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. 1996 Nov;71(5):2774–2785. doi: 10.1016/S0006-3495(96)79470-5

Mechanical characterization of skeletal muscle myofibrils.

A L Friedman 1, Y E Goldman 1
PMCID: PMC1233763  PMID: 8913614

Abstract

A new instrument, based on a technique described previously, is presented for studying mechanics of micron-scale preparations of two to three myofibrils or single myofibrils from muscle. Forces in the nanonewton to micronewton range are measurable with 0.5-ms time resolution. Programmed quick (200-microseconds) steps or ramp length changes are applied to contracting myofibrils to test their mechanical properties. Individual striations can be monitored during force production and shortening. The active isometric force, force-velocity relationship, and force transients after rapid length steps were obtained from bundles of two to three myofibrils from rabbit psoas muscle. Contrary to some earlier reports on myofibrillar mechanics, these properties are generally similar to expectations from studies on intact and skinned muscle fibers. Our experiments provide strong evidence that the mechanical properties of a fiber result from a simple summation of the myofibrillar force and shortening of independently contracting sarcomeres.

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Selected References

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

  1. Abbott R. H., Steiger G. J. Temperature and amplitude dependence of tension transients in glycerinated skeletal and insect fibrillar muscle. J Physiol. 1977 Mar;266(1):13–42. doi: 10.1113/jphysiol.1977.sp011754. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bartoo M. L., Popov V. I., Fearn L. A., Pollack G. H. Active tension generation in isolated skeletal myofibrils. J Muscle Res Cell Motil. 1993 Oct;14(5):498–510. doi: 10.1007/BF00297212. [DOI] [PubMed] [Google Scholar]
  3. Brenner B., Schoenberg M., Chalovich J. M., Greene L. E., Eisenberg E. Evidence for cross-bridge attachment in relaxed muscle at low ionic strength. Proc Natl Acad Sci U S A. 1982 Dec;79(23):7288–7291. doi: 10.1073/pnas.79.23.7288. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brenner B. The necessity of using two parameters to describe isotonic shortening velocity of muscle tissues: the effect of various interventions upon initial shortening velocity (vi) and curvature (b). Basic Res Cardiol. 1986 Jan-Feb;81(1):54–69. doi: 10.1007/BF01907427. [DOI] [PubMed] [Google Scholar]
  5. Cooke R., Bialek W. Contraction of glycerinated muscle fibers as a function of the ATP concentration. Biophys J. 1979 Nov;28(2):241–258. doi: 10.1016/S0006-3495(79)85174-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cooke R., Crowder M. S., Thomas D. D. Orientation of spin labels attached to cross-bridges in contracting muscle fibres. Nature. 1982 Dec 23;300(5894):776–778. doi: 10.1038/300776a0. [DOI] [PubMed] [Google Scholar]
  7. Cooke R., Franks K., Luciani G. B., Pate E. The inhibition of rabbit skeletal muscle contraction by hydrogen ions and phosphate. J Physiol. 1988 Jan;395:77–97. doi: 10.1113/jphysiol.1988.sp016909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cooke R. The mechanism of muscle contraction. CRC Crit Rev Biochem. 1986;21(1):53–118. doi: 10.3109/10409238609113609. [DOI] [PubMed] [Google Scholar]
  9. Crowder M. S., Cooke R. The effect of myosin sulphydryl modification on the mechanics of fibre contraction. J Muscle Res Cell Motil. 1984 Apr;5(2):131–146. doi: 10.1007/BF00712152. [DOI] [PubMed] [Google Scholar]
  10. Dantzig J. A., Goldman Y. E. Suppression of muscle contraction by vanadate. Mechanical and ligand binding studies on glycerol-extracted rabbit fibers. J Gen Physiol. 1985 Sep;86(3):305–327. doi: 10.1085/jgp.86.3.305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dantzig J. A., Hibberd M. G., Trentham D. R., Goldman Y. E. Cross-bridge kinetics in the presence of MgADP investigated by photolysis of caged ATP in rabbit psoas muscle fibres. J Physiol. 1991 Jan;432:639–680. doi: 10.1113/jphysiol.1991.sp018405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Eisenberg B. R., Kuda A. M. Discrimination between fiber populations in mammalian skeletal muscle by using ultrastructural parameters. J Ultrastruct Res. 1976 Jan;54(1):76–88. doi: 10.1016/s0022-5320(76)80010-x. [DOI] [PubMed] [Google Scholar]
  14. Ferenczi M. A., Goldman Y. E., Simmons R. M. The dependence of force and shortening velocity on substrate concentration in skinned muscle fibres from Rana temporaria. J Physiol. 1984 May;350:519–543. doi: 10.1113/jphysiol.1984.sp015216. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. 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]
  17. 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]
  18. Goldman Y. E., Hibberd M. G., Trentham D. R. Relaxation of rabbit psoas muscle fibres from rigor by photochemical generation of adenosine-5'-triphosphate. J Physiol. 1984 Sep;354:577–604. doi: 10.1113/jphysiol.1984.sp015394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Goldman Y. E. Kinetics of the actomyosin ATPase in muscle fibers. Annu Rev Physiol. 1987;49:637–654. doi: 10.1146/annurev.ph.49.030187.003225. [DOI] [PubMed] [Google Scholar]
  20. HILL A. V. The mechanics of active muscle. Proc R Soc Lond B Biol Sci. 1953 Mar 11;141(902):104–117. doi: 10.1098/rspb.1953.0027. [DOI] [PubMed] [Google Scholar]
  21. Harada Y., Sakurada K., Aoki T., Thomas D. D., Yanagida T. Mechanochemical coupling in actomyosin energy transduction studied by in vitro movement assay. J Mol Biol. 1990 Nov 5;216(1):49–68. doi: 10.1016/S0022-2836(05)80060-9. [DOI] [PubMed] [Google Scholar]
  22. Harrington W. F., Karr T., Busa W. B., Lovell S. J. Contraction of myofibrils in the presence of antibodies to myosin subfragment 2. Proc Natl Acad Sci U S A. 1990 Oct;87(19):7453–7456. doi: 10.1073/pnas.87.19.7453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Herrmann C., Lionne C., Travers F., Barman T. Correlation of ActoS1, myofibrillar, and muscle fiber ATPases. Biochemistry. 1994 Apr 12;33(14):4148–4154. doi: 10.1021/bi00180a007. [DOI] [PubMed] [Google Scholar]
  24. Hibberd M. G., Dantzig J. A., Trentham D. R., Goldman Y. E. Phosphate release and force generation in skeletal muscle fibers. Science. 1985 Jun 14;228(4705):1317–1319. doi: 10.1126/science.3159090. [DOI] [PubMed] [Google Scholar]
  25. Higuchi H., Goldman Y. E. Sliding distance between actin and myosin filaments per ATP molecule hydrolysed in skinned muscle fibres. Nature. 1991 Jul 25;352(6333):352–354. doi: 10.1038/352352a0. [DOI] [PubMed] [Google Scholar]
  26. Houadjeto M., Barman T., Travers F. What is the true ATPase activity of contracting myofibrils? FEBS Lett. 1991 Apr 9;281(1-2):105–107. doi: 10.1016/0014-5793(91)80369-e. [DOI] [PubMed] [Google Scholar]
  27. Huxley A. F. Muscular contraction. J Physiol. 1974 Nov;243(1):1–43. [PMC free article] [PubMed] [Google Scholar]
  28. 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]
  29. 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]
  30. 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]
  31. Ishijima A., Harada Y., Kojima H., Funatsu T., Higuchi H., Yanagida T. Single-molecule analysis of the actomyosin motor using nano-manipulation. Biochem Biophys Res Commun. 1994 Mar 15;199(2):1057–1063. doi: 10.1006/bbrc.1994.1336. [DOI] [PubMed] [Google Scholar]
  32. Iwazumi T. High-speed ultrasensitive instrumentation for myofibril mechanics measurements. Am J Physiol. 1987 Feb;252(2 Pt 1):C253–C262. doi: 10.1152/ajpcell.1987.252.2.C253. [DOI] [PubMed] [Google Scholar]
  33. Kawai M., Brandt P. W. Sinusoidal analysis: a high resolution method for correlating biochemical reactions with physiological processes in activated skeletal muscles of rabbit, frog and crayfish. J Muscle Res Cell Motil. 1980 Sep;1(3):279–303. doi: 10.1007/BF00711932. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Linke W. A., Popov V. I., Pollack G. H. Passive and active tension in single cardiac myofibrils. Biophys J. 1994 Aug;67(2):782–792. doi: 10.1016/S0006-3495(94)80538-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. 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]
  37. 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]
  38. Ma Y. Z., Taylor E. W. Kinetic mechanism of myofibril ATPase. Biophys J. 1994 May;66(5):1542–1553. doi: 10.1016/S0006-3495(94)80945-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Mobley B. A., Eisenberg B. R. Sizes of components in frog skeletal muscle measured by methods of stereology. J Gen Physiol. 1975 Jul;66(1):31–45. doi: 10.1085/jgp.66.1.31. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Moss R. L. The effect of calcium on the maximum velocity of shortening in skinned skeletal muscle fibres of the rabbit. J Muscle Res Cell Motil. 1982 Sep;3(3):295–311. doi: 10.1007/BF00713039. [DOI] [PubMed] [Google Scholar]
  41. Ohno T., Kodama T. Kinetics of adenosine triphosphate hydrolysis by shortening myofibrils from rabbit psoas muscle. J Physiol. 1991 Sep;441:685–702. doi: 10.1113/jphysiol.1991.sp018773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Pate E., Cooke R. Addition of phosphate to active muscle fibers probes actomyosin states within the powerstroke. Pflugers Arch. 1989 May;414(1):73–81. doi: 10.1007/BF00585629. [DOI] [PubMed] [Google Scholar]
  44. 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]
  45. 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]
  46. Reedy M. C., Reedy M. K., Tregear R. T. Two attached non-rigor crossbridge forms in insect flight muscle. J Mol Biol. 1988 Nov 20;204(2):357–383. doi: 10.1016/0022-2836(88)90582-7. [DOI] [PubMed] [Google Scholar]
  47. Reedy M. K., Holmes K. C., Tregear R. T. Induced changes in orientation of the cross-bridges of glycerinated insect flight muscle. Nature. 1965 Sep 18;207(5003):1276–1280. doi: 10.1038/2071276a0. [DOI] [PubMed] [Google Scholar]
  48. Reiser P. J., Moss R. L., Giulian G. G., Greaser M. L. Shortening velocity and myosin heavy chains of developing rabbit muscle fibers. J Biol Chem. 1985 Nov 25;260(27):14403–14405. [PubMed] [Google Scholar]
  49. Ruppersberg J. P., Rüdel R. A simple method for controlling the fluid level in a small experimental chamber during slow and rapid fluid exchange. Pflugers Arch. 1983 Apr;397(2):158–159. doi: 10.1007/BF00582056. [DOI] [PubMed] [Google Scholar]
  50. Stein L. A., Schwarz R. P., Jr, Chock P. B., Eisenberg E. Mechanism of actomyosin adenosine triphosphatase. Evidence that adenosine 5'-triphosphate hydrolysis can occur without dissociation of the actomyosin complex. Biochemistry. 1979 Sep 4;18(18):3895–3909. doi: 10.1021/bi00585a009. [DOI] [PubMed] [Google Scholar]
  51. Uyeda T. Q., Kron S. J., Spudich J. A. Myosin step size. Estimation from slow sliding movement of actin over low densities of heavy meromyosin. J Mol Biol. 1990 Aug 5;214(3):699–710. doi: 10.1016/0022-2836(90)90287-V. [DOI] [PubMed] [Google Scholar]
  52. Wang D., Pate E., Cooke R., Yount R. Synthesis of non-nucleotide ATP analogues and characterization of their chemomechanical interaction with muscle fibres. J Muscle Res Cell Motil. 1993 Oct;14(5):484–497. doi: 10.1007/BF00297211. [DOI] [PubMed] [Google Scholar]

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