Skip to main content
PMC home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1984 Sep;354:577–604. doi: 10.1113/jphysiol.1984.sp015394

Relaxation of rabbit psoas muscle fibres from rigor by photochemical generation of adenosine-5'-triphosphate.

Y E Goldman, M G Hibberd, D R Trentham
PMCID: PMC1193430  PMID: 6481645

Abstract

Correlations have been made between the mechanical and biochemical descriptions of muscle relaxation. Skinned muscle fibres in the rigor state were incubated in a solution containing P3-1-(2-nitro)phenylethyladenosine-5'-triphosphate, 'caged ATP', an inert photolabile precursor of ATP, and free Ca2+ concentration less than 10(-8) M. The mechanical response of the fibre was monitored during relaxation initiated by liberating ATP with a pulse of 347 nm light from a frequency-doubled ruby laser. Tension first dropped and then rose briefly, before finally declining to the relaxed level. Stiffness, in phase with a sinusoidal length change, declined monotonically after the laser pulse. Out-of-phase stiffness increased briefly after a delay, then returned to the base line during the final relaxation. The development of the out-of-phase stiffness signal was taken as evidence that during the relaxation some cross-bridges were present with properties similar to those in an active contraction. The tension rise and slower phase of relaxation can be explained by a mechanism in which some of the cross-bridges reattach, generate force and finally detach in the absence of Ca2+ ions. In this model cross-bridge attachment is facilitated by protein co-operativity within the myofilaments. Detailed analysis of the mechanical transients makes other possible models for the initial tension rise unlikely. Stretching or releasing fibres prior to photolysis changed the time course of the early parts of the tension transient without significant effect on the later phases or on stiffness. The tension records from stretch, release and isometric trials converged to a final common time course of relaxation. Analysis of the convergence of tension records provided a means for measuring the cross-bridge detachment rate from the thin filament as a function of ATP concentration. The apparent second-order rate constant for detachment was at least 5 X 10(5) M-1 S-1 at 20-22 degrees C. The final relaxation rate was less dependent on ATP concentration than the early convergence. The results indicate that ATP binding and cross-bridge detachment from the nucleotide-free intermediate of the cross-bridge cycle are rapid compared to the cross-bridge cycling rate.

Full text

PDF
577

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Arata T., Mukohata Y., Tonomura Y. Structure and function of the two heads of the myosin molecule. VI. ATP hydrolysis, shortening, and tension development of myofibrils. J Biochem. 1977 Sep;82(3):801–812. doi: 10.1093/oxfordjournals.jbchem.a131756. [DOI] [PubMed] [Google Scholar]
  2. Bremel R. D., Weber A. Cooperation within actin filament in vertebrate skeletal muscle. Nat New Biol. 1972 Jul 26;238(82):97–101. doi: 10.1038/newbio238097a0. [DOI] [PubMed] [Google Scholar]
  3. Curtin N. A., Gilbert C., Kretzschmar K. M., Wilkie D. R. The effect of the performance of work on total energy output and metabolism during muscular contraction. J Physiol. 1974 May;238(3):455–472. doi: 10.1113/jphysiol.1974.sp010537. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. DIEBLER H., EIGEN M., HAMMES G. G. [Relaxation spectrometric studies of fast reactions of ATP in aqueous solution]. Z Naturforsch B. 1960 Sep;15B:554–560. [PubMed] [Google Scholar]
  5. 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]
  6. Fabiato A., Fabiato F. Effects of magnesium on contractile activation of skinned cardiac cells. J Physiol. 1975 Aug;249(3):497–517. doi: 10.1113/jphysiol.1975.sp011027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Ferenczi M. A., Homsher E., Trentham D. R. The kinetics of magnesium adenosine triphosphate cleavage in skinned muscle fibres of the rabbit. J Physiol. 1984 Jul;352:575–599. doi: 10.1113/jphysiol.1984.sp015311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Goldman Y. E., Hibberd M. G., McCray J. A., Trentham D. R. Relaxation of muscle fibres by photolysis of caged ATP. Nature. 1982 Dec 23;300(5894):701–705. doi: 10.1038/300701a0. [DOI] [PubMed] [Google Scholar]
  10. Goldman Y. E., Hibberd M. G., Trentham D. R. Initiation of active contraction by photogeneration of adenosine-5'-triphosphate in rabbit psoas muscle fibres. J Physiol. 1984 Sep;354:605–624. doi: 10.1113/jphysiol.1984.sp015395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Goldman Y. E., Simmons R. M. Control of sarcomere length in skinned muscle fibres of Rana temporaria during mechanical transients. J Physiol. 1984 May;350:497–518. doi: 10.1113/jphysiol.1984.sp015215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. HUXLEY A. F. Muscle structure and theories of contraction. Prog Biophys Biophys Chem. 1957;7:255–318. [PubMed] [Google Scholar]
  13. Hill T. L. Theoretical formalism for the sliding filament model of contraction of striated muscle. Part I. Prog Biophys Mol Biol. 1974;28:267–340. doi: 10.1016/0079-6107(74)90020-0. [DOI] [PubMed] [Google Scholar]
  14. Huxley A. F. Muscular contraction. J Physiol. 1974 Nov;243(1):1–43. [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Huxley H. E., Brown W. The low-angle x-ray diagram of vertebrate striated muscle and its behaviour during contraction and rigor. J Mol Biol. 1967 Dec 14;30(2):383–434. doi: 10.1016/s0022-2836(67)80046-9. [DOI] [PubMed] [Google Scholar]
  17. Kaplan J. H., Forbush B., 3rd, Hoffman J. F. Rapid photolytic release of adenosine 5'-triphosphate from a protected analogue: utilization by the Na:K pump of human red blood cell ghosts. Biochemistry. 1978 May 16;17(10):1929–1935. doi: 10.1021/bi00603a020. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Kawai M., Brandt P. W. Two rigor states in skinned crayfish single muscle fibers. J Gen Physiol. 1976 Sep;68(3):267–280. doi: 10.1085/jgp.68.3.267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lehrer S. S., Kerwar G. Intrinsic fluorescence of actin. Biochemistry. 1972 Mar 28;11(7):1211–1217. doi: 10.1021/bi00757a015. [DOI] [PubMed] [Google Scholar]
  21. Lester H. A., Nerbonne J. M. Physiological and pharmacological manipulations with light flashes. Annu Rev Biophys Bioeng. 1982;11:151–175. doi: 10.1146/annurev.bb.11.060182.001055. [DOI] [PubMed] [Google Scholar]
  22. Levy R. M., Umazume Y., Kushmerick M. J. Ca2+ dependence of tension and ADP production in segments of chemically skinned muscle fibers. Biochim Biophys Acta. 1976 May 14;430(2):352–365. doi: 10.1016/0005-2728(76)90091-8. [DOI] [PubMed] [Google Scholar]
  23. McCray J. A., Herbette L., Kihara T., Trentham D. R. A new approach to time-resolved studies of ATP-requiring biological systems; laser flash photolysis of caged ATP. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7237–7241. doi: 10.1073/pnas.77.12.7237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. McELROY W. D., STREHLER B. L. Factors influencing the response of the bioluminescent reaction to adenosine triphosphate. Arch Biochem. 1949 Jul;22(3):420–433. [PubMed] [Google Scholar]
  25. Reuben J. P., Brandt P. W., Berman M., Grundfest H. Regulation of tension in the skinned crayfish muscle fiber. I. Contraction and relaxation in the absence of Ca (pCa is greater than 9). J Gen Physiol. 1971 Apr;57(4):385–407. doi: 10.1085/jgp.57.4.385. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Schoenberg M., Wells J. B., Podolsky R. J. Muscle compliance and the longitudinal transmission of mechanical impulses. J Gen Physiol. 1974 Dec;64(6):623–642. doi: 10.1085/jgp.64.6.623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. Taylor R. S., Weeds A. G. The magnesium-ion-dependent adenosine triphosphatase of bovine cardiac Myosin and its subfragment-1. Biochem J. 1976 Nov;159(2):301–315. doi: 10.1042/bj1590301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Weeds A. G., Taylor R. S. Separation of subfragment-1 isoenzymes from rabbit skeletal muscle myosin. Nature. 1975 Sep 4;257(5521):54–56. doi: 10.1038/257054a0. [DOI] [PubMed] [Google Scholar]
  30. White H. D., Taylor E. W. Energetics and mechanism of actomyosin adenosine triphosphatase. Biochemistry. 1976 Dec 28;15(26):5818–5826. doi: 10.1021/bi00671a020. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES