Active multistage coarsening of actin networks driven by myosin motors

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 23, 2011, Pages 9408-9413

  Soares E Silva, Marina ^a   Depken, Martin ^b   Stuhrmann, Björn ^a   Korsten, Marijn ^a   MacKintosh, Fred C ^b   Koenderink, Gijsje H ^a  

^a FOM INSTITUTE AMOLF   (Netherlands)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

Active gels; Molecular motors; Nonequilibrium; Soft condensed matter

Indexed keywords

ACTIN; F ACTIN; KINESIN; MYOSIN; MYOSIN ADENOSINE TRIPHOSPHATASE;

ACTIN FILAMENT; ARTICLE; BIOCHEMISTRY; FORCE; MICROTUBULE; MOLECULAR DYNAMICS; MOTOR ACTIVITY; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; REGULATORY MECHANISM; TENSION;

ACTINS; ACTOMYOSIN; ALGORITHMS; ANIMALS; CELL MOVEMENT; HUMANS; MICROFILAMENTS; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; MODELS, CHEMICAL; MUSCLE CONTRACTION; MYOSINS;

EID: 79959370905     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1016616108     Document Type: Article

References (54)

1. Howard J (2001) Mechanics of Motor Proteins and the Cytoskeleton (Sinauer, Sunderland, MA).
2. Karsenti E, Vernos I (2001) The mitotic spindle: A self-made machine. Science 294:543-547.
3. Vavylonis D, Wu J, Hao S, O'Shaughnessy B, Pollard T (2008) Assembly mechanism of the contractile ring for cytokinesis by fission yeast. Science 319:97-100.
4. Moores S, Sabry J, Spudich J (1996) Myosin dynamics in live Dictyostelium cells. Proc Natl Acad Sci USA 93:443-446. (Pubitemid 26038173)
5. Hird S, White J (1993) Cortical and cytoplasmic flow polarity in early embryonic cells of Caenorhabditis elegans. J Cell Biol 121:1343-1355. (Pubitemid 23174551)
6. Mayer M, Depken M, Bois JS, Julicher F, Grill SW (2010) Anisotropies in cortical tension reveal the physical basis of polarizing cortical flows. Nature 467:617-621.
7. Surrey T, Nedelec F, Leibler S, Karsenti E (2001) Physical properties determining self-organization of motors and microtubules. Science 292:1167-1171. (Pubitemid 32440939)
8. Nédélec FJ, Surrey T, Maggs AC, Leibler S (1997) Self-organization of microtubules and motors. Nature 389:305-308. (Pubitemid 27406647)
9. Hentrich C, Surrey T (2010) Microtubule organization by the antagonistic mitotic motors kinesin-5 and kinesin-14. J Cell Biol 189:465-480.
10. Urrutia R, McNiven MA, Albanesi JP, Murphy DB, Kachar B (1991) Purified kinesin promotes vesicle motility and induces active sliding between microtubules in vitro. Proc Natl Acad Sci USA 88:6701-6705. (Pubitemid 21915017)
11. Karsenti E, Nédélec F, Surrey T (2006) Modelling microtubule patterns. Nat Cell Biol 8:1204-1211. (Pubitemid 44660582)
12. Humphrey D, Duggan C, Saha D, Smith D, Kas J (2002) Active fluidization of polymer networks through molecular motors. Nature 416:413-416. (Pubitemid 34272872)
13. Smith D, et al. (2007) Molecular motor-induced instabilities and cross-linkers determine biopolymer organization. Biophys J 93:4445-4452. (Pubitemid 350294490)
14. Koenderink GH, et al. (2009) An active biopolymer network controlled by molecular motors. Proc Natl Acad Sci USA 106:15192-15197.
15. Janson E, Kolega J, Taylor D (1991) Modulation of contraction by gelation/solation in a reconstituted motile model. J Cell Biol 114:1005-1015. (Pubitemid 21909863)
16. Mizuno D, Tardin C, Schmidt CF, MacKintosh FC (2007) Nonequilibrium mechanics of active cytoskeletal networks. Science 315:370-373. (Pubitemid 46175516)
17. Bendix PM, et al. (2008) A quantitative analysis of contractility in active cytoskeletal protein networks. Biophys J 94:3126-3136.
18. Strzelecka-Golas Zewska H, Piwowar U, Pliszka B (1981) Changes in the ultrastructure of actomyosin gel during hydrolysis of ATP under various ionic conditions. Eur J Cell Biol 24:116-123. (Pubitemid 11070748)
19. DeBiasio R, LaRocca G, Post P, Taylor D (1996) Myosin II transport, organization, and phosphorylation: Evidence for cortical flow/solation- contraction coupling during cytokinesis and cell locomotion. Mol Biol Cell 7:1259-82. (Pubitemid 26260742)
20. Werner M, Munro E, Glotzer M (2007) Astral signals spatially bias cortical myosin recruitment to break symmetry and promote cytokinesis. Curr Biol 17:1286-1297. (Pubitemid 47176895)
21. Verkhovsky A, Svitkina T, Borisy G (1995) Myosin II filament assemblies in the active lamella of fibroblasts: their morphogenesis and role in the formation of actin filament bundles. J Cell Biol 131:989-1002.
22. Verkhovsky A, Borisy G (1993) Non-sarcomeric mode of myosin II organization in the fibroblast lamellum. J Cell Biol 123:637-652. (Pubitemid 23324921)
23. Mandato C, Bement W (2001) Contraction and polymerization cooperate to assemble and close actomyosin rings around Xenopus oocyte wounds. J Cell Biol 154:785-797. (Pubitemid 34292960)
24. Blanchard GB, Murugesu S, Adams RJ, Martinez-Arias A, Gorfinkiel N (2010) Cytoskeletal dynamics and supracellular organisation of cell shape fluctuations during dorsal closure. Development 137:2743-2752.
25. Franke J, Montague R, Kiehart D (2005) Nonmuscle myosin II generates forces that transmit tension and drive contraction in multiple tissues during dorsal closure. Curr Biol 15:2208-2221. (Pubitemid 41790614)
26. Martin A, Kaschube M, Wieschaus E (2008) Pulsed contractions of an actin-myosin network drive apical constriction. Nature 457:495-499.
27. Rauzi M, Verant P, Lecuit T, Lenne P (2008) Nature and anisotropy of cortical forces orienting Drosophila tissue morphogenesis. Nat Cell Biol 10:1401-1410.
28. Astrom JA, Kumar PBS, Karttunen M (2009) Aster formation and rupture transition in semi-flexible fiber networks with mobile cross-linkers. Soft Matter 5:2869-2874.
29. Kruse K, Joanny J, Julicher F, Prost J, Sekimoto K (2004) Asters, vortices, and rotating spirals in active gels of polar filaments. Phys Rev Lett 92:078101.
30. Ziebert F, Zimmermann W (2005) Nonlinear competition between asters and stripes in filament-motor systems. Eur Phys J E Soft Matter 18:41-54. (Pubitemid 41442651)
31. Lee H, Kardar M (2001) Macroscopic equations for pattern formation in mixtures of microtubules and molecular motors. Phys Rev E Stat Nonlin Soft Matter Phys 64:056113.
32. Gittes F, Mickey B, Nettleton J, Howard J (1993) Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape. J Cell Biol 120:923-934. (Pubitemid 23056298)
33. Vicente-Manzanares M, Ma X, Adelstein RS, Horwitz AR (2009) Non-muscle myosin II takes center stage in cell adhesion and migration. Nat Rev Mol Cell Biol 10:778-790.
34. Footer MJ, Kerssemakers JWJ, Theriot JA, Dogterom M (2007) Direct measurement of force generation by actin filament polymerization using an optical trap. Proc Natl Acad Sci USA 104:2181-2186. (Pubitemid 46391372)
35. MacKintosh F, Levine A (2008) Nonequilibrium mechanics and dynamics of motor-activated gels. Phys Rev Lett 100:018104.
36. Kruse K, Julicher F (2003) Self-organization and mechanical properties of active filament bundles. Phys Rev E Stat Nonlin Soft Matter Phys 67:051913.
37. Lau A, Hoffmann B, Davies A, Crocker J, Lubensky T (2003) Microrheology, stress fluctuations, and active behavior of living cells. Phys Rev Lett 91:198101-198104.
38. Huxley H (1963) Electron microscope studies on the structure of natural and synthetic protein filaments from striated muscle. J Mol Biol 7:281-308.
39. Pepe F, Drucker B (1979) The myosin filament. VI. Myosin content. J Mol Biol 130:379-393. (Pubitemid 9210674)
40. Backouche F, Haviv L, Groswasser D, Bernheim-Groswasser A (2006) Active gels: Dynamics of patterning and self-organization. Phys Biol 3:264-273. (Pubitemid 46646257)
41. Brangwynne C, Koenderink G, Mackintosh F, Weitz D (2008) Nonequilibrium microtubule fluctuations in a model cytoskeleton. Phys Rev Lett 100:118104.
42. Schaller V, Weber C, Semmrich C, Frey E, Bausch AR (2010) Polar patterns of driven filaments. Nature 467:73-77.
43. Sankararaman S, Menon G, Kumar P (2004) Self-organized pattern formation in motor-microtubule mixtures. Phys Rev E Stat Nonlin Soft Matter Phys 70:031905.
44. Eisenberg M, Guy R (1979) A proof of the hairy ball theorem. Am Math Mon 86:571-574.
45. Liverpool T, Marchetti M (2003) Instabilities of isotropic solutions of active polar filaments. Phys Rev Lett 90:138102.
46. Verkhovsky A, Svitkina T, Borisy G (1997) Polarity sorting of actin filaments in cytochalasin-treated fibroblasts. J Cell Sci 110:1693-1704. (Pubitemid 27352849)
47. Tan JL, Ravid S, Spudich JA (1992) Control of nonmuscle myosins by phosphorylation. Annu Rev Biochem 61:721-759.
48. Zhou M, Wang Y (2007) Distinct pathways for the early recruitment of myosin II and actin to the cytokinetic furrow. Mol Biol Cell 19:318-326. (Pubitemid 351186156)
49. Finer J, Simmons R, Spudich J (1994) Single myosin molecule mechanics: Piconewton forces and nanometre steps. Nature 368:113-119. (Pubitemid 24101520)
50. Kuhn JR, Pollard TD (2005) Real-time measurements of actin filament polymerization by total internal reflection fluorescence microscopy. Biophys J 88:1387-1402. (Pubitemid 40975966)
51. Pantaloni D, Clainche CL, Carlier M (2001) Mechanism of actin-based motility. Science 292:1502-1506. (Pubitemid 32493411)
52. Reichl EM, et al. (2008) Interactions between myosin and actin cross-linkers control cytokinesis contractility dynamics and mechanics. Curr Biol 18:471-480.
53. Wilson CA, et al. (2010) Myosin II contributes to cell-scale actin network treadmilling through network disassembly. Nature 465:373-377.
54. Carvalho A, Desai A, Oegema K (2009) Structural memory in the contractile ring makes the duration of cytokinesis independent of cell size. Cell 137:926-937.