Geometrical origins of contractility in disordered actomyosin networks

Physical Review X

Volumn 4, Issue 4, 2014, Pages

  Lenz, Martin ^a  

^a UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

Biological physics; Complex systems

Indexed keywords

BUCKLING; LARGE SCALE SYSTEMS; MUSCLE; SCAFFOLDS (BIOLOGY);

ACTIN FILAMENT; BIOLOGICAL PHYSICS; CONTRACTILE FORCE; DISORDERED NETWORKS; EUKARYOTIC CELLS; LOCAL DEFORMATIONS; MYOSIN MOTORS; STRIATED MUSCLES;

PROTEINS;

EID: 84921501179     PISSN: None     EISSN: 21603308     Source Type: Journal    
DOI: 10.1103/PhysRevX.4.041002     Document Type: Article

References (37)

1. A. G. Szent-Györgyi, The Early History of the Biochemistry of Muscle Contraction, J. Gen. Physiol. 123, 631 (2004).
2. F. S. Fay, K. Fujiwara, D. D. Rees, and K. E. Fogarty, Distribution of Alpha-Actinin in Single Isolated Smooth Muscle Cells, J. Cell Biol. 96, 783 (1983).
3. L. P. Cramer, M. Siebert, and T. J. Mitchison, Identification of Novel Graded Polarity Actin Filament Bundles in Locomoting Heart Fibroblasts: Implications for the Generation of Motile Force, J. Cell Biol. 136, 1287 (1997).
4. A. Carvalho, A. Desai, and K. Oegema, Structural Memory in the Contractile Ring Makes the Duration of Cytokinesis Independent of Cell Size, Cell 137, 926 (2009).
5. O. Medalia, I. Weber, A. S. Frangakis, D. Nicastro, G. Gerisch, and W. Baumeister, Macromolecular Architecture in Eukaryotic Cells Visualized by Cryoelectron Tomography, Science 298, 1209 (2002).
6. A. B. Verkhovsky, T. M. Svitkina, and G. G. Borisy, Myosin II Filament Assemblies in the Active Lamella of Fibroblasts: Their Morphogenesis and Role in the Formation of Actin Filament Bundles, J. Cell Biol. 131, 989 (1995).
7. Y. Aratyn-Schaus, P.W. Oakes, and M. L. Gardel, Dynamic and Structural Signatures of Lamellar Actomyosin Force Generation, Mol. Biol. Cell 22, 1330 (2011).
8. G. Salbreux, G. Charras, and E. Paluch, Actin Cortex Mechanics and Cellular Morphogenesis, Trends Cell Biol. 22, 536 (2012).
9. J.-F. Joanny and J. Prost, Active Gels as a Description of the Actin-Myosin Cytoskeleton, HFSP J. 3, 94 (2009).
10. F. C. MacKintosh and A. J. Levine, Nonequilibrium Mechanics and Dynamics of Motor-Activated Gels, Phys. Rev. Lett. 100, 018104 (2008).
11. T. Thoresen, M. Lenz, and M. L. Gardel, Reconstitution of Contractile Actomyosin Bundles, Biophys. J. 100, 2698 (2011).
12. M. Lenz, M. L. Gardel, and A. R. Dinner, Requirements for Contractility in Disordered Cytoskeletal Bundles, New J. Phys. 14, 033037 (2012).
13. M. Lenz, T. Thoresen, M. L. Gardel, and A. R. Dinner, Contractile Units in Disordered Actomyosin Bundles Arise from F-Actin Buckling, Phys. Rev. Lett. 108, 238107 (2012).
14. M. Murrell and M. L. Gardel, F-Actin Buckling Coordinates Contractility and Severing in a Biomimetic Actomyosin Cortex, Proc. Natl. Acad. Sci. U.S.A. 109, 20 820 (2012).
15. P. M. Bendix, G. H. Koenderink, D. Cuvelier, Z. Dogic, B. N. Koeleman, W. M. Brieher, C.M. Field, L. Mahadevan, and D. A. Weitz, A Quantitative Analysis of Contractility in Active Cytoskeletal Protein Networks, Biophys. J. 94, 3126 (2008).
16. M. Soares e Silva, M. Depken, B. Stuhrmann, M. Korsten, F. C. Mackintosh, and G. H. Koenderink, Active Multistage Coarsening of Actin Networks Driven by Myosin Motors, Proc. Natl. Acad. Sci. U.S.A. 108, 9408 (2011).
17. D. Mizuno, C. Tardin, C. F. Schmidt, and F. C. Mackintosh, Nonequilibrium Mechanics of Active Cytoskeletal Networks, Science 315, 370 (2007).
18. N. L. Dasanayake, P. J. Michalski, and A. E. Carlsson, General Mechanism of Actomyosin Contractility, Phys. Rev. Lett. 107, 118101 (2011).
19. T. B. Liverpool and M. C. Marchetti, Bridging the Microscopic and the Hydrodynamic in Active Filament Solutions, Europhys. Lett. 69, 846 (2005).
20. See Supplemental Material at http://link.aps.org/supplemental/10.1103/PhysRevX.4.041002 for detailed mathematical derivations.
21. T. Sanchez, D. T. N. Chen, S. J. DeCamp, M. Heymann, and Z. Dogic, Spontaneous Motion in Hierarchically Assembled Active Matter, Nature (London) 491, 431 (2012).
22. A.-C. Reymann, R. Boujemaa-Paterski, J.-L. Martiel, C. Guérin, W. Cao, H. F Chin, E. M. De La Cruz, M. Théry, and L. Blanchoin, Actin Network Architecture Can Determine Myosin Motor Activity, Science 336, 1310 (2012).
23. K. Kruse and F. Jülicher, Actively Contracting Bundles of Polar Filaments, Phys. Rev. Lett. 85, 1778 (2000).
24. K. Kruse and F. Jülicher, Self-Organization and Mechanical Properties of Active Filament Bundles, Phys. Rev. E 67, 051913 (2003).
25. To understand this decrease in the stall force, consider that the motor has a position-dependent force-velocity relationship. At any given position, motor velocity decreases with increasing opposing force. In the middle of the filament, the velocity in the absence of force is substantial, and correspondingly the stall force is significantly larger than zero. As the barbed end of the filament is approached, the velocity at zero force vanishes, implying that the motor's stall force goes to zero.
26. T. Odijk, Stiff Chains and Filaments under Tension, Macromolecules 28, 7016 (1995).
27. The assumption of entropic elasticity is justified for filaments subjected to forces much smaller than their buckling force, which is implicit in the rigid filament assumption used here.
28. T. B. Liverpool, M. C. Marchetti, J.-F. Joanny, and J. Prost, Mechanical Response of Active Gels, Europhys. Lett. 85, 18007 (2009).
29. T. Thoresen, M. Lenz, and M. L. Gardel, Thick Filament Regulation of Contractility in Self-Organized Actomyosin Bundles, Biophys. J. 104, 655 (2013).
30. H. Kojima, A. Ishijima, and T. Yanagida, Direct Measurement of Stiffness of Single Actin Filaments with and without Tropomyosin by In Vitro Nanomanipulation, Proc. Natl. Acad. Sci. U.S.A. 91, 12962 (1994).
31. S. S. Rosenfeld, J. Xing, L.-Q. Chen, and H. Lee Sweeney, Myosin IIB Is Unconventionally Conventional, J. Biol. Chem. 278, 27449 (2003).
32. G. H. Koenderink, Z. Dogic, F. Nakamura, P. M. Bendix, F. C. MacKintosh, J. H. Hartwig, T. P. Stossel, and D. A. Weitz, An Active Biopolymer Network Controlled by Molecular Motors, Proc. Natl. Acad. Sci. U.S.A. 106, 15192 (2009).
33. J. Alvarado, M. Sheinman, A. Sharma, F. C. MacKintosh, and G. H. Koenderink, Molecular Motors Robustly Drive Active Gels to a Critically Connected State, Nat. Phys. 9, 591 (2013).
34. 2/5, with the actin concentration c in units of mg/mL [36].
35. H. Isambert and A. C. Maggs, Dynamics and Rheology of Actin Solutions, Macromolecules 29, 1036 (1996).
36. N. L. Dasanayake and A. E. Carlsson, Stress Generation by Myosin Minifilaments in Actin Bundles, Phys. Biol. 10, 036006 (2013).
37. T. T. Falzone, M. Lenz, D. R. Kovar, and M. L. Gardel, Assembly Kinetics Determine the Architecture of a-Actinin Crosslinked F-Actin Networks, Nat. Commun. 3, 861 (2012).