Skip to main content
Log in

Proposed role of the M-band in sarcomere mechanics and mechano-sensing: a model study

  • Original Paper
  • Published:
Biomechanics and Modeling in Mechanobiology Aims and scope Submit manuscript

Abstract

In sarcomeres of striated muscles the middle parts of adjacent thick filaments are connected to each other by the M-band proteins. To understand the role of the M-band in sarcomere mechanics a model of forces which pull a thick filament to opposite Z-disks of a sarcomere is considered. Forces of actin-myosin cross-bridges, I-band titin segments and the M-band are accounted for. A continual expression for the M-band force is obtained assuming that the M-band proteins which connect neighbor thick filaments have nonlinear elastic properties. On the ascending and descending limbs of the force-length diagram cross-bridge forces tend to destabilize sarcomere while titin tries to restore its symmetric configuration. When destabilizing cross-bridge force exceeds a critical limit, symmetric configuration of a sarcomere becomes unstable and the M-band buckles. Stiffness of the M-band increases stability only if the M-band is anchored to the extra-sarcomere cytoskeleton. Realistic magnitudes of the M-band buckling require that the M-band proteins have essentially nonlinear elasticity. The buckling may explain the M-band bending and axial misalignment of the thick filaments observed in contracting muscle. We hypothesize that the buckling stretches the titin protein kinase domain localized in the M-band being the signal for mechanical control of gene expression and protein turnover in striated muscle.

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.

Similar content being viewed by others

References

  • Agarkova I, Ehler E, Lange S, Schoenauer R, Perriard JC (2003) M-band: a safeguard for sarcomere stability? J Muscle Res Cell Motil 24: 191–203

    Article  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  Google Scholar 

  • Brunello E, Bianco P, Piazzesi G et al (2006) Structural changes in the myosin filament and cross-bridges during active force development in single intact frog muscle fibres: stiffness and X-ray diffraction measurements. J Physiol 577: 971–984

    Article  Google Scholar 

  • Carlsson L, Yu JG, Thornell LG (2008) New aspects of obscurin in human striated muscles. Histochem Cell Biol 130: 91–103

    Article  Google Scholar 

  • Cunha SR, Mohler PJ (2008) Obscurin targets ankyrin-B and protein phosphatase 2A to the cardiac M-line. J Biol Chem 283: 31968–31980

    Article  Google Scholar 

  • Fukuzawa A, Lange S, Holt M et al (2008) Interactions with titin and myomesin target obscurin and obscurin-like 1 to the M-band: implications for hereditary myopathies. J Cell Sci 121: 1841–1851

    Article  Google Scholar 

  • Granzier HL, Irving TC (1995) Passive tension in cardiac muscle: contribution of collagen, titin, microtubules, and intermediate filaments. Biophys J 68: 1027–1044

    Article  Google Scholar 

  • Griffiths PJ, Bagni MA, Colombini B, Amenitsch H, Bernstorff S, Funari S, Ashley CC, Cecchi G. (2006) Effects of the number of actin-bound S1 and axial force on X-ray patterns of intact skeletal muscle. Biophys J 90: 975–984

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Hornemann T, Kempa S, Himmel M, Hayess K, Fürst DO, Wallimann T (2003) Muscle-type creatine kinase interacts with central domains of the M-band proteins myomesin and M-protein. J Mol Biol 332: 877–887

    Article  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  Google Scholar 

  • Huxley HE, Brown W (1967) The low-angle X-ray diagram of vertebrate striated muscle and its behaviour during contraction and rigor. J Mol Biol 30: 383–434

    Google Scholar 

  • Huxley HE, Faruqi AR, Kress M et al (1982) Time-resolved X-ray diffraction studies of the myosin layer-line reflections during muscle contraction. J Mol Biol 158: 637–684

    Article  Google Scholar 

  • Huxley HE, Stewart A, Sosa H, Irving T (1994) X-ray diffraction measurements of the extensibility of actin and myosin filaments in contracting muscle. Biophys J 67: 2411–2421

    Article  Google Scholar 

  • Koubassova NA, Tsaturyan AK (2002) Direct modeling of X-ray diffraction pattern from skeletal muscle in rigor. Biophys J 83: 1082–1097

    Article  Google Scholar 

  • Koubassova NA, Bershitsky SY, Ferenczi MA, Tsaturyan AK (2008) Direct modeling of X-ray diffraction pattern from contracting skeletal muscle. Biophys J 95: 2880–2894

    Article  Google Scholar 

  • Lange S, Xiang F, Yakovenko A et al (2005) The kinase domain of titin controls muscle gene expression and protein turnover. Science 308: 1599–1603

    Article  Google Scholar 

  • Leake MC, Wilson D, Gautel M, Simmons RM (2004) The elasticity of single titin molecules using a two-bead optical tweezers assay. Biophys J 87: 1112–1135

    Article  Google Scholar 

  • Linari M, Brunello E, Reconditi M et al (2005) The structural basis of the increase in isometric force production with temperature in frog skeletal muscle. J Physiol 567: 459–469

    Article  Google Scholar 

  • Liversage AD, Holmes D, Knight PJ et al (2001) Titin and the sarcomere symmetry paradox. J Mol Biol 305: 401–409

    Article  Google Scholar 

  • Luther P, Squire J (1978) Three-dimensional structure of the vertebrate muscle M-region. J Mol Biol 125: 313–324

    Article  Google Scholar 

  • Obermann WM, Gautel M, Steiner F et al (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  Google Scholar 

  • Puchner EM, Alexandrovich A, Kho AL (2008) Mechanoenzymatics of titin kinase. Proc Natl Acad Sci USA 105: 13385–13390

    Article  Google Scholar 

  • Schoenauer R, Bertoncini P, Machaidze G et al (2005) Myomesin is a molecular spring with adaptable elasticity. J Mol Biol 349: 367–379

    Article  Google Scholar 

  • Schoenauer R, Lange S, Hirschy A et al (2008) Myomesin 3, a novel structural component of the M-band in striated muscle. J Mol Biol 376: 338–351

    Article  Google Scholar 

  • Sosa H, Popp D, Ouyang G, Huxley HE (1994) Ultrastructure of skeletal muscle fibers studied by a plunge quick freezing method: myofilament lengths. Biophys J 67: 283–292

    Article  Google Scholar 

  • Telley IA, Denoth J, Stüssi E et al (2006) Half-sarcomere dynamics in myofibrils during activation and relaxation studied by tracking fluorescent markers. Biophys J 90: 514–530

    Article  Google Scholar 

  • Tsaturyan AK, Koubassova N, Ferenczi MA et al (2005) Strong binding of myosin heads stretches and twists the actin helix. Biophys J 88: 1902–1910

    Article  Google Scholar 

  • Trombitás K, Tigyi-Sebes A (1984) Cross-bridge interaction with oppositely polarized actin filaments in double-overlap zones of insect flight muscle. Nature 309(5964): 168–170

    Article  Google Scholar 

  • Vilfan A, Duke T (2003) Instabilities in the transient response of muscle. Biophys J 85: 818–827

    Article  Google Scholar 

  • Wakabayashi K, Sugimoto Y, Tanaka H et al (1994) X-ray diffraction evidence for the extensibility of actin and myosin filaments during muscle contraction. Biophys J 67: 2422–2435

    Article  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  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Andrey K. Tsaturyan.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Shabarchin, A.A., Tsaturyan, A.K. Proposed role of the M-band in sarcomere mechanics and mechano-sensing: a model study. Biomech Model Mechanobiol 9, 163–175 (2010). https://doi.org/10.1007/s10237-009-0167-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10237-009-0167-0

Keywords

Navigation