Involvement of TRPV2 and SOCE in calcium influx disorder in DMD primary human myotubes with a specific contribution of α1-syntrophin and PLC/PKC in SOCE regulation

American Journal of Physiology - Cell Physiology

Volumn 304, Issue 9, 2013, Pages

  Harisseh, Rania ^a   Chatelier, Aurélien ^a   Magaud, Christophe ^a   Déliot, Nadine ^a   Constantin, Bruno ^a  

^a UNIVERSITÉ DE POITIERS   (France)

Author keywords

1 syntrophin; Ca2+ PLC PKC; DMD; Human primary myotubes; SOCE; TRPV2

Indexed keywords

CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL 1; PHOSPHOLIPASE C; PROTEIN KINASE C; STROMAL INTERACTION MOLECULE 1; SYNTROPHIN; SYNTROPHIN ALPHA 1; TRANSIENT RECEPTOR POTENTIAL CHANNEL 1; TRANSIENT RECEPTOR POTENTIAL CHANNEL 4; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 2;

ARTICLE; CALCIUM CURRENT; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; CONTROLLED STUDY; DUCHENNE MUSCULAR DYSTROPHY; FLUORESCENCE ANALYSIS; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MYOTUBE; PRIORITY JOURNAL; PROTEIN DOMAIN; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STORE OPERATED CALCIUM ENTRY; WESTERN BLOTTING;

Α1-SYNTROPHIN; CA2+/PLC/PKC; DMD; HUMAN PRIMARY MYOTUBES; SOCE; TRPV2;

CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS; CALCIUM SIGNALING; CALCIUM-BINDING PROTEINS; CELLS, CULTURED; ESTRENES; GADOLINIUM; GENE EXPRESSION; HUMANS; IMIDAZOLES; INDOLES; MALEIMIDES; MEMBRANE PROTEINS; MUSCLE FIBERS, SKELETAL; MUSCLE PROTEINS; MUSCULAR DYSTROPHY, DUCHENNE; NEOPLASM PROTEINS; NIFEDIPINE; PATCH-CLAMP TECHNIQUES; PRIMARY CELL CULTURE; PROTEIN KINASE C; PYRROLIDINONES; SARCOPLASMIC RETICULUM; TRPC CATION CHANNELS; TRPV CATION CHANNELS; TYPE C PHOSPHOLIPASES;

MURINAE;

EID: 84878667441     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00182.2012     Document Type: Article

References (65)

1. Adams ME, Dwyer TM, Dowler LL, White RA, Froehner SC. Mouse alpha 1-and beta 2-syntrophin gene structure, chromosome localization, and homology with a discs large domain. J Biol Chem 270: 25859-25865, 1995.
2. 2+-permeable nonselective cation channels in smooth muscle cells. Cell Calcium 33: 345-356, 2003.
3. Antigny F, Jousset H, Konig S, Frieden M. Thapsigargin activates Ca(2)? entry both by store-dependent, STIM1/Orai1-mediated, and store-independent, TRPC3/PLC/PKC-mediated pathways in human endothelial cells. Cell Calcium 49: 115-127, 2011.
4. Batchelor CL, Winder SJ. Sparks, signals and shock absorbers: how dystrophin loss causes muscular dystrophy. Trends Cell Biol 16: 198-205, 2006.
5. Berchtold MW, Brinkmeier H, Muntener M. Calcium ion in skeletal muscle: its crucial role for muscle function, plasticity, and disease. Physiol Rev 80: 1215-1265, 2000.
6. Birnbaumer L. The TRPC class of ion channels: a critical review of their roles in slow, sustained increases in intracellular Ca(2?) concentrations. Annu Rev Pharmacol Toxicol 49: 395-426, 2009.
7. Bodensteiner JB, Engel AG. Intracellular calcium accumulation in Duch-enne dystrophy and other myopathies: a study of 567, 000 muscle fibers in 114 biopsies. Neurology 28: 439-446, 1978.
8. Boni LT, Rando RR. The nature of protein kinase C activation by physically defined phospholipid vesicles and diacylglycerols. J Biol Chem 260: 10819-10825, 1985.
9. Broad LM, Braun FJ, Lievremont JP, Bird GS, Kurosaki T, Putney JW Jr. Role of the phospholipase C-inositol 1, 4, 5-trisphosphate pathway in calcium release-activated calcium current and capacitative calcium entry. J Biol Chem 276: 15945-15952, 2001.
10. Cardenas C, Muller M, Jaimovich E, Perez F, Buchuk D, Quest AF, Carrasco MA. Depolarization of skeletal muscle cells induces phosphor-ylation of cAMP response element binding protein via calcium and protein kinase Calpha. J Biol Chem 279: 39122-39131, 2004.
11. Clapham DE, Runnels LW, Strubing C. The TRP ion channel family. Nat Rev Neurosci 2: 387-396, 2001.
12. Deval E, Levitsky DO, Marchand E, Cantereau A, Raymond G, Cognard C. Na(+)/Ca(2+) exchange in human myotubes: intracellular calcium rises in response to external sodium depletion are enhanced in DMD. Neuromuscul Disord 12: 665-673, 2002.
13. 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.
14. 2+entry in malignant hyperthermia-susceptible human skele-tal muscle. J Biol Chem 285: 25645-25653, 2010.
15. Edwards JN, Murphy RM, Cully TR, von WF, Friedrich O, Launiko-nis BS. Ultra-rapid activation and deactivation of store-operated Ca(2+) entry in skeletal muscle. Cell Calcium 47: 458-467, 2010.
16. Faenza I, Bavelloni A, Fiume R, Santi P, Martelli AM, Maria BA, Lo V, V, Manzoli L, Cocco L. Expression of phospholipase C beta family isoenzymes in C2C12 myoblasts during terminal differentiation. J Cell Physiol 200: 291-296, 2004.
17. Fong PY, Turner PR, Denetclaw WF, Steinhardt RA. Increased activ-ity of calcium leak channels in myotubes of Duchenne human and mdx mouse origin. Science 250: 673-676, 1990.
18. Franco A Jr, Lansman JB. Stretch-sensitive channels in developing muscle cells from a mouse cell line. J Physiol 427: 361-380, 1990.
19. Franco-Obregon A, Lansman JB. Changes in mechanosensitive channel gating following mechanical stimulation in skeletal muscle myotubes from the mdx mouse. J Physiol 539: 391-407, 2002.
20. He LP, Hewavitharana T, Soboloff J, Spassova MA, Gill DL. A functional link between store-operated and TRPC channels revealed by the 3, 5-bis(trifluoromethyl)pyrazole derivative, BTP2. J Biol Chem 280: 10997-11006, 2005.
21. Helton TD, Xu W, Lipscombe D. Neuronal L-type calcium channels open quickly and are inhibited slowly. J Neurosci 25: 10247-10251, 2005.
22. Hopf FW, Reddy P, Hong J, Steinhardt RA. A capacitative calcium current in cultured skeletal muscle cells is mediated by the calcium-specific leak channel and inhibited by dihydropyridine compounds. J Biol Chem 271: 22358-22367, 1996.
23. Hopf FW, Turner PR, Denetclaw WF Jr, Reddy P, Steinhardt RA. A critical evaluation of resting intracellular free calcium regulation in dys-trophic mdx muscle. Am J Physiol Cell Physiol 271: C1325-C1339, 1996.
24. Imbert N, Cognard C, Duport G, Guillou C, Raymond G. Abnormal calcium homeostasis in Duchenne muscular dystrophy myotubes contract-ing in vitro. Cell Calcium 18: 177-186, 1995.
25. Imbert N, Vandebrouck C, Constantin B, Duport G, Guillou C, Cognard C, Raymond G. Hypoosmotic shocks induce elevation of resting calcium level in Duchenne muscular dystrophy myotubes contract-ing in vitro. Neuromuscul Disord 6: 351-360, 1996.
26. Imbert N, Vandebrouck C, Duport G, Raymond G, Hassoni AA, Constantin B, Cullen MJ, Cognard C. Calcium currents and transients in co-cultured contracting normal and Duchenne muscular dystrophy human myotubes. J Physiol 534: 343-355, 2001.
27. 2+influx and IL-2 production in T lymphocytes. J Immunol 170: 4441-4449, 2003.
28. 2+-permeable growth factor-regulated channel. J Cell Biol 161: 957-967, 2003.
29. 2+influx via TRPV2 ameliorates muscular dystrophy in animal models. Hum Mol Genet 18: 824-834, 2009.
30. Jin W, Lo TM, Loh HH, Thayer SA. U73122 inhibits phospholipase C-dependent calcium mobilization in neuronal cells. Brain Res 642: 237-243, 1994.
31. Kanwar U, Anand RJ, Sanyal SN. The effect of nifedipine, a calcium channel blocker, on human spermatozoal functions. Contraception 48: 453-470, 1993.
32. Kanzaki M, Zhang YQ, Mashima H, Li L, Shibata H, Kojima I. Translocation of a calcium-permeable cation channel induced by insulin-like growth factor-I. Nat Cell Biol 1: 165-170, 1999.
33. 2+channel. J Biol Chem 285: 25720-25730, 2010.
34. 2+homeostasis in skeletal-muscle development and function. Skelet Muscle 1: 16, 2011.
35. 2+entry into mouse skeletal muscle fibres. J Physiol 533: 185-199, 2001.
36. Leffler A, Linte RM, Nau C, Reeh P, Babes A. A high-threshold heat-activated channel in cultured rat dorsal root ganglion neurons resem-bles TRPV2 and is blocked by gadolinium. Eur J Neurosci 26: 12-22, 2007.
37. Liberona JL, Powell JA, Shenoi S, Petherbridge L, Caviedes R, Jaimovich E. Differences in both inositol 1, 4, 5-trisphosphate mass and inositol 1, 4, 5-trisphosphate receptors between normal and dystrophic skeletal muscle cell lines. Muscle Nerve 21: 902-909, 1998.
38. 2+influx. Curr Biol 15: 1235-1241, 2005.
39. Lopez E, Jardin I, Berna-Erro A, Bermejo N, Salido GM, Sage SO, Rosado JA, Redondo PC. STIM1 tyrosine-phosphorylation is required for STIM1-Orai1 association in human platelets. Cell Signal 24: 1315-1322, 2012.
40. 2+entry in skeletal muscle on STIM1 and Orai1. J Physiol 586: 4815-4824, 2008.
41. Marchand E, Constantin B, Balghi H, Claudepierre MC, Cantereau A, Magaud C, Mouzou A, Raymond G, Braun S, Cognard C. Improve-ment of calcium handling and changes in calcium-release properties after mini-or full-length dystrophin forced expression in cultured skeletal myotubes. Exp Cell Res 297: 363-379, 2004.
42. Millay DP, Goonasekera SA, Sargent MA, Maillet M, Aronow BJ, Molkentin JD. Calcium influx is sufficient to induce muscular dystrophy through a TRPC-dependent mechanism. Proc Natl Acad Sci USA 106: 19023-19028, 2009.
43. Moran MM, Xu H, Clapham DE. TRP ion channels in the nervous system. Curr Opin Neurobiol 14: 362-369, 2004.
44. Muraki K, Iwata Y, Katanosaka Y, Ito T, Ohya S, Shigekawa M, Imaizumi Y. TRPV2 is a component of osmotically sensitive cation channels in murine aortic myocytes. Circ Res 93: 829-838, 2003.
45. Neeper MP, Liu Y, Hutchinson TL, Wang Y, Flores CM, Qin N. Activation properties of heterologously expressed mammalian TRPV2: evidence for species dependence. J Biol Chem 282: 15894-15902, 2007.
46. Pozo-Guisado E, Campbell DG, Deak M, varez-Barrientos A, Morrice NA, Alvarez IS, Alessi DR, Martin-Romero FJ. Phosphorylation of STIM1 at ERK1/2 target sites modulates store-operated calcium entry. J Cell Sci 123: 3084-3093, 2010.
47. Putney JW Jr. Capacitative calcium entry revisited. Cell Calcium 11: 611-624, 1990.
48. 2+channel function. J Cell Biol 169: 435-445, 2005.
49. Sabourin J, Harisseh R, Harnois T, Magaud C, Bourmeyster N, Deliot N, Constantin B. Dystrophin/alpha1-syntrophin scaffold regulated PLC/ PKC-dependent store-operated calcium entry in myotubes. Cell Calcium 52: 445-456, 2012.
50. Sabourin J, Lamiche C, Vandebrouck A, Magaud C, Rivet J, Cognard C, Bourmeyster N, Constantin B. Regulation of TRPC1 and TRPC4 cation channels requires an alpha1-syntrophin-dependent complex in skel-etal mouse myotubes. J Biol Chem 284: 36248-36261, 2009.
51. Salido GM, Jardin I, Rosado JA. The TRPC ion channels: association with Orai1 and STIM1 proteins and participation in capacitative and non-capacitative calcium entry. Adv Exp Med Biol 704: 413-433, 2011.
52. Smyth JT, Petranka JG, Boyles RR, Dehaven WI, Fukushima M, Johnson KL, Williams JG, Putney JW Jr. Phosphorylation of STIM1 underlies suppression of store-operated calcium entry during mitosis. Nat Cell Biol 11: 1465-1472, 2009.
53. Stiber J, Hawkins A, Zhang ZS, Wang S, Burch J, Graham V, Ward CC, Seth M, Finch E, Malouf N, Williams RS, Eu JP, Rosenberg P. STIM1 signalling controls store-operated calcium entry required for de-velopment and contractile function in skeletal muscle. Nat Cell Biol 10: 688-697, 2008.
54. Stiber JA, Rosenberg PB. The role of store-operated calcium influx in skeletal muscle signaling. Cell Calcium 49: 341-349, 2011.
55. Tinsley JM, Fairclough RJ, Storer R, Wilkes FJ, Potter AC, Squire SE, Powell DS, Cozzoli A, Capogrosso RF, Lambert A, Wilson FX, Wren SP, De LA, Davies KE. Daily treatment with SMTC1100, a novel small molecule utrophin upregulator, dramatically reduces the dystrophic symptoms in the mdx mouse. PLos One 6: e19189, 2011.
56. Turner PR, Fong PY, Denetclaw WF, Steinhardt RA. Increased cal-cium influx in dystrophic muscle. J Cell Biol 115: 1701-1712, 1991.
57. Tyler KL. Origins and early descriptions of "Duchenne muscular dystro-phy". Muscle Nerve 28: 402-422, 2003.
58. Vandebrouck A, Ducret T, Basset O, Sebille S, Raymond G, Ruegg U, Gailly P, Cognard C, Constantin B. Regulation of store-operated cal-cium entries and mitochondrial uptake by minidystrophin expression in cultured myotubes. FASEB J 20: 136-138, 2006.
59. 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.
60. Vandebrouck C, Duport G, Cognard C, Raymond G. Cationic channels in normal and dystrophic human myotubes. Neuromuscul Disord 11: 72-79, 2001.
61. Vandebrouck C, Martin D, Colson-Van SM, Debaix H, Gailly P. Involvement of TRPC in the abnormal calcium influx observed in dystro-phic (mdx) mouse skeletal muscle fibers. J Cell Biol 158: 1089-1096, 2002.
62. Vig M, Beck A, Billingsley JM, Lis A, Parvez S, Peinelt C, Koomoa DL, Soboloff J, Gill DL, Fleig A, Kinet JP, Penner R. CRACM1 multimers form the ion-selective pore of the CRAC channel. Curr Biol 16: 2073-2079, 2006.
63. 2+ pools in primary human skeletal muscle cells. Naunyn Schmiedebergs Arch Pharmacol 367: 353-363, 2003.
64. 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 583: 3600-3604, 2009.
65. 2+ channels and T-lymphocyte activation by the pyrazole derivative BTP2. J Biol Chem 279: 12427-12437, 2004.