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. 2002 Feb;82(2):929–943. doi: 10.1016/S0006-3495(02)75454-4

History-dependent mechanical properties of permeabilized rat soleus muscle fibers.

Kenneth S Campbell 1, Richard L Moss 1
PMCID: PMC1301901  PMID: 11806934

Abstract

Permeabilized rat soleus muscle fibers were subjected to repeated triangular length changes (paired ramp stretches/releases, 0.03 l(0), +/- 0.1 l(0) s(-1) imposed under sarcomere length control) to investigate whether the rate of stiffness recovery after movement increased with the level of Ca(2+) activation. Actively contracting fibers exhibited a characteristic tension response to stretch: tension rose sharply during the initial phase of the movement before dropping slightly to a plateau, which was maintained during the remainder of the stretch. When the fibers were stretched twice, the initial phase of the response was reduced by an amount that depended on both the level of Ca(2+) activation and the elapsed time since the first movement. Detailed analysis revealed three new and important findings. 1) The rates of stiffness and tension recovery and 2) the relative height of the tension plateau each increased with the level of Ca(2+) activation. 3) The tension plateau developed more quickly during the second stretch at high free Ca(2+) concentrations than at low. These findings are consistent with a cross-bridge mechanism but suggest that the rate of the force-generating power-stroke increases with the intracellular Ca(2+) concentration and cross-bridge strain.

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Selected References

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  1. Bagni M. A., Cecchi G., Colomo F., Garzella P. Absence of mechanical evidence for attached weakly binding cross-bridges in frog relaxed muscle fibres. J Physiol. 1995 Jan 15;482(Pt 2):391–400. doi: 10.1113/jphysiol.1995.sp020526. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bagni M. A., Cecchi G., Colomo F., Garzella P. Development of stiffness precedes cross-bridge attachment during the early tension rise in single frog muscle fibres. J Physiol. 1994 Dec 1;481(Pt 2):273–278. doi: 10.1113/jphysiol.1994.sp020437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Boriek A. M., Capetanaki Y., Hwang W., Officer T., Badshah M., Rodarte J., Tidball J. G. Desmin integrates the three-dimensional mechanical properties of muscles. Am J Physiol Cell Physiol. 2001 Jan;280(1):C46–C52. doi: 10.1152/ajpcell.2001.280.1.C46. [DOI] [PubMed] [Google Scholar]
  4. Brenner B. Effect of Ca2+ on cross-bridge turnover kinetics in skinned single rabbit psoas fibers: implications for regulation of muscle contraction. Proc Natl Acad Sci U S A. 1988 May;85(9):3265–3269. doi: 10.1073/pnas.85.9.3265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Campbell K. S., Lakie M. A cross-bridge mechanism can explain the thixotropic short-range elastic component of relaxed frog skeletal muscle. J Physiol. 1998 Aug 1;510(Pt 3):941–962. doi: 10.1111/j.1469-7793.1998.941bj.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Campbell K. S., Moss R. L. A thixotropic effect in contracting rabbit psoas muscle: prior movement reduces the initial tension response to stretch. J Physiol. 2000 Jun 1;525(Pt 2):531–548. doi: 10.1111/j.1469-7793.2000.00531.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cecchi G. Do cross-bridges contribute to the tension during stretch of passive muscle? J Muscle Res Cell Motil. 2000 Jan;21(1):99–100. doi: 10.1023/a:1017282323680. [DOI] [PubMed] [Google Scholar]
  8. Edman K. A., Elzinga G., Noble M. I. Enhancement of mechanical performance by stretch during tetanic contractions of vertebrate skeletal muscle fibres. J Physiol. 1978 Aug;281:139–155. doi: 10.1113/jphysiol.1978.sp012413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Edman K. A. The force bearing capacity of frog muscle fibres during stretch: its relation to sarcomere length and fibre width. J Physiol. 1999 Sep 1;519(Pt 2):515–526. doi: 10.1111/j.1469-7793.1999.0515m.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fabiato A. Computer programs for calculating total from specified free or free from specified total ionic concentrations in aqueous solutions containing multiple metals and ligands. Methods Enzymol. 1988;157:378–417. doi: 10.1016/0076-6879(88)57093-3. [DOI] [PubMed] [Google Scholar]
  11. Fitzsimons D. P., Patel J. R., Campbell K. S., Moss R. L. Cooperative mechanisms in the activation dependence of the rate of force development in rabbit skinned skeletal muscle fibers. J Gen Physiol. 2001 Feb;117(2):133–148. doi: 10.1085/jgp.117.2.133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Flitney F. W., Hirst D. G. Cross-bridge detachment and sarcomere 'give' during stretch of active frog's muscle. J Physiol. 1978 Mar;276:449–465. doi: 10.1113/jphysiol.1978.sp012246. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Freiburg A., Trombitas K., Hell W., Cazorla O., Fougerousse F., Centner T., Kolmerer B., Witt C., Beckmann J. S., Gregorio C. C. Series of exon-skipping events in the elastic spring region of titin as the structural basis for myofibrillar elastic diversity. Circ Res. 2000 Jun 9;86(11):1114–1121. doi: 10.1161/01.res.86.11.1114. [DOI] [PubMed] [Google Scholar]
  14. Getz E. B., Cooke R., Lehman S. L. Phase transition in force during ramp stretches of skeletal muscle. Biophys J. 1998 Dec;75(6):2971–2983. doi: 10.1016/S0006-3495(98)77738-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Godt R. E., Lindley B. D. Influence of temperature upon contractile activation and isometric force production in mechanically skinned muscle fibers of the frog. J Gen Physiol. 1982 Aug;80(2):279–297. doi: 10.1085/jgp.80.2.279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gordon A. M., Homsher E., Regnier M. Regulation of contraction in striated muscle. Physiol Rev. 2000 Apr;80(2):853–924. doi: 10.1152/physrev.2000.80.2.853. [DOI] [PubMed] [Google Scholar]
  17. Herbst M. Studies on the relation between latency relaxation and resting cross-bridges of frog skeletal muscle. Pflugers Arch. 1976 Jun 29;364(1):71–76. doi: 10.1007/BF01062914. [DOI] [PubMed] [Google Scholar]
  18. Hill D. K. Tension due to interaction between the sliding filaments in resting striated muscle. The effect of stimulation. J Physiol. 1968 Dec;199(3):637–684. doi: 10.1113/jphysiol.1968.sp008672. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Homsher E., Lacktis J., Regnier M. Strain-dependent modulation of phosphate transients in rabbit skeletal muscle fibers. Biophys J. 1997 Apr;72(4):1780–1791. doi: 10.1016/S0006-3495(97)78824-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Homsher E., Millar N. Kinetics of force generation and Pi release in rabbit soleus muscle fibers. Adv Exp Med Biol. 1993;332:495–503. doi: 10.1007/978-1-4615-2872-2_45. [DOI] [PubMed] [Google Scholar]
  21. Horowits R. Passive force generation and titin isoforms in mammalian skeletal muscle. Biophys J. 1992 Feb;61(2):392–398. doi: 10.1016/S0006-3495(92)81845-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Julian F. J., Sollins K. R., Sollins M. R. A model for the transient and steady-state mechanical behavior of contracting muscle. Biophys J. 1974 Jul;14(7):546–562. doi: 10.1016/S0006-3495(74)85934-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kellermayer M. S., Smith S. B., Bustamante C., Granzier H. L. Mechanical fatigue in repetitively stretched single molecules of titin. Biophys J. 2001 Feb;80(2):852–863. doi: 10.1016/S0006-3495(01)76064-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lakie M., Robson L. G. Thixotropy in frog single muscle fibres. Exp Physiol. 1990 Jan;75(1):123–125. doi: 10.1113/expphysiol.1990.sp003380. [DOI] [PubMed] [Google Scholar]
  25. Lakie M., Robson L. G. Thixotropy: stiffness recovery rate in relaxed frog muscle. Q J Exp Physiol. 1988 Mar;73(2):237–239. doi: 10.1113/expphysiol.1988.sp003137. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Lännergren J. The effect of low-level activation on the mechanical properties of isolated frog muscle fibers. J Gen Physiol. 1971 Aug;58(2):145–162. doi: 10.1085/jgp.58.2.145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Metzger J. M., Moss R. L. Calcium-sensitive cross-bridge transitions in mammalian fast and slow skeletal muscle fibers. Science. 1990 Mar 2;247(4946):1088–1090. doi: 10.1126/science.2309121. [DOI] [PubMed] [Google Scholar]
  29. Millar N. C., Homsher E. The effect of phosphate and calcium on force generation in glycerinated rabbit skeletal muscle fibers. A steady-state and transient kinetic study. J Biol Chem. 1990 Nov 25;265(33):20234–20240. [PubMed] [Google Scholar]
  30. Minajeva A., Kulke M., Fernandez J. M., Linke W. A. Unfolding of titin domains explains the viscoelastic behavior of skeletal myofibrils. Biophys J. 2001 Mar;80(3):1442–1451. doi: 10.1016/S0006-3495(01)76116-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Morgan D. L. New insights into the behavior of muscle during active lengthening. Biophys J. 1990 Feb;57(2):209–221. doi: 10.1016/S0006-3495(90)82524-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Mutungi G., Ranatunga K. W. Do cross-bridges contribute to the tension during stretch of passive muscle? A response. J Muscle Res Cell Motil. 2000 Apr;21(3):301–302. doi: 10.1023/a:1005633931146. [DOI] [PubMed] [Google Scholar]
  33. Mutungi G., Ranatunga K. W. The viscous, viscoelastic and elastic characteristics of resting fast and slow mammalian (rat) muscle fibres. J Physiol. 1996 Nov 1;496(Pt 3):827–836. doi: 10.1113/jphysiol.1996.sp021730. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Proske U., Morgan D. L. Do cross-bridges contribute to the tension during stretch of passive muscle? J Muscle Res Cell Motil. 1999 Aug;20(5-6):433–442. doi: 10.1023/a:1005573625675. [DOI] [PubMed] [Google Scholar]
  35. Razumova M. V., Bukatina A. E., Campbell K. B. Different myofilament nearest-neighbor interactions have distinctive effects on contractile behavior. Biophys J. 2000 Jun;78(6):3120–3137. doi: 10.1016/S0006-3495(00)76849-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Slawnych M. P., Seow C. Y., Huxley A. F., Ford L. E. A program for developing a comprehensive mathematical description of the crossbridge cycle of muscle. Biophys J. 1994 Oct;67(4):1669–1677. doi: 10.1016/S0006-3495(94)80639-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Stienen G. J., Versteeg P. G., Papp Z., Elzinga G. Mechanical properties of skinned rabbit psoas and soleus muscle fibres during lengthening: effects of phosphate and Ca2+. J Physiol. 1992;451:503–523. doi: 10.1113/jphysiol.1992.sp019176. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Stuyvers B. D., Miura M., Jin J. P., ter Keurs H. E. Ca(2+)-dependence of diastolic properties of cardiac sarcomeres: involvement of titin. Prog Biophys Mol Biol. 1998;69(2-3):425–443. doi: 10.1016/s0079-6107(98)00018-2. [DOI] [PubMed] [Google Scholar]
  39. Tatsumi R., Shimada K., Hattori A. Fluorescence detection of calcium-binding proteins with quinoline Ca-indicator quin2. Anal Biochem. 1997 Dec 1;254(1):126–131. doi: 10.1006/abio.1997.2369. [DOI] [PubMed] [Google Scholar]
  40. Tesi C., Colomo F., Nencini S., Piroddi N., Poggesi C. The effect of inorganic phosphate on force generation in single myofibrils from rabbit skeletal muscle. Biophys J. 2000 Jun;78(6):3081–3092. doi: 10.1016/S0006-3495(00)76845-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Walker J. W., Lu Z., Moss R. L. Effects of Ca2+ on the kinetics of phosphate release in skeletal muscle. J Biol Chem. 1992 Feb 5;267(4):2459–2466. [PubMed] [Google Scholar]

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