Force decline during fatigue is due to both a decrease in the force per individual cross-bridge and the number of cross-bridges

Journal of Physiology

Volumn 589, Issue 13, 2011, Pages 3371-3381

  Nocella, Marta ^a   Colombini, Barbara ^a   Benelli, Giulia ^a   Cecchi, Giovanni ^a   Bagni, M Angela ^a   Bruton, Joseph ^b  

^a UNIVERSITY OF FLORENCE   (Italy)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ISOLATION; CONTROLLED STUDY; FLEXOR DIGITORUM BREVIS MUSCLE; MALE; MOUSE; MUSCLE CELL; MUSCLE FATIGUE; MUSCLE FORCE; MUSCLE STIFFNESS; MUSCLE TETANIC CONTRACTION; MYOFILAMENT; NONHUMAN; OSCILLATION; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RELAXATION TIME; SKELETAL MUSCLE;

ANIMALS; MALE; MICE; MICE, INBRED C57BL; MUSCLE CONTRACTION; MUSCLE FATIGUE; MUSCLE RELAXATION; MUSCLE, SKELETAL;

EID: 79959728697     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2011.209874     Document Type: Article

References (44)

1. Allen DG, Lamb GD & Westerblad H (2008). Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 88, 287-332.
2. Bagni MA, Cecchi G & Colombini B (2005). Crossbridge properties investigated by fast ramp stretching of activated frog muscle fibres. J Physiol 565, 261-268.
3. Brunello E, Bianco P, Piazzesi G, Linari M, Reconditi M, Panine P, Narayanan T, Helsby WI, Irving M & Lombardi V (2006). Structural changes in the myosin filament and cross-bridges during active force development in single intact frog muscle fibres: stiffness and X-ray diffraction measurements. J Physiol 577, 971-984.
4. 2+] in single fibres from mouse limb muscles during repeated tetanic contractions. J Physiol 551, 179-190.
5. 2-induced acidification on the fatigue resistance of single mouse muscle fibers at 28°C. J Appl Physiol 85, 478-483.
6. Cady EB, Elshove H, Jones DA & Moll A (1989a). The metabolic causes of slow relaxation in fatigued human skeletal muscle. J Physiol 418, 327-337.
7. Cady EB, Jones DA, Lynn J & Newham DJ (1989b). Changes in force and intracellular metabolites during fatigue of human skeletal muscle. J Physiol 418, 311-325.
8. Caremani M, Dantzig J, Goldman YE, Lombardi V & Linari M (2008). Effect of inorganic phosphate on the force and number of myosin cross-bridges during the isometric contraction of permeabilized muscle fibers from rabbit psoas. Biophys J 95, 5798-5808.
9. Cecchi G, Colomo F, Lombardi V & Piazzesi G (1987). Stiffness of frog muscle fibres during rise of tension and relaxation in fixed-end or length-clamped tetani. Pflügers Arch 409, 39-46.
10. Cecchi G, Griffiths PJ & Taylor S (1982). Muscular contraction: kinetics of crossbridge attachment studied by high-frequency stiffness measurements. Science 217, 70-72.
11. Cecchi G, Griffiths PJ & Taylor S (1986). Stiffness and force in activated frog skeletal muscle fibers. Biophys J 49, 437-451.
12. Colombini B, Benelli G, Nocella M, Musarò A, Cecchi G & Bagni MA (2009). Mechanical properties of intact single fibres from wild-type and MLC/mIgf-1 transgenic mouse muscle. J Muscle Res Cell Motil 30, 199-207.
13. Colombini B, Nocella M, Bagni MA, Griffiths PJ & Cecchi G (2010). Is the cross-bridge stiffness proportional to tension during muscle fiber activation? Biophys J 98, 2582-2590.
14. Colombini B, Nocella M, Benelli G, Cecchi & Bagni MA (2008). Effect of temperature on cross-bridge properties in intact frog muscle fibers. Am J Physiol Cell Physiol 294, C1113-C1117.
15. Cooke R (2007). Modulation of the actomyosin interaction during fatigue of skeletal muscle. Muscle Nerve 36, 756-777.
16. Cooke R & Pate E (1985). The effects of ADP and phosphate on the contraction of muscle fibers. Biophys J 48, 789-798.
17. Coupland ME, Puchert E & Ranatunga KW (2001). Temperature dependence of active tension in mammalian (rabbit psoas) muscle fibres: effect of inorganic phosphate. J Physiol 536, 879-891.
18. Dantzig JA, Goldman YE, Millar NC, Lacktis J & Homsher E (1992). Reversal of the cross-bridge force-generating transition by photogeneration of phosphate in rabbit psoas muscle fibres. J Physiol 451, 247-278.
19. Dawson MJ, Gadian DG & Wilkie DR (1980). Mechanical relaxation rate and metabolism studied in fatiguing muscle by phosphorus nuclear magnetic resonance. J Physiol 299, 465-484.
20. Edman KA & Lou F (1990). Changes in force and stiffness induced by fatigue and intracellular acidification in frog muscle fibres. J Physiol 424, 133-149.
21. Edwards RH, Hill DK & Jones DA (1975). Metabolic changes associated with the slowing of relaxation in fatigued mouse muscle. J Physiol 251, 287-301.
22. Fitts RH (2008). The cross-bridge cycle and skeletal muscle fatigue. J Appl Physiol 104, 551-558.
23. Ford LE, Huxley AF & Simmons RM (1977). Tension responses to sudden length change in stimulated frog muscle fibres near slack length. J Physiol 269, 441-515.
24. 2+ movements and tension development in rat skinned skeletal muscle fibres. J Physiol 482, 123-140.
25. Griffiths PJ, Bagni MA, Colombini B, Amenitsch H, Bernstorff S, Ashley CC & Cecchi G (2002). Changes in myosin S1 orientation and force induced by a temperature increase. Proc Natl Acad Sci U S A 99, 5384-5389.
26. Hibberd MG, Dantzig JA, Trentham DR & Goldman YE (1985). Phosphate release and force generation in skeletal muscle fibers. Science 228, 1317-1319.
27. Jones DA, Turner DL, McIntyre DB & Newham DJ (2009). Energy turnover in relation to slowing of contractile properties during fatiguing contractions of the human anterior tibialis muscle. J Physiol 587, 4329-4338.
28. Lamb GD & Westerblad H (2011). Acute effects of reactive oxygen and nitrogen species on the contractile function of skeletal muscle. J Physiol 589, 2119-2127.
29. Lännergren J & Westerblad H (1991). Force decline due to fatigue and intracellular acidification in isolated fibres from mouse skeletal muscle. J Physiol 434, 307-322.
30. Linari M, Bottinelli R, Pellegrino MA, Reconditi M, Reggiani C & Lombardi V (2004). The mechanism of the force response to stretch in human skinned muscle fibres with different myosin isoforms. J Physiol 554, 335-352.
31. Mademli L, Arampatzisa A & Walsh M (2006). Effect of muscle fatigue on the compliance of the gastrocnemius medialis tendon and aponeurosis. J Biomech 39, 426-434.
32. Millar NC & Homsher E (1990). The effect of phosphate and calcium on force generation in glycerinated rabbit skeletal muscle fibers. J Biol Chem 265, 20234-20240.
33. 31P-nuclear magnetic resonance spectroscopy study. Eur J Appl Physiol Occup Physiol 69, 102-109.
34. Mulligan IP, Palmer RE, Lipscomb S, Hoskins B & Ashley CC (1999). The effect of phosphate on the relaxation of frog skeletal muscle. Pflügers Arch 437, 393-399.
35. Piazzesi G, Reconditi M, Koubassova N, Decostre V, Linari M, Lucii L & Lombardi V (2003). Temperature dependence of the force-generating process in single fibres from frog skeletal muscle. J Physiol 549, 93-106.
36. Ranatunga KW (2010). Force and power generating mechanism(s) in active muscle as revealed from temperature perturbation studies. J Physiol 588, 3657-3670.
37. Sahlin K, Harris RC, Nylind B & Hultman E (1976). Lactate content and pH in muscle obtained after dynamic exercise. Pflügers Arch 367, 143-149.
38. Stienen GJ, Kiers JL, Bottinelli R, & Reggiani C (1996). Myofibrillar ATPase activity in skinned human skeletal muscle fibres: fibre type and temperature dependence. J Physiol 493, 299-307.
39. Takagi Y, Shuman H & Goldman YE (2004). Coupling between phosphate release and force generation in muscle actomyosin. Philos Trans R Soc Lond B Biol Sci 359, 1913-1920.
40. Tesi C, Colomo F, Nencini S, Piroddi N & Poggesi C (2000). The effect of inorganic phosphate on force generation in single myofibrils from rabbit skeletal muscle. Biophys J 78, 3081-3092.
41. Westerblad H & Allen DG (1991). Changes of myoplasmic calcium concentration during fatigue in single mouse muscle fibers. J Gen Physiol 98, 615-635.
42. Westerblad H & Allen DG (1992). Changes of intracellular pH due to repetitive stimulation of single fibres from mouse skeletal muscle. J Physiol 449, 49-71.
43. Westerblad H, Bruton JD & Lännergren J (1997). The effect of intracellular pH on contractile function of intact, single fibres of mouse muscle declines with increasing temperature. J Physiol 500, 193-204.
44. Westerblad H & Lännergren J (1991). Slowing of relaxation during fatigue in single mouse muscle fibres. J Physiol 434, 323-336.