Physical model of contractile ring initiation in dividing cells

Biophysical Journal

Volumn 94, Issue 4, 2008, Pages 1155-1168

  Shlomovitz, Roie ^a   Gov, Nir S ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BIOLOGICAL MODEL; CELL DIVISION; CELL FUNCTION; CELL MEMBRANE; CELL MOTION; CELL SIZE; COMPUTER SIMULATION; ELASTICITY; MECHANICAL STRESS; MEMBRANE FLUIDITY; PHYSIOLOGY;

CELL DIVISION; CELL MEMBRANE; CELL MOVEMENT; CELL PHYSIOLOGY; CELL SIZE; COMPUTER SIMULATION; ELASTICITY; MEMBRANE FLUIDITY; MODELS, BIOLOGICAL; STRESS, MECHANICAL;

EID: 38949184275     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.107.111351     Document Type: Article

References (77)

1. Scholey, J. M., I. Brust-Mascher, and A. Mogilner. 2003. Cell division: cytoskeleton. Nature. 422:746-752.
2. Robinson, D. N., and J. A. Spudich. 2000. Towards a molecular understanding of cytokinesis. Trends Cell Biol. 10:228-237.
3. Dean, S. O., S. L. Rogers, N. Stuurman, R. D. Vale, and J. A. Spudich. 2005. Distinct pathways control recruitment and maintenance of myosin II at the cleavage furrow during cytokinesis. Proc. Natl. Acad. Sci. USA. 102:13473-13478.
4. Nanninga, N. 2001. Cytokinesis in prokaryotes and eukaryotes: common principles and different solutions. Microbiol. Mol. Biol. Rev. 65: 319-333.
5. Emoto, K., T. Kobayashi, A. Yamaji, H. Aizawa, I. Yahara, K. Inoue, and M. Umeda. 1996. Redistribution of phosphatidylethanolamine at the cleavage furrow of dividing cells during cytokinesis. Proc. Natl. Acad. Sci. USA. 93:12867-12872.
6. Umeda, M., and K. Emoto. 1999. Membrane phospholipid dynamics during cytokinesis: regulation of actin filament assembly by redistribution of membrane surface phospholipids. Chem. Phys. Lipids. 101: 81-91.
7. An, M. W., W. Z. Wu, and W. Y. Chen. 2005. Membrane phospholipid redistribution in cytokinesis: a theoretical model. Acta Biochim. Biophys. Sin. (Shanghai). 37:643-648.
8. Takeda, T., and F. Chang. 2005. Role of fission yeast Myosin I in organization ofsterol-rich membrane domains. Curr. Biol. 15:1331-1336.
9. Ng, M. M., F. Chang, and D. R. Burgess. 2005. Movement of membrane domains and requirement of membrane signaling molecules for cytokinesis. Dev. Cell. 9:781-790.
10. Gov, N., and A. Gopinathan. 2006. Dynamics of membranes driven by actin polymerization. Biophys. J. 90:454-469.
11. Roux, A., D. Cuvelier, P. Nassoy, J. Prost, P. Bassereau, and B. Goud. 2005. Role of curvature and phase transition in lipid sorting and fission of membrane tubules. EMBO J. 24:1537-1545.
12. Parthasarathy, R., C. H. Yu, and J. T. Groves. 2006. Curvature-modulated phase separation in lipid bilayer membranes. Langmuir. 22: 5095-5099.
13. Zimmerberg, J., and M. M. Kozlov. 2006. How proteins produce cellular membrane curvature. Nat. Rev. Mol. Cell Biol. 7:9-19.
14. Iglič, A., T. Slivnika, and V. Kralj-Iglič 2007. Elastic properties of biological membranes influenced by attached proteins. J. Biomech. 40: 2492-2500.
15. Iglic, A., B. Babnika, K. Bohinca, M. Fošnarič,H. Hägerstrand, and V. Kralj-Iglič 2007. On the role of anisotropy of membrane constituents in formation of a membrane neck during budding of a multicomponent membrane. J. Biomech. 40:579-585.
16. Itoh, T., and P. D. Camilli. 2006. BAR, F-BAR (EFC) and ENTH/ ANTH domains in the regulation of membrane- cytosol interfaces and membrane curvature. Biochim. Biophys. Acta. 1761:897-912.
17. Huang, K. C., R. Mukhopadhyay, and N. S. Wingreen. 2006. A curvature-mediated mechanism for localization of lipids to bacterial poles. PLoS Comput. Biol. 2:1357-1364.
18. Tsafrir, I., D. Sagi, T. Arzi, M. A. Guedeau-Boudeville, V. Frette, D. Kandel, and J. Stavans. 2001. Pearling instabilities of membrane tubes with anchored polymers. Phys. Rev. Lett. 86:1138-1141.
19. Wang, Y. L. 2001. The mechanism of cytokinesis: reconsideration and reconciliation. Cell Struct. Funct. 6:633-668.
20. Wang, Y. L. 2005. The mechanism of cortical ingression during early cytokinesis: thinking beyond the contractile ring hypothesis. Trends Cell Biol. 15:581-588.
21. Greenspan, H. P. 1977. On the dynamics of cell cleavage. J. Theor. Biol. 65:79-99.
22. Zinemanas, D., and A. Nir. 1988. On the viscous deformation of biological cells under anisotropic surface tension. J. Fluid Mech. 193: 217-241.
23. An, M., W. Wu, and W. C. WY, 2005. Membrane phospholipid redistribution in cytokinesis: a theoretical model. Acta Biochim. Biophys. Sinica. 37:643-648.
24. White, J. G., and G. G. Borisy. 1983. On the mechanisms of cytokinesis in animal cells. J. Theor. Biol. 101:289-316.
25. J.-Q. Wu, V. Sirotkin, D. R. Kovar, M. Lord, C. C. Beltzner, J. R. Kuhn, and T. D. Pollard. 2006. Assembly of the cytokinetic contractile ring from a broad band of nodes in fission yeast. J. Cell Biol. 174: 391-402.
26. Zumdieck, A., M. C. Lagomarsino, C. Tanase, K. Kruse, B. Mulder, M. Dogterom, and F. Julicher. 2005. Continuum description of the cytoskeleton: ring formation in the cell cortex. Phys. Rev. Lett. 95: 258103.
27. Biron, D., E. Alvarez-Lacalle, T. Tlusty, and E. Moses. 2005. Molecular model of the contractile ring. Phys. Rev. Lett. 95:098102.
28. Zhang, W., and D. N. Robinson. 2005. Balance of actively generated contractile and resistive forces controls cytokinesis dynamics. Proc. Natl. Acad. Sci. USA. 102:7186-7191.
29. Wu, J. Q., J. R. Kuhn, D. R. Kovar, and T. D. Pollard. 2003. Spatial and temporal pathway for assembly and constriction of the contractile ring in fission yeast cytokinesis. Dev. Cell. 5:723-734.
30. Eggert, S. U., T. J. Mitchison, and C. M. Field. 2006. Animal cytokinesis: from parts list to mechanisms. Annu. Rev. Biochem. 75: 543-566.
31. Manneville, J. B., P. Bassereau, S. Ramaswamy, and J. Prost. 2001. Active membrane fluctuations studied by micropipette aspiration. Phys. Rev. E. 64:021908.
32. Ramaswamy, S., J. Toner, and J. Prost. 2000. Nonequilibrium fluctuations, traveling waves, and instabilities in active membranes. Phys. Rev. Lett. 84:3494-3497.
33. Safran, S. A. 2003. Statistical Thermodynamics of Surfaces, Interfaces, and Membranes, 1st Ed. Westview Press, Boulder, CO.
34. Mattila, P. K., A. Pykalainen, J. Saarikangas, V. O. Paavilainen, H. Vihinen, E. Jokitalo, and P. Lappalainen. 2007. Missing- in- metastasis and IRSp53 deform PI(4,5)P2-rich membranes by an inverse BAR domain-like mechanism. J. Cell Biol. 176:953-964.
35. Finer, J. T., R. M. Simmons, and J. A. Spudich. 1994. Single myosin molecule mechanics: picoNewton forces and nanometer steps. Nature. 368:113-119.
36. Almeida, P. F. F., and W. L. C. Vaz. 1995. Handbook of Biological Physics, Vol. 1. Elsevier Science, Amsterdam, The Netherlands.
37. Effler, J. C., Y. S. Kee, J. M. Berk, M. N. Tran, P. A. Iglesias, and D. N. Robinson. 2006. Mitosis-specific mechanosensing and contractile-protein redistribution control cell shape. Curr. Biol. 16:1962-1967.
38. Margolin, W., and R. Bernander. 2004. How do prokaryotic cells cycle? Curr. Biol. 14:R768-R770.
39. Straight, A. F., and C. M. Field. 2000. Microtubules, membranes and cytokinesis. Curr. Biol. 10:R760-R770.
40. Straight, A. F., A. Cheung, J. Limouze, I. Chen, N. J. Westwood, J. R. Sellers, and T. J. Mitchison. 2003. Dissecting temporal and spatial control of cytokinesis with a Myosin II inhibitor. Science. 299:1743-1747.
41. Tosuji, H., K. Miyaji, N. Fusetani, and T. Nakazawa. 2000. Effect of calyculin A on the surface structure of unfertilized sea urchin eggs. Cell Motil. Cytoskeleton. 46:129-136.
42. Raucher, D., and M. Sheetz. 1999. Membrane expansion increases endocytosis rate during mitosis. J. Cell Biol. 144:497-506.
43. Coll, P. M., S. A. Rincon, R. A. Izquierdo, and P. Perez. 2007. Hob3p, the fission yeast ortholog of human BIN3, localizes Cdc42p to the division site and regulates cytokinesis. EMBO J. 26:1865-1877.
44. Pelham, R. J., and F. Chang. 2002. Actin dynamics in the contractile ring during cytokinesis in fission yeast. Nature. 419:82-86.
45. Tasto, J. J., J. L. Morrell, and K. L. Gould. 2003. An anillin homologue, Mid2p, acts during fission yeast cytokinesis to organize the septin ring and promote cell separation. J. Cell Biol. 160:1093-1103.
46. Shu, S., X. Liu, and E. D. Korn. 2003. Dictyostelium and Acanthamoeba myosin II assembly domains go to the cleavage furrow of Dictyostelium myosin II-null cells. Proc. Natl. Acad. Sci. USA. 100:6499-6504.
47. Robinson, D. N., and J. A. Spudich. 2004. Mechanics and regulation of cytokinesis. Curr. Opin. Cell Biol. 16:182-188.
48. Hickson, G. R. X., A. Echard, and P. H. O'Farrell. 2006. Rho-kinase controls cell shape changes during cytokinesis. Curr. Biol. 16:359-370.
49. Shuster, C. B., and D. R. Burgess. 2002. Transitions regulating the timing of cytokinesis in embryonic cells. Curr. Biol. 12:854-858.
50. Strickland, L. I., E. J. Donnelly, and D. R. Burgess. 2005. Induction of cytokinesis is independent of precisely regulated microtubule dynamics. Mol. Biol. Cell. 16:4485-4494.
51. Rodriguez, O. C., A. W. Schaefer, C. A. Mandato, P. Forscher, W. M. Bement, and C. M. Waterman-Storer. 2003. Conserved microtubule- actin interactions in cell movement and morphogenesis. Nat. Cell Biol. 5:599-609.
52. Alsop, G. B., and D. Zhang. 2003. Microtubules are the only structural constituent of the spindle apparatus required for induction of cell cleavage. J. Cell Biol. 162:383-390.
53. Alsop, G. B., and D. Zhang. 2004. Microtubules continuously dictate distribution of actin filaments and positioning of cell cleavage in grasshopper spermatocytes. J. Cell Sci. 117:1591-1602.
54. Bringmann, H., and A. A. Hyman. 2005. A cytokinesis furrow is positioned by two consecutive signals. Nature. 436:731-734.
55. Canman, J. C., L. A. Cameron, P. S. Maddox, A. Straight, J. S. Tirnauer, T. J. Mitchison, G. Fang, T. M. Kapoor, and E. D. Salmon. 2003. Determining the position of the cell division plane. Nature. 424: 1074-1078.
56. Padte, N. N., S. G. Martin, M. Howard, and F. Chang. 2006. The cell- end factor Pom1p inhibits Mid1p in specification of the cell division plane in fission yeast. Curr. Biol. 16:2480-2487.
57. Takeda, T., T. Kawate, and F. Chang. 2004. Organization of a sterol-rich membrane domain by cdc15p during cytokinesis in fission yeast. Nat. Cell Biol. 6:1142-1144.
58. Paluch, E., J. van-der Gucht, J. F. Joanny, and C. Sykes. 2006. Deformations in actin comets from rocketing beads. Biophys. J. 91: 3113-3122.
59. Motegi, F., N. V. Velarde, F. Piano, and A. Sugimoto. 2006. Two phases of astral microtubule activity during cytokinesis in C. elegans embryos. Dev. Cell. 10:509-520.
60. Bement, W. M., H. A. Benink, and G. von Dassow. 2005. A microtubule - dependent zone of active RhoA during cleavage plane specification. J. Cell Biol. 170:91-101.
61. Shuster, C. B., and D. R. Burgess. 2002. Targeted new membrane addition in the cleavage furrow is a late, separate event in cytokinesis. Proc. Natl. Acad. Sci. USA. 99:3633-3638.
62. Lister, I. M., N. J. Tolliday, and R. Li. 2006. Characterization of the minimum domain required for targeting budding yeast myosin II to the site of cell division. BMC Biol. 4:19.
63. Margolin, W. 2005. FtsZ and the division of prokaryotic cells and organelles. Nat. Rev. Mol. Cell Biol. 6:862-871.
64. Dajkovic, A., and J. Lutkenhaus. 2006. Z ring as executor of bacterial cell division. J. Mol. Microbiol. Biotechnol. 11:140-151.
65. Lu, C., M. Reedy, and H. P. Erickson. 2000. Straight and curved conformations of FtsZ are regulated by GTP hydrolysis. J. Bacteriol. 182:164-170.
66. Erickson, H. P. 2001. The FtsZ protofilament and attachment of ZipA-structural constraints on the FtsZ power stroke. Curr. Opin. Cell Biol. 13:55-60.
67. Gilson, P. R., X. C. Yu, D. Hereld, C. Barth, A. Savage, B. R. Kiefel, S. Lay, P. R. Fisher, W. Margolin, and P. L. Beech. 2003. Two Dictyostelium orthologs of the prokaryotic cell division protein FtsZ localize to mitochondria and are required for the maintenance of normal mitochondrial morphology. Eukaryot. Cell. 2:1315-1326.
68. Thanedar, S., and W. Margolin. 2004. FtsZ exhibits rapid movement and oscillation waves in helix-like patterns in Escherichia coli. Curr. Biol. 14:1167-1173.
69. Ben-Yehuda, S., and R. Losick. 2002. Asymmetric cell division in B. subtilis involves a spiral-like intermediate of the cytokinetic protein FtsZ. Cell. 109:257-266.
70. Yeong, F. M. 2005. Severing all ties between mother and daughter: cell separation in budding yeast. Mol. Microbiol. 55:1325-1331.
71. Wolkow, T. D., S. D. Harris, and J. E. Hamer. 1996. Cytokinesis in Aspergillus nidulans is controlled by cell size, nuclear positioning and mitosis. J. Cell Sci. 109:2179-2188.
72. Chang, F. 2001. Studies in fission yeast on mechanisms of cell division site placement. Cell Struct. Funct. 26:539-544.
73. Burgess, D., and F. Chang. 2005. Site selection for the cleavage furrow at cytokinesis. Trends Cell Biol. 15:156-162.
74. O'Connell, C., A. Warner, and Y. Wang. 2001. Distinct roles of the equatorial and polar cortices in the cleavage of adherent cells. Curr. Biol. 11:702-707.
75. Uyeda, T., C. Kitayama, and S. Yumura. 2000. Myosin II independent cytokinesis in Dictyostelium: its mechanism and implications. Cell Struct. Funct. 25:1-10.
76. Veksler, A., and N. S. Gov. 2007. Phase transitions of the coupled membrane - cytoskeleton modify cellular shape. Biophys. J. 93:3798-3810.
77. Miyoshi, H., S. K. Satoh, E. Yamada, and Y. Hamaguchi. 2006. Temporal change in local forces and total force all over the surface of the sea urchin egg during cytokinesis. Cell Motil. Cytoskeleton. 63:208-221.