A Mechanosensory System Controls Cell Shape Changes during Mitosis

Cell Cycle

Volumn 6, Issue 1, 2007, Pages 30-35

  Effler, Janet C ^a,b   Iglesias, Pablo A ^b   Robinson, Douglas N ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Johns Hopkins University   (United States)

Author keywords

Actin; Cell mechanics; Checkpoint; Control system; Cytokinesis; Mechanical feedback; Myosin II

Indexed keywords

BIOSENSOR; CELL CYCLE; CELL SHAPE; CYTOKINESIS; FEEDBACK SYSTEM; MECHANOTRANSDUCTION; MITOSIS; NONHUMAN; REGULATORY MECHANISM; REVIEW;

MAMMALIA;

EID: 33846575284     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.6.1.3674     Document Type: Review

References (64)

1. Fujiwara T, Bandi M, Nitta M, Ivanova EV, Bronson RT, Pellman D. Cytokinesis failure generating tetraploids promotes tumorigenesis in p53-null cells. Nature 2005; 437:1043-7.
2. Giet R, Petretti C, Prigent C. Aurora kinases, aneuploidy and cancer, a coincidence or a real link? Trends Cell Biol 2005; 15:241-50.
3. Meraldi P, Honda R, Nigg EA. Aurora-A overexpression reveals tetraploidization as a major route to centrosome amplification in p53-/- cells. EMBO J 2002; 21:483-92.
4. Gisselsson D. Mitotic instability in cancer: Is there a method in the madness? Cell Cycle 2005; 4:1007-10.
5. Wooster R, Neuhausen SL, Mangion J, Quirk Y, Ford D, Collins N, Nguyen K, Seal S, Tran T, Averill D, al. e. Localization of a breast cancer susceptibility gene, BRCA2, to chromosome 13q12-13. Science 1994; 265:2088-90.
6. Nathanson KL, Wooster R, Weber BL. Breast cancer genetics: What we know and what we need. Nat Med 2001; 7:552-6.
7. Daniels MJ, Wang Y, Lee M, Venkitaraman AR. Abnormal cytokinesis in cells deficient in the breast cancer susceptibility protein BRCA2. Science 2004; 306:876-9.
8. Effler JC, Kee Y-S, Berk JM, Tran MN, Iglesias PA, Robinson DN. Mitosis-specific mechanosensing and contractile protein redistribution control cell shape. Curr Biol 2006; 16:1962-7.
9. Rappaport R. Cytokinesis in Animal Cells. Cambridge: Cambridge University Press, 1996.
10. Robinson DN, Spudich JA. Towards a molecular understanding of cytokinesis. Trends Cell Biol 2000; 10:228-37.
11. Robinson DN, Spudich JA. Mechanics and regulation of cytokinesis. Curr Opin Cell Biol 2004; 16:182-8.
12. Shuster CB, Burgess DR. Parameters that specify the timing of cytokinesis. J Cell Biol 1999; 146:981-92.
13. Bringmann H, Hyman A. A cytokinesis furrow is positioned by two consecutive signals. Nature 2005; 436:731-4.
14. Rappaport R. Geometrical relations of the cleavage stimulus in constricted sand dollar eggs. J Exp Zool 1964; 155:225-30.
15. Wu D, Asiedu M, Adelstein RS, Wei Q. A novel guanine nucleotide exchange factor MyoGEF is required for cytokinesis. Cell Cycle 2006; 5:1234-9.
16. Bringmann H. Cytokinesis and the spindle midzone. Cell Cycle 2005; 4:1709-12.
17. Geddis AR, Kaushansky K. Endomitotic megakaryocytes form a midzone in anaphase but have a deficiency in cleavage furrow formation. Cell Cycle 2006; 5:538-45.
18. Yumura S, Uyeda TQP. Transport of myosin II to the equatorial region without its own motor activity in mitotic Dictyostelium cells. Mol Biol Cell 1997; 8:2089-99.
19. DeLozanne A, Spudich JA. Disruption of the Dictyostelium myosin heavy chain gene by homologous recombination. Science 1987; 236:1086-91.
20. Bezanilla M, Forsburg SL, Pollard TD. Identification of a second myosin-II in Schizosaccharomyces pombe: Myp2p is conditionally required for cytokinesis. Mol Biol Cell 1997; 8:2693-705.
21. Straight AF, Cheung A, Limouze J, Chen I, Westwood NJ, Sellers JR, Mitchison TJ. Dissecting temporal and spatial control of cytokinesis with a myosin II inhibitor. Science 2003; 299:1743-7.
22. Zhang W, Robinson DN. Balance of actively generated contractile and resistive forces controls cytokinesis dynamics. Proc Natl Acad Sci USA 2005; 102:7186-91.
23. Reichl EM, Effler JC, Robinson DN. The stress and strain of cytokinesis. Trends Cell Biol 2005; 15:200-6.
24. Robinson DN, Cavet G, Warrick HM, Spudich JA. Quantitation of the distribution and flux of myosin-II during cytokinesis. BMC Cell Biology 2002; 3:4.
25. Wu J-Q, Kuhn JR, Kovar DR, Pollard TD. Spatial and temporal pathway for assembly and constriction of the contractile ring in fission yeast cytokinesis. Dev Cell 2003; 5:723-34.
26. Guertin DA, Trautmann S, McCollum D. Cytokinesis in eukaryotes. Microbiol Mol Biol Rev 2002; 66:155-78.
27. Pinsky BA, Biggins S. The spindle checkpoint: tension versus attachment. Trends Cell Biol 2005; 15:486-93.
28. Pot I, Knockleby J, Aneliunas V, Nguyen T, Ah-Kye S, Liszt G, Snyder M, Hieter P, Vogel J. Spindle checkpoint maintenance requires Ame1 and Okp1. Cell Cycle 2005; 4:1448-56.
29. Stukenberg PT. Triggering p53 after cytokinesis failure. J Cell Biol 2004; 165:607-8.
30. Muhua L, Adames NR, Murphy MD, Shields CR, Cooper JA. A cytokinesis checkpoint requiring the yeast homologue of an APC-binding protein. Nature 1998; 393:487-91.
31. Norden C, Mendoza M, Dobbelaere J, Kotwaliwale CV, Biggins S, Barral Y. The nocut pathway links completion of cytokinesis to spindle midzone function to prevent chromosome breakage. Cell 2006; 125:85-98.
32. Uetake Y, Sluder G. Cell cycle progression after cleavage failure: mammalian somatic cells do not possess a "tetraploidy checkpoint". J Cell Biol 2004; 165:609-15.
33. Wong C, Stearns T. Mammalian cells lack checkpoints for tetraploidy, aberrant centrosome number, and cytokinesis failure. BMC Cell Biology 2005; 6:6.
34. Ingolia NT, Murray AW. The ups and downs of modeling the cell cycle. Curr Biol 2004; 14:R771-R7.
35. Ferrell JE. Self-perpetuating states in signal transduction: positive feedback, double-negative feedback and bistability. Curr Opin Cell Biol 2002; 14:140-8.
36. Brandman O, Ferrell JE, Li R, Meyer T. Interlinked fast and slow positive feedback loops drive reliable cell decisions. Science 2005; 310:496-8.
37. Gerisch G, Faix J, Köhler J, Müller-Tautenberger A. Actin-binding proteins required for reliable chromosome segregation in mitosis. Cell Motil Cytoskeleton 2004; 57:18-25.
38. Octtaviani E, Effler JC, Robinson DN. Enlazin, a natural fusion of two classes of canonical cytoskeletal proteins, contributes to cytokinesis dynamics. Mol Biol Cell 2006; 17:5275-86.
39. Rappaport R. Cell division: Direct measurement of maximum tension exerted by furrow of echinoderm eggs. Science 1967; 156:1241-3.
40. Poirier MG, Marko JF. Mitotic chromosomes are chromatin networks without a mechanically contiguous protein scaffold. Proc Natl Acad Sci USA 2002; 99:15393-7.
41. Poirier MG, Eroglu S, Chatenay D, Marko JF. Reversible and irreversible unfolding of mitotic newt chromosomes by applied force. Mol Biol Cell 2000; 11:269-76.
42. Jannink G, Duplantier B, Sikorav J-L. Forces on chromosomal DNA during anaphase. Biophys J 1996; 71:451-65.
43. Meyers J, Craig J, Odde DJ. Potential for control of signaling pathways via cell size and shape. Curr Biol 2006; 16:1685-93.
44. Pecreaux J, Röper J-C, Kruse K, Jülicher F, Hyman AA, Grill SW, Howard J. Spindle oscillations during asymmetric cell division require a threshold number of active cortical force generators. Curr Biol 2006; 16:2111-22.
45. Orr AW, Helmke BP, Blackman BR, Schwartz MA. Mechanisms of mechanotransduction. Dev Cell 2006; 10:11-20.
46. Choquet D, Felsenfeld DP, Sheetz MP. Extracellular matrix rigidity causes strengthening of integrin-cytoskeleton linkages. Cell 1997; 88:39-48.
47. Tamada M, Sheetz MP, Sawada Y. Activation of signaling cascade by cytoskeleton stretch. Dev Cell 2004; 7:709-18.
48. Martinac B. Mechanosensitive ion channels: molecules of mechanotransduction. J Cell Sci 2004; 117:2449-60.
49. LeMasurier M, Gillespie PG. Hair-cell mechanotransduction and cochlear amplification. Neuron 2005; 48:403-15.
50. Altman D, Sweeney HL, Spudich JA. The mechanism of myosin VI translocation and its load-induced anchoring. Cell 2004; 116:737-49.
51. Veigel C, Molloy JE, Schmitz S, Kendrick-Jones J. Load-dependent kinetics of force production by smooth muscle myosin measured with optical tweezers. Nat Cell Biol 2003; 5:980-6.
52. Purcell TJ, Sweeney HL, Spudich JA. A force-dependent state controls the coordination of processive myosin V. Proc Natl Acad Sci USA 2005; 102:13873-8.
53. Pasternak C, Spudich JA, Elson EL. Capping of surface receptors and concomitant cortical tension are generated by conventional myosin. Nature 1989; 341:549-51.
54. Girard KD, Chaney C, Delannoy M, Kuo SC, Robinson DN. Dynacortin contributes to cortical viscoelasticity and helps define the shape changes of cytokinesis. EMBO J 2004; 23:1536-46.
55. Girard KD, Kuo SC, Robinson DN. Dictyostelium myosin-II mechanochemistry promotes active behavior of the cortex on long time-scales. Proc Natl Acad Sci USA 2006; 103:2103-8.
56. Guha M, Zhou M, Wang Y-l. Cortical actin turnover during cytokinesis requires myosin II. Curr Biol 2005; 15:732-6.
57. Murthy K, Wadsworth P. Myosin-II-dependent localization and dynamics of F-actin during cytokinesis. Curr Biol 2005; 15:724-31.
58. Urven LE, Yabe T, Pelegri F. A role for non-muscle myosin II function in furrow maturation in the early zebrafish embryo. J Cell Sci 2006; 119:4342-52.
59. Zang J-H, Cavet G, Sabry JH, Wagner P, Moores SL, Spudich JA. On the role of myosin-II in cytokinesis: Division of Dictyostelium cells under adhesive and nonadhesive conditions. Mol Biol Cell 1997; 8:2617-29.
60. Rosenblatt J, Cramer LP, Baum B, McGee KM. Myosin II-dependent cortical movement is required for centrosome separation and positioning during mitotic spindle assembly. Cell 2004; 117:361-72.
61. Janmey PA, Weitz DA. Dealing with mechanics: mechanisms of force transduction in cells. Trends Biochem Sci 2004; 29:364-70.
62. Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell 2006; 126:677-89.
63. Merkel R, Simson R, Simson DA, Hohenadl M, Boulbitch A, Wallraff E, Sackmann E. A micromechanic study of cell polarity and plasma membrane cell body coupling in Dictyostelium. Biophys J 2000; 79:707-19.
64. Charras GT, Yarrow JC, Horton MA, Mahadevan L, Mitchison TJ. Non-equilibration of hydrostatic pressure in blebbing cells. Nature 2005; 435:365-9.