Early spindle assembly in Drosophila embryos: Role of a force balance involving cytoskeletal dynamics and nuclear mechanics

Molecular Biology of the Cell

Volumn 16, Issue 10, 2005, Pages 4967-4981

  Cytrynbaum, E N ^a,b   Sommi, P ^a   Brust Mascher, I ^a   Scholey, J M ^a   Mogilner, A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CELL CYCLE PROTEIN; DYNEIN ADENOSINE TRIPHOSPHATASE; PROTEIN NCD; UNCLASSIFIED DRUG;

ARTICLE; CELL NUCLEUS; CENTROSOME; CONFOCAL MICROSCOPY; CYTOSKELETON; DROSOPHILA; DYNAMICS; ELASTICITY; EMBRYO; EMBRYO DEVELOPMENT; FORCE; INTERPHASE; MICROTUBULE; MITOSIS SPINDLE; MODEL; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROPHASE;

ACTINS; ANIMALS; CELL CYCLE; CELL NUCLEUS; CENTROSOME; CYTOSKELETON; DROSOPHILA; DROSOPHILA PROTEINS; DYNEIN ATPASE; EMBRYO, NONMAMMALIAN; KINESIN; MITOTIC SPINDLE APPARATUS; MODELS, BIOLOGICAL; MOLECULAR MOTOR PROTEINS; MORPHOGENESIS;

EID: 26244443690     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E05-02-0154     Document Type: Article

References (49)

1. Bloom, K. (2002). Yeast weighs in on the elusive spindle matrix: new filaments in the nucleus. Proc. Natl. Acad. Sci. USA 99, 4757-4759.
2. Brust-Mascher, I., Civelekoglu-Scholey, G., Kwon, M., Mogilner, A., and Scholey, J. M. (2004). Model for anaphase B: role of three mitotic motors in a switch from poleward flux to spindle elongation. Proc. Natl. Acad. Sci. USA 101, 15938-15943.
3. Chang, P., Jacobson, M. K., and Mitchison, T. J. (2004). Poly(ADP-ribose) is required for spindle assembly and structure. Nature 432, 645-649.
4. Cytrynbaum, E. N., Scholey, J. M., and Mogilner, A. (2003). A force balance model of early spindle pole separation in Drosophila embryos. Biophys. J. 84, 757-769.
5. Dahl, K. N., Kahn, S. M., Wilson, K. L., and Discher, D. E. (2004). The nuclear envelope lamina network has elasticity and a compressibility limit suggestive of a molecular shock absorber. J. Cell Sci. 117, 4779-4786.
6. Dogterom, M., and Leibler, S. (1993). Physical aspects of the growth and regulation of microtubule structures. Phys. Rev. Lett. 70, 1347-1350.
7. Dogterom, M., and Yurke, B. (1997). Measurement of the force-velocity relation for growing microtubules. Science. 278, 856-860.
8. Dujardin, D. L., and Vallee, R. B. (2002). Dynein at the cortex. Curr. Opin. Cell Biol. 14, 44-49.
9. Foe, V. E., and Alberts, B. M. (1983). Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. J. Cell Sci. 61, 31-70.
10. Foe, V. E., Field, C. M., and Odell, G. M. (2000). Microtubules and mitotic cycle phase modulate spatiotemporal distributions of F-actin and myosin II in Drosophila syncytial blastoderm embryos. Development 127, 1767-1787.
11. Goshima, G., and Vale, R. D. (2003). The roles of microtubule-based motor proteins in mitosis: comprehensive RNAi analysis in the Drosophila S2 cell line. J. Cell Biol. 162, 1003-1016.
12. Grevengoed, E. E., Fox, D. T., Gates, J., and Peifer, M. (2003). Balancing different types of actin polymerization at distinct sites: roles for Abelson kinase and Enabled. J. Cell Biol. 163, 1267-1279.
13. Grill, S. W., Howard, J., Schaffer, E., Stelzer, E. H., and Hyman, A. A. (2003). The distribution of active force generators controls mitotic spindle position. Science 301, 518-521.
14. Hirakawa, E., Higuchi, H., and Toyoshima, Y. Y. (2000). Processive movement of single 22S dynein molecules occurs only at low ATP concentrations. Proc. Natl. Acad. Sci. USA 97, 2533-2537.
15. Houchmandzadeh, B., Marko, J. F., Chatenay, D., and Libchaber, A. (1997). Elasticity and structure of eukaryote chromosomes studied by micromanipulation and micropipette aspiration. J. Cell Biol. 139, 1-12.
16. Inoue, S., and Salmon, E. D. (1995). Force generation by microtubule assembly/disassembly in mitosis and related movements. Mol. Biol. Cell 6, 1619-1640.
17. Kapitein, L. C., Peterman, E. J., Kwok, B. H., Kim, J. H., Kapoor, T. M., and Schmidt, C. F. (2005). The bipolar mitotic kinesin Eg5 moves on both microtubules that it crosslinks. Nature. 435, 114-118.
18. Karabay, A., and Walker, R. A. (1999). Identification of microtubule binding sites in the Ncd tail domain. Biochemistry 38, 1838-1849.
19. Karr, T. L., and Alberts, B. M. (1986). Organization of the cytoskeleton in early Drosophila embryos. J. Cell Biol. 102, 1494-1509.
20. Kellogg, D. R., Mitchison, T. J., and Alberts, B. M. (1988). Behaviour of microtubules and actin filaments in living Drosophila embryos. Development. 103, 675-686.
21. Korey, C. A., and Van Vactor, D. (2000). From the growth cone surface to the cytoskeleton: one journey, many paths. J. Neurobiol. 44, 184-193.
22. Kwon, M., and Scholey, J. M. (2004). Spindle mechanics and dynamics during mitosis in Drosophila. Trends Cell Biol. 14, 194-205.
23. Lawrence, C. J., et al. (2004). A standardized kinesin nomenclature. J. Cell Biol. 167, 19-22.
24. Marshall, W. F., Marko, J. F., Agard, D. A., and Sedat, J. W. (2001). Chromosome elasticity and mitotic polar ejection force measured in living Drosophila embryos by four-dimensional microscopy-based motion analysis. Curr. Biol. 11, 569-578.
25. McDonald, H. B., Stewart, R. J., and Goldstein, L. S. (1990). The kinesin-like Ncd protein of Drosophila is a minus end-directed microtubule motor. Cell 63, 1159-1165.
26. McIntosh, J. R., Hepler, P. K., and Van Wie, D. G. (1969). Models for mitosis. Nature 224, 659-663.
27. Minestrini, G., Harley, A. S., and Glover, D. M. (2003). Localization of Pavarotti-KLP in living Drosophila embryos suggests roles in reorganizing the cortical cytoskeleton during the mitotic cycle. Mol. Biol. Cell 14, 4028-4038.
28. Nedelec, F. (2002). Computer simulations reveal motor properties generating stable antiparallel microtubule interactions. J. Cell Biol. 158, 1005-1015.
29. Nishida, E., Iida, K., Yonezawa, N., Koyasu, S., Yahara, I., and Sakai, H. (1987). Cofilin is a component of intranuclear and cytoplasmic acrin rods induced in cultured cells. Proc. Natl. Acad. Sci. USA 84, 5262-5266.
30. Piehl, M., and Cassimeris, L. (2003). Organization and dynamics of growing microtubule plus ends during early mitosis. Mol. Biol. Cell 14, 916-925.
31. Qi, H., Rath, U., Wang, D., Xu, Y. Z., Ding, Y., Zhang, W., Blacketer, M. J., Paddy, M. R., Girton, J., Johansen, J., and Johansen, K. M. (2004). Megator, an essential coiled-coil protein that localizes to the putative spindle matrix during mitosis in Drosophila. Mol. Biol. Cell 15, 4854-4865.
32. Robinson, J. T., Wojcik, E. J., Sanders, M. A., McGrail, M., and Hays, T. S. (1999). Cytoplasmic dynein is required for the nuclear attachment and migration of centrosomes during mitosis in Drosophila. J. Cell Biol. 146, 597-608.
33. Rodriguez, O. C., Schaefer, A. W., Mandato, C. A., Forscher, P., Bement, W. M., and Waterman-Storer, C. M. (2003). Conserved microtubule-actin interactions in cell movement and morphogenesis. Nat. Cell Biol. 5, 599-609.
34. Rosenblatt, J., Cramer, L. P., Baum, B., and McGee, K. M. (2004). Myosin II-dependent cortical movement is required for centrosome separation and positioning during mitotic spindle assembly. Cell 117, 361-372.
35. Royou, A., Field, C., Sisson, J. C., Sullivan, W., and Karess, R. (2004). Reassessing the role and dynamics of nonmuscle myosin II during furrow formation in early Drosophila embryos. Mol. Biol. Cell 15, 838-850.
36. Scholey, J. M., Brust-Mascher, I., and Mogilner, A. (2003). Cell division. Nature. 422, 746-752.
37. Scholey, J. M., Rogers, G. C., and Sharp, D. J. (2001). Mitosis, microtubules, and the matrix. J. Cell Biol. 154, 261-266.
38. Sharp, D. J., Brown, H. M., Kwon, M., Rogers, G. C., Holland, G., and Scholey, J. M. (2000a). Functional coordination of three mitotic motors in Drosophila embryos. Mol. Biol. Cell 11, 241-253.
39. Sharp, D. J., McDonald, K. L., Brown, H. M., Matthies, H. J., Walczak, C., Vale, R. D., Mitchison, T. J., and Scholey, J. M. (1999a). The bipolar kinesin, KLP61F, cross-links microtubules within interpolar microtubule bundles of Drosophila embryonic mitotic spindles. J. Cell Biol. 144, 125-138.
40. Sharp, D. J., Rogers, G. C., and Scholey, J. M. (2000b). Cytoplasmic dynein is required for poleward chromosome movement during mitosis in Drosophila embryos. Nat. Cell Biol. 2, 922-930.
41. Sharp, D. J., Yu, K. R., Sisson, J. C., Sullivan, W., and Scholey, J. M. (1999b). Antagonistic microtubule-sliding motors position mitotic centrosomes in Drosophila early embryos. Nat. Cell Biol. 1, 51-54.
42. Sprague, B. L., Pearson, C. G., Maddox, P. S., Bloom, K. S., Salmon, E. D., and Odde, D. J. (2003). Mechanisms of microtubule-based kinetochore positioning in the yeast metaphase spindle. Biophys J. 84, 3529-3546.
43. Stevenson, V., Hudson, A., Cooley, L., and Theurkauf, W. E. (2002). Arp2/3-dependent pseudocleavage [correction of psuedocleavage] furrow assembly in syncytial Drosophila embryos. Curr. Biol. 12, 705-711.
44. Stevenson, V. A., Kramer, J., Kuhn, J., and Theurkauf, W. E. (2001). Centrosomes and the Scrambled protein coordinate microtubule-independent actin reorganization. Nat. Cell Biol. 3, 68-75.
45. Sullivan, W., and Theurkauf, W. E. (1995). The cytoskeleton and morphogenesis of the early Drosophila embryo. Curr. Opin. Cell Biol. 7, 18-22.
46. Tram, U., Riggs, B., and Sullivan, W. (2001). Cleavage and gastrulation in Drosophila embryos. Macmillan Reference Ltd. In Encyclopedia of Life Sciences, London: Nature Publishing Group, 1-7.
47. Tseng, Y., Lee, J. S., Kole, T. P., Jiang, I., and Wirtz, D. (2004). Micro-organization and visco-elasticity of the interphase nucleus revealed by particle nanotracking. J. Cell Sci. 117, 2159-2167.
48. Walker, D. L., Wang, D., Jin, Y., Rath, U., Wang, Y., Johansen, J., and Johansen, K. M. (2000). Skeletor, a novel chromosomal protein that redistributes during mitosis provides evidence for the formation of a spindle matrix. J. Cell Biol. 151, 1401-1412.
49. Wells, W. A. (2001). Searching for a spindle matrix. J. Cell Biol. 154, 1102-1104.