Skip to main content
NCBI home page
Biophysical Journal logoLink to Biophysical Journal
. 1998 May;74(5):2459–2473. doi: 10.1016/S0006-3495(98)77954-8

The stiffness of skeletal muscle in isometric contraction and rigor: the fraction of myosin heads bound to actin.

M Linari 1, I Dobbie 1, M Reconditi 1, N Koubassova 1, M Irving 1, G Piazzesi 1, V Lombardi 1
PMCID: PMC1299588  PMID: 9591672

Abstract

Step changes in length (between -3 and +5 nm per half-sarcomere) were imposed on isolated muscle fibers at the plateau of an isometric tetanus (tension T0) and on the same fibers in rigor after permeabilization of the sarcolemma, to determine stiffness of the half-sarcomere in the two conditions. To identify the contribution of actin filaments to the total half-sarcomere compliance (C), measurements were made at sarcomere lengths between 2.00 and 2.15 microm, where the number of myosin cross-bridges in the region of overlap between the myosin filament and the actin filament remains constant, and only the length of the nonoverlapped region of the actin filament changes with sarcomere length. At 2.1 microm sarcomere length, C was 3.9 nm T0(-1) in active isometric contraction and 2.6 nm T0(-1) in rigor. The actin filament compliance, estimated from the slope of the relation between C and sarcomere length, was 2.3 nm microm(-1) T0(-1). Recent x-ray diffraction experiments suggest that the myosin filament compliance is 1.3 nm microm(-1) T0(-1). With these values for filament compliance, the difference in half-sarcomere compliance between isometric contraction and rigor indicates that the fraction of myosin cross-bridges attached to actin in isometric contraction is not larger than 0.43, assuming that cross-bridge elasticity is the same in isometric contraction and rigor.

Full Text

The Full Text of this article is available as a PDF (156.5 KB).

Selected References

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

  1. Bagni M. A., Cecchi G., Colomo F., Poggesi C. Tension and stiffness of frog muscle fibres at full filament overlap. J Muscle Res Cell Motil. 1990 Oct;11(5):371–377. doi: 10.1007/BF01739758. [DOI] [PubMed] [Google Scholar]
  2. Bagni M. A., Cecchi G., Colomo F., Tesi C. Plateau and descending limb of the sarcomere length-tension relation in short length-clamped segments of frog muscle fibres. J Physiol. 1988 Jul;401:581–595. doi: 10.1113/jphysiol.1988.sp017181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bagni M. A., Cecchi G., Griffiths P. J., Maéda Y., Rapp G., Ashley C. C. Lattice spacing changes accompanying isometric tension development in intact single muscle fibers. Biophys J. 1994 Nov;67(5):1965–1975. doi: 10.1016/S0006-3495(94)80679-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bershitsky S. Y., Tsaturyan A. K. Force generation and work production by covalently cross-linked actin-myosin cross-bridges in rabbit muscle fibers. Biophys J. 1995 Sep;69(3):1011–1021. doi: 10.1016/S0006-3495(95)79976-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bordas J., Diakun G. P., Diaz F. G., Harries J. E., Lewis R. A., Lowy J., Mant G. R., Martin-Fernandez M. L., Towns-Andrews E. Two-dimensional time-resolved X-ray diffraction studies of live isometrically contracting frog sartorius muscle. J Muscle Res Cell Motil. 1993 Jun;14(3):311–324. doi: 10.1007/BF00123096. [DOI] [PubMed] [Google Scholar]
  6. Cecchi G., Colomo F., Lombardi V. A loudspeaker servo system for determination of mechanical characteristics of isolated muscle fibres. Boll Soc Ital Biol Sper. 1976 May 30;52(10):733–736. [PubMed] [Google Scholar]
  7. Cooke R., Crowder M. S., Thomas D. D. Orientation of spin labels attached to cross-bridges in contracting muscle fibres. Nature. 1982 Dec 23;300(5894):776–778. doi: 10.1038/300776a0. [DOI] [PubMed] [Google Scholar]
  8. Cooke R., Franks K. All myosin heads form bonds with actin in rigor rabbit skeletal muscle. Biochemistry. 1980 May 13;19(10):2265–2269. doi: 10.1021/bi00551a042. [DOI] [PubMed] [Google Scholar]
  9. Finer J. T., Simmons R. M., Spudich J. A. Single myosin molecule mechanics: piconewton forces and nanometre steps. Nature. 1994 Mar 10;368(6467):113–119. doi: 10.1038/368113a0. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Ford L. E., Huxley A. F., Simmons R. M. The relation between stiffness and filament overlap in stimulated frog muscle fibres. J Physiol. 1981 Feb;311:219–249. doi: 10.1113/jphysiol.1981.sp013582. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Goldman Y. E., Huxley A. F. Actin compliance: are you pulling my chain? Biophys J. 1994 Dec;67(6):2131–2133. doi: 10.1016/S0006-3495(94)80700-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Goldman Y. E., Simmons R. M. Active and rigor muscle stiffness [proceedings]. J Physiol. 1977 Jul;269(1):55P–57P. [PubMed] [Google Scholar]
  14. Goldman Y. E., Simmons R. M. The stiffness of frog skinned muscle fibres at altered lateral filament spacing. J Physiol. 1986 Sep;378:175–194. doi: 10.1113/jphysiol.1986.sp016213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gordon A. M., Huxley A. F., Julian F. J. The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J Physiol. 1966 May;184(1):170–192. doi: 10.1113/jphysiol.1966.sp007909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Haselgrove J. C., Huxley H. E. X-ray evidence for radial cross-bridge movement and for the sliding filament model in actively contracting skeletal muscle. J Mol Biol. 1973 Jul 15;77(4):549–568. doi: 10.1016/0022-2836(73)90222-2. [DOI] [PubMed] [Google Scholar]
  17. Haselgrove J. C. X-ray evidence for conformational changes in the myosin filaments of vertebrate striated muscle. J Mol Biol. 1975 Feb 15;92(1):113–143. doi: 10.1016/0022-2836(75)90094-7. [DOI] [PubMed] [Google Scholar]
  18. Higuchi H., Yanagida T., Goldman Y. E. Compliance of thin filaments in skinned fibers of rabbit skeletal muscle. Biophys J. 1995 Sep;69(3):1000–1010. doi: 10.1016/S0006-3495(95)79975-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. Huxley A. F., Tideswell S. Filament compliance and tension transients in muscle. J Muscle Res Cell Motil. 1996 Aug;17(4):507–511. doi: 10.1007/BF00123366. [DOI] [PubMed] [Google Scholar]
  21. Huxley A. F., Tideswell S. Rapid regeneration of power stroke in contracting muscle by attachment of second myosin head. J Muscle Res Cell Motil. 1997 Feb;18(1):111–114. doi: 10.1023/a:1018641218961. [DOI] [PubMed] [Google Scholar]
  22. Huxley H. E., Faruqi A. R., Kress M., Bordas J., Koch M. H. Time-resolved X-ray diffraction studies of the myosin layer-line reflections during muscle contraction. J Mol Biol. 1982 Jul 15;158(4):637–684. doi: 10.1016/0022-2836(82)90253-4. [DOI] [PubMed] [Google Scholar]
  23. Huxley H. E., Kress M. Crossbridge behaviour during muscle contraction. J Muscle Res Cell Motil. 1985 Apr;6(2):153–161. doi: 10.1007/BF00713057. [DOI] [PubMed] [Google Scholar]
  24. Huxley H. E., Stewart A., Sosa H., Irving T. X-ray diffraction measurements of the extensibility of actin and myosin filaments in contracting muscle. Biophys J. 1994 Dec;67(6):2411–2421. doi: 10.1016/S0006-3495(94)80728-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Irving M. Muscle. Give in the filaments. Nature. 1995 Mar 2;374(6517):14–15. doi: 10.1038/374014a0. [DOI] [PubMed] [Google Scholar]
  26. Ishijima A., Doi T., Sakurada K., Yanagida T. Sub-piconewton force fluctuations of actomyosin in vitro. Nature. 1991 Jul 25;352(6333):301–306. doi: 10.1038/352301a0. [DOI] [PubMed] [Google Scholar]
  27. Ishijima A., Harada Y., Kojima H., Funatsu T., Higuchi H., Yanagida T. Single-molecule analysis of the actomyosin motor using nano-manipulation. Biochem Biophys Res Commun. 1994 Mar 15;199(2):1057–1063. doi: 10.1006/bbrc.1994.1336. [DOI] [PubMed] [Google Scholar]
  28. Julian F. J., Morgan D. L. Tension, stiffness, unloaded shortening speed and potentiation of frog muscle fibres at sarcomere lengths below optimum. J Physiol. 1981;319:205–217. doi: 10.1113/jphysiol.1981.sp013902. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Kojima H., Ishijima A., Yanagida T. Direct measurement of stiffness of single actin filaments with and without tropomyosin by in vitro nanomanipulation. Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):12962–12966. doi: 10.1073/pnas.91.26.12962. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Linari M., Lombardi V., Piazzesi G. Cross-bridge kinetics studied with staircase shortening in single fibres from frog skeletal muscle. J Muscle Res Cell Motil. 1997 Feb;18(1):91–101. doi: 10.1023/a:1018637118052. [DOI] [PubMed] [Google Scholar]
  31. Linari M., Woledge R. C. Comparison of energy output during ramp and staircase shortening in frog muscle fibres. J Physiol. 1995 Sep 15;487(Pt 3):699–710. doi: 10.1113/jphysiol.1995.sp020911. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Lombardi V., Piazzesi G., Ferenczi M. A., Thirlwell H., Dobbie I., Irving M. Elastic distortion of myosin heads and repriming of the working stroke in muscle. Nature. 1995 Apr 6;374(6522):553–555. doi: 10.1038/374553a0. [DOI] [PubMed] [Google Scholar]
  33. Lombardi V., Piazzesi G., Linari M. Rapid regeneration of the actin-myosin power stroke in contracting muscle. Nature. 1992 Feb 13;355(6361):638–641. doi: 10.1038/355638a0. [DOI] [PubMed] [Google Scholar]
  34. Lombardi V., Piazzesi G. The contractile response during steady lengthening of stimulated frog muscle fibres. J Physiol. 1990 Dec;431:141–171. doi: 10.1113/jphysiol.1990.sp018324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Lovell S. J., Knight P. J., Harrington W. F. Fraction of myosin heads bound to thin filaments in rigor fibrils from insect flight and vertebrate muscles. Nature. 1981 Oct 22;293(5834):664–666. doi: 10.1038/293664a0. [DOI] [PubMed] [Google Scholar]
  36. Matsubara I., Elliott G. F. X-ray diffraction studies on skinned single fibres of frog skeletal muscle. J Mol Biol. 1972 Dec 30;72(3):657–669. doi: 10.1016/0022-2836(72)90183-0. [DOI] [PubMed] [Google Scholar]
  37. Mobley B. A., Eisenberg B. R. Sizes of components in frog skeletal muscle measured by methods of stereology. J Gen Physiol. 1975 Jul;66(1):31–45. doi: 10.1085/jgp.66.1.31. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Molloy J. E., Burns J. E., Kendrick-Jones J., Tregear R. T., White D. C. Movement and force produced by a single myosin head. Nature. 1995 Nov 9;378(6553):209–212. doi: 10.1038/378209a0. [DOI] [PubMed] [Google Scholar]
  39. Månsson A. Tension transients in skeletal muscle fibres of the frog at varied tonicity of the extracellular medium. J Muscle Res Cell Motil. 1993 Feb;14(1):15–25. doi: 10.1007/BF00132176. [DOI] [PubMed] [Google Scholar]
  40. Nishiye E., Somlyo A. V., Török K., Somlyo A. P. The effects of MgADP on cross-bridge kinetics: a laser flash photolysis study of guinea-pig smooth muscle. J Physiol. 1993 Jan;460:247–271. doi: 10.1113/jphysiol.1993.sp019470. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Ostap E. M., Barnett V. A., Thomas D. D. Resolution of three structural states of spin-labeled myosin in contracting muscle. Biophys J. 1995 Jul;69(1):177–188. doi: 10.1016/S0006-3495(95)79888-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Piazzesi G., Francini F., Linari M., Lombardi V. Tension transients during steady lengthening of tetanized muscle fibres of the frog. J Physiol. 1992 Jan;445:659–711. doi: 10.1113/jphysiol.1992.sp018945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Piazzesi G., Linari M., Lombardi V. The effect of hypertonicity on force generation in tetanized single fibres from frog skeletal muscle. J Physiol. 1994 May 1;476(3):531–546. doi: 10.1113/jphysiol.1994.sp020152. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Piazzesi G., Linari M., Reconditi M., Vanzi F., Lombardi V. Cross-bridge detachment and attachment following a step stretch imposed on active single frog muscle fibres. J Physiol. 1997 Jan 1;498(Pt 1):3–15. doi: 10.1113/jphysiol.1997.sp021837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Piazzesi G., Lombardi V. A cross-bridge model that is able to explain mechanical and energetic properties of shortening muscle. Biophys J. 1995 May;68(5):1966–1979. doi: 10.1016/S0006-3495(95)80374-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Piazzesi G., Lombardi V., Ferenczi M. A., Thirlwell H., Dobbie I., Irving M. Changes in the x-ray diffraction pattern from single, intact muscle fibers produced by rapid shortening and stretch. Biophys J. 1995 Apr;68(4 Suppl):92S–98S. [PMC free article] [PubMed] [Google Scholar]
  47. Reedy M. K., Holmes K. C., Tregear R. T. Induced changes in orientation of the cross-bridges of glycerinated insect flight muscle. Nature. 1965 Sep 18;207(5003):1276–1280. doi: 10.1038/2071276a0. [DOI] [PubMed] [Google Scholar]
  48. Thomas D. D., Cooke R. Orientation of spin-labeled myosin heads in glycerinated muscle fibers. Biophys J. 1980 Dec;32(3):891–906. doi: 10.1016/S0006-3495(80)85024-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Wakabayashi K., Sugimoto Y., Tanaka H., Ueno Y., Takezawa Y., Amemiya Y. X-ray diffraction evidence for the extensibility of actin and myosin filaments during muscle contraction. Biophys J. 1994 Dec;67(6):2422–2435. doi: 10.1016/S0006-3495(94)80729-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Yamamoto T., Herzig J. W. Series elastic properties of skinned muscle fibres in contraction and rigor. Pflugers Arch. 1978 Jan 31;373(1):21–24. doi: 10.1007/BF00581144. [DOI] [PubMed] [Google Scholar]

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

RESOURCES