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. 1995 May;68(5):2032–2040. doi: 10.1016/S0006-3495(95)80380-2

Force generation and temperature-jump and length-jump tension transients in muscle fibers.

J S Davis 1, M E Rodgers 1
PMCID: PMC1282106  PMID: 7612845

Abstract

Muscle tension rises with increasing temperature. The kinetics that govern the tension rise of maximally Ca(2+)-activated, skinned rabbit psoas fibers over a temperature range of 0-30 degrees C was characterized in laser temperature-jump experiments. The kinetic response is simple and can be readily interpreted in terms of a basic three-step mechanism of contraction, which includes a temperature-sensitive rapid preequilibrium(a) linked to a temperature-insensitive rate-limiting step and followed by a temperature-sensitive tension-generating step. These data and mechanism are compared and contrasted with the more complex length-jump Huxley-Simmons phases in which all states that generate tension or bear tension are perturbed. The rate of the Huxley-Simmons phase 4 is temperature sensitive at low temperatures but plateaus at high temperatures, indicating a change in rate-limiting step from a temperature-sensitive (phase 4a) to a temperature-insensitive reaction (phase 4b); the latter appears to correlate with the slow, temperature-insensitive temperature-jump relaxation. Phase 3 is absent in the temperature-jump, which excludes it from tension generation. We confirm that de novo tension generation occurs as an order-disorder transition during phase 2slow and the equivalent, temperature-sensitive temperature-jump relaxation.

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Selected References

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

  1. Bershitsky S. Y., Tsaturyan A. K. Tension responses to joule temperature jump in skinned rabbit muscle fibres. J Physiol. 1992 Feb;447:425–448. doi: 10.1113/jphysiol.1992.sp019010. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Brenner B., Eisenberg E. Rate of force generation in muscle: correlation with actomyosin ATPase activity in solution. Proc Natl Acad Sci U S A. 1986 May;83(10):3542–3546. doi: 10.1073/pnas.83.10.3542. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brenner B. Technique for stabilizing the striation pattern in maximally calcium-activated skinned rabbit psoas fibers. Biophys J. 1983 Jan;41(1):99–102. doi: 10.1016/S0006-3495(83)84411-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chase P. B., Kushmerick M. J. Effects of pH on contraction of rabbit fast and slow skeletal muscle fibers. Biophys J. 1988 Jun;53(6):935–946. doi: 10.1016/S0006-3495(88)83174-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Davis J. S., Harrington W. F. A single order-disorder transition generates tension during the Huxley-Simmons phase 2 in muscle. Biophys J. 1993 Nov;65(5):1886–1898. doi: 10.1016/S0006-3495(93)81259-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Davis J. S., Harrington W. F. Force generation by muscle fibers in rigor: a laser temperature-jump study. Proc Natl Acad Sci U S A. 1987 Feb;84(4):975–979. doi: 10.1073/pnas.84.4.975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Davis J. S., Harrington W. F. Kinetic and physical characterization of force generation in muscle: a laser temperature-jump and length-jump study on activated and contracting rigor fibers. Adv Exp Med Biol. 1993;332:513–526. doi: 10.1007/978-1-4615-2872-2_47. [DOI] [PubMed] [Google Scholar]
  8. Davis J. S., Harrington W. F. Laser temperature-jump apparatus for the study of force changes in fibers. Anal Biochem. 1987 Mar;161(2):543–549. doi: 10.1016/0003-2697(87)90487-8. [DOI] [PubMed] [Google Scholar]
  9. Ferenczi M. A. Phosphate burst in permeable muscle fibers of the rabbit. Biophys J. 1986 Sep;50(3):471–477. doi: 10.1016/S0006-3495(86)83484-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ferenczi M. A., Simmons R. M., Sleep J. A. General considerations of cross-bridge models in relation to the dependence on MgATP concentration of mechanical parameters of skinned fibers from frog muscles. Soc Gen Physiol Ser. 1982;37:91–107. [PubMed] [Google Scholar]
  11. Ford L. E., Huxley A. F., Simmons R. M. Proceedings: Mechanism of early tension recovery after a quick release in tetanized muscle fibres. J Physiol. 1974 Jul;240(2):42P–43P. [PubMed] [Google Scholar]
  12. 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]
  13. Ford L. E., Huxley A. F., Simmons R. M. Tension transients during steady shortening of frog muscle fibres. J Physiol. 1985 Apr;361:131–150. doi: 10.1113/jphysiol.1985.sp015637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gilbert S. H., Ford L. E. Heat changes during transient tension responses to small releases in active frog muscle. Biophys J. 1988 Oct;54(4):611–617. doi: 10.1016/S0006-3495(88)82996-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Goldman Y. E., McCray J. A., Ranatunga K. W. Transient tension changes initiated by laser temperature jumps in rabbit psoas muscle fibres. J Physiol. 1987 Nov;392:71–95. doi: 10.1113/jphysiol.1987.sp016770. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Goldman Y. E., Simmons R. M. Control of sarcomere length in skinned muscle fibres of Rana temporaria during mechanical transients. J Physiol. 1984 May;350:497–518. doi: 10.1113/jphysiol.1984.sp015215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. 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]
  20. Kawai M., Zhao Y. Cross-bridge scheme and force per cross-bridge state in skinned rabbit psoas muscle fibers. Biophys J. 1993 Aug;65(2):638–651. doi: 10.1016/S0006-3495(93)81109-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lu Z., Moss R. L., Walker J. W. Tension transients initiated by photogeneration of MgADP in skinned skeletal muscle fibers. J Gen Physiol. 1993 Jun;101(6):867–888. doi: 10.1085/jgp.101.6.867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Pate E., Wilson G. J., Bhimani M., Cooke R. Temperature dependence of the inhibitory effects of orthovanadate on shortening velocity in fast skeletal muscle. Biophys J. 1994 May;66(5):1554–1562. doi: 10.1016/S0006-3495(94)80947-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ranatunga K. W. Thermal stress and Ca-independent contractile activation in mammalian skeletal muscle fibers at high temperatures. Biophys J. 1994 May;66(5):1531–1541. doi: 10.1016/S0006-3495(94)80944-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Ranatunga K. W., Wylie S. R. Temperature-dependent transitions in isometric contractions of rat muscle. J Physiol. 1983 Jun;339:87–95. doi: 10.1113/jphysiol.1983.sp014704. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sweeney H. L., Corteselli S. A., Kushmerick M. J. Measurements on permeabilized skeletal muscle fibers during continuous activation. Am J Physiol. 1987 May;252(5 Pt 1):C575–C580. doi: 10.1152/ajpcell.1987.252.5.C575. [DOI] [PubMed] [Google Scholar]
  26. Zhao Y., Kawai M. Kinetic and thermodynamic studies of the cross-bridge cycle in rabbit psoas muscle fibers. Biophys J. 1994 Oct;67(4):1655–1668. doi: 10.1016/S0006-3495(94)80638-1. [DOI] [PMC free article] [PubMed] [Google Scholar]

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