Slowed relaxation in fatigued skeletal muscle fibers of Xenopus and mouse: Contribution of [Ca2+](i) and cross-bridges

Journal of General Physiology

Volumn 109, Issue 3, 1997, Pages 385-399

  Westerblad, Håkan ^a   Lännergren, Jan ^a   Allen, David G ^a,b  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Ca2+ (i) force relation; sarcoplasmic reticulum

Indexed keywords

CALCIUM;

ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CONTROLLED STUDY; KINETICS; MOUSE; MUSCLE FATIGUE; MUSCLE FORCE; MUSCLE RELAXATION; NONHUMAN; SKELETAL MUSCLE; XENOPUS;

ANIMALS; CALCIUM; CALCIUM CHANNEL BLOCKERS; FEMALE; KINETICS; MALE; MICE; MUSCLE CONTRACTION; MUSCLE FIBERS; MUSCLE PROTEINS; MUSCLE RELAXATION; MUSCLE, SKELETAL; SARCOPLASMIC RETICULUM; XENOPUS;

EID: 0030888568     PISSN: 00221295     EISSN: None     Source Type: Journal    
DOI: 10.1085/jgp.109.3.385     Document Type: Article

References (57)

1. Allen, D.G., J. Lännergren, and H. Westerblad. 1995. Muscle cell function during prolonged activity: cellular mechanisms of fatigue. Exp. Physiol. 80:497-527.
2. Allen, D.G., J.A. Lee, and H. Westerblad. 1989. Intracellular calcium and force in isolated single muscle fibres from Xenopus. J. Physiol. (Camb. ). 415:433-458.
3. 3H]ryanodine binding to rabbit and frog skeletal muscle. Am. J. Physiol. 266:C462-C466.
4. Briden, K.L., and N.R. Alpert. 1972. The effect of shortening on the time-course of active state decay. J. Gen. Physiol. 60:202-220.
5. Byrd, S.K., L.J. McCutcheon, D.R. Hodgson, and P.D. Gollnick. 1989. Altered sarcoplasmic reticulum function after high-intensity exercise. J. Appl. Physiol. 67:2072-2077.
6. Cannell, M.B. 1986. Effect of tetanus duration on the free calcium during the relaxation of frog skeletal muscle fibres. J. Physiol. (Camb.). 376:203-218.
7. Cleworth, D.R., and K.A.P. Edman. 1972. Changes in sarcomere length during isometric tension development in frog skeletal muscle. J. Physiol. (Camb.). 227:1-17.
8. Cooke, R., K. Franks, G.B. Luciani, and E. Pate. 1988. The inhibition of rabbit skeletal muscle contraction by hydrogen ions and phosphate. J. Physiol. (Camb.). 395:77-97.
9. Curtin, N.A., and K.A.P. Edman. 1989. Effects of fatigue and reduced intracellular pH on segment dynamics in 'isometric' relaxation of frog muscle fibres. J. Physiol. (Camb.). 413:159-174.
10. Dawson, M.J., D.G. Gadian, and D.R. Wilkie. 1980. Mechanical relaxation rate and metabolism studied in fatiguing muscle by phosphorus nuclear magnetic resonance. J. Physiol. (Camb.). 299: 465-484.
11. Edman, K.A.P., and F. Lou. 1990. Changes in force and stiffness induced by fatigue and intracellular acidification in frog muscle fibres. J. Physiol. (Camb.). 424:133-149.
12. Fabiato, A., and F. Fabiato. 1978. Effects of pH on the myofilaments and the sarcoplasmic reticulum of skinned cells from cardiac and skeletal muscles. J. Physiol. (Camb.). 276:233-255.
13. Fitts, R.H. 1994. Cellular mechanisms of muscle fatigue. Physiol. Rev. 74:49-94.
14. Godt, R.E., and T.M. Nosek. 1989. Changes of intracellular milieu with fatigue or hypoxia depress contraction of skinned rabbit skeletal and cardiac muscle. J. Physiol. (Camb.). 412:155-180.
15. Gordon, A.M., and E.B. Ridgway. 1987. Extra calcium on shortening in barnacle muscle. Is the decrease in calcium binding related to decreased cross-bridge attachment, force, or length? J. Gen. Physiol. 90:321-340.
16. Hibberd, M.G., J.A. Dantzig, D.R. Trentham, and Y.E. Goldman. 1985. Phosphate release and force generation in skeletal muscle fibers. Science (Wash. DC). 228:1317-1319.
17. Hou, T.-T., J.D. Johnson, and J.A. Rall. 1993. Role of parvalbumin in relaxation of frog skeletal muscle. In Mechanism of Myofilament Sliding and Muscle Contraction. H. Sugi and G.H. Pollack, editors. Plenum Press, New York. 141-153.
18. Huxley, A.F., and R.M. Simmons. 1970. Rapid 'give' and tension 'shoulder' in the relaxation of frog muscle fibres. J. Physiol. (Camb.). 210:32-33P. (Abstr.).
19. Iwamoto, H. 1995. Strain sensitivity and turnover rate of low force cross-bridges in contracting skeletal muscle fibers in the presence of phosphate. Biophys. J. 68:243-250.
20. Josephson, R.K. 1993. Contraction dynamics and power output of skeletal muscle. Annu. Rev. Physiol. 55:527-546.
21. Klein, M.G., H. Cheng, L.F. Santana, Y.-H. Jiang, W.J. Lederer, and M.F. Schneider. 1996. Two mechanisms of quantized calcium release in skeletal muscle. Nature (Lond.). 379:455-458.
22. 2+ pump properties in frog skeletal muscle. J. Physiol. (Camb.). 441:639-671.
23. Lamb, G.D., E. Recupero, and D.G. Stephenson. 1992. Effect of myoplasmic pH on excitation-contraction coupling in skeletal muscle fibres of the toad. J. Physiol. (Camb.). 448:211-224.
24. Lännergren, J., and A. Arner. 1992. Relaxation rate of intact striated muscle fibres after flash photolysis of a caged calcium chelator (diazo-2). J. Musc. Res. Cell Motil. 13:630-634.
25. Lännergren, J., G. Elzinga, and G.J.M. Stienen. 1993. Force relaxation, labile heat and parvalbumin content of skeletal muscle fibres of Xenopus laevis. J. Physiol. (Camb.). 463:123-140.
26. Lännergren, J., and H. Westerblad. 1986. Force and membrane potential during and after fatiguing, continuous high-frequency stimulation of single Xenopus muscle fibres. Acta Physiol. Scand. 128:359-368.
27. Lännergren, J., and H. Westerblad. 1987. The temperature dependence of isometric contractions of single, intact fibres dissected from a mouse foot muscle. J. Physiol. (Camb.). 390:285-293.
28. Lännergren, J., H. Westerblad, and B. Flock. 1990. Transient appearance of vacuoles in fatigued Xenopus muscle fibres. Acta Physiol. Scand. 40:437-445.
29. Lattanzio, F.A., Jr. 1990. The effects of pH and temperature on fluorescent calcium indicators as determined with Chelex-100 and EDTA buffer systems. Biochem. Biophys. Res. Commun. 171:102-108.
30. i during fatigue and recovery of single muscle fibres from Xenopus laevis. J. Physiol. (Camb.). 433:307-326.
31. Martyn, D.A., and A.M. Gordon. 1992. Force and stiffness in glycerinated rabbit psoas fibers: effects of calcium and elevated phosphate. J. Gen. Physiol. 99:795-816.
32. Metzger, J.M., and R.L. Moss. 1990. Effects on tension and stiffness due to reduced pH in mammalian fast- and slow-twitch skinned skeletal muscle fibres. J. Physiol. (Camb.). 428:737-750.
33. Millar, N.C., and E. Homsher. 1990. The effect of phosphate and calcium on force generation in glycerinated rabbit skeletal muscle fibers. J. Biol. Chem. 265:20234-20240.
34. 2+ sequestration. FEBS Lett. 224: 331-336.
35. Nagesser, A.S., W.J. van der Laarse, and G. Elzinga. 1993. ATP formation and ATP hydrolysis during fatiguing, intermittent stimulation of different types of single muscle fibres from Xenopus laevis. J. Musc. Res. Cell Motil. 14:608-618.
36. Palmer, R.E., S.J. Simnett, I.P. Mulligan, and C.C. Ashley. 1993. Phosphate slows the rate of relaxation of single skinned frog fibres upon photolysis of diazo-2. Biophys. J. 64:A251. (Abstr.).
37. Phillips, S.K., R.W. Wiseman, R.C. Woledge, and M.J. Kushmerick. 1993. The effects of metabolic fuel on force production and resting inorganic phosphate levels in mouse skeletal muscle. J. Physiol. (Camb.). 462:135-146.
38. Potma, E.J., I.A. van Graas, and G.J.M. Stienen. 1995. Influence of inorganic phosphate and pH on ATP utilization in fast and slow skeletal muscle fibers. Biophys. J. 69:2580-2589.
39. Ritchie, J.M. 1954. The effect of nitrate on the active state of muscle. J. Physiol. (Camb.). 126:155-168.
40. 2+ release from the sarcoplasmic reticulum compared in amphibian and mammalian skeletal muscle. J. Gen. Physiol. 107:1-18.
41. 2+-ATPase activity in muscle homogenates. Anal. Biochem. 191:321-331.
42. Swartz, D.R., R.L. Moss, and M.L. Greaser. 1996. Calcium alone does not fully activate the thin filament for S1 binding to rigor myofibrils. Biophys. J. 71:1891-1904.
43. Volpe, P., M. Bravin, F. Zorzato, and A. Margreth. 1988. Isolation of terminal cisternae of frog skeletal muscle. J. Biol. Chem. 263: 9901-9907.
44. Westerblad, H., and D.G. Allen. 1991. Changes in myoplasmic calcium concentration during fatigue in single mouse muscle fibers. J. Gen. Physiol. 98:615-635.
45. Westerblad, H., and D.G. Allen. 1992. Changes of intracellular pH during repeated tetani in single mouse skeletal muscle fibres. J. Physiol. (Camb.). 449:49-71.
46. i in intact single fibres from mouse muscle. J. Physiol. (Camb.). 466:611-628.
47. i in the slowing of relaxation in fatigued single fibres from mouse skeletal muscle. J. Physiol. (Camb.). 46:729-740.
48. Westerblad, H., and D.G. Allen. 1994a. The role of sarcoplasmic reticulum in relaxation of mouse muscle; effects of 2,5-di(tert-butyl)-1,4-benzohydroquinone. J. Physiol. (Camb.). 474:291-301.
49. i during prolonged tetanic stimulation of intact, single fibres from mouse skeletal muscle. J. Physiol. (Camb.). 480:31-43.
50. i during prolonged tetanic stimulation of single fibres from Xenopus skeletal muscle. J. Physiol. (Camb.). 492:723-736.
51. Westerblad, H., and D.G. Allen. 1996b. Intracellular calibration of the calcium indicator indo-1 in isolated fibers of Xenopus muscle. Biophys. J. 71:908-917.
52. Westerblad, H., and J. Lännergren. 1986. Force and membrane potential during and after fatiguing, intermittent stimulation of single Xenopus muscle fibres. Acta Physiol. Scand. 128:369-378.
53. Westerblad, H., and J. Lännergren. 1988. The relation between force and intracellular pH in fatigued, single Xenopus muscle fibres. Acta Physiol. Scand. 133:83-89.
54. 2+ buffering contributes to slowing of relaxation in fatigued Xenopus muscle fibres. Acta Physiol. Scand. 139:243-244.
55. Westerblad, H., and J. Lännergren. 1991. Slowing of relaxation during fatigue in single mouse muscle fibres. J. Physiol. (Camb.). 434:323-336.
56. Westerblad, H., and J. Lännergren. 1994. Changes of the force-velocity relation, isometric tension and relaxation rate during fatigue in intact, single fibres of Xenopus skeletal muscle. J. Musc. Res. Cell Motil. 15:287-298.
57. 2+ and caffeine sensitivities of skinned muscle fibres. J. Appl. Physiol. 75:586-593.