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.
Graphical abstract
References
A.J. Ridley, Cell 145, 1012 (2011).
D.A. Head, A.J. Levine, F.C. MacKintosh, Phys. Rev. E 68, 061907 (2003).
K.E. Kasza, A.C. Rowat, J.Y. Liu, T.E. Angelini, C.P. Brangwynne et al., Curr. Opin. Cell Biol. 19, 101 (2007).
K.E. Kasza, G.H. Koenderink, Y.C. Lin, C.P. Broedersz, W. Messner et al., Phys. Rev. E 79, 041928 (2009).
O. Lieleg, M.M.A.E. Claessens, A.R. Bausch, Soft Matter 6, 218 (2010).
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).
J. Faix, K. Rottner, Curr. Opin. Cell Biol. 18, 18 (2006).
P.K. Mattila, P. Lappalainen, Nat. Rev. Mol. Cell Biology 9, 446 (2008).
M. Claessens, M. Bathe, E. Frey, A.R. Bausch, Nat. Mater. 5, 748 (2006).
M. Claessens, C. Semmrich, L. Ramos, A.R. Bausch, Proc. Natl. Acad. Sci. U.S.A. 105, 8819 (2008).
Y.S. Aratyn, T.E. Schaus, E.W. Taylor, G.G. Borisy, Mol. Biol. Cell 18, 3928 (2007).
N. Kureishy, V. Sapountzi, S. Prag, N. Anilkumar, J.C. Adams, BioEssays 24, 350 (2002).
D. Vignjevic, M. Schoumacher, N. Gavert, K.P. Janssen, G. Jih et al., Cancer Res. 67, 6844 (2007).
A. Li, J.C. Dawson, M. Forero-Vargas, H.J. Spence, X.Z. Yu et al., Curr. Biol. 20, 339 (2010).
A.U. Jawhari, A. Buda, M. Jenkins, K. Shehzad, C. Sarraf et al., Am. J. Pathol. 162, 69 (2003).
J. Zanet, A. Jayo, S. Plaza, T. Millard, M. Parsons et al., J. Cell Biol. 197, 477 (2012).
S. Ono, Y. Yamakita, S. Yamashiro, P.T. Matsudaira, J.R. Gnarra et al., J. Biol. Chem. 272, 2527 (1997).
D. Vignjevic, S. Kojima, T. Svitkina, G.G. Borisy, J. Cell Biol. 174, 863 (2006).
S. Jansen, A. Collins, C.S. Yang, G. Rebowski, T. Svitkina et al., J. Biol. Chem. 286, 30087 (2011).
S.Y. Yang, F.K. Huang, J.Y. Huang, S. Chen, J. Jakoncic et al., J. Biol. Chem. 288, 274 (2013).
J.A. Spudich, S. Watt, J. Biol. Chem. 246, 4866 (1971).
D. Vignjevic, D. Yarar, M.D. Welch, J. Peloquin, T. Svitkina et al., J. Cell Biol. 160, 951 (2003).
C. Semmrich, R.J. Larsen, A.R. Bausch, Soft Matter 4, 1675 (2008).
C.J. Cyron, W.A. Wall, Int. J. Num. Meth. Engin. 90, 955 (2012).
C.J. Cyron, K.W. Müller, A.R. Bausch, W.A. Wall, J. Comput. Phys. 244, 236 (2013).
C.J. Cyron, K.W. Müller, K.M. Schmoller, A.R. Bausch, W.A. Wall et al., EPL 102, 38003 (2013).
K.W. Muller, R.F. Bruinsma, O. Lieleg, A.R. Bausch, W.A. Wall et al., Phys. Rev. Lett. 112, 238102 (2014).
C.J. Cyron, W.A. Wall, Phys. Rev. E 80, 066704 (2009).
C.J. Cyron, W.A. Wall, Phys. Rev. E 82, 066705 (2010).
G.I. Bell, Science 200, 618 (1978).
O. Lieleg, M. Claessens, C. Heussinger, E. Frey, A.R. Bausch, Phys. Rev. Lett. 99, 088102 (2007).
O. Lieleg, A.R. Bausch, Phys. Rev. Lett. 99, 158105 (2007).
R. Tharmann, M. Claessens, A.R. Bausch, Phys. Rev. Lett. 98, 088103 (2007).
O. Lieleg, K.M. Schmoller, M.M.A.E. Claessens, A.R. Bausch, Biophys. J. 96, 4725 (2009).
C. Heussinger, M. Bathe, E. Frey, Phys. Rev. Lett. 99, 048101 (2007).
L. Wolff, K. Kroy, Phys. Rev. E 86, 040901 (2012).
L. Wolff, P. Fernandez, K. Kroy, Plos One 7, e40063 (2012).
C. Heussinger, New J. Phys. 14, 095029 (2012).
C. Heussinger, E. Frey, Phys. Rev. Lett. 97, 105501 (2006).
S.M. Ward, A. Weins, M.R. Pollak, D.A. Weitz, Biophys. J. 95, 4915 (2008).
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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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DOI: https://doi.org/10.1140/epje/i2015-15050-3
Keywords
- Soft Matter: Polymers and Polyelectrolytes