The ATP hydrolysis and phosphate release steps control the time course of force development in rabbit skeletal muscle

Journal of Physiology

Volumn 563, Issue 3, 2005, Pages 671-687

  Sleep, John ^a   Irving, Malcolm ^a   Burton, Kevin ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; APYRASE; CALCIUM; MYOSIN ADENOSINE TRIPHOSPHATASE; PHOSPHATE; ADENOSINE TRIPHOSPHATASE; CALCIUM ION; MYOSIN;

ACCURACY; ACTIN MYOSIN INTERACTION; ANIMAL TISSUE; ARTICLE; BIOCHEMISTRY; BIOMECHANICS; CONTROLLED STUDY; KINETICS; MALE; MUSCLE FORCE; MUSCLE ISOMETRIC CONTRACTION; MUSCLE LENGTH; MUSCLE STRETCHING; NONHUMAN; PHASE TRANSITION; PHOTOLYSIS; PRIORITY JOURNAL; PROTEIN HYDROLYSIS; PSOAS MUSCLE; RABBIT; REACTION TIME; SARCOMERE LENGTH; SKELETAL MUSCLE; TEMPERATURE SENSITIVITY; ADULT; CONFORMATIONAL TRANSITION; FORCE; HYDROLYSIS; MUSCLE CELL; MUSCLE CONTRACTION; MUSCLE STRENGTH; SARCOMERE; TEMPERATURE;

ADENOSINE TRIPHOSPHATE; ANIMALS; CALCIUM; CELLS, CULTURED; COMPUTER SIMULATION; ELASTICITY; ENERGY TRANSFER; HYDROLYSIS; ISOMETRIC CONTRACTION; KINETICS; MALE; MODELS, BIOLOGICAL; MUSCLE CELLS; MUSCLE, SKELETAL; PHOSPHATES; RABBITS; STRESS, MECHANICAL;

EID: 15844429778     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1113/jphysiol.2004.078873     Document Type: Article

References (49)

1. Allen TS, Ling N, Irving M & Goldman YE (1996). Orientation changes in myosin regulatory light chains following photorelease of ATP in skinned muscle fibers. Biophys J 70, 1847-1862.
2. Bershitsky SY & Tsaturyan AK (1992). Tension responses to Joule temperature jump in skinned rabbit muscle fibres. J Physiol 447, 425-448.
3. Brenner B (1983). Technique for stabilizing the striation pattern in maximally calcium-activated skinned rabbit psoas fibers. Biophys J 141, 99-102.
4. 2+ on cross-bridge turnover kinetics in skinned single rabbit psoas fibers: implications for regulation of muscle contraction. Proc Natl Acad Sci U S A 85 3265-3269.
5. Brenner B & Eisenberg E (1986). Rate of force generation in muscle: correlation with actomyosin ATPase activity in solution. Proc Natl Acad Sci U S A 83, 3542-3546.
6. Burton K (1992). Stiffness and cross-bridge strain following large step stretches at the end of rapid shortening in rabbit psoas skinned single fibers. Biophys J 61, A267.
7. Burton K, White H & Sleep J (2005). Muscle fibre and actomyosin kinetics using a series of metal-nucleotide substrates. J Physiol 563, 689-711.
8. 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.
9. Dantzig JA, Hibberd MG, Trentham DR & Goldman YE (1991). Cross-bridge kinetics in the presence of MgADP investigated by photolysis of caged ATP in rabbit psoas muscle fibres. J Physiol 432, 639-680.
10. Davis JS & Rodgers ME (1995). Force generation and temperature-jump and length-jump tension transients in muscle fibers. Biophys J 68, 2032-2040.
11. Dominguez R, Freyzon Y, Trybus KM & Cohen C (1998). Crystal structure of a vertebrate smooth muscle myosin motor domain and its complex with the essential light chain: visualization of the pre-power stroke state. Cell 94, 559-571.
12. Fenn WO (1923). A quantitative comparison between the energy liberated and the work performed by the isolated sartorius of the frog. J Physiol 58, 175-203.
13. Fortune NS, Geeves MA & Ranatunga KW (1991). Tension responses to rapid pressure release in glycerinated rabbit muscle fibers. Proc Natl Acad Sci U S A 88, 7323-7327.
14. Fortune NS, Geeves MA & Ranatunga KW (1994). Contractile activation and force generation in skinned rabbit muscle fibres: effects of hydrostatic pressure. J Physiol 474, 283-290.
15. Geeves MA & Holmes KC (1999). Structural mechanism of muscle contraction. Annu Rev Biochem 68, 687-728.
16. Glyn H & Sleep J (1985). Dependence of adenosine triphosphatase activity of rabbit psoas muscle fibres and myofibrils on substrate concentration. J Physiol 365, 259-276.
17. Goldman YE, Hibberd MG & Trentham DR (1984). Initiation of active contraction by photogeneration of adenosine-5′-triphosphate in rabbit psoas muscle fibres. J Physiol 354, 605-624.
18. He ZH, Chillingworth RK, Brune M, Corrie JE, Trentham DR, Webb MR & Ferenczi MA (1997). ATPase kinetics on activation of rabbit and frog permeabilized isometric muscle fibres: a real time phosphate assay. J Physiol 501, 125-148.
19. Herrmann C, Lionne C, Travers F & Barman T (1994). Correlation of ActoS1, myofibrillar, and muscle fiber ATPases. Biochemistry 33, 4148-4154.
20. Hilber K, Sun YB & Irving M (2001). Effects of sarcomere length and temperature on the rate of ATP utilisation by rabbit psoas muscle fibres. J Physiol 531, 771-780.
21. Homsher E, Irving M & Wallner A (1981). High-energy phosphate metabolism and energy liberation associated with rapid shortening in frog skeletal muscle. J Physiol 321, 423-436.
22. Huxley AF (1973). A note suggesting that the cross-bridge attachment during muscle contraction may take place in two stages. Proc R Soc Lond B Biol Sci 183, 83-86.
23. Huxley AF & Simmons RM (1971). Proposed mechanism of force generation in striated muscle. Nature 233, 533-538.
24. Huxley AF & Simmons RM (1973). Mechanical transients and the origin of muscular force. Cold Spring Harb Symp Quant Biol 37 669-680.
25. Irving M, Lombardi V, Piazzesi G & Ferenczi MA (1992). Myosin head movements are synchronous with the elementary force-generating process in muscle. Nature 357, 156-158.
26. Kawai M & Halvorson HR (1991). Two step mechanism of phosphate release and the mechanism of force generation in chemically skinned fibers of rabbit psoas muscle. Biophys J 59, 329-342.
27. Kushmerick MJ & Davies RE (1969). The chemical energetics of muscle contraction. Proc R Soc Lond B Biol Sci 174, 315-353.
28. Lombardi V, Piazzesi G, Ferenczi MA, Thirlwell H, Dobbie I & Irving M (1995). Elastic distortion of myosin heads and repriming of the working stroke in muscle. Nature 374, 553-555.
29. Lund J, Webb MR & White DC (1987). Changes in the ATPase activity of insect fibrillar flight muscle during calcium and strain activation probed by phosphate-water oxygen exchange. J Biol Chem 262, 8584-8590.
30. Lund J, Webb MR & White DC (1988). Changes in the ATPase activity of insect fibrillar flight muscle during sinusoidal length oscillation probed by phosphate-water oxygen exchange. J Biol Chem 263, 5505-5511.
31. Ma YZ & Taylor EW (1994). Kinetic mechanism of myofibril ATPase. Biophys J 66, 1542-1553.
32. Millar NC & Homsher E (1990). The effect of phosphate and calcium on force generation in glycerinated rabbit skeletal muscle fibers. A steady-state and transient kinetic study. J Biol Chem 265, 20234-20240.
33. 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.
34. Piazzesi G, Reconditi M, Linari M, Lucii L, Sun YB, Narayanan T, Boesecke P, Lombardi V & Irving M (2002). Mechanism of force generation by myosin heads in skeletal muscle. Nature 415, 659-662.
35. Provencher SW (1976). A fourier method for the analysis of exponential decay curves. Biophys J 16, 27-41.
36. Ranatunga KW, Coupland ME & Mutungi G (2002). An asymmetry in the phosphate dependence of tension transients induced by length perturbation in mammalian (rabbit psoas) muscle fibres. J Physiol 542, 899-910.
37. Rayment I, Holden HM, Whittaker M, Yohn CB, Lorenz M, Holmes KC & Milligan RA (1993). Structure of the actin-myosin complex and its implications for muscle contraction. Science 261, 58-65.
38. Rosenfeld SS & Taylor EW (1984). The ATPase mechanism of skeletal and smooth muscle acto-subfragment 1. J Biol Chem 259 11908-11919.
39. Sleep J (1989). Temperature control and exchange of the bathing solution for skinned muscle fibres. J Physiol 7P.
40. Sleep J & Burton K (1989). The use of apyrase in caged-ATP experiments. Biophys J 57, 542a.
41. Sleep J, Herrmann C, Barman T & Travers F (1994). Inhibition of ATP binding to myofibrils and acto-myosin subfragment 1 by caged ATP. Biochemistry 33, 6038-6042.
42. Smith CA & Rayment I (1995). X-ray structure of the magnesium (II)-pyrophosphate complex of the truncated head of Dictyostelium discoideum myosin to 2.7Å resolution. Biochemistry 34, 8973-8981.
43. Sun YB, Hilber K & Irving M (2001). Effect of active shortening on the rate of ATP utilisation by rabbit psoas muscle fibres. J Physiol 531, 781-791.
44. Takagi Y, Homsher EE, Goldman YE & Shuman H (2004). ATP and phosphate dependence of single rabbit skeletal actomyosin interactions under different loads. Biophys J 86, 54A.
45. Tesi C, Colomo F, Piroddi N & Poggesi C (2002). Characterization of the cross-bridge force-generating step using inorganic phosphate and BDM in myofibrils from rabbit skeletal muscles. J Physiol 541, 187-199.
46. White HD, Belknap B & Webb MR (1997). Kinetics of nucleoside triphosphate cleavage and phosphate release steps by associated rabbit skeletal actomyosin, measured using a novel fluorescent probe for phosphate. Biochemistry 36, 11828-11836.
47. White DC, Lund J & Webb MR (1988). Cross-bridge kinetics in asynchronous insect flight muscle. Adv Exp Med Biol 226, 169-179.
48. Yu LC & Brenner B (1989). Structures of actomyosin crossbridges in relaxed and rigor muscle fibers. Biophys J 55 441-453.
49. Zhao Y & Kawai M (1994). Kinetic and thermodynamic studies of the cross-bridge cycle in rabbit psoas muscle fibers. Biophys J 67, 1655-1668.