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. 1994 Oct;67(4):1655–1668. doi: 10.1016/S0006-3495(94)80638-1

Kinetic and thermodynamic studies of the cross-bridge cycle in rabbit psoas muscle fibers.

Y Zhao 1, M Kawai 1
PMCID: PMC1225527  PMID: 7819497

Abstract

The effect of temperature on elementary steps of the cross-bridge cycle was investigated with sinusoidal analysis technique in skinned rabbit psoas fibers. We studied the effect of MgATP on exponential process (C) to characterize the MgATP binding step and cross-bridge detachment step at six different temperatures in the range 5-30 degrees C. Similarly, we studied the effect of MgADP on exponential process (C) to characterize the MgADP binding step. We also studied the effect of phosphate (Pi) on exponential process (B) to characterize the force generation step and Pi-release step. From the results of these studies, we deduced the temperature dependence of the kinetic constants of the elementary steps and their thermodynamic properties. We found that the MgADP association constant (K0) and the MgATP association constant (K1) significantly decreased when the temperature was increased from 5 to 20 degrees C, implying that nucleotide binding became weaker at higher temperatures. K0 and K1 did not change much in the 20-30 degree C range. The association constant of Pi to cross-bridges (K5) did not change much with temperature. We found that Q10 for the cross-bridge detachment step (k2) was 2.6, and for its reversal step (k-2) was 3.0. We found that Q10 for the force generation step (Pi-isomerization step, k4) was 6.8, and its reversal step (k-4) was 1.6. The equilibrium constant of the detachment step (K2) was not affected much by temperature, whereas the equilibrium constant of the force generation step (K4) increased significantly with temperature increase. Thus, the force generation step consists of an endothermic reaction. The rate constant of the rate-limiting step (k6) did not change much with temperature, whereas the ATP hydrolysis rate increased significantly with temperature increase. We found that the force generation step accompanies a large entropy increase and a small free energy change; hence, this step is an entropy-driven reaction. These observations are consistent with the hypothesis that the hydrophobic interaction between residues of actin and myosin underlies the mechanism of force generation. We conclude that the force generation step is the most temperature-sensitive step among elementary steps of the cross-bridge cycle, which explains increased isometric tension at high temperatures in rabbit psoas fibers.

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Selected References

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  1. Abbott R. H., Steiger G. J. Temperature and amplitude dependence of tension transients in glycerinated skeletal and insect fibrillar muscle. J Physiol. 1977 Mar;266(1):13–42. doi: 10.1113/jphysiol.1977.sp011754. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bershitsky S. Y., Tsaturyan A. K. Tension responses to joule temperature jump in skinned rabbit muscle fibres. J Physiol. 1992 Feb;447:425–448. doi: 10.1113/jphysiol.1992.sp019010. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brenner B., Yu L. C., Chalovich J. M. Parallel inhibition of active force and relaxed fiber stiffness in skeletal muscle by caldesmon: implications for the pathway to force generation. Proc Natl Acad Sci U S A. 1991 Jul 1;88(13):5739–5743. doi: 10.1073/pnas.88.13.5739. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bressler B. H. Isometric contractile properties and instantaneous stiffness of amphibian skeletal muscle in the temperature range from 0 to 20 degrees C. Can J Physiol Pharmacol. 1981 Jun;59(6):548–554. doi: 10.1139/y81-082. [DOI] [PubMed] [Google Scholar]
  5. Chase P. B., Martyn D. A., Kushmerick M. J., Gordon A. M. Effects of inorganic phosphate analogues on stiffness and unloaded shortening of skinned muscle fibres from rabbit. J Physiol. 1993 Jan;460:231–246. doi: 10.1113/jphysiol.1993.sp019469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cooke R., Pate E. The effects of ADP and phosphate on the contraction of muscle fibers. Biophys J. 1985 Nov;48(5):789–798. doi: 10.1016/S0006-3495(85)83837-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dantzig J. A., Goldman Y. E., Millar N. C., Lacktis J., Homsher E. Reversal of the cross-bridge force-generating transition by photogeneration of phosphate in rabbit psoas muscle fibres. J Physiol. 1992;451:247–278. doi: 10.1113/jphysiol.1992.sp019163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Davis J. S., Harrington W. F. A single order-disorder transition generates tension during the Huxley-Simmons phase 2 in muscle. Biophys J. 1993 Nov;65(5):1886–1898. doi: 10.1016/S0006-3495(93)81259-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Davis J. S., Harrington W. F. Force generation by muscle fibers in rigor: a laser temperature-jump study. Proc Natl Acad Sci U S A. 1987 Feb;84(4):975–979. doi: 10.1073/pnas.84.4.975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Eastwood A. B., Wood D. S., Bock K. L., Sorenson M. M. Chemically skinned mammalian skeletal muscle. I. The structure of skinned rabbit psoas. Tissue Cell. 1979;11(3):553–566. doi: 10.1016/0040-8166(79)90062-4. [DOI] [PubMed] [Google Scholar]
  11. Eisenberg E., Greene L. E. The relation of muscle biochemistry to muscle physiology. Annu Rev Physiol. 1980;42:293–309. doi: 10.1146/annurev.ph.42.030180.001453. [DOI] [PubMed] [Google Scholar]
  12. Feldhau P., Fröhlich T., Goody R. S., Isakov M., Schirmer R. H. Synthetic inhibitors of adenylate kinases in the assays for ATPases and phosphokinases. Eur J Biochem. 1975 Sep 1;57(1):197–204. doi: 10.1111/j.1432-1033.1975.tb02291.x. [DOI] [PubMed] [Google Scholar]
  13. Ford L. E., Huxley A. F., Simmons R. M. Tension responses to sudden length change in stimulated frog muscle fibres near slack length. J Physiol. 1977 Jul;269(2):441–515. doi: 10.1113/jphysiol.1977.sp011911. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Geeves M. A., Goody R. S., Gutfreund H. Kinetics of acto-S1 interaction as a guide to a model for the crossbridge cycle. J Muscle Res Cell Motil. 1984 Aug;5(4):351–361. doi: 10.1007/BF00818255. [DOI] [PubMed] [Google Scholar]
  15. Gilbert S. H., Ford L. E. Heat changes during transient tension responses to small releases in active frog muscle. Biophys J. 1988 Oct;54(4):611–617. doi: 10.1016/S0006-3495(88)82996-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Goldman Y. E., McCray J. A., Ranatunga K. W. Transient tension changes initiated by laser temperature jumps in rabbit psoas muscle fibres. J Physiol. 1987 Nov;392:71–95. doi: 10.1113/jphysiol.1987.sp016770. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Greene L. E., Eisenberg E. Dissociation of the actin.subfragment 1 complex by adenyl-5'-yl imidodiphosphate, ADP, and PPi. J Biol Chem. 1980 Jan 25;255(2):543–548. [PubMed] [Google Scholar]
  18. Güth K., Wojciechowski R. Perfusion cuvette for the simultaneous measurement of mechanical, optical and energetic parameters of skinned muscle fibres. Pflugers Arch. 1986 Nov;407(5):552–557. doi: 10.1007/BF00657515. [DOI] [PubMed] [Google Scholar]
  19. Heinl P., Kuhn H. J., Rüegg J. C. Tension responses to quick length changes of glycerinated skeletal muscle fibres from the frog and tortoise. J Physiol. 1974 Mar;237(2):243–258. doi: 10.1113/jphysiol.1974.sp010480. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Highsmith S. The effects of temperature and salts on myosin subfragment-1 and F-actin association. Arch Biochem Biophys. 1977 Apr 30;180(2):404–408. doi: 10.1016/0003-9861(77)90054-6. [DOI] [PubMed] [Google Scholar]
  21. Huxley A. F., Simmons R. M. Proposed mechanism of force generation in striated muscle. Nature. 1971 Oct 22;233(5321):533–538. doi: 10.1038/233533a0. [DOI] [PubMed] [Google Scholar]
  22. Johnson K. A., Taylor E. W. Intermediate states of subfragment 1 and actosubfragment 1 ATPase: reevaluation of the mechanism. Biochemistry. 1978 Aug 22;17(17):3432–3442. doi: 10.1021/bi00610a002. [DOI] [PubMed] [Google Scholar]
  23. Kawai M., Brandt P. W. Sinusoidal analysis: a high resolution method for correlating biochemical reactions with physiological processes in activated skeletal muscles of rabbit, frog and crayfish. J Muscle Res Cell Motil. 1980 Sep;1(3):279–303. doi: 10.1007/BF00711932. [DOI] [PubMed] [Google Scholar]
  24. Kawai M., Halvorson H. R. Role of MgATP and MgADP in the cross-bridge kinetics in chemically skinned rabbit psoas fibers. Study of a fast exponential process (C) Biophys J. 1989 Apr;55(4):595–603. doi: 10.1016/S0006-3495(89)82857-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kawai M., Halvorson H. R. Two step mechanism of phosphate release and the mechanism of force generation in chemically skinned fibers of rabbit psoas muscle. Biophys J. 1991 Feb;59(2):329–342. doi: 10.1016/S0006-3495(91)82227-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kawai M., Saeki Y., Zhao Y. Crossbridge scheme and the kinetic constants of elementary steps deduced from chemically skinned papillary and trabecular muscles of the ferret. Circ Res. 1993 Jul;73(1):35–50. doi: 10.1161/01.res.73.1.35. [DOI] [PubMed] [Google Scholar]
  27. Kawai M., Zhao Y. Cross-bridge scheme and force per cross-bridge state in skinned rabbit psoas muscle fibers. Biophys J. 1993 Aug;65(2):638–651. doi: 10.1016/S0006-3495(93)81109-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Kodama T. Thermodynamic analysis of muscle ATPase mechanisms. Physiol Rev. 1985 Apr;65(2):467–551. doi: 10.1152/physrev.1985.65.2.467. [DOI] [PubMed] [Google Scholar]
  29. Kuhn H. J. The mechanochemistry of force production in muscle. J Muscle Res Cell Motil. 1981 Mar;2(1):7–44. doi: 10.1007/BF00712060. [DOI] [PubMed] [Google Scholar]
  30. Marston S. B., Taylor E. W. Comparison of the myosin and actomyosin ATPase mechanisms of the four types of vertebrate muscles. J Mol Biol. 1980 Jun 5;139(4):573–600. doi: 10.1016/0022-2836(80)90050-9. [DOI] [PubMed] [Google Scholar]
  31. Meyer R. A., Brown T. R., Kushmerick M. J. Phosphorus nuclear magnetic resonance of fast- and slow-twitch muscle. Am J Physiol. 1985 Mar;248(3 Pt 1):C279–C287. doi: 10.1152/ajpcell.1985.248.3.C279. [DOI] [PubMed] [Google Scholar]
  32. Rall J. A., Woledge R. C. Influence of temperature on mechanics and energetics of muscle contraction. Am J Physiol. 1990 Aug;259(2 Pt 2):R197–R203. doi: 10.1152/ajpregu.1990.259.2.R197. [DOI] [PubMed] [Google Scholar]
  33. Ranatunga K. W., Wylie S. R. Temperature-dependent transitions in isometric contractions of rat muscle. J Physiol. 1983 Jun;339:87–95. doi: 10.1113/jphysiol.1983.sp014704. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Rayment I., Holden H. M., Whittaker M., Yohn C. B., Lorenz M., Holmes K. C., Milligan R. A. Structure of the actin-myosin complex and its implications for muscle contraction. Science. 1993 Jul 2;261(5117):58–65. doi: 10.1126/science.8316858. [DOI] [PubMed] [Google Scholar]
  35. Rayment I., Rypniewski W. R., Schmidt-Bäse K., Smith R., Tomchick D. R., Benning M. M., Winkelmann D. A., Wesenberg G., Holden H. M. Three-dimensional structure of myosin subfragment-1: a molecular motor. Science. 1993 Jul 2;261(5117):50–58. doi: 10.1126/science.8316857. [DOI] [PubMed] [Google Scholar]
  36. Schoenberg M. Characterization of the myosin adenosine triphosphate (M.ATP) crossbridge in rabbit and frog skeletal muscle fibers. Biophys J. 1988 Jul;54(1):135–148. doi: 10.1016/S0006-3495(88)82938-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Schoenberg M., Eisenberg E. ADP binding to myosin cross-bridges and its effect on the cross-bridge detachment rate constants. J Gen Physiol. 1987 Jun;89(6):905–920. doi: 10.1085/jgp.89.6.905. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Sturtevant J. M. Heat capacity and entropy changes in processes involving proteins. Proc Natl Acad Sci U S A. 1977 Jun;74(6):2236–2240. doi: 10.1073/pnas.74.6.2236. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Sutoh K., Ando M., Sutoh K., Toyoshima Y. Y. Site-directed mutations of Dictyostelium actin: disruption of a negative charge cluster at the N terminus. Proc Natl Acad Sci U S A. 1991 Sep 1;88(17):7711–7714. doi: 10.1073/pnas.88.17.7711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Szilagyi L., Balint M., Sreter F. A., Gergely J. Photoaffinity labelling with an ATP analog of the N-terminal peptide of myosin. Biochem Biophys Res Commun. 1979 Apr 13;87(3):936–945. doi: 10.1016/0006-291x(79)92047-3. [DOI] [PubMed] [Google Scholar]
  41. TONOMURA Y., TOKURA S., SEKIYA K. Binding of myosin A to F-actin. J Biol Chem. 1962 Apr;237:1074–1081. [PubMed] [Google Scholar]
  42. Takashi R., Putnam S. A fluorimetric method for continuously assaying ATPase: application to small specimens of glycerol-extracted muscle fibers. Anal Biochem. 1979 Jan 15;92(2):375–382. doi: 10.1016/0003-2697(79)90674-2. [DOI] [PubMed] [Google Scholar]
  43. Tawada K., Kawai M. Covalent cross-linking of single fibers from rabbit psoas increases oscillatory power. Biophys J. 1990 Mar;57(3):643–647. doi: 10.1016/S0006-3495(90)82582-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Taylor E. W. Mechanism of actomyosin ATPase and the problem of muscle contraction. CRC Crit Rev Biochem. 1979;6(2):103–164. doi: 10.3109/10409237909102562. [DOI] [PubMed] [Google Scholar]
  45. Tregear R. T., Squire J. M. Myosin content and filament structure in smooth and striated muscle. J Mol Biol. 1973 Jun 25;77(2):279–290. doi: 10.1016/0022-2836(73)90336-7. [DOI] [PubMed] [Google Scholar]
  46. Trybus K. M., Taylor E. W. Transient kinetics of adenosine 5'-diphosphate and adenosine 5'-(beta, gamma-imidotriphosphate) binding to subfragment 1 and actosubfragment 1. Biochemistry. 1982 Mar 16;21(6):1284–1294. doi: 10.1021/bi00535a028. [DOI] [PubMed] [Google Scholar]
  47. Zhao Y., Kawai M. BDM affects nucleotide binding and force generation steps of the cross-bridge cycle in rabbit psoas muscle fibers. Am J Physiol. 1994 Feb;266(2 Pt 1):C437–C447. doi: 10.1152/ajpcell.1994.266.2.C437. [DOI] [PubMed] [Google Scholar]
  48. Zhao Y., Kawai M. The effect of the lattice spacing change on cross-bridge kinetics in chemically skinned rabbit psoas muscle fibers. II. Elementary steps affected by the spacing change. Biophys J. 1993 Jan;64(1):197–210. doi: 10.1016/S0006-3495(93)81357-2. [DOI] [PMC free article] [PubMed] [Google Scholar]

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