Cellular and Molecular Bioengineering

, Volume 6, Issue 1, pp 3–12 | Cite as

Role of the Actin–Myosin Catch Bond on Actomyosin Aggregate Formation

Article

Abstract

Actin and myosin, which are key components of contractile machinery, are responsible for cell shape changes, movement, and tissue deformation during morphogenesis. To generate contractile forces, actin and myosin combine to form aggregates with functional structures. On the molecular scale, because the actin–myosin catch-bond behavior reinforces the actin–myosin bond when the force exerted on the bond increases, actin–myosin kinetics is likely modulated by the actomyosin-generated force as well as the external force. The catch-bond behavior is anticipated to couple the mechanical and kinetic aspects of actomyosin aggregate formation. In this study, to unveil new aspects of actomyosin aggregate formation, we employed two mathematical models based on coarse-grained particle dynamics that describe actomyosin dynamics with and without the catch bond. Comparing the computational simulation results obtained from two models, we observed that the catch-bond behavior assists in the assemblage of myosin in a random actomyosin network even at low myosin concentrations and accelerates the completion of aggregate formation at relatively higher concentrations. The actin–myosin catch bond is anticipated to support foci formation from a random actomyosin network at the cell cortex during morphogenesis.

keywords

Actomyosin structure Catch bond Soft active matter 

References

  1. 1.
    Aström, J. A., P. B. S. Kumar, and M. Karttunen. Aster formation and rupture transition in semi-flexible fiber networks with mobile cross-linkers. Soft Matter 5:2869–2874, 2009.CrossRefGoogle Scholar
  2. 2.
    Backouche, F., L. Haviv, D. Groswasser, and A. Bernheim-Groswasser. Active gels: dynamics of patterning and self-organization. Phys. Biol. 3:264–273, 2006.CrossRefGoogle Scholar
  3. 3.
    Blanchard, G. B., S. Murugesu, R. J. Adams, A. Martinez-Arias, and N. Gorfinkiel. Cytoskeletal dynamics and supracellular organisation of cell shape fluctuations during dorsal closure. Development 137:2743–2752, 2010.CrossRefGoogle Scholar
  4. 4.
    Debold, E. P., J. B. Patlak, and D. M. Warshaw. Slip sliding away: load-dependence of velocity generated by skeletal muscle myosin molecules in the laser trap. Biophys. J. 89:L34–L36, 2005.CrossRefGoogle Scholar
  5. 5.
    Finer, J. T., R. M. Simmons, and J. A. Spudich. Single myosin molecule mechanics: piconewton forces and nanometre steps. Nature 368:113–119, 1994.CrossRefGoogle Scholar
  6. 6.
    Fynewever, H., and A. Yethiraj. Phase behavior of semiflexible tangent hard sphere chains. J. Chem. Phys. 108:1636–1644, 1998.CrossRefGoogle Scholar
  7. 7.
    Guo, B., and W. H. Guilford. Mechanics of actomyosin bonds in different nucleotide states are tuned to muscle contraction. Proc. Natl Acad. Sci. U.S.A. 103:9844–9849, 2006.CrossRefGoogle Scholar
  8. 8.
    Hall, A. Rho GTPases and the actin cytoskeleton. Science 279:509–514, 1998.CrossRefGoogle Scholar
  9. 9.
    He, L., X. Wang, H. L. Tang, and D. J. Montell. Tissue elongation requires oscillating contractions of a basal actomyosin network. Nat. Cell Biol. 12:1133–1142, 2010.CrossRefGoogle Scholar
  10. 10.
    Hill, A. V. The heat of shortening and dynamic constants of muscle. Proc. R. Soc. B 126:136–195, 1938.CrossRefGoogle Scholar
  11. 11.
    Inoue, Y., S. Tsuda, K. Nakagawa, M. Hojo, and T. Adachi. Modeling myosin-dependent rearrangement and force generation in an actomyosin network. J. Theor. Biol. 281:65–73, 2011.CrossRefGoogle Scholar
  12. 12.
    Kaya, M., and H. Higuchi. Nonlinear elasticity and an 8-nm working stroke of single myosin molecules in myofilaments. Science 329:686–689, 2010.CrossRefGoogle Scholar
  13. 13.
    Kim, T., W. Hwang, H. Lee, and R. D. Kamm. Computational analysis of viscoelastic properties of crosslinked actin networks. PLoS Comput. Biol. 5:e1000439, 2009.Google Scholar
  14. 14.
    Kitamura, K., M. Tokunaga, A. H. Iwane, and T. Yanagida. A single myosin head moves along an actin filament with regular steps of 5.3 nanometres. Nature 397:129–134, 1999.CrossRefGoogle Scholar
  15. 15.
    Köhler, S., V. Schaller, and A. R. Bausch. Structure formation in active networks. Nat. Mater. 10:462–468, 2011.CrossRefGoogle Scholar
  16. 16.
    Kojima, H., A. Ishijima, and A. Yanagida. Direct measurement of stiffness of single actin filaments with and without tropomyosin by in vitro nanomanipulation. Proc. Natl Acad. Sci. U.S.A. 91:12962–12966, 1994.CrossRefGoogle Scholar
  17. 17.
    Martin, A. C. Pulsation and stabilization: contractile forces that underlie morphogenesis. Dev. Biol. 341:114–125, 2010.CrossRefGoogle Scholar
  18. 18.
    Martin, A. C., M. Kaschube, and E. F. Wieschaus. Pulsed contractions of an actin–myosin network drive apical constriction. Nature 457:495–499, 2009.CrossRefGoogle Scholar
  19. 19.
    McCullough, B. R., L. Blanchoin, J.-L. Martiel, and E. M. De La Cruz. Cofilin increases the bending flexibility of actin filaments: implications for severing and cell mechanics. J. Mol. Biol. 381:550–558, 2008.CrossRefGoogle Scholar
  20. 20.
    McGough, A., B. Pope, W. Chiu, and A. Weeds. Cofilin changes the twist of F-actin: implications for actin filament dynamics and cellular function. J. Cell Biol. 138:771–781, 1997.CrossRefGoogle Scholar
  21. 21.
    Molloy, J. E., J. E. Burns, J. Kendrick-Jones, R. T. Tregear, and D. C. S. White. Movement and force produced by a single myosin head. Nature 378:209–212, 1995.CrossRefGoogle Scholar
  22. 22.
    Nishizaka, T., H. Miyata, H. Yoshikawa, S. Ishiwata, and K. Kinosita, Jr. Unbinding force of a single motor molecule of muscle measured using optical tweezers. Nature 377:251–254, 1995.CrossRefGoogle Scholar
  23. 23.
    Pereverzev, Y. V., O. V. Prezhdo, M. Forero, E. V. Sokurenko, and W. E. Thomas. The two-pathway model for the catch-slip transition in biological adhesion. Biophys. J. 89:1446–1454, 2005.CrossRefGoogle Scholar
  24. 24.
    Reif, F. Fundamental of Statistical and Thermal Physics. New York: McGraw-Hill, 1985.Google Scholar
  25. 25.
    Silva, M. S., M. Depken, B. Stuhrmann, M. Korsten, F. C. MacKintosh, and G. H. Koenderink. Active multistage coarsening of actin networks driven by myosin motors. Proc. Natl Acad. Sci. U.S.A. 108:9408–9413, 2011.CrossRefGoogle Scholar
  26. 26.
    Théry, M. Micropatterning as a tool to decipher cell morphogenesis and functions. J. Cell Sci. 123:4201–4213, 2010.CrossRefGoogle Scholar
  27. 27.
    Tseng, Q., E. Duchemin-Pelletier, A. Deshiere, M. Balland, H. Guillou, O. Filhol, and M. Thérya. Spatial organization of the extracellular matrix regulates cell-cell junction positioning. Proc. Natl Acad. Sci. U.S.A. 109:1506–1511, 2012.CrossRefGoogle Scholar
  28. 28.
    Verkhovsky, A. B., T. M. Svitkina, and B. B. Borisy. Polarity sorting of actin filaments in cytochalasin-treated fibroblasts. J. Cell Sci. 110:1693–1704, 1997.Google Scholar
  29. 29.
    Walcott, S., P. M. Fagnant, K. M. Trybus, and D. M. Warshaw. Smooth muscle heavy meromyosin phosphorylated on one of its two heads supports force and motion. J. Biol. Chem. 284:18244–18251, 2009.CrossRefGoogle Scholar
  30. 30.
    Wang, S., and P. G. Wolynes. Active contractility in actomyosin networks. Proc. Natl Acad. Sci. U.S.A. 109:6446–6451, 2012.CrossRefGoogle Scholar
  31. 31.
    Yumura, S., M. Ueda, Y. Sako, T. Kitanishi-Yumura, and T. Yanagida. Multiple mechanisms for accumulation of myosin II filaments at the equator during cytokinesis. Traffic 9:2089–2099, 2008.CrossRefGoogle Scholar

Copyright information

© Biomedical Engineering Society 2012

Authors and Affiliations

  1. 1.Institute for Frontier Medical SciencesKyoto UniversityKyotoJapan

Personalised recommendations