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. 1997 Feb;72(2 Pt 1):814–821. doi: 10.1016/s0006-3495(97)78715-0

Strain Dependence of the Elastic Properties of Force-Producing Cross-Bridges in Rigor Skeletal Muscle

Uulke A van der Heide *,#, Martijn Ketelaars *,#, Ben W Treijtel *, Evert L de Beer #, Tugendhold Blangé *
PMCID: PMC1185604  PMID: 9017206

Abstract

Stretch and release experiments carried out on skinned single fibers of frog skeletal muscle under rigor conditions indicate that the elastic properties of the fiber depend on strain. For modulation frequencies below 1000 Hz, the results show an increase in Young's modulus of 20% upon a stretch of 1 nm/half-sarcomere. Remarkably, the strain dependence of Young's modulus decreases at higher frequencies to about 10% upon a 1-nm/half-sarcomere stretch at a modulation frequency of 10 kHz. This suggests that the cause of the effect is less straightforward than originally believed: a simple slackening of the filaments would result in an equally large strain dependence at all frequencies, whereas strain-dependent properties of the actin filaments should show up most clearly at higher frequencies. We believe that the reduction of the strain dependence points to transitions of the cross-bridges between distinct force-producing states. This is consistent with the earlier observation that Young's modulus in rigor increases toward higher frequencies

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Selected References

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

  1. Blangé T., Stienen G. J. Transmission phenomena and early tension recovery in skinned muscle fibres of the frog. Pflugers Arch. 1985 Sep;405(1):12–18. doi: 10.1007/BF00591091. [DOI] [PubMed] [Google Scholar]
  2. De Winkel M. E., Blangé T., Treijtel B. W. High frequency characteristics of elasticity of skeletal muscle fibres kept in relaxed and rigor state. J Muscle Res Cell Motil. 1994 Apr;15(2):130–144. doi: 10.1007/BF00130424. [DOI] [PubMed] [Google Scholar]
  3. De Winkel M. E., Blangé T., Treijtel B. W. The complex Young's modulus of skeletal muscle fibre segments in the high frequency range determined from tension transients. J Muscle Res Cell Motil. 1993 Jun;14(3):302–310. doi: 10.1007/BF00123095. [DOI] [PubMed] [Google Scholar]
  4. Fabiato A., Fabiato F. Calculator programs for computing the composition of the solutions containing multiple metals and ligands used for experiments in skinned muscle cells. J Physiol (Paris) 1979;75(5):463–505. [PubMed] [Google Scholar]
  5. 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]
  6. HUXLEY A. F. Muscle structure and theories of contraction. Prog Biophys Biophys Chem. 1957;7:255–318. [PubMed] [Google Scholar]
  7. 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]
  8. 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]
  9. Jung D. W., Blangé T., de Graaf H., Treijtel B. W. Elastic properties of relaxed, activated, and rigor muscle fibers measured with microsecond resolution. Biophys J. 1988 Nov;54(5):897–908. doi: 10.1016/S0006-3495(88)83026-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. 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]
  12. Kushmerick M. J., Davies R. E. The chemical energetics of muscle contraction. II. The chemistry, efficiency and power of maximally working sartorius muscles. Appendix. Free energy and enthalpy of atp hydrolysis in the sarcoplasm. Proc R Soc Lond B Biol Sci. 1969 Dec 23;174(1036):315–353. doi: 10.1098/rspb.1969.0096. [DOI] [PubMed] [Google Scholar]
  13. Lymn R. W., Taylor E. W. Mechanism of adenosine triphosphate hydrolysis by actomyosin. Biochemistry. 1971 Dec 7;10(25):4617–4624. doi: 10.1021/bi00801a004. [DOI] [PubMed] [Google Scholar]
  14. Pate E., Cooke R. A model of crossbridge action: the effects of ATP, ADP and Pi. J Muscle Res Cell Motil. 1989 Jun;10(3):181–196. doi: 10.1007/BF01739809. [DOI] [PubMed] [Google Scholar]
  15. Smith D. A., Geeves M. A. Strain-dependent cross-bridge cycle for muscle. Biophys J. 1995 Aug;69(2):524–537. doi: 10.1016/S0006-3495(95)79926-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Stienen G. J., Blangé T. Tension responses to rapid length changes in skinned muscle fibres of the frog. Pflugers Arch. 1985 Sep;405(1):5–11. doi: 10.1007/BF00591090. [DOI] [PubMed] [Google Scholar]
  17. Stienen G. J., Güth K., Rüegg J. C. Force and force transients in skeletal muscle fibres of the frog skinned by freeze-drying. Pflugers Arch. 1983 Jun 1;397(4):272–276. doi: 10.1007/BF00580260. [DOI] [PubMed] [Google Scholar]
  18. Tozeren A. The influence of doubly attached crossbridges on the mechanical behavior of skeletal muscle fibers under equilibrium conditions. Biophys J. 1987 Nov;52(5):901–906. doi: 10.1016/S0006-3495(87)83284-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Tözeren A., Schoenberg M. The effect of cross-bridge clustering and head-head competition on the mechanical response of skeletal muscle under equilibrium conditions. Biophys J. 1986 Nov;50(5):875–884. doi: 10.1016/S0006-3495(86)83528-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. van den Hooff H., Blangé T., van der Tweel L. H. A displacement servosystem for muscle research permitting 50 micrometers length changes within 40 microseconds. Pflugers Arch. 1982 Nov 1;395(2):152–155. doi: 10.1007/BF00584729. [DOI] [PubMed] [Google Scholar]

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