Skip to main content
Log in

Sarcomere dynamics during muscular contraction and their implications to muscle function

  • Review Paper
  • Published:
Journal of Muscle Research and Cell Motility Aims and scope Submit manuscript

Abstract

This article attempts to identify the key aspects of sarcomere inhomogeneity and the dynamics of sarcomere length changes in muscle contraction experiments and focuses on understanding the mechanics of myofibrils or muscle fibres when viewed as independent units of biological motors (the half-sarcomeres) connected in series. Muscle force generation has been interpreted traditionally on the basis of the kinetics of crossbridge cycling, i.e. binding of myosin heads to actin and consecutive force generating conformational change of the head, under controlled conditions and assuming uniformity of sarcomere or half-sarcomere behaviour. However, several studies have shown that re-distribution of internal strain within myofibrils and muscle fibres may be a key player, particularly, during stretch or relaxation so that force kinetics parameters are strongly affected by sarcomere dynamics. Here, we aim to shed light on how force generation, crossbridge kinetics, and the complex sarcomere movements are to be linked and which mechanical concepts are necessary to develop a comprehensive contraction model of a myofibril.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Agarkova I, Auerbach D, Ehler E, Perriard JC (2000) A novel marker for vertebrate embryonic heart, the EH-myomesin isoform. J Biol Chem 275:10256–10264

    Article  PubMed  CAS  Google Scholar 

  • Agarkova I, Perriard JC (2005) The M-band: an elastic web that crosslinks thick filaments in the center of the sarcomere. Trends Cell Biol 15:477–485

    Article  PubMed  CAS  Google Scholar 

  • Anazawa T, Yasuda K, Ishiwata S (1992) Spontaneous oscillation of tension and sarcomere length in skeletal myofibrils. Microscopic measurement and analysis. Biophys J 61:1099–1108

    PubMed  CAS  Google Scholar 

  • Bagni MA, Cecchi G, Colombini B (2005) Crossbridge properties investigated by fast ramp stretching of activated frog muscle fibres. J Physiol 565:261–268

    Article  PubMed  CAS  Google Scholar 

  • Bagni MA, Cecchi G, Colomo F, Tesi C (1988) Plateau and descending limb of the sarcomere length-tension relation in short length-clamped segments of frog muscle fibres. J Physiol 401:581–595

    PubMed  CAS  Google Scholar 

  • Bagni MA, Colombini B, Geiger P, Berlinguer Palmini R, Cecchi G (2004) A non cross-bridge calcium-dependent stiffness in frog muscle fibers. Am J Physiol Cell Physiol 286:C1353–C1357

    Article  PubMed  CAS  Google Scholar 

  • Bartoo ML, Popov VI, Fearn LA, Pollack GH (1993) Active tension generation in isolated skeletal myofibrils. J Muscle Res Cell Motil 14:498–510

    Article  PubMed  CAS  Google Scholar 

  • Brenner B, Eisenberg E (1986) Rate of force generation in muscle: correlation with actomyosin ATPase activity in solution. Proc Natl Acad Sci USA 83:3542–3546

    Article  PubMed  CAS  Google Scholar 

  • Cecchi G, Griffiths PJ, Bagni MA, Ashley CC, Maeda Y (1991) Time-resolved changes in equatorial x-ray diffraction and stiffness during rise of tetanic tension in intact length-clamped single muscle fibers. Biophys J 59:1273–1283

    PubMed  CAS  Google Scholar 

  • Cheung A, Dantzig JA, Hollingworth S, Baylor SM, Goldman YE, Mitchison TJ, Straight AF (2002) A small-molecule inhibitor of skeletal muscle myosin II. Nat Cell Biol 4:83–88

    Article  PubMed  CAS  Google Scholar 

  • Colomo F, Piroddi N, Poggesi C, te Kronnie G, Tesi C (1997) Active and passive forces of isolated myofibrils from cardiac and fast skeletal muscle of the frog. J Physiol 500:535–548

    PubMed  CAS  Google Scholar 

  • Cooke R (1997) Actomyosin interaction in striated muscle. Physiol Rev 77:671–697

    PubMed  CAS  Google Scholar 

  • Coupland ME, Ranatunga KW (2003) Force generation induced by rapid temperature jumps in intact mammalian (rat) skeletal muscle fibres. J Physiol 548:439–449

    Article  PubMed  CAS  Google Scholar 

  • Danuser G (1997) Quantitative stereo vision for the stereo light microscope. Dissertation, ETH Zurich

  • Decostre V, Bianco P, Lombardi V, Piazzesi G (2005) Effect of temperature on the working stroke of muscle myosin. Proc Natl Acad Sci USA 102:13927–13932

    Article  PubMed  CAS  Google Scholar 

  • Denoth J, Stussi E, Csucs G, Danuser G (2002) Single muscle fiber contraction is dictated by inter-sarcomere dynamics. J Theor Biol 216:101–122

    Article  PubMed  Google Scholar 

  • Edman KA, Caputo C, Lou F (1993) Depression of tetanic force induced by loaded shortening of frog muscle fibres. J Physiol 466:535–552

    PubMed  CAS  Google Scholar 

  • Edman KA, Elzinga G, Noble MI (1982) Residual force enhancement after stretch of contracting frog single muscle fibers. J Gen Physiol 80:769–784

    Article  PubMed  CAS  Google Scholar 

  • Edman KA, Flitney FW (1982) Laser diffraction studies of sarcomere dynamics during ‘isometric’ relaxation in isolated muscle fibres of the frog. J Physiol 329:1–20

    PubMed  CAS  Google Scholar 

  • Edman KA, Reggiani C (1984a) Length-tension-velocity relationships studied in short consecutive segments of intact muscle fibres of the frog. Adv Exp Med Biol 170:495–509

    PubMed  CAS  Google Scholar 

  • Edman KA, Reggiani C (1984b) Redistribution of sarcomere length during isometric contraction of frog muscle fibres and its relation to tension creep. J Physiol 351:169–198

    PubMed  CAS  Google Scholar 

  • Edman KA, Reggiani C (1987) The sarcomere length-tension relation determined in short segments of intact muscle fibres of the frog. J Physiol 385:709–732

    PubMed  CAS  Google Scholar 

  • Friedman AL, Goldman YE (1996) Mechanical characterization of skeletal muscle myofibrils. Biophys J 71:2774–2785

    Article  PubMed  CAS  Google Scholar 

  • Galler S, Hopflinger MC, Andruchov O, Andruchova O, Grassberger H (2005) Effects of vanadate, phosphate and 2,3-butanedione monoxime (BDM) on skinned molluscan catch muscle. Pflugers Arch 449(4):372–383

    Google Scholar 

  • Goldspink G (2005) Mechanical signals, IGF-I gene splicing, and muscle adaptation. Physiology 20:232–238

    Article  PubMed  CAS  Google Scholar 

  • Gordon AM, Homsher E, Regnier M (2000) Regulation of contraction in striated muscle. Physiol Rev 80:853–924

    PubMed  CAS  Google Scholar 

  • Gordon AM, Huxley AF, Julian FJ (1966) The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J Physiol 184:170–192

    PubMed  CAS  Google Scholar 

  • Granzier H, Kellermayer M, Helmes M, Trombitas K (1997) Titin elasticity and mechanism of passive force development in rat cardiac myocytes probed by thin-filament extraction. Biophys J 73:2043–2053

    PubMed  CAS  Google Scholar 

  • Grove BK, Kurer V, Lehner C, Doetschman TC, Perriard JC, Eppenberger HM (1984) A new 185,000-dalton skeletal muscle protein detected by monoclonal antibodies. J Cell Biol 98:518–524

    Article  PubMed  CAS  Google Scholar 

  • Guo B, Guilford WH (2006) Mechanics of actomyosin bonds in different nucleotide states are tuned to muscle contraction. Proc Natl Acad Sci USA 103:9844–9849

    Article  PubMed  CAS  Google Scholar 

  • Herzog W (2005) Force enhancement following stretch of activated muscle: critical review and proposal for mechanisms. Med Biol Eng Comput 43:173–180

    Article  PubMed  CAS  Google Scholar 

  • Hilber K, Galler S (1998) Improvement of the measurements on skinned muscle fibres by fixation of the fibre ends with glutaraldehyde. J Muscle Res Cell Motil 19:365–372

    Article  PubMed  CAS  Google Scholar 

  • Hill AV (1953) The mechanics of active muscle. Proc R Soc London, B 141:104–117

    Article  CAS  Google Scholar 

  • Hill AV (1970) First and last experiments in muscle mechanics. Cambridge University Press, London

    Google Scholar 

  • Hill M, Wernig A, Goldspink G (2003) Muscle satellite (stem) cell activation during local tissue injury and repair. J Anat 203:89–99

    Article  PubMed  CAS  Google Scholar 

  • Horowits R, Podolsky RJ (1987) The positional stability of thick filaments in activated skeletal muscle depends on sarcomere length: evidence for the role of titin filaments. J Cell Biol 105:2217–2223

    Article  PubMed  CAS  Google Scholar 

  • Huxley AF (1957) Muscle structure and theories of contraction. Prog Biophys Mol Biol 7:255–318

    CAS  Google Scholar 

  • Huxley AF, Lombardi V, Peachey LD (1981) A system for fast recording of longitudinal displacement of a striated muscle fiber. J Physiol 317:12–13P

    Google Scholar 

  • Huxley AF, Simmons RM (1971) Proposed mechanism of force generation in striated muscle. Nature 233:533–538

    Article  PubMed  CAS  Google Scholar 

  • Huxley AF, Simmons RM (1973) Mechanical transients and origin of muscular force. Cold Spring Harb Symp Quant Biol 37:669–680

    CAS  Google Scholar 

  • Huxley AF, Tideswell S (1996) Filament compliance and tension transients in muscle. J Muscle Res Cell Motil 17:507–511

    Article  PubMed  CAS  Google Scholar 

  • Iwazumi T (1987) High-speed ultrasensitive instrumentation for myofibril mechanics measurements. Am J Physiol 252:C253–C262

    PubMed  CAS  Google Scholar 

  • Julian FJ (1969) Activation in a skeletal muscle contraction model with a modification for insect fibrillar muscle. Biophys J 9:547–570

    PubMed  CAS  Google Scholar 

  • Julian FJ, Morgan DL (1979) Intersarcomere dynamics during fixed-end tetanic contractions of frog muscle fibres. J Physiol 293:365–378

    PubMed  CAS  Google Scholar 

  • Kawai M, Brandt PW (1980) 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 1:279–303

    Article  PubMed  CAS  Google Scholar 

  • Kellermayer MS, Granzier HL (1996) Calcium-dependent inhibition of in vitro thin-filament motility by native titin. FEBS Lett 380:281–286

    Article  PubMed  CAS  Google Scholar 

  • Kulke M, Fujita-Becker S, Rostkova E, Neagoe C, Labeit D, Manstein DJ, Gautel M, Linke WA (2001) Interaction between PEVK-titin and actin filaments: origin of a viscous force component in cardiac myofibrils. Circ Res 89:874–881

    PubMed  CAS  Google Scholar 

  • Labeit D, Watanabe K, Witt C, Fujita H, Wu Y, Lahmers S, Funck T, Labeit S, Granzier H (2003) Calcium-dependent molecular spring elements in the giant protein titin. Proc Natl Acad Sci USA 100:13716–13721

    Article  PubMed  CAS  Google Scholar 

  • Linari M, Dobbie I, Reconditi M, Koubassova N, Irving M, Piazzesi G, Lombardi V (1998) The stiffness of skeletal muscle in isometric contraction and rigor: the fraction of myosin heads bound to actin. Biophys J 74:2459–2473

    PubMed  CAS  Google Scholar 

  • Linke WA, Ivemeyer M, Labeit S, Hinssen H, Ruegg JC, Gautel M (1997) Actin-titin interaction in cardiac myofibrils: probing a physiological role. Biophys J 73:905–919

    PubMed  CAS  Google Scholar 

  • Linke WA, Popov VI, Pollack GH (1994) Passive and active tension in single cardiac myofibrils. Biophys J 67:782–792

    PubMed  CAS  Google Scholar 

  • Lionne C, Iorga B, Candau R, Travers F (2003) Why choose myofibrils to study muscle myosin ATPase? J Muscle Res Cell Motil 24:139–148

    Article  PubMed  CAS  Google Scholar 

  • Littlefield R, Fowler VM (2002) Measurement of thin filament lengths by distributed deconvolution analysis of fluorescence images. Biophys J 82:2548–2564

    PubMed  CAS  Google Scholar 

  • Luo Y, Cooke R, Pate E (1994) Effect of series elasticity on delay in development of tension relative to stiffness during muscle activation. Am J Physiol 267:C1598–C1606

    PubMed  CAS  Google Scholar 

  • Luther PK, Padron R, Ritter S, Craig R, Squire JM (2003) Heterogeneity of Z-band structure within a single muscle sarcomere: implications for sarcomere assembly. J Mol Biol 332:161–169

    Article  PubMed  CAS  Google Scholar 

  • Mantovani M, Heglund NC, Cavagna GA (2001) Energy transfer during stress relaxation of contracting frog muscle fibres. J Physiol 537:923–939

    Article  PubMed  CAS  Google Scholar 

  • Morgan DL (1990) New insights into the behavior of muscle during active lengthening. Biophys J 57:209–221

    PubMed  CAS  Google Scholar 

  • Morgan DL (1994) An explanation for residual increased tension in striated muscle after stretch during contraction. Exp Physiol 79:831–838

    PubMed  CAS  Google Scholar 

  • Morgan DL, Mochon S, Julian FJ (1982) A quantitative model of intersarcomere dynamics during fixed-end contractions of single frog muscle fibers. Biophys J 39:189–196

    PubMed  CAS  Google Scholar 

  • Morgan DL, Proske U (1984) Mechanical properties of toad slow muscle attributed to non-uniform sarcomere lengths. J Physiol 349:107–117

    PubMed  CAS  Google Scholar 

  • Mulligan IP, Palmer RE, Lipscomb S, Hoskins B, Ashley CC (1999) The effect of phosphate on the relaxation of frog skeletal muscle. Pflugers Arch 437:393–399

    Article  PubMed  CAS  Google Scholar 

  • Mutungi G, Ranatunga KW (2000) Sarcomere length changes during end-held (isometric) contractions in intact mammalian (rat) fast and slow muscle fibres. J Muscle Res Cell Motil 21:565–575

    Article  PubMed  CAS  Google Scholar 

  • Nishiyama K (1984) Analysis of mechanical behavior of muscle by a multi-sarcomere model. Adv Exp Med Biol 170:637–639

    PubMed  CAS  Google Scholar 

  • Obermann WM, Gautel M, Steiner F, van der Ven PF, Weber K, Furst DO (1996) The structure of the sarcomeric M band: localization of defined domains of myomesin, M-protein, and the 250-kD carboxy-terminal region of titin by immunoelectron microscopy. J Cell Biol 134:1441–1453

    Article  PubMed  CAS  Google Scholar 

  • Ostap EM (2002) 2,3-Butanedione monoxime (BDM) as a myosin inhibitor. J Muscle Res Cell Motil 23:305–308

    Article  PubMed  CAS  Google Scholar 

  • Peterson DR, Rassier DE, Herzog W (2004) Force enhancement in single skeletal muscle fibres on the ascending limb of the force-length relationship. J Exp Biol 207:2787–2791

    Article  PubMed  Google Scholar 

  • Piazzesi G, Francini F, Linari M, Lombardi V (1992) Tension transients during steady lengthening of tetanized muscle fibres of the frog. J Physiol 445:659–711

    PubMed  CAS  Google Scholar 

  • Piazzesi G, Lucii L, Lombardi V (2002) The size and the speed of the working stroke of muscle myosin and its dependence on the force. J Physiol 545:145–151

    Article  PubMed  CAS  Google Scholar 

  • Piazzesi G, Reconditi M, Koubassova N, Decostre V, Linari M, Lucii L, Lombardi V (2003) Temperature dependence of the force-generating process in single fibres from frog skeletal muscle. J Physiol 549:93–106

    Article  PubMed  CAS  Google Scholar 

  • Pinniger GJ, Bruton JD, Westerblad H, Ranatunga KW (2005) Effects of a myosin-II inhibitor (N-benzyl-p-toluene sulphonamide, BTS) on contractile characteristics of intact fast-twitch mammalian muscle fibres. J Muscle Res Cell Motil 26(2–3):135–141

    Google Scholar 

  • Pinniger GJ, Ranatunga KW, Offer GW (2006) Crossbridge and non-crossbridge contributions to tension in lengthening muscle: force-induced reversal of the power stroke. J Physiol 573:627–643

    Article  PubMed  CAS  Google Scholar 

  • Piroddi N, Belus A, Eiras S, Tesi C, van der Velden J, Poggesi C, Stienen GJ (2006) No direct effect of creatine phosphate on the cross-bridge cycle in cardiac myofibrils. Pflugers Arch 452:3–6

    Article  PubMed  CAS  Google Scholar 

  • Poggesi C, Tesi C, Stehle R (2005) Sarcomeric determinants of striated muscle relaxation kinetics. Pflugers Arch 449:505–517

    Article  PubMed  CAS  Google Scholar 

  • Rassier DE, Herzog W (2004) Active force inhibition and stretch-induced force enhancement in frog muscle treated with BDM. J Appl Physiol 97:1395–1400

    Article  PubMed  Google Scholar 

  • Rassier DE, Herzog W, Pollack GH (2003a) Dynamics of individual sarcomeres during and after stretch in activated single myofibrils. Proc R Soc Lond B Biol Sci 270:1735–1740

    Article  Google Scholar 

  • Rassier DE, Herzog W, Pollack GH (2003b) Stretch-induced force enhancement and stability of skeletal muscle myofibrils. Adv Exp Med Biol 538: 501–515; discussion 515

    Google Scholar 

  • Rudel R, Zite-Ferenczy F (1979) Interpretation of light diffraction by cross-striated muscle as Bragg reflexion of light by the lattice of contractile proteins. J Physiol 290:317–330

    PubMed  CAS  Google Scholar 

  • Saldana RP, Smith DA (1991) Four aspects of creep phenomena in striated muscle. J Muscle Res Cell Motil 12:517–531

    Article  PubMed  CAS  Google Scholar 

  • Schachar R, Herzog W, Leonard T (2002) Force enhancement above the initial isometric force on the descending limb of the force-length relationship. J Biomech 35:1299–1306

    Article  PubMed  CAS  Google Scholar 

  • Shah SB, Su FC, Jordan K, Milner DJ, Friden J, Capetanaki Y, Lieber RL (2002) Evidence for increased myofibrillar mobility in desmin-null mouse skeletal muscle. J Exp Biol 205:321–325

    PubMed  Google Scholar 

  • Shaw MA, Ostap EM, Goldman YE (2003) Mechanism of inhibition of skeletal muscle actomyosin by N-benzyl-p-toluenesulfonamide. Biochemistry 42:6128–6135

    Article  PubMed  CAS  Google Scholar 

  • Shitaka Y, Kimura C, Iio T, Miki M (2004) Kinetics of the structural transition of muscle thin filaments observed by fluorescence resonance energy transfer. Biochemistry 43:10739–10747

    Article  PubMed  CAS  Google Scholar 

  • Simnett SJ, Johns EC, Lipscomb S, Mulligan IP, Ashley CC (1998) Effect of pH, phosphate, and ADP on relaxation of myocardium after photolysis of diazo 2. Am J Physiol 275:H951–H960

    PubMed  CAS  Google Scholar 

  • Stehle R, Krüger M, Pfitzer G (2002a) Force kinetics and individual sarcomere dynamics in cardiac myofibrils after rapid Ca(2+) changes. Biophys J 83:2152–2161

    PubMed  CAS  Google Scholar 

  • Stehle R, Krüger M, Scherer P, Brixius K, Schwinger RH, Pfitzer G (2002b) Isometric force kinetics upon rapid activation and relaxation of mouse, guinea pig and human heart muscle studied on the subcellular myofibrillar level. Basic Res Cardiol 97(Suppl 1):127–135

    Google Scholar 

  • Stehle R, Solzin J, Iorga B, Gomez D, Blaudeck N, Pfitzer G (2006) Mechanical properties of sarcomeres during cardiac myofibrillar relaxation: stretch-induced cross-bridge detachment contributes to early diastolic filling. J Muscle Res Cell Motil 27:423–434

    Article  PubMed  CAS  Google Scholar 

  • Sugi H, Tsuchiya T (1998) Muscle mechanics I: intact single muscle fibres. In: Sugi H (ed) Current methods in muscle physiology: advantages, problems and limitations, 1st edn. Oxford University Press, New York

    Google Scholar 

  • Sun YB, Hilber K, Irving M (2001) Effect of active shortening on the rate of ATP utilisation by rabbit psoas muscle fibres. J Physiol 531:781–791

    Article  PubMed  CAS  Google Scholar 

  • Tatsumi R, Maeda K, Hattori A, Takahashi K (2001) Calcium binding to an elastic portion of connectin/titin filaments. J Muscle Res Cell Motil 22:149–162

    Article  PubMed  CAS  Google Scholar 

  • Telley IA, Denoth J, Ranatunga KW (2003) Inter-sarcomere dynamics in muscle fibres. A neglected subject? Adv Exp Med Biol 538:481–500

    PubMed  CAS  Google Scholar 

  • Telley IA, Denoth J, Stussi E, Pfitzer G, Stehle R (2006a) Half-sarcomere dynamics in myofibrils during activation and relaxation studied by tracking fluorescent markers. Biophys J 90:514–530

    Article  PubMed  CAS  Google Scholar 

  • Telley IA, Stehle R, Ranatunga KW, Pfitzer G, Stussi E, Denoth J (2006b) Dynamic behaviour of half-sarcomeres during and after stretch in activated psoas myofibrils: sarcomere asymmetry but no ‘sarcomere popping’. J Physiol 573:173–185

    Article  PubMed  CAS  Google Scholar 

  • Tesi C, Colomo F, Piroddi N, Poggesi C (2002a) Characterization of the cross-bridge force-generating step using inorganic phosphate and BDM in myofibrils from rabbit skeletal muscles. J Physiol 541:187–199

    Article  PubMed  CAS  Google Scholar 

  • Tesi C, Piroddi N, Colomo F, Poggesi C (2002b) Relaxation kinetics following sudden Ca(2+) reduction in single myofibrils from skeletal muscle. Biophys J 83:2142–2151

    PubMed  CAS  Google Scholar 

  • Veigel C, Molloy JE, Schmitz S, Kendrick-Jones J (2003) Load-dependent kinetics of force production by smooth muscle myosin measured with optical tweezers. Nat Cell Biol 5:980–986

    Article  PubMed  CAS  Google Scholar 

  • Wang K, Ramirez-Mitchell R (1983) A network of transverse and longitudinal intermediate filaments is associated with sarcomeres of adult vertebrate skeletal muscle. J Cell Biol 96:562–570

    Article  PubMed  CAS  Google Scholar 

  • Yaniv Y, Sivan R, Landesberg A (2006) Stability, controllability, and observability of the “four state” model for the sarcomeric control of contraction. Ann Biomed Eng 34:778–789

    Article  PubMed  Google Scholar 

  • Yildiz A, Selvin PR (2005) Fluorescence imaging with one nanometer accuracy: application to molecular motors. Acc Chem Res 38:574–582

    Article  PubMed  CAS  Google Scholar 

  • Zahalak GI (1997) Can muscle fibers be stable on the descending limbs of their sarcomere length-tension relations? J Biomech 30:1179–1182

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors are grateful to KW Ranatunga (Bristol) and Robert Stehle (Cologne) for valuable suggestions on the manuscript, and to the reviewers of this article for constructive comments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jachen Denoth.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Telley, I.A., Denoth, J. Sarcomere dynamics during muscular contraction and their implications to muscle function. J Muscle Res Cell Motil 28, 89–104 (2007). https://doi.org/10.1007/s10974-007-9107-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10974-007-9107-8

Keywords

Navigation