Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1993 Jun 1;90(11):5148–5152. doi: 10.1073/pnas.90.11.5148

On the regeneration of the actin-myosin power stroke in contracting muscle.

Y D Chen 1, B Brenner 1
PMCID: PMC46672  PMID: 8506362

Abstract

The transient behavior of muscle in double-or multiple-step length perturbations [Lombardi, V., Piazzesi, G. & Linari, M. (1992) Nature (London) 355, 638-641] is simulated with a "conventional" cross-bridge model, which has been reported [Eisenberg, E., Hill, T. L. & Chen, Y. (1980) Biophys. J. 29, 195-227] to account for many mechanical, as well as biochemical, muscle data. The quick recovery of tension after double- or multiple-length perturbations was calculated for the model without any readjustment of its original parameters. The regeneration rate of the quick tension recovery of the model is fast and comparable to that measured experimentally by Lombardi et al. For multiple-step "stair-case"-type length releases, the tension response reaches a steady-state shape after three or four steps, and the average ATP turnover is much slower than the regeneration of the quick tension recovery. Our simulation shows that the experimental findings of Lombardi et al. can easily be reproduced by this simple conventional cross-bridge model, in which the completion of one work-producing power stroke is coupled to the hydrolysis of one ATP molecule. Thus, to account for the data of Lombardi et al., there is no need to assume that cross-bridges can execute multiple power strokes per ATPase cycle, although cross-bridges may well be able to do so. The mechanism that underlies the fast regeneration of the quick tension recovery in the conventional model used here is discussed.

Full text

PDF
5148

Selected References

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

  1. Brenner B. Mechanical and structural approaches to correlation of cross-bridge action in muscle with actomyosin ATPase in solution. Annu Rev Physiol. 1987;49:655–672. doi: 10.1146/annurev.ph.49.030187.003255. [DOI] [PubMed] [Google Scholar]
  2. Brenner B. Rapid dissociation and reassociation of actomyosin cross-bridges during force generation: a newly observed facet of cross-bridge action in muscle. Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10490–10494. doi: 10.1073/pnas.88.23.10490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brenner B. The cross-bridge cycle in muscle. Mechanical, biochemical, and structural studies on single skinned rabbit psoas fibers to characterize cross-bridge kinetics in muscle for correlation with the actomyosin-ATPase in solution. Basic Res Cardiol. 1986;81 (Suppl 1):1–15. doi: 10.1007/978-3-662-11374-5_1. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. 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]
  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. 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]
  8. HUXLEY A. F. Muscle structure and theories of contraction. Prog Biophys Biophys Chem. 1957;7:255–318. [PubMed] [Google Scholar]
  9. 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]
  10. 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]
  11. Huxley A. Muscle. A fine time for contractual alterations. Nature. 1992 May 14;357(6374):110–110. doi: 10.1038/357110a0. [DOI] [PubMed] [Google Scholar]
  12. Irving M., Lombardi V., Piazzesi G., Ferenczi M. A. Myosin head movements are synchronous with the elementary force-generating process in muscle. Nature. 1992 May 14;357(6374):156–158. doi: 10.1038/357156a0. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. 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]
  15. 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]
  16. 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]
  17. 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]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES