Negative modulation of inositol 1,4,5-trisphosphate type 1 receptor expression prevents dystrophin-deficient muscle cells death

American Journal of Physiology - Cell Physiology

Volumn 297, Issue 5, 2009, Pages

  Mondin, Ludivine ^a   Balghi, Haouaria ^a   Constantin, Bruno ^a   Cognard, Christian ^a   Sebille, Stéphane ^a  

^a UNIVERSITÉ DE POITIERS   (France)

Author keywords

Calcium regulation; Cyclosporin A; Muscular dystrophy

Indexed keywords

2 AMINOETHOXYDIPHENYLBORANE; CALCIUM; CYCLOSPORIN A; DYSTROPHIN; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; RNA;

ANIMAL CELL; ARTICLE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL DEATH; CELL SURVIVAL; INCUBATION TIME; MOUSE; MUSCLE CELL; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; BLOTTING, WESTERN; CALCIUM SIGNALING; CELL DEATH; CYCLOSPORINE; DYSTROPHIN; ENZYME INHIBITORS; GENE EXPRESSION; GENE EXPRESSION REGULATION; IMAGE PROCESSING, COMPUTER-ASSISTED; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; MICE; MICROSCOPY, CONFOCAL; MUSCLE FIBERS, SKELETAL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING;

EID: 70449644676     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00048.2009     Document Type: Article

References (51)

1. Alderton JM, Ahmed SA, Smith LA, Steinhardt RA. Evidence for a vesicle-mediated maintenance of store-operated calcium channels in a human embryonic kidney cell line. Cell Calcium 28: 161-169, 2000.
2. Alderton JM, Steinhardt RA. Calcium influx through calcium leak channels is responsible for the elevated levels of calcium-dependent proteolysis in dystrophic myotubes. J Biol Chem 275: 9452-9460, 2000. (Pubitemid 30185173)
3. Allen DL, Leinwand LA. Intracellular calcium and myosin isoform transitions. Calcineurin and calcium-calmodulin kinase pathways regulate preferential activation of the IIa myosin heavy chain promoter. J Biol Chem 277: 45323-45330, 2002.
4. Balghi H, Sebille S, Constantin B, Patri S, Thoreau V, Mondin L, Mok E, Kitzis A, Raymond G, Cognard C. Mini-dystrophin expression down-regulates overactivation of G protein-mediated IP3 signaling pathway in dystrophin-deficient muscle cells. J Gen Physiol 127: 171-182, 2006. (Pubitemid 43177139)
5. Balghi H, Sebille S, Mondin L, Cantereau A, Constantin B, Raymond G, Cognard C. Mini-dystrophin expression down-regulates IP3-mediated calcium release events in resting dystrophin-deficient muscle cells. J Gen Physiol 128: 219-230, 2006. (Pubitemid 44156759)
6. Basset O, Boittin FX, Cognard C, Constantin B, Ruegg UT. Bcl-2 overexpression prevents calcium overload and subsequent apoptosis in dystrophic myotubes. Biochem J 395: 267-276, 2006.
7. Batchelor CL, Winder SJ. Sparks, signals and shock absorbers: how dystrophin loss causes muscular dystrophy. Trends Cell Biol 16: 198-205, 2006.
8. Bellinger AM, Reiken S, Carlson C, Mongillo M, Liu X, Rothman L, Matecki S, Lacampagne A, Marks AR. Hypernitrosylated ryanodine receptor calcium release channels are leaky in dystrophic muscle. Nat Med 15: 325-330, 2009.
9. Berridge MJ. Inositol trisphosphate and calcium signalling. Nature 361: 315-325, 1993.
10. Billaud EM. Clinical pharmacology of immunosuppressive drugs: year 2000-time for alternatives. Therapie 55: 177-183, 2000.
11. Bodensteiner JB, Engel AG. Intracellular calcium accumulation in Duchenne dystrophy and other myopathies: a study of 567,000 muscle fibers in 114 biopsies. Neurology 28: 439-446, 1978.
12. Cameron AM, Nucifora FC Jr, Fung ET, Livingston DJ, Aldape RA, Ross CA, Snyder SH. FKBP12 binds the inositol 1,4,5-trisphosphate receptor at leucine-proline (1400 -1401) and anchors calcineurin to this FK506-like domain. J Biol Chem 272: 27582-27588, 1997.
13. Campbell KP. Three muscular dystrophies: loss of cytoskeleton- extracellular matrix linkage. Cell 80: 675-679, 1995.
14. Carrasco MA, Figueroa S. Inositol 1,4,5-trisphosphate 3-kinase activity in frog skeletal muscle. Comp Biochem Physiol B Biochem Mol Biol 110: 747-753, 1995.
15. Constantin B, Sebille S, Cognard C. New insights in the regulation of calcium transfers by muscle dystrophin-based cytoskeleton: implications in DMD. J Muscle Res Cell Motil 27: 375-386, 2006. (Pubitemid 44325616)
16. Duncan CJ. Role of intracellular calcium in promoting muscle damage: a strategy for controlling the dystrophic condition. Experientia 34: 1531-1535, 1978.
17. Dunn SE, Burns JL, Michel RN. Calcineurin is required for skeletal muscle hypertrophy. J Biol Chem 274: 21908-21912, 1999. (Pubitemid 129519743)
18. Enan E, Matsumura F. Specific inhibition of calcineurin by type II synthetic pyrethroid insecticides. Biochem Pharmacol 43: 1777-1784, 1992.
19. Endesfelder S, Bucher S, Kliche A, Reszka R, Speer A. Transfection of normal primary human skeletal myoblasts with p21 and p57 antisense oligonucleotides to improve their proliferation: a first step towards an alternative molecular therapy approach of Duchenne muscular dystrophy. J Mol Med 81: 355-362, 2003.
20. England SB, Nicholson LV, Johnson MA, Forrest SM, Love DR, Zubrzycka-Gaarn EE, Bulman DE, Harris JB, Davies KE. Very mild muscular dystrophy associated with the deletion of 46% of dystrophin. Nature 343: 180-182, 1990.
21. Ervasti JM, Campbell KP. Dystrophin-associated glycoproteins: their possible roles in the pathogenesis of Duchenne muscular dystrophy. Mol Cell Biol Hum Dis Ser 3: 139-166, 1993.
22. Furuichi T, Mikoshiba K. Inositol 1, 4, 5-trisphosphate receptor-mediated Ca2+ signaling in the brain. J Neurochem 64: 953-960, 1995.
23. Genazzani AA, Carafoli E, Guerini D. Calcineurin controls inositol 1,4,5-trisphosphate type 1 receptor expression in neurons. Proc Natl Acad Sci USA 96: 5797-5801, 1999.
24. Gordienko DV, Bolton TB. Crosstalk between ryanodine receptors and IP(3) receptors as a factor shaping spontaneous Ca(2+)-release events in rabbit portal vein myocytes. J Physiol 542: 743-762, 2002.
25. Hanson CJ, Bootman MD, Roderick HL. Cell signalling: IP3 receptors channel calcium into cell death. Curr Biol 14: R933-R935, 2004.
26. Hoffman EP, Brown RH Jr, Kunkel LM. Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 51: 919-928, 1987. (Pubitemid 18099471)
27. Jaimovich E, Reyes R, Liberona JL, Powell JA. IP3 receptors, IP3 transients, and nucleus-associated Ca2+ signals in cultured skeletal muscle. Am J Physiol Cell Physiol 278: C998-C1010, 2000.
28. Lemasters JJ, Qian T, Bradham CA, Brenner DA, Cascio WE, Trost LC, Nishimura Y, Nieminen AL, Herman B. Mitochondrial dysfunction in the pathogenesis of necrotic and apoptotic cell death. J Bioenerg Biomembr 31: 305-319, 1999. (Pubitemid 30058566)
29. 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. (Pubitemid 28262287)
30. Liu J, Farmer JD Jr, Lane WS, Friedman J, Weissman I, Schreiber SL. Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 66: 807-815, 1991. (Pubitemid 121001714)
31. MacMillan D, Currie S, Bradley KN, Muir TC, McCarron JG. In smooth muscle, FK506-binding protein modulates IP3 receptor-evoked Ca2+ release by mTOR and calcineurin. J Cell Sci 118: 5443-5451, 2005.
32. Mallouk N, Jacquemond V, Allard B. Elevated subsarcolemmal Ca2+ in mdx mouse skeletal muscle fibers detected with Ca2+-activated K+ channels. Proc Natl Acad Sci USA 97: 4950-4955, 2000.
33. Marchand E, Constantin B, Balghi H, Claudepierre MC, Cantereau A, Magaud C, Mouzou A, Raymond G, Braun S, Cognard C. Improvement 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.
34. Marchand E, Constantin B, Vandebrouck C, Raymond G, Cognard C. Calcium homeostasis and cell death in Sol8 dystrophin-deficient cell line in culture. Cell Calcium 29: 85-96, 2001. (Pubitemid 32156829)
35. Messina S, Bitto A, Aguennouz M, Minutoli L, Monici MC, Altavilla D, Squadrito F, Vita G. Nuclear factor kappa-B blockade reduces skeletal muscle degeneration and enhances muscle function in Mdx mice. Exp Neurol 198: 234-241, 2006. (Pubitemid 43243761)
36. Misra UK, Gawdi G, Pizzo SV. Cyclosporin A inhibits inositol 1,4,5- trisphosphate binding to its receptors and release of calcium from intracellular stores in peritoneal macrophages. J Immunol 161: 6122-6127, 1998.
37. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65: 55-63, 1983. (Pubitemid 14203433)
38. Mulle C, Benoit P, Pinset C, Roa M, Changeux JP. Calcitonin gene-related peptide enhances the rate of desensitization of the nicotinic acetylcholine receptor in cultured mouse muscle cells. Proc Natl Acad Sci USA 85: 5728-5732, 1988. (Pubitemid 18207108)
39. Pedersen SF, Owsianik G, Nilius B. TRP channels: an overview. Cell Calcium 38: 233-252, 2005.
40. Powell JA, Carrasco MA, Adams DS, Drouet B, Rios J, Muller M, Estrada M, Jaimovich E. IP(3) receptor function and localization in myotubes: an unexplored Ca(2+) signaling pathway in skeletal muscle. J Cell Sci 114: 3673-3683, 2001. (Pubitemid 33041049)
41. Rios E, Pizarro G. Voltage sensor of excitation-contraction coupling in skeletal muscle. Physiol Rev 71: 849-908, 1991.
42. Stupka N, Gregorevic P, Plant DR, Lynch GS. The calcineurin signal transduction pathway is essential for successful muscle regeneration in mdx dystrophic mice. Acta Neuropathol (Berl) 107: 299-310, 2004. (Pubitemid 38477356)
43. Ursu D, Sebille S, Dietze B, Freise D, Flockerzi V, Melzer W. Excitation-contraction coupling in skeletal muscle of a mouse lacking the dihydropyridine receptor subunit gamma1. J Physiol 533: 367-377, 2001. (Pubitemid 32519994)
44. Valdes JA, Gaggero E, Hidalgo J, Leal N, Jaimovich E, Carrasco MA. NFAT activation by membrane potential follows a calcium pathway distinct from other activity-related transcription factors in skeletal muscle cells. Am J Physiol Cell Physiol 294: C715-C725, 2008.
45. Valdes JA, Hidalgo J, Galaz JL, Puentes N, Silva M, Jaimovich E, Carrasco MA. NF-kappaB activation by depolarization of skeletal muscle cells depends on ryanodine and IP3 receptor-mediated calcium signals. Am J Physiol Cell Physiol 292: C1960-C1970, 2007.
46. Vandebrouck A, Ducret T, Basset O, Sebille S, Raymond G, Ruegg U, Gailly P, Cognard C, Constantin B. Regulation of store-operated calcium entries and mitochondrial uptake by minidystrophin expression in cultured myotubes. FASEB J 20: 136-138, 2006.
47. 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. (Pubitemid 46213507)
48. Weinblatt ME. The role of current strategies in the future treatment of rheumatoid arthritis. Rheumatology (Oxford) 38, Suppl 2: 19-23, 1999.
49. Yokota T, Lu QL, Morgan JE, Davies KE, Fisher R, Takeda S, Partridge TA. Expansion of revertant fibers in dystrophic mdx muscles reflects activity of muscle precursor cells and serves as an index of muscle regeneration. J Cell Sci 119: 2679-2687, 2006. (Pubitemid 44184004)
50. 2+ signaling between inositol trisphosphate and ryanodine receptors. Am J Physiol Lung Cell Mol Physiol 285: L680-L690, 2003.
51. 2+ in muscle. Am J Physiol Cell Physiol 288: C377-C388, 2005.