The action potential-evoked sarcoplasmic reticulum calcium release is impaired in mdx mouse muscle fibres

Journal of Physiology

Volumn 557, Issue 1, 2004, Pages 59-75

  Woods, Christopher E ^a   Novo, David ^a   DiFranco, Marino ^a   Vergara, Julio L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CALCIUM ION; DYSTROPHIN; EGTAZIC ACID; MYOSIN II; TOLUENESULFONAMIDE DERIVATIVE; ADENOSINE TRIPHOSPHATASE INHIBITOR; CALCIUM; N BENZYL 4 TOLUENE SULPHONAMIDE; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CELL ISOLATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DISEASE MODEL; DUCHENNE MUSCULAR DYSTROPHY; EXTENSOR DIGITORUM LONGUS MUSCLE; FLEXOR MUSCLE; FLUORESCENCE ANALYSIS; IMMOBILIZED CELL CULTURE; MOUSE; MUSCLE CELL; MUSCLE CONTRACTILITY; MUSCLE CONTRACTION; MUSCLE WEAKNESS; NONHUMAN; PRIORITY JOURNAL; SARCOPLASMIC RETICULUM; SIMULATION; SKELETAL MUSCLE; ACTION POTENTIAL AMPLITUDE; ACTION POTENTIAL EVOKED SARCOPLASMIC RETICULUM CALCIUM RELEASE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CONTRACTILE DYSFUNCTION; FLEXOR DIGITORUM BREVIS MUSCLE; MUSCLE DISEASE; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE;

ACTION POTENTIALS; ALGORITHMS; ANIMALS; CALCIUM; CHELATING AGENTS; EGTAZIC ACID; ELECTROPHYSIOLOGY; FLUORESCENT DYES; MICE; MICE, INBRED MDX; MUSCLE FIBERS; MUSCULAR DYSTROPHY, DUCHENNE; SARCOPLASMIC RETICULUM;

EID: 2942696374     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1113/jphysiol.2004.061291     Document Type: Article

References (63)

1. Baylor SM & Hollingworth S (2003). Sarcoplasmic reticulum calcium release compared in slow-twitch and fast-twitch fibres of mouse muscle. J Physiol 551, 125-138.
2. Bers DM, Patton CW & Nuccitelli R (1994). A practical guide to the preparation of Ca2+ buffers. Meth Cell Biol 40, 3-29.
3. Bressler BH, Jasch LG, Ovalle WK & Slonecker CE (1983). Changes in isometric contractile properties of fast-twitch and slow-twitch skeletal muscle of C57BL/6J dy2J/dy2J dystrophic mice during postnatal development. Exp Neurol 80, 457-470.
4. Cheung A, Dantzig JA, Hollingworth S, Baylor SM, Goldman YE, Mitchison TJ & Straight AF (2002). A small-molecule inhibitor of skeletal muscle myosin II. Nat Cell Biol 4, 83-88.
5. Coirault C, Lambert F, Marchand-Adam S, Attal P, Chemla D & Lecarpentier Y (1999). Myosin molecular motor dysfunction in dystrophic mouse diaphragm. Am J Physiol 277, C1170-C1176.
6. Culligan K, Banville N, Dowling P & Ohlendieck K (2002). Drastic reduction of calsequestrin-like proteins and impaired calcium binding in dystrophic mdx muscle. J Appl Physiol 92, 435-445.
7. Dangain J & Vrbova G (1984). Muscle development in mdx mutant mice. Muscle Nerve 7, 700-704.
8. Delbono O & Stefani E (1993). Calcium transients in single mammalian skeletal muscle fibres. J Physiol 463, 689-707.
9. DiFranco M, Novo D & Vergara J (2002). Characterization of the calcium release domains during excitation contraction coupling in skeletal muscle fibres. Pflugers Arch 443, 508-519.
10. DiGregorio DA, Peskoff A & Vergara JL (1999). Measurement of action potential-induced presynaptic calcium domains at a cultured neuromuscular junction. J Neurosci 19, 7846-7859.
11. Durbeej M & Campbell KP (2002). Muscular dystrophies involving the dystrophin-glycoprotein complex: an overview of current mouse models. Curr Opin Genet Dev 12, 349-361.
12. Emery AEH (1993). Duchenne Muscular Dystrophy. Oxford University Press, Oxford; New York.
13. Emery AE (2002). The muscular dystrophies. Lancet 359, 687-695.
14. Escobar AL, Cifuentes F & Vergara JL (1995). Detection of Ca(2+)-transients elicited by flash photolysis of DM-nitrophen with a fast calcium indicator. FEBS Lett 364, 335-338.
15. Escobar AL, Velez P, Kim AM, Cifuentes F, Fill M & Vergara JL (1997). Kinetic properties of DM-nitrophen and calcium indicators: rapid transient response to flash photolysis. Pflugers Arch 434, 615-631.
16. Eusebi F, Miledi R & Takahashi T (1980). Calcium transients in mammalian muscles. Nature 284, 560-561.
17. 2+. J Physiol 420, 337-353.
18. Friedrich O, Both M, Gillis JM, Chamberlain JS & Fink RH (2003). Mini-dystrophin restores L-type calcium currents in skeletal muscle of transgenic mdx mice. J Physiol 555, 251-265.
19. Gillis JM (1999). Understanding dystrophinopathies: an inventory of the structural and functional consequences of the absence of dystrophin in muscles of the mdx mouse. J Muscle Res Cell Motil 20, 605-625.
20. Godt RE (1974). Calcium-activated tension of skinned muscle fibers of the frog. Dependence on magnesium adenosine triphosphate concentration. J General Physiol 63, 722-739.
21. Grynkiewicz G, Poenie M & Tsien RY (1985). A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 260, 3440-3450.
22. Head SI (1993). Membrane potential, resting calcium and calcium transients in isolated muscle fibres from normal and dystrophic mice. J Physiol 469, 11-19.
23. Head SI, Stephenson DG & Williams DA (1990). Properties of enzymatically isolated skeletal fibres from mice with muscular dystrophy. J Physiol 422, 351-367.
24. 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.
25. Hille B & Campbell DT (1976). An improved vaseline gap voltage clamp for skeletal muscle fibers. J General Physiol 67, 265-293.
26. Hirota A, Chandler WK, Southwick PL & Waggoner AS (1989). Calcium signals recorded from two new purpurate indicators inside frog cut twitch fibers. J General Physiol 94, 597-631.
27. Hocherman SD & Bezanilla F (1996). A patch-clamp study of delayed rectifier currents in skeletal muscle of control and mdx mice. J Physiol 493, 113-128.
28. Hoffman EP, Brown RH Jr & Kunkel LM (1987a). Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 51, 919-928.
29. Hoffman EP, Knudson CM, Campbell KP & Kunkel LM (1987b). Subcellular fractionation of dystrophin to the triads of skeletal muscle. Nature 330, 754-758.
30. Hollingworth S, Marshall MW & Robson E (1990). Excitation contraction coupling in normal and mdx mice. Muscle Nerve 13, 16-20.
31. Hollingworth S, Zhao M & Baylor SM (1996). The amplitude and time course of the myoplasmic free [Ca2+] transient in fast-twitch fibers of mouse muscle. J General Physiol 108, 455-469.
32. Kargacin ME & Kargacin GJ (1996). The sarcoplasmic reticulum calcium pump is functionally altered in dystrophic muscle. Biochim Biophys Acta 1290, 4-8.
33. 2+ release in frog skeletal muscle revealed by supercharging pulses. J Physiol 511, 509-518.
34. Klug G, Reichmann H & Pette D (1985). Decreased parvalbumin contents in skeletal muscles of C57BL/6J (dy2J/dy2J) dystrophic mice. Muscle Nerve 8, 576-579.
35. Knudson CM, Hoffman EP, Kahl SD, Kunkel LM & Campbell KP (1988). Evidence for the association of dystrophin with the transverse tubular system in skeletal muscle. J Biol Chem 263, 8480-8484.
36. McArdle A, Edwards RH & Jackson MJ (1995). How does dystrophin deficiency lead to muscle degeneration? - evidence from the mdx mouse. Neuromuscul Disord 5, 445-456.
37. Mathes C, Bezanilla F & Weiss RE (1991). Sodium current and membrane potential in EDL muscle fibers from normal and dystrophic (mdx) mice. Am J Physiol 261, C718-C725.
38. Mathias RT, Cohen IS & Oliva C (1990). Limitations of the whole cell patch clamp technique in the control of intracellular concentrations. Biophys J 58, 759-770.
39. Maylie J, Irving M, Sizto NL & Chandler WK (1987). Comparison of arsenazo III optical signals in intact and cut frog twitch fibers. J General Physiol 89, 41-81.
40. Melzer W, Rios E & Schneider MF (1987). A general procedure for determining the rate of calcium release from the sarcoplasmic reticulum in skeletal muscle fibers. Biophys J 51, 849-863.
41. Nagerl UV, Novo D, Mody I & Vergara JL (2000). Binding kinetics of calbindin-D (28k) determined by flash photolysis of caged Ca(2+). Biophys J 79, 3009-3018.
42. Novo D, DiFranco M & Vergara JL (2003). Comparison between the predictions of diffusion-reaction models and localized Ca2+ transients in amphibian skeletal muscle fibers. Biophys J 85, 1080-1097.
43. Palade P & Vergara J (1982). Arsenazo III and antipyrylazo III calcium transients in single skeletal muscle fibers. J General Physiol 79, 679-707.
44. Pape PC, Jong DS & Chandler WK (1995). Calcium release and its voltage dependence in frog cut muscle fibers equilibrated with 20 mM EGTA. J General Physiol 106, 259-336.
45. Parry DJ & Parslow HG (1981). Fiber type susceptibility in the dystrophic mouse. Exp Neurol 73, 674-685.
46. Parslow HG & Parry DJ (1981). Slowing of fast-twitch muscle in the dystrophic mouse. Exp Neurol 73, 686-699.
47. Petrof BJ, Stedman HH, Shrager JB, Eby J, Sweeney HL & Kelly AM (1993). Adaptations in myosin heavy chain expression and contractile function in dystrophic mouse diaphragm. Am J Physiol 265, C834-C841.
48. Pusch M & Neher E (1988). Rates of diffusional exchange between small cells and a measuring patch pipette. Pflugers Arch 411, 204-211.
49. Raymackers JM, Gailly P, Schoor MC, Pette D, Schwaller B, Hunziker W, Celio MR & Gillis JM (2000). Tetanus relaxation of fast skeletal muscles of the mouse made parvalbumin deficient by gene inactivation. J Physiol 527, 355-364.
50. Sano M, Yokota T, Endo T & Tsukagoshi H (1990). A developmental change in the content of parvalbumin in normal and dystrophic mouse (mdx) muscle. J Neurol Sci 97, 261-272.
51. Shaw MA, Ostap EM & Goldman YE (2003). Mechanism of inhibition of skeletal muscle actomyosin by N-benzyl-p-toluenesulfonamide. Biochemistry 42, 6128-6135.
52. Song L-S, Sham JSK, Stern MD, Lakatta EG & Cheng H (1998). Direct measurement of SR release flux by tracking 'Ca spikes' in rat cardiac myocytes. J Physiol 512, 677-691.
53. Szentesi P, Jacquemond V, Kovacs L & Csernoch L (1997). Intramembrane charge movement and sarcoplasmic calcium release in enzymatically isolated mammalian skeletal muscle fibres. J Physiol 505, 371-384.
54. Turner PR, Fong PY, Denetclaw WF & Steinhardt RA (1991). Increased calcium influx in dystrophic muscle. J Cell Biol 115, 1701-1712.
55. Turner PR, Westwood T, Regen CM & Steinhardt RA (1988). Increased protein degradation results from elevated free calcium levels found in muscle from mdx mice. Nature 335, 735-738.
56. Tutdibi O, Brinkmeier H, Rudel R & Fohr KJ (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.
57. Vergara J & DiFranco M (1992). Imaging of calcium transients during excitation-contraction coupling in skeletal muscle fibers. Adv Exp Med Biol 311, 227-236.
58. Vergara JL, DiFranco M & Novo D (2001). Dimensions of calcium release domains in frog skeletal muscle fibers. Proc SPIE 4259, 133-143.
59. Wang ZM, Messi ML & Delbono O (1999). Patch-clamp recording of charge movement, Ca(2+) current, and Ca(2+) transients in adult skeletal muscle fibers. Biophys J 77, 2709-2716.
60. Watchko JF, O'Day TL & Hoffman EP (2002). Functional characteristics of dystrophic skeletal muscle: insights from animal models. J Appl Physiol 93, 407-417.
61. Wood DS, Sorenson MM, Eastwood AB, Charash WE & Reuben JP (1978). Duchenne dystrophy: abnormal generation of tension and Ca++ regulation in single skinned fibers. Neurology 28, 447-457.
62. Woods CE, Novo D & Vergara J (2003). Global calcium transients in normal and dystrophic muscle fibers. Biophysical Society Meeting 84, 572a.
63. Woods CE & Vergara JL (2002). A combined method for confocal detection of Ca2+ signals and fluorescence-recovery-after-photobleaching (FRAP). Biophys J (Annu Meeting Abstracts) 82, 278a.