF »
Inhibition of endogenous TRP1 decreases capacitative Ca2+ entry and attenuates pulmonary artery smooth muscle cell proliferation.
M. Sweeney, Y. Yu, O. Platoshyn, S. Zhang, S. S. McDaniel, and J. X.-J. Yuan (2002)
Am J Physiol Lung Cell Mol Physiol 283, L144-L155
   Abstract »    Full Text »    PDF »
Two-state Conformational Changes in Inositol 1,4,5-Trisphosphate Receptor Regulated by Calcium.
K. Hamada, T. Miyata, K. Mayanagi, J. Hirota, and K. Mikoshiba (2002)
J. Biol. Chem. 277, 21115-21118
   Abstract »    Full Text »    PDF »
M. Trebak, G. St. J. Bird, R. R. McKay, and J. W. Putney Jr. (2002)
J. Biol. Chem. 277, 21617-21623
   Abstract »    Full Text »    PDF »
Calcium Influx Factor from Cytochrome P-450 Metabolism and Secretion-like Coupling Mechanisms for Capacitative Calcium Entry in Corneal Endothelial Cells.
Q. Xie, Y. Zhang, C. Zhai, and J. A. Bonanno (2002)
J. Biol. Chem. 277, 16559-16566
   Abstract »    Full Text »    PDF »
The Role of Endogenous Human Trp4 in Regulating Carbachol-induced Calcium Oscillations in HEK-293 Cells.
X. Wu, G. Babnigg, T. Zagranichnaya, and M. L. Villereal (2002)
J. Biol. Chem. 277, 13597-13608
   Abstract »    Full Text »    PDF »
Cloning and Functional Expression of Human Short TRP7, a Candidate Protein for Store-operated Ca2+ Influx.
A. Riccio, C. Mattei, R. E. Kelsell, A. D. Medhurst, A. R. Calver, A. D. Randall, J. B. Davis, C. D. Benham, and M. N. Pangalos (2002)
J. Biol. Chem. 277, 12302-12309
   Abstract »    Full Text »    PDF »
TRP Channel Proteins and Signal Transduction.
B. Minke and B. Cook (2002)
Physiol Rev 82, 429-472
   Abstract »    Full Text »    PDF »
Transient Receptor Potential 1 Regulates Capacitative Ca2+ Entry and Ca2+ Release from Endoplasmic Reticulum in B Lymphocytes.
Y. Mori, M. Wakamori, T. Miyakawa, M. Hermosura, Y. Hara, M. Nishida, K. Hirose, A. Mizushima, M. Kurosaki, E. Mori, et al. (2002)
J. Exp. Med. 195, 673-681
   Abstract »    Full Text »    PDF »
Calcium Transients in the Garter Snake Vomeronasal Organ.
A. R. Cinelli, D. Wang, P. Chen, W. Liu, and M. Halpern (2002)
J Neurophysiol 87, 1449-1472
   Abstract »    Full Text »    PDF »
Expression of Trp3 Determines Sensitivity of Capacitative Ca2+ Entry to Nitric Oxide and Mitochondrial Ca2+ Handling. EVIDENCE FOR A ROLE OF Trp3 AS A SUBUNIT OF CAPACITATIVE Ca2+ ENTRY CHANNELS.
B. Thyagarajan, M. Poteser, C. Romanin, H. Kahr, M. X. Zhu, and K. Groschner (2001)
J. Biol. Chem. 276, 48149-48158
   Abstract »    Full Text »    PDF »
Stabilization of Cortical Actin Induces Internalization of Transient Receptor Potential 3 (Trp3)-associated Caveolar Ca2+ Signaling Complex and Loss of Ca2+ Influx without Disruption of Trp3-Inositol Trisphosphate Receptor Association.
T. Lockwich, B. B. Singh, X. Liu, and I. S. Ambudkar (2001)
J. Biol. Chem. 276, 42401-42408
   Abstract »    Full Text »    PDF »
Activation of Inositol 1,4,5-Trisphosphate Receptor Is Essential for the Opening of Mouse TRP5 Channels.
H. Kanki, M. Kinoshita, A. Akaike, M. Satoh, Y. Mori, and S. Kaneko (2001)
Mol. Pharmacol. 60, 989-998
   Abstract »    Full Text »    PDF »
Potentiation and inhibition of Ca2+ release-activated Ca2+ channels by 2-aminoethyldiphenyl borate (2-APB) occurs independently of IP3 receptors.
M. Prakriya and R. S Lewis (2001)
J. Physiol. 536, 3-19
   Abstract »    Full Text »    PDF »
Ion Channels and Their Functional Role in Vascular Endothelium.
B. Nilius and G. Droogmans (2001)
Physiol Rev 81, 1415-1459
   Abstract »    Full Text »    PDF »
Human Trp3 forms both inositol trisphosphate receptor-dependent and receptor-independent store-operated cation channels in DT40 avian B lymphocytes.
G. Vazquez, J.-P. Lievremont, G. St. J. Bird, and J. W. Putney Jr. (2001)
PNAS 98, 11777-11782
   Abstract »    Full Text »    PDF »
Essential control of an endothelial cell ISOC by the spectrin membrane skeleton.
S. Wu, J. Sangerman, M. Li, G. H. Brough, S. R. Goodman, and T. Stevens (2001)
J. Cell Biol. 154, 1225-1234
   Abstract »    Full Text »    PDF »
2-Aminoethoxydiphenyl Borate Directly Inhibits Store-Operated Calcium Entry Channels in Human Platelets.
Y. Dobrydneva and P. Blackmore (2001)
Mol. Pharmacol. 60, 541-552
   Abstract »    Full Text »    PDF »

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