A single charge in the actin binding domain of fascin can independently tune the linear and non-linear response of an actin bundle network

Abstract

Actin binding proteins (ABPs) not only set the structure of actin filament assemblies but also mediate the frequency-dependent viscoelastic moduli of cross-linked and bundled actin networks. Point mutations in the actin binding domain of those ABPs can tune the association and dissociation dynamics of the actin/ABP bond and thus modulate the network mechanics both in the linear and non-linear response regime. We here demonstrate how the exchange of a single charged amino acid in the actin binding domain of the ABP fascin triggers such a modulation of the network rheology. Whereas the overall structure of the bundle networks is conserved, the transition point from strain-hardening to strain-weakening sensitively depends on the cross-linker off-rate and the applied shear rate. Our experimental results are consistent both with numerical simulations of a cross-linked bundle network and a theoretical description of the bundle network mechanics which is based on non-affine bending deformations and force-dependent cross-link dynamics.

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References

  1. 1.

    A.J. Ridley, Cell 145, 1012 (2011).

    Article  Google Scholar 

  2. 2.

    D.A. Head, A.J. Levine, F.C. MacKintosh, Phys. Rev. E 68, 061907 (2003).

    Article  ADS  Google Scholar 

  3. 3.

    K.E. Kasza, A.C. Rowat, J.Y. Liu, T.E. Angelini, C.P. Brangwynne et al., Curr. Opin. Cell Biol. 19, 101 (2007).

    Article  Google Scholar 

  4. 4.

    K.E. Kasza, G.H. Koenderink, Y.C. Lin, C.P. Broedersz, W. Messner et al., Phys. Rev. E 79, 041928 (2009).

    Article  ADS  Google Scholar 

  5. 5.

    O. Lieleg, M.M.A.E. Claessens, A.R. Bausch, Soft Matter 6, 218 (2010).

    Article  ADS  Google Scholar 

  6. 6.

    J.M. Tse, G. Cheng, J.A. Tyrrell, S.A. Wilcox-Adelman, Y. Boucher et al., Proc. Natl. Acad. Sci. U.S.A. 109, 911 (2012).

    Article  ADS  Google Scholar 

  7. 7.

    J. Faix, K. Rottner, Curr. Opin. Cell Biol. 18, 18 (2006).

    Article  Google Scholar 

  8. 8.

    P.K. Mattila, P. Lappalainen, Nat. Rev. Mol. Cell Biology 9, 446 (2008).

    Article  Google Scholar 

  9. 9.

    M. Claessens, M. Bathe, E. Frey, A.R. Bausch, Nat. Mater. 5, 748 (2006).

    Article  ADS  Google Scholar 

  10. 10.

    M. Claessens, C. Semmrich, L. Ramos, A.R. Bausch, Proc. Natl. Acad. Sci. U.S.A. 105, 8819 (2008).

    Article  ADS  Google Scholar 

  11. 11.

    Y.S. Aratyn, T.E. Schaus, E.W. Taylor, G.G. Borisy, Mol. Biol. Cell 18, 3928 (2007).

    Article  Google Scholar 

  12. 12.

    N. Kureishy, V. Sapountzi, S. Prag, N. Anilkumar, J.C. Adams, BioEssays 24, 350 (2002).

    Article  Google Scholar 

  13. 13.

    D. Vignjevic, M. Schoumacher, N. Gavert, K.P. Janssen, G. Jih et al., Cancer Res. 67, 6844 (2007).

    Article  Google Scholar 

  14. 14.

    A. Li, J.C. Dawson, M. Forero-Vargas, H.J. Spence, X.Z. Yu et al., Curr. Biol. 20, 339 (2010).

    Article  Google Scholar 

  15. 15.

    A.U. Jawhari, A. Buda, M. Jenkins, K. Shehzad, C. Sarraf et al., Am. J. Pathol. 162, 69 (2003).

    Article  Google Scholar 

  16. 16.

    J. Zanet, A. Jayo, S. Plaza, T. Millard, M. Parsons et al., J. Cell Biol. 197, 477 (2012).

    Article  Google Scholar 

  17. 17.

    S. Ono, Y. Yamakita, S. Yamashiro, P.T. Matsudaira, J.R. Gnarra et al., J. Biol. Chem. 272, 2527 (1997).

    Article  Google Scholar 

  18. 18.

    D. Vignjevic, S. Kojima, T. Svitkina, G.G. Borisy, J. Cell Biol. 174, 863 (2006).

    Article  Google Scholar 

  19. 19.

    S. Jansen, A. Collins, C.S. Yang, G. Rebowski, T. Svitkina et al., J. Biol. Chem. 286, 30087 (2011).

    Article  Google Scholar 

  20. 20.

    S.Y. Yang, F.K. Huang, J.Y. Huang, S. Chen, J. Jakoncic et al., J. Biol. Chem. 288, 274 (2013).

    Article  Google Scholar 

  21. 21.

    J.A. Spudich, S. Watt, J. Biol. Chem. 246, 4866 (1971).

    Google Scholar 

  22. 22.

    D. Vignjevic, D. Yarar, M.D. Welch, J. Peloquin, T. Svitkina et al., J. Cell Biol. 160, 951 (2003).

    Article  Google Scholar 

  23. 23.

    C. Semmrich, R.J. Larsen, A.R. Bausch, Soft Matter 4, 1675 (2008).

    Article  ADS  Google Scholar 

  24. 24.

    C.J. Cyron, W.A. Wall, Int. J. Num. Meth. Engin. 90, 955 (2012).

    MATH  MathSciNet  Google Scholar 

  25. 25.

    C.J. Cyron, K.W. Müller, A.R. Bausch, W.A. Wall, J. Comput. Phys. 244, 236 (2013).

    Article  ADS  MathSciNet  Google Scholar 

  26. 26.

    C.J. Cyron, K.W. Müller, K.M. Schmoller, A.R. Bausch, W.A. Wall et al., EPL 102, 38003 (2013).

    Article  ADS  Google Scholar 

  27. 27.

    K.W. Muller, R.F. Bruinsma, O. Lieleg, A.R. Bausch, W.A. Wall et al., Phys. Rev. Lett. 112, 238102 (2014).

    Article  ADS  Google Scholar 

  28. 28.

    C.J. Cyron, W.A. Wall, Phys. Rev. E 80, 066704 (2009).

    Article  ADS  Google Scholar 

  29. 29.

    C.J. Cyron, W.A. Wall, Phys. Rev. E 82, 066705 (2010).

    Article  ADS  Google Scholar 

  30. 30.

    G.I. Bell, Science 200, 618 (1978).

    Article  ADS  Google Scholar 

  31. 31.

    O. Lieleg, M. Claessens, C. Heussinger, E. Frey, A.R. Bausch, Phys. Rev. Lett. 99, 088102 (2007).

    Article  ADS  Google Scholar 

  32. 32.

    O. Lieleg, A.R. Bausch, Phys. Rev. Lett. 99, 158105 (2007).

    Article  ADS  Google Scholar 

  33. 33.

    R. Tharmann, M. Claessens, A.R. Bausch, Phys. Rev. Lett. 98, 088103 (2007).

    Article  ADS  Google Scholar 

  34. 34.

    O. Lieleg, K.M. Schmoller, M.M.A.E. Claessens, A.R. Bausch, Biophys. J. 96, 4725 (2009).

    Article  ADS  Google Scholar 

  35. 35.

    C. Heussinger, M. Bathe, E. Frey, Phys. Rev. Lett. 99, 048101 (2007).

    Article  ADS  Google Scholar 

  36. 36.

    L. Wolff, K. Kroy, Phys. Rev. E 86, 040901 (2012).

    Article  ADS  Google Scholar 

  37. 37.

    L. Wolff, P. Fernandez, K. Kroy, Plos One 7, e40063 (2012).

    Article  ADS  Google Scholar 

  38. 38.

    C. Heussinger, New J. Phys. 14, 095029 (2012).

    Article  ADS  Google Scholar 

  39. 39.

    C. Heussinger, E. Frey, Phys. Rev. Lett. 97, 105501 (2006).

    Article  ADS  Google Scholar 

  40. 40.

    S.M. Ward, A. Weins, M.R. Pollak, D.A. Weitz, Biophys. J. 95, 4915 (2008).

    Article  ADS  Google Scholar 

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Correspondence to O. Lieleg.

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Maier, M., Müller, K.W., Heussinger, C. et al. A single charge in the actin binding domain of fascin can independently tune the linear and non-linear response of an actin bundle network. Eur. Phys. J. E 38, 50 (2015). https://doi.org/10.1140/epje/i2015-15050-3

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Keywords

  • Soft Matter: Polymers and Polyelectrolytes