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. 1996 Sep;71(3):1475–1484. doi: 10.1016/S0006-3495(96)79348-7

On the theory of muscle contraction: filament extensibility and the development of isometric force and stiffness.

S M Mijailovich 1, J J Fredberg 1, J P Butler 1
PMCID: PMC1233614  PMID: 8874021

Abstract

The newly discovered extensibility of actin and myosin filaments challenges the foundation of the theory of muscle mechanics. We have reformulated A. F. Huxley's sliding filament theory to explicitly take into account filament extensibility. During isometric force development, growing cross-bridge tractions transfer loads locally between filaments, causing them to extend and, therefore, to slide locally relative to one another. Even slight filament extensibility implies that 1) relative displacement between the two must be nonuniform along the region of filament overlap, 2) cross-bridge strain must vary systematically along the overlap region, and importantly, 3) the local shortening velocities, even at constant overall sarcomere length, reduce force below the level that would have developed if the filaments had been inextensible. The analysis shows that an extensible filament system with only two states (attached and detached) displays three important characteristics: 1) muscle stiffness leads force during force development; 2) cross-bridge stiffness is significantly higher than previously assessed by inextensible filament models; and 3) stiffness is prominently dissociated from the number of attached cross-bridges during force development. The analysis also implies that the local behavior of one myosin head must depend on the state of neighboring attachment sites. This coupling occurs exclusively through local sliding velocities, which can be significant, even during isometric force development. The resulting mechanical cooperativity is grounded in fiber mechanics and follows inevitably from filament extensibility.

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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., Schoenberg M. A model of force production that explains the lag between crossbridge attachment and force after electrical stimulation of striated muscle fibers. Biophys J. 1988 Dec;54(6):1105–1114. doi: 10.1016/S0006-3495(88)83046-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Eisenberg E., Hill T. L., Chen Y. Cross-bridge model of muscle contraction. Quantitative analysis. Biophys J. 1980 Feb;29(2):195–227. doi: 10.1016/S0006-3495(80)85126-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Eisenberg E., Hill T. L. Muscle contraction and free energy transduction in biological systems. Science. 1985 Mar 1;227(4690):999–1006. doi: 10.1126/science.3156404. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. 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]
  7. 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]
  8. 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]
  9. HUXLEY A. F. Muscle structure and theories of contraction. Prog Biophys Biophys Chem. 1957;7:255–318. [PubMed] [Google Scholar]
  10. Huxley A. F. A note suggesting that the cross-bridge attachment during muscle contraction may take place in two stages. Proc R Soc Lond B Biol Sci. 1973 Feb 27;183(1070):83–86. doi: 10.1098/rspb.1973.0006. [DOI] [PubMed] [Google Scholar]
  11. Huxley A. F. Muscular contraction. J Physiol. 1974 Nov;243(1):1–43. [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. 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]
  14. Huxley H. E. The mechanism of muscular contraction. Science. 1969 Jun 20;164(3886):1356–1365. doi: 10.1126/science.164.3886.1356. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. 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]
  17. 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]
  18. Mijailovich S. M., Stamenović D., Brown R., Leith D. E., Fredberg J. J. Dynamic moduli of rabbit lung tissue and pigeon ligamentum propatagiale undergoing uniaxial cyclic loading. J Appl Physiol (1985) 1994 Feb;76(2):773–782. doi: 10.1152/jappl.1994.76.2.773. [DOI] [PubMed] [Google Scholar]
  19. Mijailovich S. M., Stamenović D., Fredberg J. J. Toward a kinetic theory of connective tissue micromechanics. J Appl Physiol (1985) 1993 Feb;74(2):665–681. doi: 10.1152/jappl.1993.74.2.665. [DOI] [PubMed] [Google Scholar]
  20. Thorson J., White D. C. Distributed representations for actin-myosin interaction in the oscillatory contraction of muscle. Biophys J. 1969 Mar;9(3):360–390. doi: 10.1016/S0006-3495(69)86392-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]

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