Skip to main content
PMC home page
Biophysical Journal logoLink to Biophysical Journal
. 1993 Jan;64(1):197–210. doi: 10.1016/S0006-3495(93)81357-2

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.

Y Zhao 1, M Kawai 1
PMCID: PMC1262317  PMID: 7679297

Abstract

The actin-myosin lattice spacing of rabbit psoas fibers was osmotically compressed with a dextran T-500, and its effect on the elementary steps of the cross-bridge cycle was investigated. Experiments were performed at the saturating Ca (pCa 4.5-4.9), 200 mM ionic strength, pH 7.0, and at 20 degrees C, and the results were analyzed by the following cross-bridge scheme: [formula: see text] where A = actin, M = myosin head, S = MgATP, D = MgADP, and P = Pi = phosphate. From MgATP and MgADP studies on exponential process (C) and (D), the association constants of cross-bridges to MgADP (K0), MgATP (K1a), the rate constants of the isomerization of the AM S state (k1b and k-1b), and the rate constants of the cross-bridge detachment step (k2 and k-2) were deduced. From Pi study on process (B), the rate constants of the cross-bridge attachment (power stroke) step (k4- and k-4) and the association constant of Pi ions to cross-bridges (K5) were deduced. From ATP hydrolysis measurement, the rate constant of ADP-isomerization (rate-limiting) step (k6) was deduced. These kinetic constants were studied as functions of dextran concentrations. Our results show that nucleotide binding, the ATP-isomerization, and the cross-bridge detachment steps are minimally affected by the compression. The rate constant of the reverse power stroke step (k-4) decreases with mild compression (0-6.3% dextran), presumably because of the stabilization of the attached cross-bridges in the AM*DP state. The rate constant of the power stroke step (k4) does not change with mild compression, but it decreases with higher compression (> 6.3% dextran), presumably because of an increased difficulty in performing the power stroke. These results are consistent with the observation that isometric tension increases with a low level of compression and decreases with a high level of compression. Our results also show that the association constant K5 of Pi with cross-bridge state AM*D is not changed with compression. Our result further show that the ATP hydrolysis rate decreased with compression, and that the rate constants of the ADP-isomerization step (k6) becomes progressively less with compression. The effect of compression on the power stroke step and rate-limiting step implies that a large-scale molecular rearrangement in the myosin head takes place in these two slow reaction steps.

Full text

PDF
197

Selected References

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

  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. 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]
  3. Arheden H., Arner A., Hellstrand P. Force-velocity relation and rate of ATP hydrolysis in osmotically compressed skinned smooth muscle of the guinea pig. J Muscle Res Cell Motil. 1987 Apr;8(2):151–160. doi: 10.1007/BF01753991. [DOI] [PubMed] [Google Scholar]
  4. Berman M. R., Maughan D. W. Axial elastic modulus as a function of relative fiber width in relaxed skinned skeletal muscle fibers. Pflugers Arch. 1982 Mar;393(1):99–103. doi: 10.1007/BF00582400. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Egelman E. H., Francis N., DeRosier D. J. Helical disorder and the filament structure of F-actin are elucidated by the angle-layered aggregate. J Mol Biol. 1983 Jun 5;166(4):605–629. doi: 10.1016/s0022-2836(83)80286-1. [DOI] [PubMed] [Google Scholar]
  7. 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]
  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. Fujime S., Ishiwata S. Dynamic study of F-actin by quasielastic scattering of laser light. J Mol Biol. 1971 Nov 28;62(1):251–265. doi: 10.1016/0022-2836(71)90144-6. [DOI] [PubMed] [Google Scholar]
  10. Glyn H., Sleep J. Dependence of adenosine triphosphatase activity of rabbit psoas muscle fibres and myofibrils on substrate concentration. J Physiol. 1985 Aug;365:259–276. doi: 10.1113/jphysiol.1985.sp015770. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Godt R. E., Maughan D. W. Influence of osmotic compression on calcium activation and tension in skinned muscle fibers of the rabbit. Pflugers Arch. 1981 Oct;391(4):334–337. doi: 10.1007/BF00581519. [DOI] [PubMed] [Google Scholar]
  12. Greene L. E., Eisenberg E. Cooperative binding of myosin subfragment-1 to the actin-troponin-tropomyosin complex. Proc Natl Acad Sci U S A. 1980 May;77(5):2616–2620. doi: 10.1073/pnas.77.5.2616. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gulati J., Babu A. Critical dependence of calcium-activated force on width in highly compressed skinned fibers of the frog. Biophys J. 1985 Nov;48(5):781–787. doi: 10.1016/S0006-3495(85)83836-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Hammes G. G. Relaxation spectrometry of biological systems. Adv Protein Chem. 1968;23:1–57. doi: 10.1016/s0065-3233(08)60399-x. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. 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]
  18. Ishiwata S., Fujime S. Effect of calcium ions on the flexibility of reconstituted thin filaments of muscle studied by quasielastic scattering of laser light. J Mol Biol. 1972 Jul 28;68(3):511–522. doi: 10.1016/0022-2836(72)90103-9. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Kawai M., Güth K., Winnikes K., Haist C., Rüegg J. C. The effect of inorganic phosphate on the ATP hydrolysis rate and the tension transients in chemically skinned rabbit psoas fibers. Pflugers Arch. 1987 Jan;408(1):1–9. doi: 10.1007/BF00581833. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. 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]
  23. Kawai M., Schulman M. I. Crossbridge kinetics in chemically skinned rabbit psoas fibres when the actin-myosin lattice spacing is altered by dextran T-500. J Muscle Res Cell Motil. 1985 Jun;6(3):313–332. doi: 10.1007/BF00713172. [DOI] [PubMed] [Google Scholar]
  24. Kawai M., Wray J. S., Güth K. Effect of ionic strength on crossbridge kinetics as studied by sinusoidal analysis, ATP hydrolysis rate and X-ray diffraction techniques in chemically skinned rabbit psoas fibres. J Muscle Res Cell Motil. 1990 Oct;11(5):392–402. doi: 10.1007/BF01739760. [DOI] [PubMed] [Google Scholar]
  25. Krasner B., Maughan D. The relationship between ATP hydrolysis and active force in compressed and swollen skinned muscle fibers of the rabbit. Pflugers Arch. 1984 Feb;400(2):160–165. doi: 10.1007/BF00585033. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Lienhard G. E., Secemski I. I. P 1 ,P 5 -Di(adenosine-5')pentaphosphate, a potent multisubstrate inhibitor of adenylate kinase. J Biol Chem. 1973 Feb 10;248(3):1121–1123. [PubMed] [Google Scholar]
  28. Matsubara I., Umazume Y., Yagi N. Lateral filamentary spacing in chemically skinned murine muscles during contraction. J Physiol. 1985 Mar;360:135–148. doi: 10.1113/jphysiol.1985.sp015608. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. Schoenberg M. Geometrical factors influencing muscle force development. I. The effect of filament spacing upon axial forces. Biophys J. 1980 Apr;30(1):51–67. doi: 10.1016/S0006-3495(80)85076-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sleep J. A., Hutton R. L. Exchange between inorganic phosphate and adenosine 5'-triphosphate in the medium by actomyosin subfragment 1. Biochemistry. 1980 Apr 1;19(7):1276–1283. doi: 10.1021/bi00548a002. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. 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]
  34. 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]
  35. Winkelmann D. A., Baker T. S., Rayment I. Three-dimensional structure of myosin subfragment-1 from electron microscopy of sectioned crystals. J Cell Biol. 1991 Aug;114(4):701–713. doi: 10.1083/jcb.114.4.701. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES