Literature DB >> 29114058

Filament rigidity and connectivity tune the deformation modes of active biopolymer networks.

Samantha Stam1,2, Simon L Freedman3,4, Shiladitya Banerjee3,5,6, Kimberly L Weirich3, Aaron R Dinner2,3,7, Margaret L Gardel8,3,4.   

Abstract

Molecular motors embedded within collections of actin and microtubule filaments underlie the dynamics of cytoskeletal assemblies. Understanding the physics of such motor-filament materials is critical to developing a physical model of the cytoskeleton and designing biomimetic active materials. Here, we demonstrate through experiments and simulations that the rigidity and connectivity of filaments in active biopolymer networks regulates the anisotropy and the length scale of the underlying deformations, yielding materials with variable contractility. We find that semiflexible filaments can be compressed and bent by motor stresses, yielding materials that undergo predominantly biaxial deformations. By contrast, rigid filament bundles slide without bending under motor stress, yielding materials that undergo predominantly uniaxial deformations. Networks dominated by biaxial deformations are robustly contractile over a wide range of connectivities, while networks dominated by uniaxial deformations can be tuned from extensile to contractile through cross-linking. These results identify physical parameters that control the forces generated within motor-filament arrays and provide insight into the self-organization and mechanics of cytoskeletal assemblies.

Entities:  

Keywords:  actin; active matter; agent-based simulation; mechanics; myosin

Mesh:

Substances:

Year:  2017        PMID: 29114058      PMCID: PMC5703288          DOI: 10.1073/pnas.1708625114

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  55 in total

1.  Purified kinesin promotes vesicle motility and induces active sliding between microtubules in vitro.

Authors:  R Urrutia; M A McNiven; J P Albanesi; D B Murphy; B Kachar
Journal:  Proc Natl Acad Sci U S A       Date:  1991-08-01       Impact factor: 11.205

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3.  Active multistage coarsening of actin networks driven by myosin motors.

Authors:  Marina Soares e Silva; Martin Depken; Björn Stuhrmann; Marijn Korsten; Fred C MacKintosh; Gijsje H Koenderink
Journal:  Proc Natl Acad Sci U S A       Date:  2011-05-18       Impact factor: 11.205

4.  Contractility in an extensile system.

Authors:  Kasimira T Stanhope; Vikrant Yadav; Christian D Santangelo; Jennifer L Ross
Journal:  Soft Matter       Date:  2017-06-14       Impact factor: 3.679

5.  Preparation of myosin and its subfragments from rabbit skeletal muscle.

Authors:  S S Margossian; S Lowey
Journal:  Methods Enzymol       Date:  1982       Impact factor: 1.600

6.  Structure of macrophage actin-binding protein molecules in solution and interacting with actin filaments.

Authors:  J H Hartwig; T P Stossel
Journal:  J Mol Biol       Date:  1981-01-25       Impact factor: 5.469

7.  Epithelial rotation promotes the global alignment of contractile actin bundles during Drosophila egg chamber elongation.

Authors:  Maureen Cetera; Guillermina R Ramirez-San Juan; Patrick W Oakes; Lindsay Lewellyn; Michael J Fairchild; Guy Tanentzapf; Margaret L Gardel; Sally Horne-Badovinac
Journal:  Nat Commun       Date:  2014-11-21       Impact factor: 14.919

8.  Myosin motors fragment and compact membrane-bound actin filaments.

Authors:  Sven K Vogel; Zdenek Petrasek; Fabian Heinemann; Petra Schwille
Journal:  Elife       Date:  2013-01-08       Impact factor: 8.140

9.  Non-sarcomeric mode of myosin II organization in the fibroblast lamellum.

Authors:  A B Verkhovsky; G G Borisy
Journal:  J Cell Biol       Date:  1993-11       Impact factor: 10.539

10.  Active contraction of microtubule networks.

Authors:  Peter J Foster; Sebastian Fürthauer; Michael J Shelley; Daniel J Needleman
Journal:  Elife       Date:  2015-12-23       Impact factor: 8.140

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  22 in total

Review 1.  From isolated structures to continuous networks: A categorization of cytoskeleton-based motile engineered biological microstructures.

Authors:  Rachel Andorfer; Joshua D Alper
Journal:  Wiley Interdiscip Rev Nanomed Nanobiotechnol       Date:  2019-02-11

2.  Self-organizing motors divide active liquid droplets.

Authors:  Kimberly L Weirich; Kinjal Dasbiswas; Thomas A Witten; Suriyanarayanan Vaikuntanathan; Margaret L Gardel
Journal:  Proc Natl Acad Sci U S A       Date:  2019-05-21       Impact factor: 11.205

3.  A Versatile Framework for Simulating the Dynamic Mechanical Structure of Cytoskeletal Networks.

Authors:  Simon L Freedman; Shiladitya Banerjee; Glen M Hocky; Aaron R Dinner
Journal:  Biophys J       Date:  2017-07-25       Impact factor: 4.033

4.  The actin filament bundling protein α-actinin-4 actually suppresses actin stress fibers by permitting actin turnover.

Authors:  James Peter Kemp; William M Brieher
Journal:  J Biol Chem       Date:  2018-07-26       Impact factor: 5.157

5.  Assembly of a persistent apical actin network by the formin Frl/Fmnl tunes epithelial cell deformability.

Authors:  Benoit Dehapiot; Raphaël Clément; Hervé Alégot; Gabriella Gazsó-Gerhát; Jean-Marc Philippe; Thomas Lecuit
Journal:  Nat Cell Biol       Date:  2020-06-01       Impact factor: 28.824

6.  Interplay of structure, elasticity, and dynamics in actin-based nematic materials.

Authors:  Rui Zhang; Nitin Kumar; Jennifer L Ross; Margaret L Gardel; Juan J de Pablo
Journal:  Proc Natl Acad Sci U S A       Date:  2017-12-28       Impact factor: 11.205

7.  The Actin Cytoskeleton as an Active Adaptive Material.

Authors:  Shiladitya Banerjee; Margaret L Gardel; Ulrich S Schwarz
Journal:  Annu Rev Condens Matter Phys       Date:  2019-12-06       Impact factor: 16.109

Review 8.  Balancing forces in migration.

Authors:  Patrick W Oakes
Journal:  Curr Opin Cell Biol       Date:  2018-05-23       Impact factor: 8.382

9.  Nonequilibrium phase diagrams for actomyosin networks.

Authors:  Simon L Freedman; Glen M Hocky; Shiladitya Banerjee; Aaron R Dinner
Journal:  Soft Matter       Date:  2018-09-26       Impact factor: 3.679

10.  Actin bundle architecture and mechanics regulate myosin II force generation.

Authors:  Kimberly L Weirich; Samantha Stam; Edwin Munro; Margaret L Gardel
Journal:  Biophys J       Date:  2021-03-31       Impact factor: 4.033

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