Published 16 September 2002. doi:10.1083/jcb.200203091
© The Rockefeller University Press,
0021-9525/2002/9/1089 $5.00
The Journal of Cell Biology, Volume 158, Number 6, September 16, 2002 1089-1096
Involvement of TRPC in the abnormal calcium influx observed in dystrophic (mdx) mouse skeletal muscle fibers
Clarisse Vandebrouck,
Dominique Martin,
Monique Colson-Van Schoor,
Huguette Debaix and
Philippe Gailly
Département de Physiologie, Université Catholique de Louvain (UCL 5540), 1200 Brussels, Belgium
Address correspondence to P. Gailly, Département de Physiologie, Université Catholique de Louvain (UCL 5540), Av. Hippocrate 55, 1200 Brussels, Belgium. Tel.: 32-2-764-55-42. Fax: 32-2-764-55-80. E-mail: gailly{at}fymu.ucl.ac.be
Duchenne muscular dystrophy results from the lack of dystrophin, a cytoskeletal protein associated with the inner surface membrane, in skeletal muscle. The absence of dystrophin induces an abnormal increase of sarcolemmal calcium influx through cationic channels in adult skeletal muscle fibers from dystrophic (mdx) mice. We observed that the activity of these channels was increased after depletion of the stores of calcium with thapsigargin or caffeine. By analogy with the situation observed in nonexcitable cells, we therefore hypothesized that these store-operated channels could belong to the transient receptor potential channel (TRPC) family. We measured the expression of TRPC isoforms in normal and mdx adult skeletal muscles fibers, and among the seven known isoforms, five were detected (TRPC1, 2, 3, 4, and 6) by RT-PCR. Western blot analysis and immunocytochemistry of normal and mdx muscle fibers demonstrated the localization of TRPC1, 4, and 6 proteins at the plasma membrane. Therefore, an antisense strategy was used to repress these TRPC isoforms. In parallel with the repression of the TRPCs, we observed that the occurrence of calcium leak channels was decreased to one tenth of its control value (patch-clamp technique), showing the involvement of TRPC in the abnormal calcium influx observed in dystrophic fibers.
Key Words: calcium channels; dystrophy; sarcoplasmic reticulum; capacitative entry; TRP channel

CiteULike
Complore
Connotea
Del.icio.us
Digg
Facebook
Reddit
Technorati
Twitter What's this?
This article has been cited by other articles:
-
Millay, D. P., Goonasekera, S. A., Sargent, M. A., Maillet, M., Aronow, B. J., Molkentin, J. D.
(2009). Calcium influx is sufficient to induce muscular dystrophy through a TRPC-dependent mechanism. Proc. Natl. Acad. Sci. USA
106: 19023-19028
[Abstract]
[Full Text]
-
Dirksen, R. T.
(2009). Checking your SOCCs and feet: the molecular mechanisms of Ca2+ entry in skeletal muscle. J. Physiol.
587: 3139-3147
[Abstract]
[Full Text]
-
Lanner, J. T., Bruton, J. D., Assefaw-Redda, Y., Andronache, Z., Zhang, S.-J., Severa, D., Zhang, Z.-B., Melzer, W., Zhang, S.-L., Katz, A., Westerblad, H.
(2009). Knockdown of TRPC3 with siRNA coupled to carbon nanotubes results in decreased insulin-mediated glucose uptake in adult skeletal muscle cells. FASEB J.
23: 1728-1738
[Abstract]
[Full Text]
-
Launikonis, B. S., Stephenson, D. G., Friedrich, O.
(2009). Rapid Ca2+ flux through the transverse tubular membrane, activated by individual action potentials in mammalian skeletal muscle. J. Physiol.
587: 2299-2312
[Abstract]
[Full Text]
-
Burdi, R., Rolland, J.-F., Fraysse, B., Litvinova, K., Cozzoli, A., Giannuzzi, V., Liantonio, A., Camerino, G. M., Sblendorio, V., Capogrosso, R. F., Palmieri, B., Andreetta, F., Confalonieri, P., De Benedictis, L., Montagnani, M., De Luca, A.
(2009). Multiple pathological events in exercised dystrophic mdx mice are targeted by pentoxifylline: outcome of a large array of in vivo and ex vivo tests. J. Appl. Physiol.
106: 1311-1324
[Abstract]
[Full Text]
-
Iwata, Y., Katanosaka, Y., Arai, Y., Shigekawa, M., Wakabayashi, S.
(2009). Dominant-negative inhibition of Ca2+ influx via TRPV2 ameliorates muscular dystrophy in animal models. Hum Mol Genet
18: 824-834
[Abstract]
[Full Text]
-
Abramowitz, J., Birnbaumer, L.
(2009). Physiology and pathophysiology of canonical transient receptor potential channels. FASEB J.
23: 297-328
[Abstract]
[Full Text]
-
Louis, M., Zanou, N., Van Schoor, M., Gailly, P.
(2008). TRPC1 regulates skeletal myoblast migration and differentiation. J. Cell Sci.
121: 3951-3959
[Abstract]
[Full Text]
-
Gervasio, O. L., Whitehead, N. P., Yeung, E. W., Phillips, W. D., Allen, D. G.
(2008). TRPC1 binds to caveolin-3 and is regulated by Src kinase - role in Duchenne muscular dystrophy. J. Cell Sci.
121: 2246-2255
[Abstract]
[Full Text]
-
Stiber, J. A., Zhang, Z.-S., Burch, J., Eu, J. P., Zhang, S., Truskey, G. A., Seth, M., Yamaguchi, N., Meissner, G., Shah, R., Worley, P. F., Williams, R. S., Rosenberg, P. B.
(2008). Mice Lacking Homer 1 Exhibit a Skeletal Myopathy Characterized by Abnormal Transient Receptor Potential Channel Activity. Mol. Cell. Biol.
28: 2637-2647
[Abstract]
[Full Text]
-
Reggiani, C.
(2008). Between channels and tears: aim at ROS to save the membrane of dystrophic fibres. J. Physiol.
586: 1779-1779
[Full Text]
-
Launikonis, B. S., Rios, E.
(2007). Store-operated Ca2+ entry during intracellular Ca2+ release in mammalian skeletal muscle. J. Physiol.
583: 81-97
[Abstract]
[Full Text]
-
Gailly, P., De Backer, F., Van Schoor, M., Gillis, J. M.
(2007). In situ measurements of calpain activity in isolated muscle fibres from normal and dystrophin-lacking mdx mice. J. Physiol.
582: 1261-1275
[Abstract]
[Full Text]
-
Lipskaia, L., Pinet, C., Fromes, Y., Hatem, S., Cantaloube, I., Coulombe, A., Lompre, A.-M.
(2007). Mutation of {delta}-Sarcoglycan Is Associated with Ca2+-Dependent Vascular Remodeling in the Syrian Hamster. Am. J. Pathol.
171: 162-171
[Abstract]
[Full Text]
-
Ju, Y.-K., Chu, Y., Chaulet, H., Lai, D., Gervasio, O. L., Graham, R. M., Cannell, M. B., Allen, D. G.
(2007). Store-Operated Ca2+ Influx and Expression of TRPC Genes in Mouse Sinoatrial Node. Circ. Res.
100: 1605-1614
[Abstract]
[Full Text]
-
Vandebrouck, A., Sabourin, J., Rivet, J., Balghi, H., Sebille, S., Kitzis, A., Raymond, G., Cognard, C., Bourmeyster, N., Constantin, B.
(2007). Regulation of capacitative calcium entries by {alpha}1-syntrophin: association of TRPC1 with dystrophin complex and the PDZ domain of {alpha}1-syntrophin. FASEB J.
21: 608-617
[Abstract]
[Full Text]
-
Nilius, B., Owsianik, G., Voets, T., Peters, J. A.
(2007). Transient Receptor Potential Cation Channels in Disease. Physiol. Rev.
87: 165-217
[Abstract]
[Full Text]
-
Bush, E. W., Hood, D. B., Papst, P. J., Chapo, J. A., Minobe, W., Bristow, M. R., Olson, E. N., McKinsey, T. A.
(2006). Canonical Transient Receptor Potential Channels Promote Cardiomyocyte Hypertrophy through Activation of Calcineurin Signaling. J. Biol. Chem.
281: 33487-33496
[Abstract]
[Full Text]
-
Boittin, F.-X., Petermann, O., Hirn, C., Mittaud, P., Dorchies, O. M., Roulet, E., Ruegg, U. T.
(2006). Ca2+-independent phospholipase A2 enhances store-operated Ca2+ entry in dystrophic skeletal muscle fibers. J. Cell Sci.
119: 3733-3742
[Abstract]
[Full Text]
-
Ducret, T., Vandebrouck, C., Cao, M. L., Lebacq, J., Gailly, P.
(2006). Functional role of store-operated and stretch-activated channels in murine adult skeletal muscle fibres. J. Physiol.
575: 913-924
[Abstract]
[Full Text]
-
Lafoux, A., Divet, A., Gervier, P., Huchet-Cadiou, C.
(2006). Greater Susceptibility of the Sarcoplasmic Reticulum to H2O2 Injuries in Diaphragm Muscle from mdx Mice. J. Pharmacol. Exp. Ther.
318: 1359-1367
[Abstract]
[Full Text]
-
Allard, B., Couchoux, H., Pouvreau, S., Jacquemond, V.
(2006). Sarcoplasmic reticulum Ca2+ release and depletion fail to affect sarcolemmal ion channel activity in mouse skeletal muscle. J. Physiol.
575: 69-81
[Abstract]
[Full Text]
-
Balghi, H., Sebille, S., Mondin, L., Cantereau, A., Constantin, B., Raymond, G., Cognard, C.
(2006). Mini-dystrophin Expression Down-regulates IP3-mediated Calcium Release Events in Resting Dystrophin-deficient Muscle Cells. JGP
128: 219-230
[Abstract]
[Full Text]
-
Inoue, R., Jensen, L. J., Shi, J., Morita, H., Nishida, M., Honda, A., Ito, Y.
(2006). Transient Receptor Potential Channels in Cardiovascular Function and Disease. Circ. Res.
99: 119-131
[Abstract]
[Full Text]
-
Lee, E. H., Cherednichenko, G., Pessah, I. N., Allen, P. D.
(2006). Functional Coupling between TRPC3 and RyR1 Regulates the Expressions of Key Triadic Proteins. J. Biol. Chem.
281: 10042-10048
[Abstract]
[Full Text]
-
Balghi, H., Sebille, S., Constantin, B., Patri, S., Thoreau, V., Mondin, L., Mok, E., Kitzis, A., Raymond, G., Cognard, C.
(2006). Mini-dystrophin Expression Down-regulates Overactivation of G Protein-mediated IP3 Signaling Pathway in Dystrophin-deficient Muscle Cells. JGP
127: 171-182
[Abstract]
[Full Text]
-
Allen, D. G, Whitehead, N. P, Yeung, E. W
(2005). Mechanisms of stretch-induced muscle damage in normal and dystrophic muscle: role of ionic changes. J. Physiol.
567: 723-735
[Abstract]
[Full Text]
-
Sampieri, A., Diaz-Munoz, M., Antaramian, A., Vaca, L.
(2005). The Foot Structure from the Type 1 Ryanodine Receptor Is Required for Functional Coupling to Store-operated Channels. J. Biol. Chem.
280: 24804-24815
[Abstract]
[Full Text]
-
Chakkalakal, J. V., Thompson, J., Parks, R. J., Jasmin, B. J.
(2005). Molecular, cellular, and pharmacological therapies for Duchenne/Becker muscular dystrophies. FASEB J.
19: 880-891
[Abstract]
[Full Text]
-
Yeung, E. W., Whitehead, N. P., Suchyna, T. M., Gottlieb, P. A., Sachs, F., Allen, D. G.
(2005). Effects of stretch-activated channel blockers on [Ca2+]i and muscle damage in the mdx mouse. J. Physiol.
562: 367-380
[Abstract]
[Full Text]
-
Basset, O., Boittin, F.-X., Dorchies, O. M., Chatton, J.-Y., van Breemen, C., Ruegg, U. T.
(2004). Involvement of Inositol 1,4,5-Trisphosphate in Nicotinic Calcium Responses in Dystrophic Myotubes Assessed by Near-plasma Membrane Calcium Measurement. J. Biol. Chem.
279: 47092-47100
[Abstract]
[Full Text]
-
Cherednichenko, G., Hurne, A. M., Fessenden, J. D., Lee, E. H., Allen, P. D., Beam, K. G., Pessah, I. N.
(2004). Conformational activation of Ca2+ entry by depolarization of skeletal myotubes. Proc. Natl. Acad. Sci. USA
101: 15793-15798
[Abstract]
[Full Text]
-
Mikkelsen, U. R., Fredsted, A., Gissel, H., Clausen, T.
(2004). Excitation-induced Ca2+ influx and muscle damage in the rat: loss of membrane integrity and impaired force recovery. J. Physiol.
559: 271-285
[Abstract]
[Full Text]
-
Rosenberg, P., Hawkins, A., Stiber, J., Shelton, J. M., Hutcheson, K., Bassel-Duby, R., Shin, D. M., Yan, Z., Williams, R. S.
(2004). TRPC3 channels confer cellular memory of recent neuromuscular activity. Proc. Natl. Acad. Sci. USA
101: 9387-9392
[Abstract]
[Full Text]
-
Morel, J.-L., Rakotoarisoa, L., Jeyakumar, L. H., Fleischer, S., Mironneau, C., Mironneau, J.
(2004). Decreased Expression of Ryanodine Receptors Alters Calcium-induced Calcium Release Mechanism in mdx Duodenal Myocytes. J. Biol. Chem.
279: 21287-21293
[Abstract]
[Full Text]
-
Pang, Y., Bounelis, P., Chatham, J. C., Marchase, R. B.
(2004). Hexosamine Pathway Is Responsible for Inhibition by Diabetes of Phenylephrine-Induced Inotropy. Diabetes
53: 1074-1081
[Abstract]
[Full Text]
-
Hunton, D. L., Zou, L., Pang, Y., Marchase, R. B.
(2004). Adult rat cardiomyocytes exhibit capacitative calcium entry. Am. J. Physiol. Heart Circ. Physiol.
286: H1124-H1132
[Abstract]
[Full Text]
-
Abramovici, H., Hogan, A. B., Obagi, C., Topham, M. K., Gee, S. H.
(2003). Diacylglycerol Kinase-{zeta} Localization in Skeletal Muscle Is Regulated by Phosphorylation and Interaction with Syntrophins. Mol. Biol. Cell
14: 4499-4511
[Abstract]
[Full Text]
-
Yeung, E. W, Head, S. I, Allen, D. G
(2003). Gadolinium reduces short-term stretch-induced muscle damage in isolated mdx mouse muscle fibres. J. Physiol.
552: 449-458
[Abstract]
[Full Text]
-
Iwata, Y., Katanosaka, Y., Arai, Y., Komamura, K., Miyatake, K., Shigekawa, M.
(2003). A novel mechanism of myocyte degeneration involving the Ca2+-permeable growth factor-regulated channel. JCB
161: 957-967
[Abstract]
[Full Text]