L-type Ca2+ channel function is linked to dystrophin expression in mammalian muscle

PLoS ONE

Volumn 3, Issue 3, 2008, Pages

  Friedrich, Oliver ^a   von Wegner, Frederic ^a   Chamberlain, Jeffrey S ^b   Fink, Rainer H A ^a   Rohrbach, Petra ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL L TYPE; DYSTROPHIN; MYOSIN; 1,4 DIHYDROPYRIDINE; 1,4-DIHYDROPYRIDINE; CALCIUM; CALCIUM CHANNEL BLOCKING AGENT; DIHYDROPYRIDINE DERIVATIVE;

AMPLITUDE MODULATION; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; FEMALE; IMAGE ANALYSIS; IMMUNOFLUORESCENCE; MALE; MAMMAL; MOUSE; MUSCLE CELL; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; STAINING; VOLTAGE CLAMP; AGING; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CONFOCAL MICROSCOPY; DUCHENNE MUSCULAR DYSTROPHY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE;

MAMMALIA; MUS;

AGING; ANIMALS; CALCIUM; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS, L-TYPE; DIHYDROPYRIDINES; DYSTROPHIN; FEMALE; GENE EXPRESSION REGULATION; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED MDX; MICROSCOPY, CONFOCAL; MUSCLE FIBERS; MUSCULAR DYSTROPHY, DUCHENNE; MYOSINS; SIGNAL TRANSDUCTION;

EID: 45849108306     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0001762     Document Type: Article

References (76)

1. Boland BJ, Silbert PL, Groover RV, Wollan PC, Silverstein MD (1996) Skeletal, cardiac and smooth muscle failure in Duchenne muscular dystrophy. Pediatr Neurol 14: 7-12.
2. Melacini P, Vianello A, Villanova C, Fanin M, Miorin M, et al. (1996) Cardiac and respiratory involvement in advanced stage Duchenne muscular dystrophy. Neuromuscul Disord 6: 367-376.
3. Chamberlain JS (2002) Gene therapy of muscular dystrophy. Hum Mol Genetics 11(20): 2355-2362.
4. Denti MA, Rosa A, D'Antona G, Sthandier O, De Angelis FG, et al. (2006) Body-wide gene therapy of Duchenne muscular dystrophy in the mdx mouse model. Proc Natl Acad Sci USA 103: 3758-3763.
5. Hoffman EP, Brown RH, Kunkel LM (1987) Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 51: 919-928.
6. Blake DJ, Weir A, Newey SE, Davies KE (2002) Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol Rev 82: 291-329.
7. Ervasti JM, Campbell KP (1993) A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J Cell Biol 122: 809-823.
8. Moens P, Baatsen PHWW, Marechal G (1993) Increased susceptibility of EDL muscles from mdx mice to damage induced by contractions with stretch. J Muscle Res Cell Motil 14: 446-451.
9. Petrof BJ, Shrager JB, Stedman HH, Kelly AM, Sweeney HL (1993) Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc Natl Acad Sci USA 90: 3710-3714.
10. Head SI, Williams DA, Stephenson DG (1992) Abnormalities in structure and function of limb skeletal muscle fibres of dystrophic mdx mice. Proc R. Soc Lond B Biol Sci 248: 163-169.
11. Constantin B, Sebille S, Cognard C (2006) New insights in the regulation of calcium transfers by muscle dystrophin-based cytoskeleton: implications in DMD. J Muscle Res Cell Motil 27(5-7): 375-386.
12. Divet A, Lompre AM, Huchet-Cadiou C (2005) Effect of cyclopiazonic acid, an inhibitor of the sarcoplasmic reticulum Ca-ATPase, on skeletal muscles from normal and mdx mice. Acta Physiol Scand 184: 173-186.
13. i and muscle damage in the mdx mouse. J Physiol 562-2: 367-380.
14. Wang X, Weisleder N, Collet C, Zhou J, Chu Y, et al. (2005) Uncontrolled calcium sparks act as a dystrophic signal for mammalian muscle. Nat Cell Biol 7(5): 525-530.
15. Woods CE, Novo D, DiFranco M, Capote J, Vergara JL (2005) Propagation in the transverse tubular system and voltage dependence of calcium release in normal and mdx mouse muscle fibres. J Physiol 568.3: 867-880.
16. Tutdibi O, Brinkmeier H, Rüdel R, Fohr EJ (1999) Increased calcium entry into dystrophin-deficient muscle fibres of mdx and adr-mdx mice is reduced by ion channel blockers. J Physiol 515: 859-868.
17. Vandebrouck A, Ducret T, Basset O, Sebille S, Raymond G, et al. (2006) Regulation of store-operated calcium entries and mitochondrial uptake by minidystrophin expression in cultured myotubes. FASEB J 20(1): 136-138.
18. Coirault C, Lambert F, Pourny JC, Lecarpentier Y (2002) Velocity of actomyosin sliding in vitro is reduced in dystrophic mouse diaphragm. Am J Respir Crit Care Med 165(2): 250-253.
19. 2+. J Physiol (London) 420: 337-353.
20. Messina S, Altavilla, D, Aguennouz M, Seminara P, Minutoli L, et al. (2006) Lipid peroxidation blunts nuclear factor κB activation, reduces skeletal muscle degeneration, and enhances muscle function in mdx mice. Am J Pathol 168(3): 918-926.
21. Messina S, Bitto A, Aguennouz M, Minutoli L, Monici MC, et al. (2006) Nuclear factor κB blockade reduces skeletal muscle degeneration and enhances muscle function in mdx mice. Exp Neurol 198(1): 234-241.
22. 2+/calmodulin signalling exacerbates the dystrophic phenotype in mdx mouse muscle. Hum Mol Genet 15(9): 1423-1435.
23. Senter L, Ceoldo S, Petrusa MM, Salviati G (1995) Phosphorylation of dystrophin: effects on actin binding. Biochem Biophys Res Commun 206(1): 57-63.
24. Kumar AK, Khandelwal N, Malya R, Reid MB, Boriek AM (2004) Loss of dystrophin causes aberrant mechanotransduction in, skeletal muscle fibers. FASEB J 18: 102-113.
25. Friedrich O, Both M, Gillis JM, Chamberlain JS, Fink RHA (2004) Mini-dystrophin restores L-type calcium currents in skeletal muscle of transgenic mdx mice. J Physiol 555.1: 251-265.
26. Turner PR, Fong PY, Denetclaw WF, Steinhardt RA (1991) Increased calcium influx in dystrophic muscle. J Cell Biol 115(6): 1701-1712.
27. Fong PY, Turner PR, Denetclaw WF, Steinhardt RA (1990) Increased activity of calcium leak channels in myotubes of Duchenne human and mdx mouse origin. Science 250: 673-676.
28. 2+ homeostasis and of survival in collagenase-isolated muscle fibres from normal and mdx: mice. J Physiol 542(1): 855-865.
29. Gailly P, Boland B, Himpens B, Casteels R, Gillis JM (1993) Critical evaluation of cytosolic calcium determination in resting muscle fibres from normal and dystrophic (mdx) mice. Cell Calcium 14(6): 473-483.
30. 2+ release and depletion fail to affect sarcolemmal ion channel activity in mouse skeletal muscle. J Physiol 575.1: 68-81.
31. Vandebrouck A, Martin D, Colson-Van Shoor M, Debaix H, Gailly P (2002) Involvement of TRPC in the abnormal calcium influx observed in dystrophic mdx mouse skeletal muscle fibres. J Cell Biol 158: 1089-1096.
32. 2+ release. J Cell Biol 174(5): 639-645.
33. 2+ in skeletal muscle fibres from aging mice. Biophys J 78(4): 1947-1954.
34. Ge Y, Molloy MP, Chamberlain JS, Andrews PC (2004) Differential expression of the skeletal muscle proteome in mdx mice at different ages. Electrophoresis 25(15): 2576-2585.
35. Francini F, Bencini C, Squecco R (1996) Activation of L-type calcium channel in twitch skeletal muscle fibres of the frog. J Physiol 494.1: 121-140.
36. 2+ ions in excitation-contraction coupling of skeletal muscle fibres. Biochim Biophys Acta 1241(1): 59-116.
37. 2+ entry into mouse skeletal muscle fibres. J Physiol 533: 185-199.
38. Gonzalez-Serratos H, Valle-Aguilera R, Lathrop DA, del Carmen Garcia M (1982) Slow inward calcium currents have no obvious role in muscle excitation-contraction coupling. Nature 298: 292-294.
39. 2+ in malignant hyperthermia and central core disease. Biochem Biophys Res Commun 322(4): 1256-1266.
40. 2+ signalling and muscle disease. Eur J Biochem 267(17): 5291-5297.
41. Hoffman EP, Morgan JE, Watkins SC, Partridge TA (1990) Somatic reversion/ suppression of the mouse mdx phenotype in vivo. J Neur Sci 99: 9-25.
42. Phelps S, Hauser MA, Cole NM, Rafael JA, Hinkle RT, et al. (1995) Expression of full-length and truncated dystrophin mini-genes in transgenic mdx mice. Hum Mol Genet 4: 1251-1258.
43. Gregorevic P, Blankinship MJ, Allen JM, Crawford RW, Meuse L, et al. (2004) Systemic delivery of genes to striated muscles using adeno-associated viral vectors. Nat Med 10(8): 828-834.
44. 2+ channel by the actin-binding protein alpha-actinin and dystrophin. Am J Physiol Cell Physiol 282(6): C1502-C1511.
45. Woolf PJ, Lu S, Cornford-Nairn RA, Watson M, Xia XH, et al. (2006) Alterations in dihydropyridine receptors in dystrophin-deficient cardiac muscle. Am J Physiol Heart Circ Physiol 290: 2439-2445.
46. Bulfield G, Siller WG, Wight PAL, Moore KJ (1984) X-chromosome-linked muscular dystrophy (mdx) in the mouse. Proc Natl Acad Sci USA 81: 1189-1192.
47. Harper SQ, Hauser MA, DelloRusso C, Duan D, Crawford RW, et al. (2002) Modular flexibility of dystrophin: implications for gene therapy of Duchenne muscular dystrophy. Nat Med 8(3): 253-261.
48. Friedrich O, Ehmer T, Fink RHA (1999) Calcium currents during contraction and shortening in enzymatically isolated murine skeletal muscle fibres. J Physiol 517(3): 757-770.
49. Almers W, Fink R, Palade PT (1981) Calcium depletion in frog muscle tubules: the decline of calcium current under maintained depolarization. J Physiol 312: 177-207.
50. 2+ depletion in the transverse tubular system of mammalian muscle. Biophys J 80(5): 2046-2055.
51. Collet C, Csernoch L, Jacquemond V (2003) Intramembrane charge movement and L-type calcium current in skeletal muscle fibres isolated from control and mdx mice. Biophys J 84(1): 251-265.
52. Bangham AD, Horne RW, Glauert AM, Dingle JT, Lucy JA (1962) Action of saponin on biological cell membranes. Nature 196: 952-955.
53. Launikonis BS, Stephenson DG (1997) Effect of saponin treatment on the sarcoplasmic reticulum of rat, cane toad and crustacean (yabby) skeletal muscle. J Physiol 504: 425-437.
54. Both M, Vogel M, Friedrich O, v Wegner F, Künsting T, et al. (2004) Second harmonic imaging of intrinsic signals in muscle fibres in situ. J Biomed Opt 9(5): 882-892.
55. Pastoret C, Sebille A (1995) Age-related differences in regeneration of dystrophic (mdx) and normal muscle in the mouse. Muscle Nerve 18(10): 1147-1154.
56. Pastoret C, Sebille A (1993) Mdx mice show progressive weakness and muscle deterioration with age. J Neurol Sci 129(2): 97-105.
57. Allard B (2006) Sarcolemmal ion channels in dystrophin-deficient skeletal muscle fibres. J Muscle Res Cell Motil 27(5-7): 367-373.
58. Marchand E, Constantin B, Balghi H, Claudepierre MC, Cantereau A, et al. (2004) 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.
59. Yokota T, Lu QL, Morgan JE, Davies KE, Fisher R, et al. (2006) Expansion of revertant fibres in dystrophic mdx muscles reflects activity of muscle precursor cells as an index of muscle regeneration. J Cell Sci 119: 2679-2687.
60. Straub V, Bittner RE, Leger JJ, Voit T (1992) Direct visualization of the dystrophin network on skeletal muscle fiber membrane. J Cell Biol 119(5): 1183-1191.
61. Dulhunty A (1984) Heterogeneity of t-tubule geometry in vertebrate skeletal muscle fibres. J Muscle Res Cell Motil 5: 333-347.
62. Launikonis BS, Stephenson DG (2002) Tubular system volume changes in twitch fibres from toad and rat skeletal muscle assessed by confocal microscopy. J Physiol 538: 607-618.
63. Pereon Y, Dettbarn C, Navarro J, Noireaud J, Palade PT (1997) Dihydropyridine receptor gene expression in skeletal muscle from mdx and control mice. Biochim Biophys Acta 1362: 201-207.
64. Cullen MJ, Walsh J, Nicholson LVB, Harris JB (1990) Ultrastructural localization of dystrophin in human muscle by using gold immuno-labelling. Proc R. Soc Lond (Biol) 240: 197-210.
65. Frank JS, Mottino G, Chen F, Peri V, Holland P, et al. (1994) Subcellular distribution of dystrophin in isolated adult and neonatal cardiac myocytes. Am J Physiol Cell Physiol 267: C1707-C1716.
66. Hoffman EP, Knudson CM, Campbell KP, Kunkel LM (1987) Subcellular fractionation of dystrophin to the triads of skeletal muscle. Nature 330: 754-758.
67. 2+ channels by dystrophin, the actin cytoskeleton, and cAMP-dependent protein kinase. Proc Nat Acad Sci USA 102: 4191-4196.
68. Imbert N, Vandebrouck C, Duport G, Raymond G, Hassoni AA, et al. (2001) Calcium currents and transients in co-cultured contracting normal and Duchenne muscular dystrophy human myotubes. J Physiol 534.2: 343-355.
69. Matsumura K, Tome FMS, Collin H, Leturcq F, Jean-Pierre M, et al. (1994) Expression of dystrophin-associated proteins in dystrophin-positive muscle fibers (revertants) in Duchenne muscular dystrophy. Neuromuscul Disord 4: 115-120.
70. Decrouy A, Renaud JM, Davis HL, Lunde JA, Dickson G, et al. (1997) Mini-dystrophin gene transfer in mdx4cv diaphragm muscle fibers increases sarcolemmal stability. Gene Ther 4(5): 401-408.
71. McCarter GC, Steinhardt RA (2000) Increased activity of calcium leak channels caused by proteolysis near sarcolemmal ruptures. J Membr Biol 176(2): 169-174.
72. Alderton JM, Steinhardt RA (2000) Calcium influx through calcium leak channels is responsible for the elevated levels of calcium-dependent protcolysis in dystrophic myotubes. J Biol Chem 275(13): 9452-9460.
73. + channels in muscle fibers from control and mdx mice. Biophys J 82: 3012-3021.
74. Woods CE, Novo D, DiFranco M, Vergara JL (2004) The action potential-evoked sarcoplasmic reticulum calcium release is impaired in mdx mouse muscle fibres. J Physiol 557.1: 59-75.
75. Schwartz LM, McCleskey EW, Almers W (1985) Dihydropyridine receptors in muscle are voltage-dependent but most are not functional calcium channels. Nature 314: 747-750.
76. Liu M, Yue Y, Harper SQ, Grange RW, Chamberlain JS, et al. (2005) Adeno-associated virus-mediated microdystrophin expression protects young mdx muscle from contraction-induced injury. Mol Ther 11(2): 245-256.