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Journal of Muscle Research & Cell Motility

, Volume 26, Issue 6–8, pp 375–379 | Cite as

The sarcomeric M-band during development and in disease

  • Stephan Lange
  • Irina Agarkova
  • Jean-Claude Perriard
  • Elisabeth EhlerEmail author
Article

Abstract

The C-terminus of connectin/titin at the M-band of the sarcomere interacts with several structural as well as potential signalling proteins. One of these is myomesin, which can also bind to myosin and has been suggested to function as an integral structural linker of the thick filaments into the sarcomere. Recent evidence that myomesin possesses the ability to form antiparallel dimers via its C-terminal domain has prompted us to propose a novel three-dimensional model for the sarcomeric M-band. A splice variant of myomesin, termed EH-myomesin, contains an additional segment that has disordered conformation and functions as an entropic spring. It is expressed in a subset of muscle types that are characterised by a broader operational range and are more resistant to damage caused by eccentric contraction. In addition, it is also re-expressed in dilated cardiomyopathy. DRAL/FHL-2 is another protein that interacts with the M-band portion of connectin/titin and which probably functions as an adaptor for the compartmentalisation of metabolic enzymes. Together these results suggest that the M-band is crucial for sarcomere function and maintenance and that its molecular composition can be adapted to divergent physiological needs in different muscle types, which may help to cope with pathological alterations.

Keywords

Eccentric Contraction Muscle Type PEVK Domain Precardiac Mesoderm Entropic Spring 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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Notes

Acknowledgements

Supported by Swiss National Science Foundation (3100-063486), a grant by the Swiss Cardiovascular Research & Training Network sponsored by SUK, and a grant from Swiss Society for Research Against Myopathies. We are grateful for all the helpful discussions with colleagues past and present.

References

  1. Agarkova I, Auerbach D, Ehler E, Perriard J-C, (2000) A novel marker for vertebrate embryonic heart, the EH-myomesin isoformJ Biol Chem 275:10256–10264CrossRefPubMedGoogle Scholar
  2. Agarkova I, Ehler E, Lange S, Schoenauer R, Perriard J-C, (2003) M-band: a safeguard for sarcomere stabilityJ Muscle Res Cell Motil 24:191–203CrossRefPubMedGoogle Scholar
  3. Agarkova I, Schoenauer R, Ehler E, Carlsson L, Carlsson E, Thornell LE, Perriard J-C, (2004) The molecular composition of the sarcomeric M-band correlates with muscle fiber typeEur J Cell Biol 83:1–12CrossRefPubMedGoogle Scholar
  4. Auerbach D, Bantle S, Keller S, Hinderling V, Leu M, Ehler E, Perriard JC, (1999) Different domains of the M-band protein myomesin are involved in myosin binding and M-band targetingMol Biol Cell 10:1297–1308PubMedGoogle Scholar
  5. Brockett CL, Morgan DL, Gregory JE, Proske U, (2002) Damage to different motor units from active lengthening of the medial gastrocnemius muscle of the catJ Appl Physiol 92:1104–1110PubMedGoogle Scholar
  6. Du A, Sanger JM, Linask KK, Sanger JW, (2003) Myofibrillogenesis in the first cardiomyocytes formed from isolated quail precardiac mesodermDev Biol 257:382–394CrossRefPubMedGoogle Scholar
  7. Ehler E, Perriard J-C, (2001) Emergence of the first myofibrils and targeting mechanisms directing sarcomere assembly in developing cardiomyocytes. In: Dube DK, (ed.) Myofibrillogenesis. Birkhäuser, Boston pp 41–58Google Scholar
  8. Ehler E, Rothen BM, Hämmerle SP, Komiyama M, Perriard J-C, (1999) Myofibrillogenesis in the developing chicken heart: assembly of Z-disk, M-line and the thick filamentsJ Cell Sci 112:1529–1539PubMedGoogle Scholar
  9. Gotthardt M, Hammer RE, Hubner N, Monti J, Witt CC, McNabb M, Richardson JA, Granzier H, Labeit S, Herz J, (2003) Conditional expression of mutant M-line titins results in cardiomyopathy with altered sarcomere structureJ Biol Chem 278:6059–6065CrossRefPubMedGoogle Scholar
  10. 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-proteinJ Mol Biol 332:877–887CrossRefPubMedGoogle Scholar
  11. Huxley H, Hanson J, (1954) Changes in the cross-striations of muscle during contraction and stretch and their structural interpretationNature 173:973–976PubMedCrossRefGoogle Scholar
  12. Lange S, Auerbach D, McLoughlin P, Perriard E, Schäfer BW, Perriard JC, Ehler E, (2002) Subcellular targeting of metabolic enzymes to titin in heart muscle may be mediated by DRAL/FHL-2J Cell Sci 115:4925–4936CrossRefPubMedGoogle Scholar
  13. Lange S, Himmel M, Auerbach D, Agarkova I, Hayess K, Fürst DO, Perriard J-C, Ehler E, (2005) Dimerisation of myomesin: implications for the structure of the sarcomeric M-bandJ Mol Biol 345:289–298CrossRefPubMedGoogle Scholar
  14. Luther PK, Crowther RA, (1984) Three-dimensional reconstruction from tilted sections of fish muscle M-bandNature 307:566–568CrossRefPubMedGoogle Scholar
  15. Macpherson PCD, Schork MA, Faulkner JA, (1996) Contraction-induced injury to single fiber segments from fast and slow muscles of rats by single stretchesAm J Physiol 271:C1438–1446PubMedGoogle Scholar
  16. Maruyama K, Natori R, Nonomura Y, (1976) New elastic protein from muscleNature 262:58–60CrossRefPubMedGoogle Scholar
  17. Mayans O, van der Ven PF, Wilm M, Mues A, Young P, Fürst DO, Wilmanns M, Gautel M, (1998) Structural basis for activation of the titin kinase domain during myofibrillogenesisNature 395:863–869CrossRefPubMedGoogle Scholar
  18. McElhinny AS, Kakinuma K, Sorimachi H, Labeit S, Gregorio CC, (2002) Muscle-specific RING finger-1 interacts with titin to regulate sarcomeric M-line and thick filament structure and may have nuclear functions via its interaction with glucocorticoid modulatory element binding protein-1J Cell Biol 157:125–136CrossRefPubMedGoogle Scholar
  19. Obermann WM, Plessmann U, Weber K, Fürst DO, (1995) Purification and biochemical characterization of myomesin, a myosin-binding and titin-binding protein, from bovine skeletal muscleEur J Biochem 233:110–115CrossRefPubMedGoogle Scholar
  20. Obermann WM, Gautel M, Steiner F, van der Ven PF, Weber K, Fürst 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 microscopyJ Cell Biol 134:1441–1453CrossRefPubMedGoogle Scholar
  21. Obermann WM, Gautel M, Weber K, Fürst DO, (1997) Molecular structure of the sarcomeric M band: mapping of titin and myosin binding domains in myomesin and the identification of a potential regulatory phosphorylation site in myomesinEMBO J 16:211–220CrossRefPubMedGoogle Scholar
  22. Pask HT, Jones KL, Luther PK, Squire JM, (1994) M-band structure, M-bridge interactions and contraction speed in vertebrate cardiac musclesJ Muscle Res Cell Motil 15:633–645CrossRefPubMedGoogle Scholar
  23. Person V, Kostin S, Suzuki K, Labeit S, Schaper J, (2000) Antisense oligonucleotide experiments elucidate the essential role of titin in sarcomerogenesis in adult rat cardiomyocytes in long-term cultureJ Cell Sci 113:3851–3859PubMedGoogle Scholar
  24. Pizon V, Iakovenko A, Van Der Ven PF, Kelly R, Fatu C, Furst DO, Karsenti E, Gautel M, (2002) Transient association of titin and myosin with microtubules in nascent myofibrils directed by the MURF2 RING-finger proteinJ Cell Sci 115:4469–4482CrossRefPubMedGoogle Scholar
  25. Schoenauer R, Bertoncini P, Machaidze G, Aebi U, Perriard JC, Hegner M and Agarkova I (2005) Myomesin is a molecular spring with adaptable elasticity. J Mol Biol 349: 367–379Google Scholar
  26. Schultheiss T, Lin ZX, Lu MH, Murray J, Fischman DA, Weber K, Masaki T, Imamura M, Holtzer H, (1990) Differential distribution of subsets of myofibrillar proteins in cardiac nonstriated and striated myofibrilsJ Cell Biol 110:1159–1172CrossRefPubMedGoogle Scholar
  27. Squire J, (1981) The Structural Basis of Muscle Contraction. Plenum Press, New YorkGoogle Scholar
  28. Tompa P, (2002) Intrinsically unstructured proteinsTrends Biochem Sci 27:527–533CrossRefPubMedGoogle Scholar
  29. van der Ven P, Bartsch J, Gautel M, Jockusch H, Do F, (2000) A functional knock-out of titin results in defective myofibril assemblyJ Cell Sci 113:1405–1414PubMedGoogle Scholar
  30. Varriano-Marston E, Franzini-Armstrong C, Haselgrove JC, (1984) The structure and disposition of crossbridges in deep-etched fish muscle J Muscle Res Cell Motil 5:363–386CrossRefPubMedGoogle Scholar
  31. Young P, Ferguson C, Banuelos S, Gautel M, (1998) Molecular structure of the sarcomeric Z-disk: two types of titin interactions lead to an asymmetrical sorting of α-actininEMBO J 17:1614–1624CrossRefPubMedGoogle Scholar
  32. Young P, Ehler E, Gautel M, (2001) Obscurin, a giant sarcomeric Rho guanine nucleotide exchange factor protein involved in sarcomere assemblyJ Cell Biol 154:123–136CrossRefPubMedGoogle Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • Stephan Lange
    • 1
    • 2
  • Irina Agarkova
    • 2
  • Jean-Claude Perriard
    • 2
  • Elisabeth Ehler
    • 1
    Email author
  1. 1.The Randall Division of Cell & Molecular Biophysics and the Cardiovascular DivisionKing’s College LondonLondonUK
  2. 2.Institute of Cell BiologyETH Zurich-HonggerbergZurichSwitzerland

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