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      Filament Nucleation Tunes Mechanical Memory in Active Polymer Networks

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          Abstract

          Incorporating growth into contemporary material functionality presents a grand challenge in materials design. The F-actin cytoskeleton is an active polymer network which serves as the mechanical scaffolding for eukaryotic cells, growing and remodeling in order to determine changes in cell shape. Nucleated from the membrane, filaments polymerize and grow into a dense network whose dynamics of assembly and disassembly, or ‘turnover’, coordinates both fluidity and rigidity. Here, we vary the extent of F-actin nucleation from a membrane surface in a biomimetic model of the cytoskeleton constructed from purified protein. We find that nucleation of F-actin mediates the accumulation and dissipation of polymerization-induced F-actin bending energy. At high and low nucleation, bending energies are low and easily relaxed yielding an isotropic material. However, at an intermediate critical nucleation, stresses are not relaxed by turnover and the internal energy accumulates 100-fold. In this case, high filament curvatures template further assembly of F-actin, driving the formation and stabilization of vortex-like topological defects. Thus, nucleation coordinates mechanical and chemical timescales to encode shape memory into active materials.

          Graphical Abstract

          Structural and mechanical properties of reconstituted networks of protein polymers can be tuned by varying the amount of actin nucleator. Small and large concentrations of nucleators produce networks that relax easily, but at intermediate level of nucleation long lived topological defects are formed.

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          Author and article information

          Contributors
          Journal
          101190390
          34533
          Adv Funct Mater
          Adv Funct Mater
          Advanced functional materials
          1616-301X
          1616-3028
          8 May 2020
          25 September 2019
          5 December 2019
          05 December 2020
          : 29
          : 49
          : 1905243
          Affiliations
          Department of Biomedical Engineering, Yale University, 10 Hillhouse Avenue, New Haven, CT, USA
          Department of Physics and Astronomy, University College London, Gower Street, London WC1E 6BT, UK
          Department of Biomedical Engineering, Yale University, 10 Hillhouse Avenue, New Haven, CT, USA
          Department of Molecular Genetics and Cell Biology, The University of Chicago, 920 E. 58th St., CSLC 212, Chicago, IL, 60637, USA
          206 S Martin Jischke Drive, MJIS 3031, Weldon School of Biomedical Engineering, Purdue University ,West Lafayette, IN, USA
          Department of Physics and Astronomy, University College London, Gower Street, London WC1E 6BT, UK
          Systems Biology Institute, 850 West Campus Drive, West Haven, CT, USA
          Department of Biomedical Engineering, Yale University, 10 Hillhouse Avenue, New Haven, CT, USA
          Department of Physics, Yale University, 217 Prospect Street, New Haven, CT, USA
          Author notes

          Author Contributions

          MM and DK designed and conceived the experimental work. DK provided reagents and supplies. VY developed and performed agent-based simulations. SB and DB developed the continuum model. MM, TK, VY, & APT analyzed the data. VY, SB, DB, and MM wrote the paper.

          Article
          PMC7286550 PMC7286550 7286550 nihpa1053023
          10.1002/adfm.201905243
          7286550
          32523502
          45059bba-e92b-41ed-8268-ad3f10783308
          History
          Categories
          Article

          nucleation,defects,turnover,memory,actin
          nucleation, defects, turnover, memory, actin

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