The European Physical Journal E

, Volume 21, Issue 3, pp 209–222 | Cite as

Growth of attached actin filaments

Regular Article

Abstract.

In several studies of actin-based cellular motility, the barbed ends of actin filaments have been observed to be attached to moving obstacles. Filament growth in the presence of such filament-obstacle interactions is studied via Brownian dynamics simulations of a three-dimensional energy-based model. We find that with a binding energy greater than 24kBT and a highly directional force field, a single actin filament is able to push a small obstacle for over a second at a speed of half of the free filament elongation rate. These results are consistent with experimental observations of plastic beads in cell extracts. Calculations of an external force acting on a single-filament-pushed obstacle show that for typical in vitro free-actin concentrations, a 3pN pulling force maximizes the obstacle speed, while a 4pN pushing force almost stops the obstacle. Extension of the model to treat beads propelled by many filaments suggests that most of the propulsive force could be generated by attached filaments.

PACS.

82.35.Pq Biopolymers, biopolymerization 87.15.Aa Theory and modeling; computer simulation 87.15.Rn Reactions and kinetics; polymerization 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    C.S. Peskin, G.M. Odell, G.F. Oster, Biophys. J. 65, 316 (1993).CrossRefGoogle Scholar
  2. 2.
    A. Mogilner, G. Oster, Biophys. J. 71, 3030 (1996).CrossRefGoogle Scholar
  3. 3.
    S.C. Kuo, J.L. McGrath, Nature 407, 1026 (2000).CrossRefADSGoogle Scholar
  4. 4.
    D.J. Olbris, J. Herzfeld, Biochim. Biophys. Acta 1495, 140 (2000).CrossRefGoogle Scholar
  5. 5.
    F. Gerbal, V. Laurent, A. Ott, M.F. Carlier, P. Chaikin, J. Prost, Eur. Biophys. J. 29, 134 (2000).CrossRefGoogle Scholar
  6. 6.
    Y. Marcy, J. Prost, M.F. Carlier, C. Sykes, Proc. Natl. Acad. Sci. U.S.A. 101, 5992 (2004).CrossRefADSGoogle Scholar
  7. 7.
    L.A. Cameron, T.M. Svitkina, D. Vignjevic, J.A. Theriot, G.G. Borisy, Curr. Biol. 11, 130 (2001).CrossRefGoogle Scholar
  8. 8.
    R.B. Dickinson, D.L. Purich, Biophys. J. 82, 605 (2002).CrossRefGoogle Scholar
  9. 9.
    A. Mogilner, G. Oster, Biophys. J. 84, 1591 (2003).CrossRefGoogle Scholar
  10. 10.
    M.D. Welch, J. Rosenblatt, J. Skoble, D.A. Portnoy, T.J. Mitchison, Science 281, 105 (1998).CrossRefADSGoogle Scholar
  11. 11.
    G. Cicchetti, P. Maurer, P. Wagener, C. Kocks, J. Biol. Chem. 274, 33616 (1999).CrossRefGoogle Scholar
  12. 12.
    T.D. Pollard, W.C. Earnshaw, Cell Biology, 1st ed. (Saunders, Philadelphia, PA, 2002).Google Scholar
  13. 13.
    H.N. Higgs, L. Blanchoin, T.D. Pollard, Biochemistry 38, 15212 (1999).CrossRefGoogle Scholar
  14. 14.
    T.D. Pollard, J. Cell Biol. 103, 2747 (1986).CrossRefGoogle Scholar
  15. 15.
    L.A. Cameron, J.R. Robbins, M.J. Footer, J.A. Theriot, Mol. Biol. Cell 15, 2312 (2004). CrossRefGoogle Scholar
  16. 16.
    M.T. Valentine, Z.E. Perlman, M.L. Gardel, J.H. Shin, P. Matsudaira, T.J. Mitchison, D.A. Weitz, Biophys. J. 86, 4004 (2004).CrossRefGoogle Scholar
  17. 17.
    H. Salman, Y. Gil, R. Granek, M. Elbaum, Chem. Phys. 284, 389 (2002).CrossRefADSGoogle Scholar
  18. 18.
    M.T. Valentine, Z.E. Perlman, T.J. Mitchison, D.A. Weitz, Biophys. J. 88, 680 (2005).CrossRefGoogle Scholar
  19. 19.
    H.C. Berg, Random Walks in Biology (Princeton University Press, Princeton, NJ, 1983).Google Scholar
  20. 20.
    R.D. Mullins, J.A. Heuser, T.D. Pollard, Proc. Natl. Acad. Sci. U.S.A. 95, 6181 (1998).CrossRefADSGoogle Scholar
  21. 21.
    D. Pantaloni, R. Boujemaa, D. Didry, P. Gounon, M.F. Carlier, Nat. Cell Biol. 2, 385 (2000).CrossRefGoogle Scholar
  22. 22.
    D.R. Kovar, T.D. Pollard, Proc. Natl. Acad. Sci. U.S.A. 101, 14725 (2004).CrossRefADSGoogle Scholar
  23. 23.
    M. Doi, S.F. Edwards, The Theory of Polymer Dynamics (Oxford University Press, Oxford, 1986).Google Scholar
  24. 24.
    W.H. Press, B.P. Flannery, S.A. Teukolsky, W.T. Vetterling, Numerical Recipes in C, 2nd ed. (Cambridge University Press, Cambridge, 1992).Google Scholar
  25. 25.
    E.A.J.F. Peters, T.M.A.O.M. Barenbrug, Phys. Rev. E 66, 056702 (2002).CrossRefADSGoogle Scholar
  26. 26.
    A.C. Brańka, D.M. Heyes, Phys. Rev. E 58, 2611 (1998).CrossRefADSGoogle Scholar
  27. 27.
    P. Hänggi, P. Talkner, M. Borkovec, Rev. Mod. Phys. 62, 251 (1990).CrossRefADSGoogle Scholar
  28. 28.
    A. Upadhyaya, J.R. Chabot, A. Andreeva, A. Samadani, A. van Oudenaarden, Proc. Natl. Acad. Sci. U.S.A. 100, 4521 (2003).CrossRefADSGoogle Scholar
  29. 29.
    P.A. Giardini, D.A. Fletcher, J.A. Theriot, Proc. Natl. Acad. Sci. U.S.A. 100, 6493 (2003).CrossRefADSGoogle Scholar
  30. 30.
    H. Boukellal, O. Campás, J.F. Joanny, J. Prost, C. Sykes, Phys. Rev. E 69, 061906 (2004).CrossRefADSGoogle Scholar
  31. 31.
    A.E. Carlsson, Biophys. J. 84, 2907 (2003).CrossRefGoogle Scholar
  32. 32.
    J. Prost, The physics of Listeria propulsion, in Physics of Biomolecules and Cells, Proceedings of Les Houches 2001 Summer School, edited by H. Flyvbjerg, F. Julicher, P. Ormos, F. David (Springer, Berlin, 2002) pp. 215--236.Google Scholar
  33. 33.
    N.C. Price, R.A. Dwek, R.G. Ratcliffe, M.R. Wormald, Principles and Problems in Physical Chemistry for Biochemists, 3rd ed. (Oxford University Press, New York, 2001).Google Scholar
  34. 34.
    J. Zalevsky, I. Grigorova, R.D. Mullins, J. Biol. Chem. 276, 3468 (2001).CrossRefGoogle Scholar
  35. 35.
    D.T. Haynie, Biological Thermodynamics, 1st ed. (Cambridge University Press, Cambridge, 2001).Google Scholar
  36. 36.
    A.W. Murray, M.W. Kirschner, Nature 339, 275 (1989).CrossRefADSGoogle Scholar
  37. 37.
    R.O. Dendy, Plasma Physics: An Introductory Course, 1st ed. (Cambridge University Press, Cambridge, 1993).Google Scholar
  38. 38.
    T.E. Angelini, H. Liang, W. Wriggers, G.C.L. Wong, Proc. Natl. Acad. Sci. U.S.A. 100, 8634 (2003).CrossRefADSGoogle Scholar
  39. 39.
    R.H. Crowell, W.E. Slesnick, Calculus with Analytic Geometry (W.W. Norton and Co., New York, 1968).Google Scholar

Copyright information

© EDP Sciences, Società Italiana di Fisica and Springer-Verlag 2006

Authors and Affiliations

  1. 1.Department of PhysicsWashington UniversityUSA

Personalised recommendations