Neuromuscular Disorders
Volume 18, Issue 6 , Pages 501-513 , June 2008

Transient receptor potential cation channels in normal and dystrophic mdx muscle

Received 15 January 2008 ,Revised 28 March 2008 ,Accepted 8 April 2008.

References 

  1. Hoffman EP, Brown RH, Kunkel LM. Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell. 1987;51:919–928
  2. Campbell KP. Three muscular dystrophies: loss of cytoskeleton-extracellular matrix linkage. Cell. 1995;80:675–679
  3. Emery AEH, Emery MHL. Refining the clinical picture. In:  Emery AEH editors. The history of a genetic disease: Duchenne muscular dystrophy or Meryons´s disease. London: The Royal Society of Medicine Press Ltd; 1995;p. 89–99
  4. Hoffman EP, Gorospe JRM. The animal models of Duchenne muscular dystrophy: windows on the pathophysiological consequences of dystrophin deficiency. Curr Top Membr. 1991;38:113–154
  5. Rüdel R, Brinkmeier H. 76th ENMC international workshop: pathophysiology and therapy in the mdx mouse 21–23 January 2000, Naarden, The Netherlands. Neuromuscul Disord. 2002;12:415–420
  6. Alderton JM, Steinhardt RA. How calcium influx through calcium leak channels is responsible for the elevated levels of calcium-dependent proteolysis in dystrophic myotubes. Trends Cardiovasc Med. 2000;10:268–272
  7. Dowling P, Doran P, Ohlendieck K. Drastic reduction of sarcalumenin in Dp427 (dystrophin of 427kDa)-deficient fibres indicates that abnormal calcium handling plays a key role in muscular dystrophy. Biochem J. 2004;379:479–488
  8. Gailly P. New aspects of calcium signaling in skeletal muscle cells: implications in Duchenne muscular dystrophy. Biochim Biophys Acta. 2002;1600:38–44
  9. Berchtold MW, Brinkmeier H, Müntener M. Calcium ion in skeletal muscle: its crucial role for muscle function, plasticity, and disease. Physiol Rev. 2000;80:1215–1265
  10. Gillis JM. Membrane abnormalities and Ca homeostasis in muscles of the mdx mouse, an animal model of the Duchenne muscular dystrophy: a review. Acta Physiol Scand. 1996;156:397–406
  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. 1978;28:439–446
  12. Jackson MJ, Jones DA, Edwards RH. Measurements of calcium and other elements in muscle biopsy samples from patients with Duchenne muscular dystrophy. Clin Chim Acta. 1985;147:215–221
  13. Glesby MJ, Rosenmann E, Nylen EG, Wrogemann K. Serum CK, calcium, magnesium, and oxidative phosphorylation in mdx mouse muscular dystrophy. Muscle Nerve. 1988;11:852–856
  14. 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. 1993;14:473–483
  15. Head SI. Membrane potential, resting calcium and calcium transients in isolated muscle fibres from normal and dystrophic mice. J Physiol. 1993;469:11–19
  16. Pressmar J, Brinkmeier H, Seewald MJ, Naumann T, Rüdel R. Intracellular Ca2+ concentrations are not elevated in resting cultured muscle from Duchenne (DMD) patients and in MDX mouse muscle fibres. Pflügers Arch. 1994;426:499–505
  17. Basset O, Boittin FX, Dorchies OM, Chatton JY, van Breemen C, Rüegg UT. Involvement of inositol 1,4,5-trisphosphate in nicotinic calcium responses in dystrophic myotubes assessed by near-plasma membrane calcium measurement. J Biol Chem. 2004;279:47092–47100
  18. 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. 2000;97:4950–4955
  19. MacLennan PA, McArdle A, Edwards RH. Effects of calcium on protein turnover of incubated muscles from mdx mice. Am J Physiol. 1991;260:E594–E598
  20. Jimena I, Pena J, Luque E, Vaamonde R. Muscle hypertrophy experimentally induced by administration of denervated muscle extract. J Neuropathol Exp Neurol. 1993;52:379–386
  21. Culligan K, Banville N, Dowling P, Ohlendieck K. Drastic reduction of calsequestrin-like proteins and impaired calcium binding in dystrophic mdx muscle. J Appl Physiol. 2002;92:435–445
  22. Friedrich O, Both M, Gillis JM, Chamberlain JS, Fink RH. Mini-dystrophin restores L-type calcium currents in skeletal muscle of transgenic mdx mice. J Physiol. 2004;555:251–265
  23. Yeung EW, Whitehead NP, Suchyna TM, Gottlieb PA, Sachs F, Allen DG. Effects of stretch-activated channel blockers on [Ca2+]i and muscle damage in the mdx mouse. J Physiol. 2005;562:367–380
  24. Fraysse B, Liantonio A, Cetrone M, et al. The alteration of calcium homeostasis in adult dystrophic mdx muscle fibers is worsened by a chronic exercise in vivo. Neurobiol Dis. 2004;17:144–154
  25. 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. 2006;24:466–474
  26. Boittin FX, Petermann O, Hirn C, et al. Ca2+-independent phospholipase A2 enhances store-operated Ca2+ entry in dystrophic skeletal muscle fibers. J Cell Sci. 2006;119:3733–3742
  27. 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. 2006;575:913–924
  28. Tutdibi O, Brinkmeier H, Rüdel R, Föhr KJ. Increased calcium entry into dystrophin-deficient muscle fibres of MDX and ADR-MDX mice is reduced by ion channel blockers. J Physiol. 1999;515:859–868
  29. 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. 2002;158:1089–1096
  30. Montell C. The TRP superfamily of cation channels. Sci STKE. 2005;2005:re3
  31. Iwata Y, Katanosaka Y, Arai Y, Komamura K, Miyatake K, Shigekawa M. A novel mechanism of myocyte degeneration involving the Ca2+-permeable growth factor-regulated channel. J Cell Biol. 2003;161:957–967
  32. Kunert-Keil C, Bisping F, Krüger J, Brinkmeier H. Tissue-specific expression of TRP channel genes in the mouse and its variation in three different mouse strains. BMC Genomics. 2006;7:159
  33. Smith PK, Krohn RI, Hermanson GT, et al. Measurement of protein using bicinchoninic acid. Anal Biochem. 1985;150:76–85
  34. Allen DG, Whitehead NP, Yeung EW. Mechanisms of stretch-induced muscle damage in normal and dystrophic muscle: role of ionic changes. J Physiol. 2005;567:723–735
  35. 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. 2006;27:375–386
  36. Imbert N, Vandebrouck C, Duport G, et al. Calcium currents and transients in co-cultured contracting normal and Duchenne muscular dystrophy human myotubes. J Physiol. 2001;534:343–355
  37. Lansman JB, Franco-Obregon A. Mechanosensitive ion channels in skeletal muscle: a link in the membrane pathology of muscular dystrophy. Clin Exp Pharmacol Physiol. 2006;33:649–656
  38. Vandebrouck A, Sabourin J, Rivet J, et al. Regulation of capacitative calcium entries by alpha1-syntrophin: association of TRPC1 with dystrophin complex and the PDZ domain of alpha1-syntrophin. FASEB J. 2007;21:608–617
  39. Feske S, Gwack Y, Prakriya M, et al. A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature. 2006;441:179–185
  40. Ambudkar IS, Ong HL, Liu X, Bandyopadhyay B, Cheng KT. TRPC1: the link between functionally distinct store-operated calcium channels. Cell Calcium. 2007;42:213–223
  41. Turk R, Sterrenburg E, de Meijer EJ, van Ommen GJ, den Dunnen JT, Hoen PA. Muscle regeneration in dystrophin-deficient mdx mice studied by gene expression profiling. BMC Genomics. 2005;6:98
  42. Rouger K, Le Cunff M, Steenman M, et al. Global/temporal gene expression in diaphragm and hindlimb muscles of dystrophin-deficient (mdx) mice. Am J Physiol Cell Physiol. 2002;283:C773–C784
  43. Smyth JT, Lemonnier L, Vazquez G, Bird GS, Putney JW. Dissociation of regulated trafficking of TRPC3 channels to the plasma membrane from their activation by phospholipase C. J Biol Chem. 2006;281:11712–11720
  44. Dietrich A, Mederos YSM, Gollasch M, et al. Increased vascular smooth muscle contractility in TRPC6−/− mice. Mol Cell Biol. 2005;25:6980–6989
  45. Nilius B, Prenen J, Tang J, et al. Regulation of the Ca2+ sensitivity of the nonselective cation channel TRPM4. J Biol Chem. 2005;280:6423–6433
  46. Liedtke W. TRPV4 plays an evolutionary conserved role in the transduction of osmotic and mechanical stimuli in live animals. J Physiol. 2005;567:53–58
  47. Monteilh-Zoller MK, Hermosura MC, Nadler MJ, Scharenberg AM, Penner R, Fleig A. TRPM7 provides an ion channel mechanism for cellular entry of trace metal ions. J Gen Physiol. 2003;121:49–60
  48. Chakkalakal JV, Michel SA, Chin ER, Michel RN, Jasmin BJ. Targeted inhibition of Ca2+/calmodulin signaling exacerbates the dystrophic phenotype in mdx mouse muscle. Hum Mol Genet. 2006;15:1423–1435
  49. Zhu MX. Multiple roles of calmodulin and other Ca2+-binding proteins in the functional regulation of TRP channels. Pflügers Arch. 2005;451:105–115
  50. Schaefer M, Plant TD, Obukhov AG, Hofmann T, Gudermann T, Schultz G. Receptor-mediated regulation of the nonselective cation channels TRPC4 and TRPC5. J Biol Chem. 2000;275:17517–17526
  51. Plant TD, Schaefer M. Receptor-operated cation channels formed by TRPC4 and TRPC5. Naunyn Schmiedebergs Arch Pharmacol. 2005;371:266–276
  52. Xu XZ, Moebius F, Gill DL, Montell C. Regulation of melastatin, a TRP-related protein, through interaction with a cytoplasmic isoform. Proc Natl Acad Sci USA. 2001;98:10692–10697
  53. Liu X, Bandyopadhyay BC, Singh BB, Groschner K, Ambudkar IS. Molecular analysis of a store-operated and 2-acetyl-sn-glycerol-sensitive non-selective cation channel. Heteromeric assembly of TRPC1–TRPC3. J Biol Chem. 2005;280:21600–21606
  54. Bulfield G, Siller WG, Wight PA, Moore KJ. X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc Natl Acad Sci USA. 1984;81:1189–1192
  55. Dangain J, Vrbova G. Muscle development in mdx mutant mice. Muscle Nerve. 1984;7:700–704
  56. Torres LF, Duchen LW. The mutant mdx: inherited myopathy in the mouse. Morphological studies of nerves, muscles and end-plates. Brain. 1987;110:269–299
  57. Pastoret C, Sebille A. mdx mice show progressive weakness and muscle deterioration with age. J Neurol Sci. 1995;129:97–105

PII: S0960-8966(08)00100-4

doi: 10.1016/j.nmd.2008.04.003

Neuromuscular Disorders
Volume 18, Issue 6 , Pages 501-513 , June 2008