Direct detection of deformation modes on varying length scales in active biopolymer networks

Correlated flows and forces that emerge from active matter orchestrate complex processes such as shape regulation and deformations in biological cells and tissues. The active materials central to cellular mechanics are cytoskeletal networks, where molecular motor activity drives deformations and remodeling. Here, we investigate deformation modes in actin networks driven by the molecular motor myosin II through quantitative fluorescence microscopy. We examine the deformation anisotropy at different length scales in networks of entangled, cross-linked, and bundled actin. In sparsely cross-linked networks, we find myosin-dependent biaxial buckling modes across length scales. In cross-linked bundled networks, uniaxial contraction is predominate on long length scales, while the uniaxial or biaxial nature of the deformation depends on bundle microstructure at shorter length scales. The anisotropy of deformations may provide insight to regulation of collective behavior in a variety of active materials.

[1]  J. Guan,et al.  Light-activated mitochondrial fission through optogenetic control of mitochondria-lysosome contacts , 2022, Nature Communications.

[2]  D. B. Brückner,et al.  3D printed protein-based robotic structures actuated by molecular motor assemblies , 2022, Nature Materials.

[3]  Chih-Cheng Chen,et al.  Force From Filaments: The Role of the Cytoskeleton and Extracellular Matrix in the Gating of Mechanosensitive Channels , 2022, Frontiers in Cell and Developmental Biology.

[4]  A. Bausch,et al.  Pattern formation and polarity sorting of driven actin filaments on lipid membranes , 2021, Proceedings of the National Academy of Sciences.

[5]  Maria Bohnert Tether Me, Tether Me Not-Dynamic Organelle Contact Sites in Metabolic Rewiring. , 2020, Developmental cell.

[6]  E. Munro,et al.  Actin bundle architecture and mechanics regulate myosin II force generation , 2020, bioRxiv.

[7]  M. Gardel,et al.  The Actin Cytoskeleton as an Active Adaptive Material. , 2020, Annual review of condensed matter physics.

[8]  I. Aranson,et al.  The 2020 motile active matter roadmap , 2019, Journal of physics. Condensed matter : an Institute of Physics journal.

[9]  F. Nédélec,et al.  Polarity sorting drives remodeling of actin-myosin networks , 2018, Journal of Cell Science.

[10]  M. Gardel,et al.  Tunable structure and dynamics of active liquid crystals , 2018, Science Advances.

[11]  Yusuke Hirabayashi,et al.  Optogenetic Control of Endoplasmic Reticulum-Mitochondria Tethering. , 2017, ACS synthetic biology.

[12]  M. Gardel,et al.  Filament rigidity and connectivity tune the deformation modes of active biopolymer networks , 2017, Proceedings of the National Academy of Sciences.

[13]  M. Leptin,et al.  A theory that predicts behaviors of disordered cytoskeletal networks , 2017, bioRxiv.

[14]  C. Santangelo,et al.  Contractility in an extensile system. , 2017, Soft matter.

[15]  Suriyanarayanan Vaikuntanathan,et al.  Liquid behavior of cross-linked actin bundles , 2017, Proceedings of the National Academy of Sciences.

[16]  F. Nédélec,et al.  Architecture and Connectivity Govern Actin Network Contractility , 2016, Current Biology.

[17]  M. Betterton,et al.  Microscopic origins of anisotropic active stress in motor-driven nematic liquid crystals. , 2016, Soft matter.

[18]  C. Broedersz,et al.  Fiber networks amplify active stress , 2015, Proceedings of the National Academy of Sciences.

[19]  P. Reddy,et al.  Mitochondrial division and fusion in metabolism. , 2015, Current opinion in cell biology.

[20]  Margaret L. Gardel,et al.  Actomyosin sliding is attenuated in contractile biomimetic cortices , 2014, Molecular biology of the cell.

[21]  S. Ramaswamy,et al.  Hydrodynamics of soft active matter , 2013 .

[22]  M. Gardel,et al.  F-actin buckling coordinates contractility and severing in a biomimetic actomyosin cortex , 2012, Proceedings of the National Academy of Sciences.

[23]  Daniel T. N. Chen,et al.  Spontaneous motion in hierarchically assembled active matter , 2012, Nature.

[24]  Matthew West,et al.  ER Tubules Mark Sites of Mitochondrial Division , 2011, Science.

[25]  D. Kovar,et al.  Actin Filament Bundling by Fimbrin Is Important for Endocytosis, Cytokinesis, and Polarization in Fission Yeast* , 2011, The Journal of Biological Chemistry.

[26]  Fred C. MacKintosh,et al.  Active multistage coarsening of actin networks driven by myosin motors , 2011, Proceedings of the National Academy of Sciences.

[27]  A. Bausch,et al.  Structure formation in active networks. , 2011, Nature materials.

[28]  Erwin Frey,et al.  Polar patterns of driven filaments , 2010, Nature.

[29]  D. Kovar,et al.  Fimbrin and Tropomyosin Competition Regulates Endocytosis and Cytokinesis Kinetics in Fission Yeast , 2010, Current Biology.

[30]  J. Israelachvili,et al.  Bilayer edges catalyze supported lipid bilayer formation. , 2010, Biophysical journal.

[31]  M. C. Marchetti,et al.  Mechanical response of active gels , 2008, 0807.3031.

[32]  D Groswasser,et al.  Active gels : dynamics of patterning and self-organization , 2006 .

[33]  A. Ridley,et al.  Regulators and effectors of Small Gtpases: Rho Family , 2006 .

[34]  D. Ingber,et al.  Mechanical behavior in living cells consistent with the tensegrity model , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[35]  J. Bartles Parallel actin bundles and their multiple actin-bundling proteins. , 2000, Current opinion in cell biology.

[36]  E. Salmon,et al.  Actomyosin-based Retrograde Flow of Microtubules in the Lamella of Migrating Epithelial Cells Influences Microtubule Dynamic Instability and Turnover and Is Associated with Microtubule Breakage and Treadmilling , 1997, The Journal of cell biology.

[37]  S. Leibler,et al.  Self-organization of microtubules and motors , 1997, Nature.

[38]  G. Borisy,et al.  Non-sarcomeric mode of myosin II organization in the fibroblast lamellum , 1993, The Journal of cell biology.

[39]  D. Murphy,et al.  Purified kinesin promotes vesicle motility and induces active sliding between microtubules in vitro. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[40]  S. Lowey,et al.  Preparation of myosin and its subfragments from rabbit skeletal muscle. , 1982, Methods in enzymology.

[41]  J. Cooper,et al.  Preparation of smooth muscle alpha-actinin. , 1982, Methods in enzymology.

[42]  A. Bretscher Fimbrin is a cytoskeletal protein that crosslinks F-actin in vitro. , 1981, Proceedings of the National Academy of Sciences of the United States of America.