Kinesin-5-dependent poleward flux and spindle length control in Drosophila embryo mitosis

Molecular Biology of the Cell

Volumn 20, Issue 6, 2009, Pages 1749-1762

  Brust Mascher, Ingrid ^a   Sommi, Patrizia ^a   Cheerambathur, Dhanya K ^a   Scholey, Jonathan M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; KINESIN; KINESIN 5; PROTEIN KLP61F; UNCLASSIFIED DRUG;

ANAPHASE; ARTICLE; CENTROMERE; CENTROSOME; CONTROLLED STUDY; DROSOPHILA; EMBRYO; GENE DOSAGE; METAPHASE; MICROTUBULE; MITOSIS SPINDLE; NONHUMAN; PRIORITY JOURNAL; PROMETAPHASE; PROTEIN FUNCTION;

ANAPHASE; ANIMALS; CHROMOSOMES; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; KINESIN; MALE; MICROTUBULE-ASSOCIATED PROTEINS; MITOSIS; MITOTIC SPINDLE APPARATUS; MUTATION; TIME FACTORS;

EID: 65249190848     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E08-10-1033     Document Type: Article

References (74)

1. Bettencourt-Dias, M., et al. (2004). Genome-wide survey of protein kinases required for cell cycle progression. Nature 432, 980-987.
2. Blower, M. D., and Karpen, G. H. (2001). The role of Drosophila CID in kinetochore formation, cell-cycle progression and heterochromatin interac-tions. Nat. Cell Biol. 3, 730-739.
3. 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.
4. Brust-Mascher, I., and Scholey, J. M. (2002). Microtubule flux and sliding in mitotic spindles of Drosophila embryos. Mol. Biol. Cell 13, 3967-3975.
5. Brust-Mascher, I., and Scholey, J. M. (2007). Mitotic spindle dynamics in Drosophila. Int. Rev. Cytol. 259, 139-172.
6. Burbank, K. S., Mitchison, T. J., and Fisher, D. S. (2007). Slide-and-cluster models for spindle assembly. Curr. Biol. 17, 1373-1383.
7. Cameron, L. A., Yang, G., Cimini, D., Canman, J. C., Kisurina-Evgenieva, O.,Khodjakov, A., Danuser, G., and Salmon, E. D. (2006). Kinesin 5-independent poleward flux of kinetochore microtubules in PtK1 cells. J. Cell Biol. 173,173-179.
8. Cheerambathur, D. K., Brust-Mascher, I., Civelekoglu-Scholey, G., and Scholey, J. M. (2008). Dynamic partitioning of mitotic kinesin-5 crosslinkers between microtubule-bound and freely diffusing states. J. Cell Biol. 182,421-428.
9. Cheerambathur, D. K., Civelekoglu-Scholey, G., Brust-Mascher, I., Sommi, P.,Mogilner, A., and Scholey, J. M. (2007). Quantitative analysis of an anaphase B switch: predicted role for a microtubule catastrophe gradient. J. Cell Biol.177, 995-1004.
10. Civelekoglu-Scholey, G., and Scholey, J. M. (2007). Mitotic motors: kinesin-5 takes a brake. Curr. Biol. 17, R544-R547.
11. Civelekoglu-Scholey, G., Sharp, D. J., Mogilner, A., and Scholey, J. M. (2006) Model of chromosome motility in Drosophila embryos: adaptation of a general mechanism for rapid mitosis. Biophys. J. 90, 3966-3982.
12. Cole, D. G., Saxton, W. M., Sheehan, K. B., and Scholey, J. M. (1994). A "slow" homotetrameric kinesin-related motor protein purified from Drosophila embryos. J. Biol. Chem. 269, 22913-22916.
13. Cottingham, F. R., Gheber, L., Miller, D. L., and Hoyt, M. A. (1999). Novel roles for Saccharomyces cerevisiae mitotic spindle motors. J. Cell Biol. 147, 335-350.
14. Cytrynbaum,E. N.,Sommi,P.,Brust-Mascher,I.,Scholey,J. M.,and Mogilner, A. (2005). Early spindle assembly in Drosophila embryos: role of a force balance involving cytoskeletal dynamics and nuclear mechanics. Mol. Biol.Cell 16, 4967-4981.
15. Enos, A. P., and Morris, N. R. (1990). Mutation of a gene that encodes a kinesin-like protein blocks nuclear division in A. nidulans. Cell 60, 1019-1027.
16. Gadde, S., and Heald, R. (2004). Mechanisms and molecules of the mitoticspindle. Curr. Biol. 14, R797-R805.
17. Gaglio,T., Saredi, A.,Bingham,J. B., Hasbani, M. J.,Gill,S. R., Schroer,T. A.,and Compton, D. A. (1996). Opposing motor activities are required for the organization of the mammalian mitotic spindle pole. J. Cell Biol. 135, 399-414.
18. Gardner, M. K., et al. (2008). Chromosome congression by kinesin-5 motor- mediated disassembly of longer kinetochore microtubules. Cell 135, 894-906.
19. Gordon, D. M., and Roof, D. M. (1999). The kinesin-related protein Kip1p of Saccharomyces cerevisiae is bipolar. J. Biol. Chem. 274, 28779-28786.
20. Goshima, G., Nedelec, F., and Vale, R. D. (2005a). Mechanisms for focusing mitotic spindle poles by minus end-directed motor proteins. J. Cell Biol. 171,229-240.
21. 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.
22. Goshima, G., Wollman, R., Goodwin, N., Zhang, J. M., Scholey, J. M., Vale,R. D., and Stuurman, N. (2007). Genes required for mitotic spindle assembly in Drosophila S2 cells. Science 316, 417-421.
23. Goshima, G., Wollman, R., Kelso, R. J., Stuurman, N., Scholey, J. M., and Vale,R. D. (2005b). Length control of the metaphase spindle. Curr. Biol. 15, 1979-1988.
24. Heald, R., Tournebize, R., Habermann, A., Karsenti, E., and Hyman, A. (1997).Spindle assembly in Xenopus egg extracts: respective roles of centrosomes and microtubule self-organization. J. Cell Biol. 138, 615-628.
25. Heck, M. M., Pereira, A., Pesavento, P., Yannoni, Y., Spradling, A. C., and Goldstein, L. S. (1993). The kinesin-like protein KLP61F is essential for mitosis in Drosophila. J. Cell Biol. 123, 665-679.
26. Henikoff, S., Ahmad, K., Platero, J. S., and van Steensel, B. (2000). Heterochro-matic deposition of centromeric histone H3-like proteins. Proc. Natl. Acad. Sci. USA 97, 716-721.
27. Hildebrandt, E. R., Gheber, L., Kingsbury, T., and Hoyt, M. A. (2006). Ho-motetrameric form of Cin8p, a Saccharomyces cerevisiae kinesin-5 motor, is essential for its in vivo function. J. Biol. Chem. 281, 26004-26013.
28. Johansen, K. M., and Johansen, J. (2007). Cell and molecular biology of the spindle matrix. Int. Rev. Cytol. 263, 155-206.
29. 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 micro-tubules that it crosslinks. Nature 435, 114-118.
30. Kapoor, T. M., Mayer, T. U., Coughlin, M. L., and Mitchison, T. J. (2000).Probing spindle assembly mechanisms with monastrol, a small molecule inhibitor of the mitotic kinesin, Eg5. J. Cell Biol. 150, 975-988.
31. Kapoor, T. M., and Mitchison, T. J. (2001). Eg5 is static in bipolar spindles relative to tubulin: evidence for a static spindle matrix. J. Cell Biol. 154,1125-1133.
32. Karsenti, E., and Vernos, I. (2001). The mitotic spindle: a self-made machine. Science 294, 543-547.
33. Kashina, A. S., Baskin, R. J., Cole, D. G., Wedaman, K. P., Saxton, W. M., and Scholey, J. M. (1996a). A bipolar kinesin. Nature 379, 270-272.
34. Kashina, A. S., Scholey, J. M., Leszyk, J. D., and Saxton, W. M. (1996b). Anessential bipolar mitotic motor. Nature 384, 225
35. Krzysiak, T. C., Grabe, M., and Gilbert, S. P. (2008). Getting in sync with dimeric Eg5. Initiation and regulation of the processive run. J. Biol. Chem. 283, 2078-2087.
36. Kwon, M., Morales-Mulia, S., Brust-Mascher, I., Rogers, G. C., Sharp, D. J.,and Scholey, J. M. (2004). The chromokinesin, KLP3A, dives mitotic spindle pole separation during prometaphase and anaphase and facilitates chromatid motility. Mol. Biol. Cell 15, 219-233.
37. Maddox, P., Desai, A., Oegema, K., Mitchison, T. J., and Salmon, E. D. (2002). Poleward microtubule flux is a major component of spindle dynamics and anaphase a in mitotic Drosophila embryos. Curr. Biol. 12, 1670-1674.
38. Maiato, H., and Sunkel, C. E. (2004). Kinetochore-microtubule interactions during cell division. Chromosome Res. 12, 585-597.
39. Mayer, T. U., Kapoor, T. M., Haggarty, S. J., King, R. W., Schreiber, S. L., and Mitchison, T. J. (1999). Small molecule inhibitor of mitotic spindle bipolarity identified in a phenotype-based screen. Science 286, 971-974.
40. McIntosh, J. R., Hepler, P., and Van Wie, D. G. (1969). Model for mitosis.Nature 224, 659-663.
41. Megraw, T. L., Kao, L. R., and Kaufman, T. C. (2001). Zygotic development without functional mitotic centrosomes. Curr. Biol. 11, 116-120.
42. Mogilner, A., Wollman, R., Civelekoglu-Scholey, G., and Scholey, J. M. (2006).Modeling Mitosis. Trends Cell Biol. 16, 88-96.
43. Morales-Mulia, S., and Scholey, J. M. (2005). Spindle pole organization in Drosophila S2 cells by dynein, abnormal spindle protein (Asp), and KLP10A.Mol. Biol. Cell 16, 3176-3186.
44. Postner, M. A., Miller, K. G., and Wieschaus, E. (1992). Maternal effect muta-tions of the sponge locus affect actin cytoskeletal rearrangement in Drosophila melanogaster embryos. J. Cell Biol. 119, 1205-1218.
45. Rogers, G. C., Rogers, S. L., Schwimmer, T. A., Ems-McClung, S. C., Walczak,C. E., Vale, R. D., Scholey, J. M., and Sharp, D. J. (2004). Two mitotic kinesins cooperate to drive sister chromatid separation during anaphase. Nature 427,364-370.
46. Rogers, G. C., Rogers, S. L., and Sharp, D. J. (2005). Spindle microtubules in flux. J. Cell Sci. 118, 1105-1116.
47. Saunders, A. M., Powers, J., Strome, S., and Saxton, W. M. (2007). Kinesin-5 acts as a brake in anaphase spindle elongation. Curr. Biol. 17, R453-454.
48. Saunders, W., Lengyel, V., and Hoyt, M. A. (1997). Mitotic spindle function in Saccharomyces cerevisiae requires a balance between different types of kinesin-related motors. Mol. Biol. Cell 8, 1025-1033.
49. Saunders, W. S., and Hoyt, M. A. (1992). Kinesin-related proteins required forstructural integrity of the mitotic spindle. Cell 70, 451-458.
50. Saunders, W. S., Koshland, D., Eshel, D., Gibbons, I. R., and Hoyt, M. A.(1995). Saccharomyces cerevisiae kinesin- and dynein-related proteins required for anaphase chromosome segregation. J. Cell Biol. 128, 617-624.
51. Sawin, K. E., LeGuellec, K., Philippe, M., and Mitchison, T. J. (1992). Mitotic spindle organization by a plus-end-directed microtubule motor. Nature 359,540-543.
52. Sawin, K. E., and Mitchison, T. J. (1995). Mutations in the kinesin-like protein Eg5 disrupting localization to the mitotic spindle. Proc. Natl. Acad. Sci. USA 92, 4289-4293.
53. Scholey, J. M. (1998). Functions of motor proteins in echinoderm embryos: anargument in support of antibody inhibition experiments. Cell Motil. Cytoske-let. 39, 257-260.
54. 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.
55. 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.
56. 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.
57. Sharp, D. J., Rogers, G. C., and Scholey, J. M. (2000c). Microtubule motors in mitosis. Nature 407, 41-47.
58. Sharp, D. J., Yu, K. R., Sisson, J. C., Sullivan, W., and Scholey, J. M. (1999b). Antagonistic microtubule-sliding motors position mitotic centrosomes in Dro-sophila early embryos. Nat. Cell Biol 1, 51-54.
59. Shirasu-Hiza, M., Perlman, Z. E., Wittmann, T., Karsenti, E., and Mitchison, T. J. (2004). Eg5 causes elongation of meiotic spindles when flux-associated microtubule depolymerization is blocked. Curr. Biol. 14, 1941-1945.
60. Silverman-Gavrila, R. V., and Wilde, A. (2006). Ran is required before meta-phase for spindle assembly and chromosome alignment and after metaphase for chromosome segregation and spindle midbody organization. Mol. Biol.Cell 17, 2069-2080.
61. Stevenson, V. A., Kramer, J., Kuhn, J., and Theurkauf, W. E. (2001). Centro-somes and the Scrambled protein coordinate microtubule-independent actin reorganization. Nat. Cell Biol. 3, 68-75.
62. Straight, A. F., Sedat, J. W., and Murray, A. W. (1998). Time-lapse microscopy reveals unique roles for kinesins during anaphase in budding yeast. J. Cell Biol. 143, 687-694.
63. Tao, L., Mogilner, A., Civelekoglu-Scholey, G., Wollman, R., Evans, J., Stahlberg,H., and Scholey, J. M. (2006). A homotetrameric kinesin-5, KLP61F, bundles microtubules and antagonizes Ncd in motility assays. Curr. Biol. 16, 2293-2302.
64. Tikhonenko, I., Nag, D. K., Martin, N., and Koonce, M. P. (2008). Kinesin-5 is not essential for mitotic spindle elongation in Dictyostelium. Cell Motil. Cy-toskelet. 65, 853-862.
65. Tsai, M. Y., Wang, S., Heidinger, J. M., Shumaker, D. K., Adam, S. A.,Goldman, R. D., and Zheng, Y. (2006). A mitotic lamin B matrix induced by RanGTP required for spindle assembly. Science 311, 1887-1893.
66. Uteng,M., Hentrich, C.,Miura,K., Bieling,P., and Surrey,T. (2008). Poleward transport of Eg5 by dynein-dynactin in Xenopus laevis egg extract spindles.J. Cell Biol. 182, 715-726.
67. Valentine, M.T., Fordyce, P.M., and Block, S.M. (2006a). Eg5 steps it up! Cell Div. 1, 31-38.
68. Valentine,M. T.,Fordyce,P. M.,Krzysiak,T. C.,Gilbert,S. P.,and Block,S. M.(2006b). Individual dimers of the mitotic kinesin motor Eg5 step processively and support substantial loads in vitro. Nat. Cell Biol. 8, 470-476.
69. Van den Wildenberg, S., Tao, L, Kapitein, L, Schmidt, C. F., Scholey, J. M., and Peterman, E.J.G. (2008). The homotetrameric kinesin-5 KLP61F preferentially crosslinks microtubules into antiparallel orientations. Curr. Biol. 18, 1860-1864.
70. Wadsworth, P., and Khodjakov, A. (2004). E pluribus unum: towards a universal mechanism for spindle assembly. Trends Cell Biol. 14, 413-419.
71. Walczak, C. E., and Heald, R. (2008). Mechanisms of mitotic spindle assembly and function. Int. Rev. Cytol. 265, 111-158.
72. Walczak, C. E., Vernos, I., Mitchison, T. J., Karsenti, E., and Heald, R. (1998).A model for the proposed roles of different microtubule-based motor proteins in establishing spindle bipolarity. Curr. Biol. 8, 903-913.
73. Wilson, P. G., Fuller, M. T., and Borisy, G. G. (1997). Monastral bipolar spindles: implications for dynamic centrosome organization. J. Cell Sci. 110(Pt 4), 451-464.
74. Wollman, R., Civelekoglu-Scholey, G., Scholey, J. M., and Mogilner, A. (2008).Reverse engineering of force integration during mitosis in the Drosophila embryo. Mol. Syst. Biol. 4, 195