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PNAS 96 (26): 14955-14960
Copyright © 1999 by the National Academy of Sciences.
BIOLOGICAL SCIENCES / CELL BIOLOGY |
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*, ,
Darren M. Brown*, ,
Ning Qin*, ,
Meisheng Jiang*,
Alexander Dietrich*,
Michael Xi Zhu ,
Zhangguo Chen ,
Mariel Birnbaumer*, ,¶,
Katsuhiko Mikoshiba||, and
Lutz Birnbaumer*,¶,**,
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; 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+.
 G.B., D.M.B., and N.Q. contributed equally to this work.
 To whom reprint requests should be sent at the * address. E-mail: lutzb{at}ucla.edu.
See commentary on page 14669.
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- IRBIT, a Novel Inositol 1,4,5-Trisphosphate (IP3) Receptor-binding Protein, Is Released from the IP3 Receptor upon IP3 Binding to the Receptor.
- H. Ando, A. Mizutani, T. Matsu-ura, and K. Mikoshiba (2003)
J. Biol. Chem.
278, 10602-10612
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- The mouse C-type transient receptor potential 2 (TRPC2) channel: Alternative splicing and calmodulin binding to its N terminus.
- E. Yildirim, A. Dietrich, and L. Birnbaumer (2003)
PNAS
100, 2220-2225
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- Epidermal Growth Factor-induced Depletion of the Intracellular Ca2+ Store Fails to Activate Capacitative Ca2+ Entry in a Human Salivary Cell Line.
- B.-X. Zhang, X. Ma, C.-K. Yeh, M. D. Lifschitz, M. X. Zhu, and M. S. Katz (2002)
J. Biol. Chem.
277, 48165-48171
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- Endogenously Expressed Trp1 Is Involved in Store-mediated Ca2+ Entry by Conformational Coupling in Human Platelets.
- J. A. Rosado, S. L. Brownlow, and S. O. Sage (2002)
J. Biol. Chem.
277, 42157-42163
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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
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- 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
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- 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
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- Comparison of Human TRPC3 Channels in Receptor-activated and Store-operated Modes. DIFFERENTIAL SENSITIVITY TO CHANNEL BLOCKERS SUGGESTS FUNDAMENTAL DIFFERENCES IN CHANNEL COMPOSITION.
- M. Trebak, G. St. J. Bird, R. R. McKay, and J. W. Putney Jr. (2002)
J. Biol. Chem.
277, 21617-21623
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- 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
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- 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
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- TRP Channel Proteins and Signal Transduction.
- B. Minke and B. Cook (2002)
Physiol Rev
82, 429-472
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- 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
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- 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
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- 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
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- 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
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- 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
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- 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
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- 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
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- Ion Channels and Their Functional Role in Vascular Endothelium.
- B. Nilius and G. Droogmans (2001)
Physiol Rev
81, 1415-1459
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- 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
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- 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
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- 2-Aminoethoxydiphenyl Borate Directly Inhibits Store-Operated Calcium Entry Channels in Human Platelets.
- Y. Dobrydneva and P. Blackmore (2001)
Mol. Pharmacol.
60, 541-552
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- Physiology, Phylogeny, and Functions of the TRP Superfamily of Cation Channels.
- C. Montell (2001)
Sci. STKE
2001, re1
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- Mechanisms of capacitative calcium entry.
- J. W. Putney Jr, L. M. Broad, F.-J. Braun, J.-P. Lievremont, and G. S. J. Bird (2001)
J. Cell Sci.
114, 2223-2229
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