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Molecular motors robustly drive active gels to a critically connected state

Abstract

Living systems naturally exhibit internal driving: active, molecular processes drive non-equilibrium phenomena such as metabolism or migration. Active gels constitute a fascinating class of internally driven matter, in which molecular motors exert localized stresses inside polymer networks. There is evidence that network crosslinking is required to allow motors to induce macroscopic contraction. Yet a quantitative understanding of how network connectivity enables contraction is lacking. Here we show experimentally that myosin motors contract crosslinked actin polymer networks to clusters with a scale-free size distribution. This critical behaviour occurs over an unexpectedly broad range of crosslink concentrations. To understand this robustness, we developed a quantitative model of contractile networks that takes into account network restructuring: motors reduce connectivity by forcing crosslinks to unbind. Paradoxically, to coordinate global contractions, motor activity should be low. Otherwise, motors drive initially well-connected networks to a critical state where ruptures form across the entire network.

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Figure 1: Experiments with motor-driven networks show that initial connectivity controls the length scale of contraction.
Figure 2: Cluster size distributions depend on network connectivity, exhibiting power-law distributions when ξ1ξ2L.
Figure 3: Simulations show that motors can drive initially well-connected networks to a critical state.
Figure 4: Simulation and experiment both show that increased motor force reduces cluster size.
Figure 5: The critically connected regime broadens with increasing force.

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Acknowledgements

This work is part of the research programme of the Foundation for Fundamental Research on Matter (FOM), which is part of the Netherlands Organisation for Scientific Research (NWO). G.H.K. and J.A. were funded by a Vidi grant from the Netherlands Organisation for Scientific Research (NWO). We thank M. Kuit-Vinkenoog, M. Preciado-López and F. C. Tsai (AMOLF, Amsterdam, Netherlands) for help with purifications, S. Hansen and R. D. Mullins (UCSF, San Francisco, USA) for the fascin plasmid, K. Miura (EMBL, Heidelberg, Germany) for the Temporal Colour Code ImageJ plugin, as well as C. Broedersz (Princeton University, NJ, USA) and M.A.J. Michels (TU Eindhoven) for insightful discussions.

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J.A. and G.H.K. designed the experiments. J.A. performed the experiments. M.S., A.S., and F.C.M. designed the simulations. M.S. and A.S. performed the simulations. All authors contributed to the writing of the paper.

Corresponding authors

Correspondence to Fred C. MacKintosh or Gijsje H. Koenderink.

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The authors declare no competing financial interests.

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Alvarado, J., Sheinman, M., Sharma, A. et al. Molecular motors robustly drive active gels to a critically connected state. Nature Phys 9, 591–597 (2013). https://doi.org/10.1038/nphys2715

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