Role of TRPC1 channel in skeletal muscle function

American Journal of Physiology - Cell Physiology

Volumn 298, Issue 1, 2010, Pages

  Zanou, Nadège ^a   Shapovalov, Georges ^b   Louis, Magali ^a   Tajeddine, Nicolas ^a   Gallo, Chiara ^b   Van Schoor, Monique ^a   Anguish, Isabelle ^b   Cao, My Linh ^a   Schakman, Olivier ^a   Dietrich, Alexander ^c   Lebacq, Jean ^a   Ruegg, Urs ^b   Roulet, Emmanuelle ^b   Birnbaumer, Lutz ^d   Gailly, Philippe ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b UNIVERSITY OF GENEVA   (Switzerland)

^c PHILIPPS UNIVERSITY MARBURG   (Germany)

^d NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

Calcium; Canonical transient receptor potential 1; Fatigue

Indexed keywords

CALCIUM ION; MUSCLE PROTEIN; SMALL CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; TRANSIENT RECEPTOR POTENTIAL CHANNEL 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CELL MEMBRANE CONDUCTANCE; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; ENDURANCE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; MUSCLE; MUSCLE CELL; MUSCLE FATIGUE; MUSCLE FUNCTION; MUSCLE ISOMETRIC CONTRACTION; MYOPATHY; NONHUMAN; NUCLEOTIDE SEQUENCE; PATCH CLAMP; PHYSICAL ACTIVITY; PRIORITY JOURNAL; REST; SKELETAL MUSCLE;

ANIMALS; CALCIUM; CYCLOPHILINS; DNA; DNA PRIMERS; GENE AMPLIFICATION; HETEROZYGOTE; ISOMETRIC CONTRACTION; MICE; MICE, KNOCKOUT; MUSCLE CONTRACTION; MUSCLE FATIGUE; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRPC CATION CHANNELS;

MUS;

EID: 73649147054     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00241.2009     Document Type: Article

References (76)

1. Abramowitz J, Birnbaumer L. Physiology and pathophysiology of canonical transient receptor potential channels. FASEB J 23: 297-328, 2009.
2. Allen DG. Skeletal muscle function: role of ionic changes in fatigue, damage and disease. Clin Exp Pharmacol Physiol 31: 485-493, 2004.
3. Allen DG, Lamb GD, Westerblad H. Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 88: 287-332, 2008.
4. Allen DG, Lannergren J, Westerblad H. Muscle cell function during prolonged activity: cellular mechanisms of fatigue. Exp Physiol 80: 497-527, 1995.
5. Allen DG, Westerblad H. Role of phosphate and calcium stores in muscle fatigue. J Physiol 536: 657-665, 2001.
6. Ambudkar IS. TRPC1: a core component of store-operated calcium channels. Biochem Soc Trans 35: 96-100, 2007.
7. Ambudkar IS, Ong HL, Liu X, Bandyopadhyay B, Cheng KT. TRPC1: the link between functionally distinct store-operated calcium channels. Cell Calcium 42: 213-223, 2007.
8. Armstrong CM, Bezanilla FM, Horowicz P. Twitches in the presence of ethylene glycol bis(beta-aminoethyl ether)-N,N′tetracetic acid. Biochim Biophys Acta 267: 605-608, 1972.
9. Bai CX, Giamarchi A, Rodat-Despoix L, Padilla F, Downs T, Tsiokas L, Delmas P. Formation of a new receptor-operated channel by heteromeric assembly of TRPP2 and TRPC1 subunits. EMBO Rep 9: 472-479, 2008.
10. Baylor SM, Chandler WK, Marshall MW. Sarcoplasmic reticulum calcium release in frog skeletal muscle fibres estimated from Arsenazo III calcium transients. J Physiol 344: 625-666, 1983.
11. Beech DJ, Xu SZ, McHugh D, Flemming R. TRPC1 store-operated cationic channel subunit. Cell Calcium 33: 433-440, 2003.
12. Berbey C, Allard B. Electrically silent divalent cation entries in resting and active voltage-controlled muscle fibers. Biophys J 96: 2648-2657, 2009.
13. Bianchi CP, Shanes AM. Calcium influx in skeletal muscle at rest, during activity, and during potassium contracture. J Gen Physiol 42: 803-815, 1959.
14. 2+ entry and vascular tone in intact aorta. Am J Physiol Heart Circ Physiol 295: H2466-H2474, 2008.
15. Brooks SV, Faulkner JA. Contractile properties of skeletal muscles from young, adult and aged mice. J Physiol 404: 71-82, 1988.
16. Carlson CG, Makiejus RV. A noninvasive procedure to detect muscle weakness in the mdx mouse. Muscle Nerve 13: 480-484, 1990.
17. Chen CM, Kraut N, Groudine M, Weintraub H. I-mf, a novel myogenic repressor, interacts with members of the MyoD family. Cell 86: 731-741, 1996.
18. Cheung A, Dantzig JA, Hollingworth S, Baylor SM, Goldman YE, Mitchison TJ, Straight AF. A small-molecule inhibitor of skeletal muscle myosin II. Nat Cell Biol 4: 83-88, 2002.
19. Clapham DE. A STIMulus package puts orai calcium channels to work. Cell 136: 814-816, 2009.
20. Dawson MJ, Gadian DG, Wilkie DR. Mechanical relaxation rate and metabolism studied in fatiguing muscle by phosphorus nuclear magnetic resonance. J Physiol 299: 465-484, 1980.
21. DeHaven WI, Jones BF, Petranka JG, Smyth JT, Tomita T, Bird GS, Putney JW Jr. TRPC channels function independently of STIM1 and Orai1. J Physiol 587: 2275-2298, 2009.
22. Dietrich A, Kalwa H, Storch U, Mederos YSM, Salanova B, Pinkenburg O, Dubrovska G, Essin K, Gollasch M, Birnbaumer L, Gudermann T. Pressure-induced and store-operated cation influx in vascular smooth muscle cells is independent of TRPC1. Pflügers Arch 455: 465-477, 2007.
23. 2+ entry in skeletal muscle. J Physiol 587: 3149-3151, 2009.
24. Ducret T, Vandebrouck C, Cao ML, Lebacq J, Gailly P. Functional role of store-operated and stretch-activated channels in murine adult skeletal muscle fibres. J Physiol 575: 913-924, 2006.
25. 2+ release in mammalian skeletal muscle. Am J Physiol Cell Physiol 289: C1502-C1512, 2005.
26. Edwards RH, Hill DK, Jones DA. Metabolic changes associated with the slowing of relaxation in fatigued mouse muscle. J Physiol 251: 287-301, 1975.
27. Endo M. Calcium release from the sarcoplasmic reticulum. Physiol Rev 57: 71-108, 1977.
28. Feske S, Gwack Y, Prakriya M, Srikanth S, Puppel SH, Tanasa B, Hogan PG, Lewis RS, Daly M, Rao A. A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 441: 179-185, 2006.
29. Franco-Obregon A Jr, Lansman JB. Mechanosensitive ion channels in skeletal muscle from normal and dystrophic mice. J Physiol 481: 299-309, 1994.
30. Gailly P. New aspects of calcium signaling in skeletal muscle cells: implications in Duchenne muscular dystrophy. Biochim Biophys Acta 1600: 38-44, 2002.
31. Gailly P, Boland B, Himpens B, Casteels R, Gillis JM. Critical evaluation of cytosolic calcium determination in resting muscle fibres from normal and dystrophic (mdx) mice. Cell Calcium 14: 473-483, 1993.
32. Gailly P, De Backer F, Van Schoor M, Gillis JM. In situ measurements of calpain activity in isolated muscle fibres from normal and dystrophinlacking mdx mice. J Physiol 582: 1261-1275, 2007.
33. 2+ entry coupling" in fibroblasts expressing the rat neurotensin receptor. J Physiol 491: 635-646, 1996.
34. Gailly P, Hermans E, Octave JN, Gillis JM. Specific increase of genetic expression of parvalbumin in fast skeletal muscles of mdx mice. FEBS Lett 326: 272-274, 1993.
35. Gervasio OL, Whitehead NP, Yeung EW, Phillips WD, Allen DG. TRPC1 binds to caveolin-3 and is regulated by Src kinase-role in Duchenne muscular dystrophy. J Cell Sci 121: 2246-2255, 2008.
36. 2+ uptake in rat skeletal muscle. Am J Physiol Regul Integr Comp Physiol 276: R331-R339, 1999.
37. Gottlieb P, Folgering J, Maroto R, Raso A, Wood TG, Kurosky A, Bowman C, Bichet D, Patel A, Sachs F, Martinac B, Hamill OP, Honore E. Revisiting TRPC1 and TRPC6 mechanosensitivity. Pflügers Arch 455: 1097-1103, 2008.
38. Hewavitharana T, Deng X, Soboloff J, Gill DL. Role of STIM and Orai proteins in the store-operated calcium signaling pathway. Cell Calcium 42: 173-182, 2007.
39. Hill A, Kupalov P. Anaerobic and aerobic activity in isolated muscle. Proc R Soc Lond B 105: 313-322, 1929.
40. + overload and enhanced cell death. J Gen Physiol 132: 199-208, 2008.
41. 2+ influx via TRPV2 ameliorates muscular dystrophy in animal models. Hum Mol Genet 18: 824-834, 2009.
42. Jones DA, de Ruiter CJ, de Haan A. Change in contractile properties of human muscle in relationship to the loss of power and slowing of relaxation seen with fatigue. J Physiol 576: 913-922, 2006.
43. Kabbara AA, Allen DG. The role of calcium stores in fatigue of isolated single muscle fibres from the cane toad. J Physiol 519: 169-176, 1999.
44. 2+ influx requires the channel function of Orai1 and TRPC1. J Biol Chem 284: 9733-9741, 2009.
45. 2+ release in mammalian skeletal muscle. J Physiol 583: 81-97, 2007.
46. 2+ flux through the transverse tubular membrane, activated by individual action potentials in mammalian skeletal muscle. J Physiol 587: 2299-2312, 2009.
47. Liao Y, Erxleben C, Abramowitz J, Flockerzi V, Zhu MX, Armstrong DL, Birnbaumer L. Functional interactions among Orai1, TRPCs, and STIM1 suggest a STIM-regulated heteromeric Orai/TRPC model for SOCE/Icrac channels. Proc Natl Acad Sci USA 105: 2895-2900, 2008.
48. 2+ channels. Role of acidic amino acid residues in the S5-S6 region. J Biol Chem 278: 11337-11343, 2003.
49. Louis M, Zanou N, Van Schoor M, Gailly P. TRPC1 regulates skeletal myoblast migration and differentiation. J Cell Sci 121: 3951-3959, 2008.
50. 2+ entry in skeletal muscle on STIM1 and Orai1. J Physiol 586: 4815-4824, 2008.
51. Ma R, Rundle D, Jacks J, Koch M, Downs T, Tsiokas L. Inhibitor of myogenic family, a novel suppressor of store-operated currents through an interaction with TRPC1. J Biol Chem 278: 52763-52772, 2003.
52. Marechal G, Beckers-Bleukx G. Force-velocity relation and isomyosins in soleus muscles from two strains of mice (C57 and NMRI). Pflügers Arch 424: 478-487, 1993.
53. Maroto R, Raso A, Wood TG, Kurosky A, Martinac B, Hamill OP. TRPC1 forms the stretch-activated cation channel in vertebrate cells. Nat Cell Biol 7: 179-185, 2005.
54. Martonosi AN, Pikula S. The network of calcium regulation in muscle. Acta Biochim Pol 50: 1-30, 2003.
55. Merritt JE, Jacob R, Hallam TJ. Use of manganese to discriminate between calcium influx and mobilization from internal stores in stimulated human neutrophils. J Biol Chem 264: 1522-1527, 1989.
56. Mizunoya W, Wakamatsu J, Tatsumi R, Ikeuchi Y. Protocol for high-resolution separation of rodent myosin heavy chain isoforms in a mini-gel electrophoresis system. Anal Biochem 377: 111-113, 2008.
57. Peel SE, Liu B, Hall IP. ORAI and store-operated calcium influx in human airway smooth muscle cells. Am J Respir Cell Mol Biol 38: 744-749, 2008.
58. 2+ handling and survival in mdx skeletal muscle cells. FEBS Lett 439: 357-362, 1998.
59. Raymackers JM, Debaix H, Colson-Van Schoor M, De Backer F, Tajeddine N, Schwaller B, Gailly P, Gillis JM. Consequence of parvalbumin deficiency in the mdx mouse: histological, biochemical and mechanical phenotype of a new double mutant. Neuromuscul Disord 13: 376-387, 2003.
60. Raymackers JM, Gailly P, Schoor MC, Pette D, Schwaller B, Hunziker W, Celio MR, Gillis JM. Tetanus relaxation of fast skeletal muscles of the mouse made parvalbumin deficient by gene inactivation. J Physiol 527: 355-364, 2000.
61. Rolland JF, De Luca A, Burdi R, Andreetta F, Confalonieri P, Conte Camerino D. Overactivity of exercise-sensitive cation channels and their impaired modulation by IGF-1 in mdx native muscle fibers: beneficial effect of pentoxifylline. Neurobiol Dis 24: 466-474, 2006.
62. 2+-permeable channels in animal cells. Handb Exp Pharmacol: 23-52, 2007.
63. Saleh SN, Albert AP, Peppiatt CM, Large WA. Angiotensin II activates two cation conductances with distinct TRPC1 and TRPC6 channel properties in rabbit mesenteric artery myocytes. J Physiol 577: 479-495, 2006.
64. Schakman O, Gilson H, de Coninck V, Lause P, Verniers J, Havaux X, Ketelslegers JM, Thissen JP. Insulin-like growth factor-I gene transfer by electroporation prevents skeletal muscle atrophy in glucocorticoidtreated rats. Endocrinology 146: 1789-1797, 2005.
65. Soboloff J, Spassova MA, Dziadek MA, Gill DL. Calcium signals mediated by STIM and Orai proteins-a new paradigm in inter-organelle communication. Biochim Biophys Acta 1763: 1161-1168, 2006.
66. Stephenson DG, Lamb GD, Stephenson GM. Events of the excitationcontraction-relaxation (E-C-R) cycle in fast- and slow-twitch mammalian muscle fibres relevant to muscle fatigue. Acta Physiol Scand 162: 229-245, 1998.
67. Stiber JA, Zhang ZS, Burch J, Eu JP, Zhang S, Truskey GA, Seth M, Yamaguchi N, Meissner G, Shah R, Worley PF, Williams RS, Rosenberg PB. Mice lacking Homer 1 exhibit a skeletal myopathy characterized by abnormal transient receptor potential channel activity. Mol Cell Biol 28: 2637-2647, 2008.
68. Suchyna TM, Sachs F. Mechanosensitive channel properties and membrane mechanics in mouse dystrophic myotubes. J Physiol 581: 369-387, 2007.
69. Turner PR, Westwood T, Regen CM, Steinhardt RA. Increased protein degradation results from elevated free calcium levels found in muscle from mdx mice. Nature 335: 735-738, 1988.
70. Vandebrouck A, Sabourin J, Rivet J, Balghi H, Sebille S, Kitzis A, Raymond G, Cognard C, Bourmeyster N, Constantin B. Regulation of capacitative calcium entries by alpha1-syntrophin: association of TRPC1 with dystrophin complex and the PDZ domain of alpha1-syntrophin. FASEB J 21: 608-617, 2007.
71. Vandebrouck C, Martin D, Colson-Van Schoor M, Debaix H, Gailly P. Involvement of TRPC in the abnormal calcium influx observed in dystrophic (mdx) mouse skeletal muscle fibers. J Cell Biol 158: 1089-1096, 2002.
72. 2+]i to the slowing of relaxation in fatigued single fibres from mouse skeletal muscle. J Physiol 468: 729-740, 1993.
73. 2+]i and cross-bridges. J Gen Physiol 109: 385-399, 1997.
74. Worley PF, Zeng W, Huang GN, Yuan JP, Kim JY, Lee MG, Muallem S. TRPC channels as STIM1-regulated store-operated channels. Cell Calcium 42: 205-211, 2007.
75. Yuan JP, Zeng W, Huang GN, Worley PF, Muallem S. STIM1 heteromultimerizes TRPC channels to determine their function as storeoperated channels. Nat Cell Biol 9: 636-645, 2007.
76. Zanou N, Iwata Y, Schakman O, Lebacq J, Wakabayashi S, Gailly P. Essential role of TRPV2 ion channel in the sensitivity of dystrophic muscle to eccentric contractions. FEBS Lett (October 16, 2009). doi: 10.1016/j.febslet.2009.10.033.