Force to divide: Structural and mechanical requirements for actomyosin ring contraction

Biophysical Journal

Volumn 105, Issue 3, 2013, Pages 547-554

  Mendes Pinto, Inês ^a   Rubinstein, Boris ^a   Li, Rong ^a,b  

^a STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MYOSIN ADENOSINE TRIPHOSPHATASE;

ANIMAL; ARTICLE; BIOMECHANICS; CELL DIVISION; CHEMISTRY; CYTOSKELETON; HUMAN; METABOLISM; MOTION; ULTRASTRUCTURE;

ACTOMYOSIN; ANIMALS; BIOMECHANICAL PHENOMENA; CELL DIVISION; CYTOSKELETON; HUMANS; MOTION;

EID: 84881422916     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2013.06.033     Document Type: Review

References (57)

1. R.A. Green, E. Paluch, and K. Oegema Cytokinesis in animal cells Annu. Rev. Cell Dev. Biol. 28 2012 29 58
2. M.K. Balasubramanian, E. Bi, and M. Glotzer Comparative analysis of cytokinesis in budding yeast, fission yeast and animal cells Curr. Biol. 14 2004 R806 R818
3. R. Rappaport Cell division: direct measurement of maximum tension exerted by furrow of echinoderm eggs Science 156 1967 1241 1243
4. T.E. Schroeder Cytokinesis: filaments in the cleavage furrow Exp. Cell Res. 53 1968 272 276
5. T.E. Schroeder The contractile ring. II. Determining its brief existence, volumetric changes, and vital role in cleaving Arbacia eggs J. Cell Biol. 53 1972 419 434
6. H.L. Sweeney, and A. Houdusse Structural and functional insights into the myosin motor mechanism Annu. Rev. Biophys 39 2010 539 557
7. Y.S. Kee, and D.N. Robinson Motor proteins: myosin mechanosensors Curr. Biol. 18 2008 R860 R862
8. C. Rüegg, and C. Veigel R.H. Fink Molecular motors: force and movement generated by single myosin II molecules News Physiol. Sci. 17 2002 213 218
9. J.E. Molloy, and J.E. Burns D.C. White Movement and force produced by a single myosin head Nature 378 1995 209 212
10. M. Kovács, and K. Thirumurugan J.R. Sellers Load-dependent mechanism of nonmuscle myosin 2 Proc. Natl. Acad. Sci. USA 104 2007 9994 9999
11. C. Veigel, and J.E. Molloy J. Kendrick-Jones Load-dependent kinetics of force production by smooth muscle myosin measured with optical tweezers Nat. Cell Biol. 5 2003 980 986
12. E.M. Reichl, and Y. Ren D.N. Robinson Interactions between myosin and actin crosslinkers control cytokinesis contractility dynamics and mechanics Curr. Biol. 18 2008 471 480
13. D.J. Fishkind, and Y.L. Wang Orientation and three-dimensional organization of actin filaments in dividing cultured cells J. Cell Biol. 123 1993 837 848
14. P. Maupin, and T.D. Pollard Arrangement of actin filaments and myosin-like filaments in the contractile ring and of actin-like filaments in the mitotic spindle of dividing HeLa cells J. Ultrastruct. Mol. Struct. Res. 94 1986 92 103
15. K. Murthy, and P. Wadsworth Myosin-II-dependent localization and dynamics of F-actin during cytokinesis Curr. Biol. 15 2005 724 731
16. T. Kamasaki, M. Osumi, and I. Mabuchi Three-dimensional arrangement of F-actin in the contractile ring of fission yeast J. Cell Biol. 178 2007 765 771
17. M. Lord, E. Laves, and T.D. Pollard Cytokinesis depends on the motor domains of myosin-II in fission yeast but not in budding yeast Mol. Biol. Cell 16 2005 5346 5355
18. R. Neujahr, C. Heizer, and G. Gerisch Myosin II-independent processes in mitotic cells of Dictyostelium discoideum: redistribution of the nuclei, re-arrangement of the actin system and formation of the cleavage furrow J. Cell Sci. 110 1997 123 137
19. J.H. Zang, and G. Cavet J.A. Spudich On the role of myosin-II in cytokinesis: division of Dictyostelium cells under adhesive and nonadhesive conditions Mol. Biol. Cell 8 1997 2617 2629
20. X. Ma, and M. Kovács R.S. Adelstein Nonmuscle myosin II exerts tension but does not translocate actin in vertebrate cytokinesis Proc. Natl. Acad. Sci. USA 109 2012 4509 4514
21. N.L. Dasanayake, P.J. Michalski, and A.E. Carlsson General mechanism of actomyosin contractility Phys. Rev. Lett. 107 2011 118101
22. A.E. Carlsson Contractile stress generation by actomyosin gels Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 74 2006 051912
23. J.M. Arnold Cleavage furrow formation in a telolecithal egg (Loligo pealii). I. Filaments in early furrow formation J. Cell Biol. 41 1969 894 904
24. J.G. Bluemink Cytokinesis and cytochalasin-induced furrow regression in the first-cleavage zygote of Xenopus laevis Z. Zellforsch. Mikrosk. Anat. 121 1971 102 126
25. 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 1997 1287 1305
26. I. Mabuchi Biochemical aspects of cytokinesis Int. Rev. Cytol. 101 1986 175 213
27. M.P. Murrell, and M.L. Gardel F-actin buckling coordinates contractility and severing in a biomimetic actomyosin cortex Proc. Natl. Acad. Sci. USA 109 2012 20820 20825
28. A. Zemel, and A. Mogilner Motor-induced sliding of microtubule and actin bundles Phys. Chem. Chem. Phys. 11 2009 4821 4833
29. Y.S. Kee, and Y. Ren D.N. Robinson A mechanosensory system governs myosin II accumulation in dividing cells Mol. Biol. Cell 23 2012 1510 1523
30. T. Luo, and K. Mohan D.N. Robinson Understanding the cooperative interaction between myosin II and actin cross-linkers mediated by actin filaments during mechanosensation Biophys. J. 102 2012 238 247
31. K. Mohan, P.A. Iglesias, and D.N. Robinson Separation anxiety: stress, tension and cytokinesis Exp. Cell Res. 318 2012 1428 1434
32. N. Gerald, and J. Dai A. De Lozanne A role for Dictyostelium racE in cortical tension and cleavage furrow progression J. Cell Biol. 141 1998 483 492
33. M.R. Stachowiak, and B. O'Shaughnessy Recoil after severing reveals stress fiber contraction mechanisms Biophys. J. 97 2009 462 471
34. E.M. Craig, S. Dey, and A. Mogilner The emergence of sarcomeric, graded-polarity and spindle-like patterns in bundles of short cytoskeletal polymers and two opposite molecular motors J. Phys. Cond. Matter. 23 2011 374102
35. K. Kruse, and F. Jülicher Actively contracting bundles of polar filaments Phys. Rev. Lett. 85 2000 1778 1781
36. M. Lenz, M.L. Gardel, and A.R. Dinner Requirements for contractility in disordered cytoskeletal bundles New J. Phys. 14 2012 033037 10.1088/1367-2630/ 14/3/033037
37. M. Lenz, and T. Thoresen A.R. Dinner Contractile units in disordered actomyosin bundles arise from F-actin buckling Phys. Rev. Lett. 108 2012 238107
38. J. Berro, and A. Michelot J.L. Martiel Attachment conditions control actin filament buckling and the production of forces Biophys. J. 92 2007 2546 2558
39. M. Soares e Silva, and M. Depken G.H. Koenderink Active multistage coarsening of actin networks driven by myosin motors Proc. Natl. Acad. Sci. USA 108 2011 9408 9413
40. A. Carvalho, A. Desai, and K. Oegema Structural memory in the contractile ring makes the duration of cytokinesis independent of cell size Cell 137 2009 926 937
41. P. Hotulainen, and E. Paunola P. Lappalainen Actin-depolymerizing factor and cofilin-1 play overlapping roles in promoting rapid F-actin depolymerization in mammalian nonmuscle cells Mol. Biol. Cell 16 2005 649 664
42. N. Kaji, and K. Ohashi K. Mizuno Cell cycle-associated changes in Slingshot phosphatase activity and roles in cytokinesis in animal cells J. Biol. Chem. 278 2003 33450 33455
43. K. Ono, and M. Parast S. Ono Specific requirement for two ADF/cofilin isoforms in distinct actin-dependent processes in Caenorhabditis elegans J. Cell Sci. 116 2003 2073 2085
44. M.P. Somma, and B. Fasulo M. Gatti Molecular dissection of cytokinesis by RNA interference in Drosophila cultured cells Mol. Biol. Cell 13 2002 2448 2460
45. I. Mendes Pinto, and B. Rubinstein R. Li Actin depolymerization drives actomyosin ring contraction during budding yeast cytokinesis Dev. Cell 22 2012 1247 1260
46. A. Zumdieck, and K. Kruse F. Jülicher Stress generation and filament turnover during actin ring constriction PLoS ONE 2 2007 e696
47. W. Zhang, and D.N. Robinson Balance of actively generated contractile and resistive forces controls cytokinesis dynamics Proc. Natl. Acad. Sci. USA 102 2005 7186 7191
48. C.C. Poirier, and W.P. Ng P.A. Iglesias Deconvolution of the cellular force-generating subsystems that govern cytokinesis furrow ingression PLOS Comput. Biol. 8 2012 e1002467
49. J.C. Effler, and Y.S. Kee D.N. Robinson Mitosis-specific mechanosensing and contractile-protein redistribution control cell shape Curr. Biol. 16 2006 1962 1967
50. M. Guha, M. Zhou, and Y.L. Wang Cortical actin turnover during cytokinesis requires myosin II Curr. Biol. 15 2005 732 736
51. C.A. Wilson, and M.A. Tsuchida J.A. Theriot Myosin II contributes to cell-scale actin network treadmilling through network disassembly Nature 465 2010 373 377
52. A.C. Reymann, and R. Boujemaa-Paterski L. Blanchoin Actin network architecture can determine myosin motor activity Science 336 2012 1310 1314
53. E. Prochniewicz, and H.F. Chin E.M. De La Cruz Myosin isoform determines the conformational dynamics and cooperativity of actin filaments in the strongly bound actomyosin complex J. Mol. Biol. 396 2010 501 509
54. E.M. De La Cruz How cofilin severs an actin filament Biophys. Rev 1 2009 51 59
55. B.R. McCullough, and E.E. Grintsevich E.M. De La Cruz Cofilin-linked changes in actin filament flexibility promote severing Biophys. J. 101 2011 151 159
56. J. Sedzinski, and M. Biro E. Paluch Polar actomyosin contractility destabilizes the position of the cytokinetic furrow Nature 476 2011 462 466
57. S.A. Proctor, and N. Minc F. Chang Contributions of turgor pressure, the contractile ring, and septum assembly to forces in cytokinesis in fission yeast Curr. Biol. 22 2012 1601 1608