The myofibrillar complex and fatigue: A review

Canadian Journal of Applied Physiology

Volumn 29, Issue 3, 2004, Pages 330-356

  Vandenboom, Rene ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Actin; Muscle contraction; Myosin

Indexed keywords

ACTIN; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; CALCIUM; LACTIC ACID; MUSCLE PROTEIN; MYOSIN; PHOSPHATE; PROTON; REACTIVE OXYGEN METABOLITE; REGULATOR PROTEIN;

CALCIUM CELL LEVEL; CONFERENCE PAPER; ENZYME ACTIVITY; HUMAN; HYDROLYSIS KINETICS; MOLECULAR MECHANICS; MOTOR PERFORMANCE; MUSCLE CONTRACTILITY; MUSCLE FATIGUE; MUSCLE FIBRIL; MUSCLE FORCE; MUSCLE METABOLISM; MUSCLE STRENGTH; MYOFILAMENT; NONHUMAN; OXIDATION REDUCTION REACTION; PH MEASUREMENT; PROTEIN BINDING; PROTEIN FUNCTION; TEMPERATURE DEPENDENCE; THERMODYNAMICS;

EID: 3042656412     PISSN: 10667814     EISSN: None     Source Type: Journal    
DOI: 10.1139/h04-022     Document Type: Conference Paper

References (95)

1. Adams, G.R., Fisher, M.J., and Meyer, R.A. (1991). Hypercapnic acidosis and increased H2PO4- concentration do not decrease force in cat skeletal muscle. Am. J. Physiol. 260: C805-C812.
2. Allen, D.G., Lannergren, J., and Westerblad, H. (1995). Muscle cell function during prolonged activity: Cellular mechanisms of fatigue. Exp. Physiol. 80: 497-527.
3. Allen, D.G., Lannergen, J., and Westerblad, H. (2002). Intracellular ATP measured with luciferin/luciferase in isolated single mouse skeletal muscle fibres. Pflugers Arch. 443: 836-842.
4. Allen, D.G., Lee, J.A., and Westerblad, H. (1989). Intracellular calcium and tension during fatigue in isolated single muscle fibres from Xenopus laevis. J. Physiol. (Lond.) 415: 433-458.
5. Altringham, J.D., and Johnston, I.A. (1985). Effects of phosphate on the contractile properties of fast and slow muscle fibres from an Antarctic fish. J. Physiol. (Lond.) 368: 491-500.
6. Andrade, F.H., Reid, M.B., Allen, D.G., and Westerblad, H. (1998). Effect of hydrogen peroxide and dithiothreitol on contractile function of single skeletal muscle fibres from the mouse. J. Physiol. (Lond.) 509: 565-575.
7. Andrade, F.H., Reid, M.B., and Westerblad, H. (2001), Contractile response of skeletal muscle to low peroxide concentrations: Myofibrillar calcium sensitivity as a likely target for redox-modulation. FASEB J. 15: 309-311.
8. Bagshaw, C.R., and Trentham, D.R. (1973). The reversibility of the adenosine triphosphate cleavage by myosin. Biochem J. 133: 323-328.
9. Barany, M. (1967) ATPase activity of myosin correlated with speed of muscle shortening. J. Gen. Physiol. 50: 197-218.
10. Barclay, J.K., and Hansel, M. (1991). Free radicals may contribute to oxidative skeletal muscle fatigue. Can. J. Physiol. Pharmacol. 69: 279-284.
11. 2+ binding of rabbit skeletal myofilaments. J. Biol. Chem. 259: 3181-3186.
12. 2+ release from the sarcoplasmic reticulum of rat skeletal muscle fibers. J. Appl. Physiol. 81: 731-737.
13. 2-induced acidification on the fatigue resistance of single mouse muscle fibers at 28 degrees C. J. Appl. Physiol. 85: 478-483.
14. Cady, E.B., Jones, D.A., Lynn, J., and Newham, D.J. (1989). Changes in force and intracellular metabolites during fatigue of human skeletal muscle. J. Physiol. (Lond.) 418: 311-325.
15. Callahan, L.A., She, Z.W., and Nosek, T.M. (2001). Superoxide, hydroxyl radical, and hydrogen peroxide effects on single-diaphragm fiber contractile apparatus. J. Appl. Physiol. 90: 45-54.
16. Chase, P.B., and Kushmerick, M.J. (1988). Effects of pH on contraction of rabbit fast and slow skeletal muscle fibers. Biophys. J. 53: 935-946.
17. Chase, P.B., and Kushmerick, M.J. (1995). Effect of physiological ADP concentrations on contraction of single skinned fibers from rabbit fast and slow muscles. Am. J. Physiol. 268: C480-C490.
18. Cooke, R. (1997). Actomyosin interaction in striated muscle. Physiol. Rev. 77: 671-697.
19. Cooke, R., Franks, K., Luciana, G.B., and Pate, E. (1988). The inhibition of rabbit skeletal muscle contraction by hydrogen ions and phosphate. J. Physiol. (Lond.) 395: 77-97.
20. Cooke, R., and Pate, E. (1985). The effects of ADP and phosphate on the contraction of muscle fibers. Biophys. J. 48: 789-798.
21. Cooke, R. and Pate, E. (1990) The inhibition of muscle contraction by the products of ATP hydrolysis. In: E.W. Taylor (Ed.), Biochemistry of Exercise VII pp. 59-73. Champaign, Illinois: Human Kinetics.
22. Coupland, M.E., Puchert, E., and Ranatunga, K.W. (2001). Temperature dependence of active tension in mammalian (rabbit psoas) muscle fibres: Effect of inorganic phosphate. J. Physiol. (Lond.) 536: 879-891.
23. Dantzig, J.A., Goldman, Y.E., Millar, N.C., Lacktis, J., and Homsher, E. (1992). Reversal of the cross-bridge force-generating transition by photogeneration of phosphate in rabbit psoas muscle fibres. J. Physiol. (Lond.) 451: 247-278.
24. Davies, K.J., Quintanilha, A.T., Brooks, G.A., and Packer, L. (1982). Free radicals and tissue damage produced by exercise. Biochem. Biophys. Res. Commun. 107: 1198-1205.
25. Dawson, M.J., Gadian, D.G., and Wilkie, D.R. (1977). Contraction and recovery of living muscles studies by 31P nuclear magnetic resonance. J. Physiol. (Lond.) 267: 703-735.
26. Dawson, M.J., Gadian, D.G., and Wilkie, D.R. (1978). Muscular fatigue investigated by phosphorus nuclear magnetic resonance. Nature 274: 861-866.
27. Dawson, M.J., Gadian, D.G., and Wilkie, D.R. (1980). Mechanical relaxation rate and metabolism studied in fatiguing muscle by phosphorus nuclear magnetic resonance. J. Physiol. (Lond.) 299: 465-484.
28. + on skinned single fiber function. Biophys. J. 83(2): 445a.
29. 2+-activated force of skinned fibers from the soleus, cardiac and adductor magnus muscles of rabbits. Pflugers Arch. 376: 55-65.
30. Edman, K.A.P., and Lou, F. (1990). Changes in force and stiffness induced by fatigue and intracellular acidification in frog muscle fibres. J. Physiol. (Lond.) 424: 133-149.
31. Edman, K.A.P., and Lou, F. (1992). Myofibrillar fatigue versus failure of activation during repetitive stimulation of frog muscle fibres. J. Physiol. (Lond.) 457: 655-673.
32. Edman, K.A.P., and Mattiazzi, A. (1981). Effects of fatigue and altered pH on isometric force and velocity of shortening at zero load in frog muscle fibres. J. Muscle Res. Cell Motil. 2: 321-334.
33. Edwards, R.H., Hill, D.K., and Jones, D.A. (1975). Metabolic changes associated with the slowing of relaxation in fatigued mouse muscle. J. Physiol. (Lond.) 251: 287-301.
34. Fabiato, A., and Fabiato, F. (1978). Effects of pH on the myofilaments and the sarcoplasmic reticulum of skinned cells from cardiac and skeletal muscles. J. Physiol. (Lond.) 276: 233-255.
35. Ferenczi, M.A., Goldman, Y.E., and Simmons, R.M. (1984). The dependence of force and shortening velocity on substrate concentration in skinned muscle fibres from Rana temporaria. J. Physiol. (Lond.) 350: 519-543.
36. Finer, J.T., Simmons, R.M., and Spudich, J.A. (1994). Single myosin molecule mechanics: Piconewton forces and nanometre steps. Nature 368: 113-119.
37. Fitts, R.H. (1994). Cellular mechanisms of muscle fatigue. Physiol. Rev. 74: 49-94.
38. Godt, R.E., and Nosek, T.M. (1989). Changes of intracellular milieu with fatigue or hypoxia depress contraction of skinned rabbit skeletal and cardiac muscle. J. Physiol. (Lond.) 412: 155-180.
39. Goldman, Y.E., Hibberd, M.G., McCray, J.A., and Trentham, D.R. (1982). Relaxation of muscle fibres by photolysis of caged ATP. Nature 300: 701-705.
40. Gordon, A.M., Homsher, E., and Regnier, M. (2000). Regulation of muscle contraction. Physiol. Rev. 80: 853-924.
41. Grange, R.W., Vandenboom, R., and Houston M.E. (1995). Myosin phosphorylation augments force-displacement and force-velocity relationships of mouse fast muscle. Am. J. Physiol. 269: C713-C724.
42. Gulick, A.M., and Rayment, I. (1997). Structural studies on myosin II: Communication between distant protein domains. Bioessays 19: 561-569.
43. Hermansen, L., and Osnes, J.B. (1972). Blood and muscle pH after maximal exercise in man. J. Appl. Physiol. 32: 304-308.
44. Hibberd, M.G., Dantzig, J.A., Trentham, D.R., and Goldman, Y.E. (1985). Phosphate release and force generation in skeletal muscle fibers. Science 228: 1317-1319.
45. Hultman, E., and Sjoholm, H. (1983). Energy metabolism and contraction force of human skeletal muscle in situ during electrical stimulation. J Physiol. (Lond.) 345: 525-532.
46. Karatzaferi, C., Mybergh, K.H., Chinn, M.K., Franks-Skiba, K., and Cooke, R. (2003). Effect of an ADP analog on isometric force and ATPase activity of active muscle fibers. Am. J. Physiol. 284: C816-C825.
47. Kolbeck, R.C., She, Z.W., Callahan, L.A., and Nosek, T.M. (1997). Increased superoxide production during fatigue in the perfused rat diaphragm. Am. J. Respir. Crit. Care Med. 156: 140-145.
48. Kushmerick, M.J., and Meyer, R.A. (1985). Chemical changes in rat leg muscle by phosphorus nuclear magnetic resonance. Am. J. Physiol. 248: C542-C549.
49. Lamb, G.D., and Posterino, G.S. (2003). Effects of oxidation and reduction on contractile function in skeletal muscle fibres of the rat. J. Physiol. (Lond.) 546: 149-163.
50. 2+]i during fatigue and recovery of single muscle fibres from Xenopus laevis. J. Physiol. (Lond.) 433: 307-326.
51. McKillop, D.F., and Geeves, M.A. (1993). Regulation of the interaction between actin and myosin subfragment 1: Evidence for three states of the thin filament. Biophys. J. 65: 693-701.
52. Metzger, J.M. (1996a). Effects of phosphate and ADP on shortening velocity during maximal and submaximal calcium activation of the thin filament in skeletal muscle fibers. Biophys. J. 70: 409-417.
53. Metzger, J.M. (1996b). pH dependence of myosin binding-induced activation of the thin filament in cardiac myocytes and skeletal fibers. Am. J. Physiol. 270: H1008-H1014.
54. Metzger, J.M., and Fitts, R.H. (1987). Role of intracellular pH in muscle fatigue. J. Appl. Physiol. 62: 1392-1397.
55. Metzger, J.M., and Moss, R.L. (1987). Greater hydrogen ion-induced depression of tension and velocity in skinned single fibres of rat fast than slow muscles. J. Physiol. (Lond.) 393: 727-742.
56. Metzger, J.M., and Moss, R.L. (1990). Effects on tension and stiffness due to reduced pH in mammalian fast- and slow-twitch skinned skeletal muscle fibres. J. Physiol. (Lond.) 428: 737-750.
57. Meyer, R.A., Adams, G.R., Fisher, M.J., Dillon, P.F., Krisanda, J.M., Brown, T.R., and Kushmerick, M.J. (1991). Effect of decreased pH on force and phosphocreatine in mammalian skeletal muscle. Can. J. Physiol. Pharm. 69: 305-130.
58. Miller, R.G., Bosca, M.D., Moussavi, R.S., Carson, P.J., and Weiner, M.W. (1988). 31P nuclear magnetic resonance studies of high energy phosphates and pH in human muscle fatigue. Comparison of aerobic and anaerobic exercise. J. Clin. Invest. 81: 1190-1196.
59. Moss, R.L. (1986). Effects on shortening velocity of rabbit skeletal muscle due to variations in the level of thin-filament activation. J. Physiol. (Lond.) 377: 487-505.
60. Nagesser, A.S., Van der Laarse, W.J., and Elzinga, G. (1992). Metabolic changes with fatigue in different types of single muscle fibres of Xenopus laevis. J. Physiol. (Lond.) 448: 511-523.
61. Nagesser, A.S., Van der Laarse, W.J., and Elzinga, G. (1993). ATP formation and ATP hydrolysis during fatiguing, intermittent stimulation of different types of single muscle fibres from Xenopus laevis. J. Muscle Res. Cell Motil. 14: 608-618.
62. Nassar-Gentina, V., Passonneau, J.V., Vergara, J.L., and Rapaport, S.I. (1978). Metabolic correlates of fatigue and of recovery from fatigue in single frog muscle fibers. J. Gen. Physiol. 72: 593-606.
63. Nosek, T.M., Fender, K.Y., and Godt, R.E. (1987). It is diprotonated inorganic phosphate that depresses force in skinned skeletal muscle fibers. Science 236: 191-193.
64. 2+ release channel in frog skeletal muscle. Am. J. Physiol. 271: C810-C818.
65. Pate, E., Bhimani, M., Franks-Skiba, K., and Cooke, R. (1995). Reduced effect of pH on skinned rabbit psoas muscle mechanics at high temperatures: Implications for fatigue. J. Physiol. (Lond.) 486: 689-694.
66. Persechini, A., Stull, J.T., and Cooke, R. (1985). The effect of myosin phosphorylation on the contractile properties of skinned rabbit skeletal muscle fibers. J. Biol. Chem. 260: 7951-7954.
67. Piazzesi, G., Lucii, L., and Lombardi, V. (2002). The size and the speed of the working stroke of muscle myosin and its dependence on the force. J. Physiol. (Lond.) 545: 145-151.
68. 2+-activation of single permeabilized fibres from fast- and slow-twitch skeletal muscles of rats. J. Muscle Res. Cell Motil. 21: 747-752.
69. Posterino, G.S., Dutka, T.L., and Lamb, G.D. (2001). L(+)-lactate does not affect twitch and tetanic responses in mechanically skinned mammalian muscle fibres. Pflugers Arch. 442: 197-203.
70. Posterino, G.S., and Fryer, M.W. (2000). Effects of high myoplasmic L-lactate concentration on E-C coupling in mammalian skeletal muscle. J. Appl. Physiol. 89: 517-528.
71. Ranatunga, K.W. (1987). Effects of acidosis on tension development in mammalian skeletal muscle. Muscle Nerve 10: 439-445.
72. Rayment, I., Holden, H.M., Whittaker, M., Yohn, C.B., Lorenz, M., Holmes, K.C., and Milligan, R.A. (1993a). Structure of the actin-myosin complex and its implications for muscle contraction. Science 261: 58-65.
73. Rayment, I., Rypniewski, W.R., Schmidt-Base, K., Smith, R., Tomchick, D.R., Benning, M.M., Winkleman, D.A., Wesenberg, G., and Holden. H.M. (1993b). Three-dimensional structure of myosin subfragment-1: A molecular motor. Science 261: 50-58.
74. Reid, M.B. (2001). Invited review: Redox modulation of skeletal muscle contraction: What we know and what we don't. J. Appl. Physiol. 90: 724-731.
75. Siemankowski, R.F., Wiseman, M.O., and White H.D. (1985). ADP dissociation from actomyosin subfragment 1 is sufficiently slow to limit the unloaded shortening velocity in vertebrate muscle. Proc. Natl. Acad. Sci. USA 82: 658-662.
76. Stienen, G.J., Roosemalen, M.C., Wilson, M.G., and Elzinga, G. (1990). Depression of force by phosphate in skinned skeletal muscle fibers of the frog. Am. J. Physiol. 259: C349-C357.
77. Taylor, E.W. (1977). Transient phase of adenosine triphosphate hydrolysis by myosin, heavy meromyosin, and subfragment 1. Biochem. 16: 732-739.
78. Vale, R.D., and Milligan, R.A. (2000). The way things move: Looking under the hood of molecular motor proteins. Science 288: 88-95.
79. 2+] in intact frog skeletal muscle fibres. J. Physiol. (Lond.) 511: 171-180.
80. Vandenboom, R., Hannon, J.D., and Sieck, G.C. (2002). Isotonic force modulates force redevelopment rate of intact frog skeletal muscle fibers: Evidence for cross-bridge induced thin filament activation. J. Physiol. (Lond.) 543: 555-566.
81. Vandenboom, R., and Houston M.E. (1996). Phosphorylation of myosin and twitch potentiation in fatigued skeletal muscle. Can. J. Physiol. Pharmacol. 74: 1315-1321.
82. Vandenboom, R., Xeni, J., Bestic, M., and Houston, M.E. (1997). Increased force development rates of fatigued skeletal muscle graded to myosin light chain phosphate content. Am. J. Physiol. 41: R1980-R1984.
83. Vibert, P., Craig, R., and Lehman, W. (1997) Steric-model for activation of muscle thin filaments. J. Mol. Biol. 266: 8-14.
84. Weiss, S., Rossi, R., Pellegrini, M.A., and Geeves, M.A. (2001). Differing ADP release rates from myosin heavy chain is forms define the shortening velocity of skeletal muscle fibers. J. Biol. Chem. 276: 45902-45908.
85. West, T.G., Curtin, N.A., Ferenczi, M.A., He, Z.H., Sun, Y.B, Irving, M., and Woledge, R.C. (2003). Actomyosin energy turnover declines while force remains constant during isometric muscle contraction. J. Physiol. (Lond.) 555: 27-43.
86. Westerblad, H., and Allen, D.G. (1991). Changes of myoplasmic calcium concentration during fatigue in single mouse muscle fibers. J. Gen. Physiol. 98: 615-635.
87. Westerblad, H., and Allen, D.G. (1993). The influence of intracellular pH on contraction, relaxation and [Ca2+]i in intact single fibres from mouse muscle. J. Physiol. (Lond.) 466: 611-628.
88. Westerblad, H., Allen, D.G., and Lannergren, J. (2002). Muscle fatigue: Lactic acid or inorganic phosphate the major cause? News Physiol. Sci. 17: 17-21.
89. Westerblad, H., Bruton, J.D., and Lannergen, J. (1997) The effect of intracellular pH on contractile function of intact, single fibres of mouse muscle declines with increasing temperature. J. Physiol. (Lond.) 500: 193-204.
90. Westerblad, H., Dahlstedt, A.J., and Lannergren, J. (1998). Mechanisms underlying reduced maximum shortening velocity during fatigue of intact, single fibres of mouse muscle. J. Physiol. (Lond.) 510: 269-277.
91. Westerblad, H., and Lannergen, J. (1995). Reduced maximum shortening velocity in the absence of phosphocreatine observed in intact fibres of Xenopus skeletal muscle. J. Physiol. (Lond.) 482: 383-390.
92. Westerblad, H., Lee, J., Lannergen, J., and Allen, D.G. (1991). Cellular mechanisms of fatigue in skeletal muscle. Am. J. Physiol. 261: C195-C209.
93. Widrick, J.J. (2002). Effect of P(i) on unloaded shortening velocity of slow and fast mammalian muscle fibers. Am. J. Physiol. 282: C647-C653.
94. Wiseman, R.W., Beck, T.W., and Chase, P.B. (1996). Effect of intracellular pH on force development depends on temperature in intact skeletal muscle from mouse. Am. J. Physiol. 271: C878-C886.
95. Yanagida, T., and Iwane, A.H. (2000). A large step for myosin. Proc. Natl. Acad. Sci. USA 97: 9357-9359.