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. 1996 Oct;71(4):1905–1913. doi: 10.1016/S0006-3495(96)79389-X

Endothermic force generation in fast and slow mammalian (rabbit) muscle fibers.

K W Ranatunga 1
PMCID: PMC1233657  PMID: 8889165

Abstract

Isometric tension responses to rapid temperature jumps (T-jumps) of 3-7 degrees C were examined in single skinned fibers isolated from rabbit psoas (fast) and soleus (slow) muscles. T-jumps were induced by an infrared laser pulse (wavelength 1.32 microns, pulse duration 0.2 ms) obtained from a Nd-YAG laser, which heated the fiber and bathing buffer solution in a 50-microliter trough. After a T-jump, the temperature near the fiber remained constant for approximately 0.5 s, and the temperature could be clamped for longer periods by means of Peltier units assembled on the back trough wall. A T-jump produced a step decrease in tension in both fast and slow muscle fibers in rigor, indicating thermal expansion. In maximally Ca-activated (pCa approximately 4) fibers, the increase of steady tension with heating (3-35 degrees C) was approximately sigmoidal, and a T-jump at any temperature induced a more complex tension transient than in rigor fibers. An initial (small amplitude) step decrease in tension followed by a rapid recovery (tau(1); see Davis and Harrington, 1993) was seen in some records from both fiber types, which presumably was an indirect consequence of thermal expansion. The net rise in tension after a T-jump was biexponential, and its time course was characteristically different in the two fibers. At approximately 12 degrees C the reciprocal time constants for the two exponential components (tau(2) and tau(3), respectively, were approximately 70.s(-1) and approximately 15.s(-1) in fast fibers and approximately 20.s(-1) and approximately 3.s(-1) in slow fibers. In both fibers, tau(2) ("endothermic force regeneration") became faster with an increase in temperature. Furthermore, tau(3) was temperature sensitive in slow fibers but not in fast fibers. The results are compared and contrasted with previous findings from T-jump experiments on fast fibers. It is observed that the fast/slow fiber difference in the rate of endothermic force generation (three- to fourfold) is considerably smaller than the reported differences in the "phosphate release steps" (> 30-fold).

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Selected References

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  1. Bershitsky SYu, Tsaturyan A. K. Effect of joule temperature jump on tension and stiffness of skinned rabbit muscle fibers. Biophys J. 1989 Nov;56(5):809–816. doi: 10.1016/S0006-3495(89)82727-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. Dantzig J. A., Goldman Y. E., Millar N. C., Lacktis J., Homsher E. Reversal of the cross-bridge force-generating transition by photogeneration of phosphate in rabbit psoas muscle fibres. J Physiol. 1992;451:247–278. doi: 10.1113/jphysiol.1992.sp019163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. 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]
  6. 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]
  7. Davis J. S., Rodgers M. E. Force generation and temperature-jump and length-jump tension transients in muscle fibers. Biophys J. 1995 May;68(5):2032–2040. doi: 10.1016/S0006-3495(95)80380-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Davis J. S., Rodgers M. E. Indirect coupling of phosphate release to de novo tension generation during muscle contraction. Proc Natl Acad Sci U S A. 1995 Nov 7;92(23):10482–10486. doi: 10.1073/pnas.92.23.10482. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Fortune N. S., Geeves M. A., Ranatunga K. W. Contractile activation and force generation in skinned rabbit muscle fibres: effects of hydrostatic pressure. J Physiol. 1994 Jan 15;474(2):283–290. doi: 10.1113/jphysiol.1994.sp020021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fortune N. S., Geeves M. A., Ranatunga K. W. Pressure sensitivity of active tension in glycerinated rabbit psoas muscle fibres: effects of ADP and phosphate. J Muscle Res Cell Motil. 1989 Apr;10(2):113–123. doi: 10.1007/BF01739967. [DOI] [PubMed] [Google Scholar]
  12. Fortune N. S., Geeves M. A., Ranatunga K. W. Tension responses to rapid pressure release in glycerinated rabbit muscle fibers. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7323–7327. doi: 10.1073/pnas.88.16.7323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Galler S., Hilber K., Pette D. Force responses following stepwise length changes of rat skeletal muscle fibre types. J Physiol. 1996 May 15;493(Pt 1):219–227. doi: 10.1113/jphysiol.1996.sp021377. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. HAJDU S. Behaviour of frog and rat muscle at higher temperatures. Enzymologia. 1950 Nov 15;14(4):187–193. [PubMed] [Google Scholar]
  16. 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]
  17. Irving M. Muscle. Give in the filaments. Nature. 1995 Mar 2;374(6517):14–15. doi: 10.1038/374014a0. [DOI] [PubMed] [Google Scholar]
  18. Irving M., St Claire Allen T., Sabido-David C., Craik J. S., Brandmeier B., Kendrick-Jones J., Corrie J. E., Trentham D. R., Goldman Y. E. Tilting of the light-chain region of myosin during step length changes and active force generation in skeletal muscle. Nature. 1995 Jun 22;375(6533):688–691. doi: 10.1038/375688a0. [DOI] [PubMed] [Google Scholar]
  19. Martyn D. A., Chase P. B. Faster force transient kinetics at submaximal Ca2+ activation of skinned psoas fibers from rabbit. Biophys J. 1995 Jan;68(1):235–242. doi: 10.1016/S0006-3495(95)80179-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Millar N. C., Homsher E. Kinetics of force generation and phosphate release in skinned rabbit soleus muscle fibers. Am J Physiol. 1992 May;262(5 Pt 1):C1239–C1245. doi: 10.1152/ajpcell.1992.262.5.C1239. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Ranatunga K. W. Temperature-dependence of shortening velocity and rate of isometric tension development in rat skeletal muscle. J Physiol. 1982 Aug;329:465–483. doi: 10.1113/jphysiol.1982.sp014314. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ranatunga K. W. The force-velocity relation of rat fast- and slow-twitch muscles examined at different temperatures. J Physiol. 1984 Jun;351:517–529. doi: 10.1113/jphysiol.1984.sp015260. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. 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]
  26. Stephenson D. G., Williams D. A. Temperature-dependent calcium sensitivity changes in skinned muscle fibres of rat and toad. J Physiol. 1985 Mar;360:1–12. doi: 10.1113/jphysiol.1985.sp015600. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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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