Cell-sized spherical confinement induces the spontaneous formation of contractile actomyosin rings in vitro

Nature Cell Biology

Volumn 17, Issue 4, 2015, Pages 480-489

  Miyazaki, Makito ^a   Chiba, Masataka ^a   Eguchi, Hiroki ^a   Ohki, Takashi ^a   Ishiwata, Shin'ichi ^a,b  

^a WASEDA UNIVERSITY   (Japan)

^b Waseda University   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

MYOSIN; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN HEAVY CHAIN; MYOSIN V; ACTIN; MYOSIN II;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ARTICLE; CELL SHAPE; CELL STRUCTURE; CONTRACTILE RING; CONTROLLED STUDY; CYTOKINESIS; OLIGOMERIZATION; PRIORITY JOURNAL; ANIMAL; CELL DIVISION; METABOLISM; PHYSIOLOGY;

ANIMALIA;

ACTIN CYTOSKELETON; ACTINS; ACTOMYOSIN; ANIMALS; CELL DIVISION; CELL SHAPE; CYTOKINESIS; MYOSIN TYPE II; MYOSIN TYPE V;

EID: 84925938722     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3142     Document Type: Article

References (62)

1. Glotzer, M. The molecular requirements for cytokinesis. Science 307, 1735-1739 (2005).
2. Eggert, U. S., Mitchison, T. J. & Field, C. M. Animal cytokinesis: from parts list to mechanisms. Annu. Rev. Biochem. 75, 543-566 (2006).
3. Pollard, T. D. Mechanics of cytokinesis in eukaryotes. Curr. Opin. Cell Biol. 22, 50-56 (2010).
4. Fededa, J. P. & Gerlich, D. W. Molecular control of animal cell cytokinesis. Nat. Cell Biol. 14, 440-447 (2012).
5. Watanabe, S. et al. mDia2 induces the actin scaffold for the contractile ring and stabilizes its position during cytokinesis in NIH 3T3 cells. Mol. Biol. Cell 19, 2328-2338 (2008).
6. Matsumura, F. Regulation of myosin II during cytokinesis in higher eukaryotes. Trends Cell Biol. 15, 371-377 (2005).
7. Kovar, D. R., Harris, E. S., Mahaffy, R., Higgs, H. N. & Pollard, T. D. Control of the assembly of ATP-And ADP-Actin by formins and profilin. Cell 124, 423-435 (2006).
8. Fujiwara, K., Porter, M. E. & Pollard, T. D. Alpha-Actinin localization in the cleavage furrow during cytokinesis. J. Cell Biol. 79, 268-275 (1978).
9. Mabuchi, I. et al. Alpha-Actinin from sea urchin eggs: biochemical properties, interaction with actin, and distribution in the cell during fertilization and cleavage. J. Cell Biol. 100, 375-383 (1985).
10. Mukhina, S., Wang, Y-L. & Murata-Hori, M.-Actinin is required for tightly regulated remodeling of the actin cortical network during cytokinesis. Dev. Cell 13, 554-565 (2007).
11. Laporte, D., Ojkic, N., Vavylonis, D. & Wu, J-Q.-Actinin and fimbrin cooperate with myosin II to organize actomyosin bundles during contractile-ring assembly. Mol. Biol. Cell 23, 3094-3110 (2012).
12. Field, C. M. & Alberts, B. M. Anillin, a contractile ring protein that cycles from the nucleus to the cell cortex. J. Cell Biol. 131, 165-178 (1995).
13. Kinoshita, M., Field, C. M., Coughlin, M. L., Straight, A. F. & Mitchison, T. J. Selfand actin-Templated assembly of mammalian septins. Dev. Cell 3, 791-802 (2002).
14. Mavrakis, M. et al. Septins promote F-Actin ring formation by crosslinking actin filaments into curved bundles. Nat. Cell Biol. 16, 322-334 (2014).
15. Mabuchi, I. & Okuno, M. The effect of myosin antibody on the division of starfish blastomeres. J. Cell Biol. 74, 251-263 (1977).
16. Zhou, M. & Wang, Y-L. Distinct pathways for the early recruitment of myosin II and actin to the cytokinetic furrow. Mol. Biol. Cell 19, 318-326 (2008).
17. Vavylonis, D., Wu, J-Q., Hao, S., OShaughnessy, B. & Pollard, T. D. Assembly mechanism of the contractile ring for cytokinesis by fission yeast. Science 319, 97-100 (2008).
18. Soares e Silva, M. et al. Self-organized patterns of actin filaments in cell-sized confinement. Soft Matter 7, 10631-10641 (2011).
19. Claessens, M. M. A. E., Tharmann, R., Kroy, K. & Bausch, A. R. Microstructure and viscoelasticity of confined semiflexible polymer networks. Nat. Phys. 2, 186-189 (2006).
20. Harris, A. Location of cellular adhesions to solid substrata. Dev. Biol. 35, 97-114 (1973).
21. Cramer, L. P. & Mitchison, T. J. Investigation of the mechanism of retraction of the cell margin and rearward flow of nodules during mitotic cell rounding. Mol. Biol. Cell 8, 109-119 (1997).
22. Maddox, A. S. & Burridge, K. RhoA is required for cortical retraction and rigidity during mitotic cell rounding. J. Cell Biol. 160, 255-265 (2003).
23. Stewart, M. P. et al. Hydrostatic pressure and the actomyosin cortex drive mitotic cell rounding. Nature 469, 226-230 (2011).
24. Sanger, J. M., Reingold, A. M. & Sanger, J. W. Cell surface changes during mitosis and cytokinesis of epithelial cells. Cell Tissue Res. 237, 409-417 (1984).
25. Gibson, M. C., Patel, A. B., Nagpal, R. & Perrimon, N. The emergence of geometric order in proliferating metazoan epithelia. Nature 442, 1038-1041 (2006).
26. Kondo, T. & Hayashi, S. Mitotic cell rounding accelerates epithelial invagination. Nature 494, 125-129 (2013).
27. Hase, M. & Yoshikawa, K. Structural transition of actin filament in a cell-sized water droplet with a phospholipid membrane. J. Chem. Phys. 124, 104903 (2006).
28. Negishi, M., Sakaue, T., Takiguchi, K. & Yoshikawa, K. Cooperation between giant DNA molecules and actin filaments in a microsphere. Phys. Rev. E 81, 051921 (2010).
29. Asakura, S. & Oosawa, F. On interaction between two bodies immersed in a solution of macromolecules. J. Chem. Phys. 22, 1255-1256 (1954).
30. Takiguchi, K. Heavy meromyosin induces sliding movements between antiparallel actin filaments. J. Biochem. 109, 520-527 (1991).
31. Tanaka-Takiguchi, Y. et al. The elongation and contraction of actin bundles are induced by double-headed myosins in a motor concentration-dependent manner. J. Mol. Biol. 341, 467-476 (2004).
32. Fujime, S. Quasi-elastic light scattering from solutions of macromolecules. II. Doppler broadening of light scattered from solutions of semi-flexible polymers, Factin. J. Phys. Soc. Jpn 29, 751-759 (1970).
33. Fujime, S. & Ishiwata, S. Dynamic study of F-Actin by quasielastic scattering of laser light. J. Mol. Biol. 62, 251-265 (1971).
34. Gittes, F., Mickey, B., Nettleton, J. & Howard, J. Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape. J. Cell Biol. 120, 923-934 (1993).
35. Isambert, H. et al. Flexibility of actin filaments derived from thermal fluctuations. Effect of bound nucleotide, phalloidin, and muscle regulatory proteins. J. Biol. Chem. 270, 11437-11444 (1995).
36. Reymann, A-C. et al. Actin network architecture can determine myosin motor activity. Science 336, 1310-1314 (2012).
37. Nishizaka, T., Miyata, H., Yoshikawa, H., Ishiwata, S. & Kinosita, K. Jr Unbinding force of a single motor molecule of muscle measured using optical tweezers. Nature 377, 251-254 (1995).
38. Guo, B. & Guilford, W. H. Mechanics of actomyosin bonds in different nucleotide states are tuned to muscle contraction. Proc. Natl Acad. Sci. USA 103, 9844-9849 (2006).
39. Sanger, J. M. & Sanger, J. W. Banding and polarity of actin filaments in interphase and cleaving cells. J. Cell Biol. 86, 568-575 (1980).
40. Maupin, P. & Pollard, T. D. Arrangement of actin filaments and myosinlike filaments in the contractile ring and of actin-like filaments in the mitotic spindle of dividing HeLa cells. J. Ultrastruct. Mol. Struct. Res. 94, 92-103 (1986).
41. Schroeder, T. E. The contractile ring II. Determining its brief existence, volumetric changes, and vital role in cleaving Arbacia eggs. J. Cell Biol. 53, 419-434 (1972).
42. Kamasaki, T., Osumi, M. & Mabuchi, I. Three-dimensional arrangement of F-Actin in the contractile ring of fission yeast. J. Cell Biol. 178, 765-771 (2007).
43. Zumdieck, A., Kruse, K., Bringmann, H., Hyman, A. A. & Jülicher, F. Stress generation and filament turnover during actin ring constriction. PLoS ONE 2, e696 (2007).
44. Mishra, M. et al. In vitro contraction of cytokinetic ring depends on myosin II but not on actin dynamics. Nat. Cell Biol. 15, 853-859 (2013).
45. Mendes Pinto, I., Rubinstein, B. & Li, R. Force to divide: structural and mechanical requirements for actomyosin ring contraction. Biophys. J. 105, 547-554 (2013).
46. Mishra, M. et al. Cylindrical cellular geometry ensures fidelity of division site placement in fission yeast. J. Cell Sci. 125, 3850-3857 (2012).
47. Alvarado, J., Sheinman, M., Sharma, A., MacKintosh, F. C. & Koenderink, G. H. Molecular motors robustly drive active gels to a critically connected state. Nat. Phys. 9, 591-597 (2013).
48. Carvalho, A., Desai, A. & Oegema, K. Structural memory in the contractile ring makes the duration of cytokinesis independent of cell size. Cell 137, 926-937 (2009).
49. Haviv, L., Gillo, D., Backouche, F. & Bernheim-Groswasser, A. A cytoskeletal demolition worker: myosin II acts as an actin depolymerization agent. J. Mol. Biol. 375, 325-330 (2008).
50. Uyeda, T. Q. P., Kron, S. J. & Spudich, J. A. Myosin step size. Estimation from slow sliding movement of actin over low densities of heavy meromyosin. J. Mol. Biol. 214, 699-710 (1990).
51. Harris, D. E. & Warshaw, D. M. Smooth and skeletal muscle myosin both exhibit low duty cycles at zero load in vitro. J. Biol. Chem. 268, 14764-14768 (1993).
52. De La Cruz, E. M., Wells, A. L., Rosenfeld, S. S., Ostap, E. M. & Sweeney, H. L. The kinetic mechanism of myosin V. Proc. Natl Acad. Sci. USA 96, 13726-13731 (1999).
53. Moore, J. R., Krementsova, E. B., Trybus, K. M. & Warshaw, D. M. Myosin V exhibits a high duty cycle and large unitary displacement. J. Cell Biol. 155, 625-635 (2001).
54. O'Connell, C. B. & Wang, Y-L. Mammalian spindle orientation and position respond to changes in cell shape in a dynein-dependent fashion. Mol. Biol. Cell 11, 1765-1774 (2000).
55. Minc, N., Burgess, D. & Chang, F. Influence of cell geometry on division-plane positioning. Cell 144, 414-426 (2011).
56. Ohki, T., Mikhailenko, S. V., Arai, T., Ishii, S. & Ishiwata, S. Improvement of the yields of recombinant actin and myosin V-HMM in the insect cell/baculovirus system by the addition of nutrients to the high-density cell culture. J. Muscle Res. Cell Motil. 33, 351-358 (2012).
57. Gopalakrishna, R. & Anderson, W. B. Ca2C-induced hydrophobic site on calmodulin: application for purification of calmodulin by phenyl-Sepharose affinity chromatography. Biochem. Biophys. Res. Commun. 104, 830-836 (1982).
58. Thoresen, T., Lenz, M. & Gardel, M. L. Thick filament length and isoform composition determine self-organized contractile units in actomyosin bundles. Biophys. J. 104, 655-665 (2013).
59. Chiba, M., Miyazaki, M. & Ishiwata, S. Quantitative analysis of the lamellarity of giant liposomes prepared by the inverted emulsion method. Biophys. J. 107, 346-354 (2014).
60. Falzone, T. T., Oakes, P. W., Sees, J., Kovar, D. R. & Gardel, M. L. Actin assembly factors regulate the gelation kinetics and architecture of F-Actin networks. Biophys. J. 104, 1709-1719 (2013).
61. De La Cruz, E. M. & Pollard, T. D. Kinetics and thermodynamics of phalloidin binding to actin filaments from three divergent species. Biochemistry 35, 14054-14061 (1996).
62. Pollard, T. D. Rate constants for the reactions of ATP-And ADP-Actin with the ends of actin filaments. J. Cell Biol. 103, 2747-2754 (1986).