Taxol-stabilized microtubules can position the cytokinetic furrow in mammalian cells

Molecular Biology of the Cell

Volumn 16, Issue 9, 2005, Pages 4423-4436

  Shannon, Katie B ^a   Canman, Julie C ^b   Moree, C Ben ^a   Tirnauer, Jennifer S ^c   Salmon, E D ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF OREGON   (United States)

^c UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CELL PROTEIN; INNER CENTROMERE PROTEIN; MYOSIN; PACLITAXEL; UNCLASSIFIED DRUG;

ANAPHASE; ANIMAL CELL; ARTICLE; CELL DIVISION; CELL INTERACTION; CELL KINETICS; CELL SUBPOPULATION; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOKINESIS; MAMMAL CELL; METAPHASE; MICROTUBULE; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN STABILITY; RAT;

ANAPHASE; ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; CELL COMMUNICATION; CELL LINE; CYTOKINESIS; HUMANS; IMMUNOHISTOCHEMISTRY; MICROTUBULES; MITOTIC SPINDLE APPARATUS; PACLITAXEL; POTOROIDAE;

MAMMALIA;

EID: 24344494350     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E04-11-0974     Document Type: Article

References (66)

1. Adams, R. R., Maiato, H., Earnshaw, W. C., and Carmena, M. (2001). Essential roles of Drosophila inner centromere protein (INCENP) and aurora B. in histone H3 phosphorylation, metaphase chromosome alignment, kinetochore disjunction, and chromosome segregation. J. Cell Biol. 153, 865-880.
2. Adams, R. ., Tavares, A. A., Salzberg, A., Bellen, H. J., and Glover, D. M. (1998). pavarotti encodes a kinesin-like protein required to organize the central spindle and contractile ring for cytokinesis. Genes Dev. 12, 1483-1494.
3. Alsop, G. B., and Zhang, D. (2003). Microtubules are the only structural constituent of the spindle apparatus required for induction of cell cleavage. J. Cell Biol. 162, 383-390.
4. Amin-Hanjani, S., and Wadsworth, P. (1991). Inhibition of spindle elongation by taxol. Cell Motil. Cytoskeleton 20, 136-144.
5. Amos, L. A., and Lowe, J. (1999). How Taxol stabilises microtubule structure. Chem. Biol. 6, R65-R69.
6. Arnal, I., and Wade, R. H. (1995). How does taxol stabilize microtubules? Curr. Biol. 5, 900-908.
7. Beams, H. W., and Evans, T. C. (1940). Some effects of colchicine upon the first cleavage in Arbacia punctulata. The Biol. Bull. 79, 188-198.
8. Canman, J. C., Cameron, L. A., Maddox, P. S., Straight, A., Tirnauer, J. S., Mitchison, T. J., Fang, G., Kapoor, T. M., and Salmon, E. D. (2003). Determining the position of the cell division plane. Nature 424, 1074-1078.
9. Canman, J. C., Hoffman, D. B., and Salmon, E. D. (2000). The role of pre- and post-anaphase microtubules in the cytokinesis phase of the cell cycle. Curr. Biol. 10, 611-614.
10. Canman, J. C., Salmon, E. D., and Fang, G. (2002). Inducing precocious anaphase in cultured mammalian cells. Cell Motil. Cytoskeleton 52, 61-65.
11. Cao, L. G., and Wang, Y. L. (1996). Signals from the spindle midzone are required for the stimulation of cytokinesis in cultured epithelial cells. Mol. Biol. Cell 7, 225-232.
12. Conklin, E. G. (1917). Effects of centrifugal force on the structure and development of the eggs of Crepidula. J. Exp. Zool. 22, 311-419.
13. Cooke, C. A., Heck, M. M., and Earnshaw, W. C. (1987). The inner centromere protein (INCENP) antigens: movement from inner centromere to midbody during mitosis. J. Cell Biol. 105, 2053-2067.
14. De Brabander, M., Geuens, G., Nuydens, R., Willebrords, R., Aerts, F., and De Mey, J. (1986). Microtubule dynamics during the cell cycle: the effects of taxol and nocodazole on the microtubule system of Pt K2 cells at different stages of the mitotic cycle. Int. Rev. Cytol. 101, 215-274.
15. De Brabander, M., Geuens, G., Nuydens, R., Willebrords, R., and De Mey, J. (1981). Taxol induces the assembly of free microtubules in living cells and blocks the organizing capacity of the centrosomes and kinetochores. Proc. Natl. Acad. Sci. USA 78, 5608-5612.
16. Dechant, R., and Glotzer, M. (2003). Centrosome separation and central spindle assembly act in redundant pathways that regulate microtubule density and trigger cleavage furrow formation. Dev. Cell 4, 333-344.
17. Eckley, D. M., Ainsztein, A. M., Mackay, A. M., Goldberg, I. G., and Earnshaw, W. C. (1997). Chromosomal proteins and cytokinesis: patterns of cleavage furrow formation and inner centromere protein positioning in mitotic heterokaryons and mid-anaphase cells. J. Cell Biol. 136, 1169-1183.
18. Field, C. M., and Alberts, B. M. (1995). Anillin, a contractile ring protein that cycles from the nucleus to the cell cortex. J. Cell Biol. 131, 165-178.
19. Fishkind, D. J., and Wang, Y. L. (1993). Orientation and three-dimensional organization of actin filaments in dividing cultured cells. J. Cell Biol. 123, 837-848.
20. Hamaguchi, Y. (1975). Microinjection of colchicine into sea urchin eggs. Dev Growth Differ 17, 111-117.
21. Hamaguchi, Y. (1998). Displacement of cleavage plane in the sea urchin egg by locally applied taxol. Cell Motil. Cytoskeleton 40, 211-219.
22. Harvey, E. B. (1935). The mitotic figure and cleavage plane in the egg of Parechinus microtuberculatus, as influenced by centrifugal force. Biol. Bull. 69, 287-297.
23. Hiramoto, Y. (1956). Cell division without mitotic apparatus in sea urchin eggs. Exp. Cell Res. 11, 630-636.
24. Hyman, A., Drechsel, D., Kellogg, D., Salser, S., Sawin, K., Steffen, P., Wordeman, L., and Mitchison, T. (1991). Preparation of modified tubulins. Methods Enzymol 196, 478-485.
25. Jiang, W., Jimenez, G., Wells, N. J., Hope, T. J., Wahl, G. M., Hunter, T., and Fukunaga, R. (1998). PRC 1, a human mitotic spindle-associated CDK substrate protein required for cytokinesis. Mol Cell 2, 877-885.
26. Kishi, K., Sasaki, T., Kuroda, S., Itoh, T., and Takai, Y. (1993). Regulation of cytoplasmic division of Xenopus embryo by rho p21 and its inhibitory GDP/GTP exchange protein (rho GDI). J. Cell Biol. 120, 1187-1195.
27. Kuriyama, R., Gustus, C., Terada, Y., Uetake, Y., and Matuliene, J. (2002). CHO1, a mammalian kinesin-like protein, interacts with F-actin and is involved in the terminal phase of cytokinesis. J. Cell Biol. 156, 783-790.
28. Luo, X., Fang, G., Coldiron, M., Lin, Y., Yu, H., Kirschner, M. W., and Wagner, G. (2000). Structure of the Mad2 spindle assembly checkpoint protein and its interaction with Cdc20. Nat. Struct. Biol. 7, 224-229.
29. Mabuchi, I., Hamaguchi, Y., Fujimoto, H., Morii, N., Mishima, M., and Narumiya, S. (1993). A rho-like protein is involved in the organisation of the contractile ring in dividing sand dollar eggs. Zygote 1, 325-331.
30. Mabuchi, I., and Okuno, M. (1977). The effect of myosin antibody on the division of starfish blastomeres. J. Cell Biol. 74, 251-263.
31. Mackay, A. M., Ainsztein, A. M., Eckley, D. M., and Earnshaw, W. C. (1998). A dominant mutant of inner centromere protein (INCENP), a chromosomal protein, disrupts prometaphase congression and cytokinesis. J. Cell Biol. 140, 991-1002.
32. Maddox, P. S., Moree, B., Canman, J. C., and Salmon, E. D. (2003). Spinning disk confocal microscope system for rapid high-resolution, multimode, fluorescence speckle microscopy and green fluorescent protein imaging in living cells. Methods Enzymol. 360, 597-617.
33. Martineau, S. N., Andreassen, P. R., and Margolis, R. L. (1995). Delay of HeLa cell cleavage into interphase using dihydrocytochalasin B: retention of a postmitotic spindle and telophase disc correlates with synchronous cleavage recovery. J. Cell Biol. 131, 191-205.
34. Matuliene, J., and Kuriyama, R. (2002). Kinesin-like protein CHO1 is required for the formation of midbody matrix and the completion of cytokinesis in mammalian cells. Mol. Biol. Cell 13, 1832-1845.
35. Mollinari, C., Kleman, J. P., Jiang, W., Schoehn, G., Hunter, T., and Margolis, R. L. (2002). PRC1 is a microtubule binding and bundling protein essential to maintain the mitotic spindle midzone. J. Cell Biol. 157, 1175-1186.
36. Mollinari, C., Kleman, J. P., Saoudi, Y., Jablonski, S. A., Perard, J., Yen, T. J., and Margolis, R. L. (2005). Ablation of PRC1 by small interfering RNA demonstrates that cytokinetic abscission requires a central spindle bundle in mammalian cells, whereas completion of furrowing does not. Mol. Biol. Cell 16, 1043-1055.
37. Morrison, E. E., Wardleworth, B. N., Askham, J. M., Markham, A. F., and Meredith, D. M. (1998). EB1, a protein which interacts with the APC tumour suppressor, is associated with the microtubule cytoskeleton throughout the cell cycle. Oncogene 17, 3471-3477.
38. Murata-Hori, M., and Wang, Y. L. (2002). Both midzone and astral microtubules are involved in the delivery of cytokinesis signals: insights from the mobility of aurora B. J. Cell Biol. 159, 45-53.
39. O'Connell, C. B., Wheatley, S. P., Ahmed, S., and Wang, Y. L. (1999). The small GTP-binding protein rho regulates cortical activities in cultured cells during division. J. Cell Biol. 144, 305-313.
40. Oegema, K., Savoian, M. S., Mitchison, T. J., and Field, C. M. (2000). Functional analysis of a human homologue of the Drosophila actin binding protein anillin suggests a role in cytokinesis. J. Cell Biol. 150, 539-552.
41. Rappaport, R. (1985). Repeated furrow formation from a single mitotic apparatus in cylindrical sand dollar eggs. J. Exp. Zool. 234, 167-171.
42. Rappaport, R. (1986). Establishment of the mechanism of cytokinesis in animal cells. Int. Rev. Cytol. 105, 245-281.
43. Rappaport, R., and Ebstein, R. P. (1965). Duration of stimulus and latent periods preceding furrow formation in sand dollar eggs. J. Exp. Zool. 158, 373-382.
44. Rappaport, R., and Rappaport, B. N. (1974). Establishment of cleavage furrows by the mitotic spindle. J. Exp. Zool. 189, 189-196.
45. Rieder, C. L., and Hard, R. (1990). Newt lung epithelial cells: cultivation, use, and advantages for biomedical research. Int. Rev. Cytol. 122, 153-220.
46. Rusan, N. M., Fagerstrom, C. J., Yvon, A. M., and Wadsworth, P. (2001). Cell cycle-dependent changes in microtubule dynamics in living cells expressing green fluorescent protein-alpha tubulin. Mol. Biol. Cell 12, 971-980.
47. Salmon, E. D., and Wolniak, S. M. (1984). Taxol stabilization of mitotic spindle microtubules: analysis using calcium-induced depolymerization. Cell Motil. 4, 155-167.
48. Salmon, E. D., and Wolniak, S. M. (1990). Role of microtubules in stimulating cytokinesis in animal cells. Ann. N.Y. Acad. Sci. 582, 88-98.
49. Sanger, J. M., Mittal, B., Dome, J. S., and Sanger, J. W. (1989). Analysis of cell division using fluorescently labeled actin and myosin in living PtK2 cells. Cell Motil. Cytoskeleton 14, 201-219.
50. Savoian, M. S., Earnshaw, W. C., Khodjakov, A., and Rieder, C. L. (1999). Cleavage furrows formed between centrosomes lacking an intervening spindle and chromosomes contain microtubule bundles, INCENP, and CHO1 but not CENP-E. Mol. Biol. Cell 10, 297-311.
51. Schiff, P. B., Fant, J., and Horwitz, S. B. (1979). Promotion of microtubule assembly in vitro by taxol. Nature 277, 665-667.
52. Schiff, P. B., and Horwitz, S. B. (1980). Taxol stabilizes microtubules in mouse fibroblast cells. Proc. Natl. Acad. Sci. USA 77, 1561-1565.
53. Schroeder, T. E. (1972). The contractile ring. II. Determining its brief existence, volumetric changes, and vital role in cleaving Arbacia eggs. J. Cell Biol. 53, 419-434.
54. Shannon, K. B., Canman, J. C., and Salmon, E. D. (2002). Mad2 and BubR1 function in a single checkpoint pathway that responds to a loss of tension. Mol. Biol. Cell 13, 3706-3719.
55. Snyder, J. A., and McLelland, S. L. (1996). Taxol reduces the rate of cytokinesis in PtKl cells. Cell Biol. Int. 20, 573-578.
56. Snyder, J. A., and Mullins, J. M. (1993). Analysis of spindle microtubule organization in untreated and taxol-treated PtK1 cells. Cell Biol. Int. 17, 1075-1084.
57. Straight, A. F., Cheung, A., Limouze, J., Chen, I., Westwood, N. J., Sellers, J. R., and Mitchison, T. J. (2003). Dissecting temporal and spatial control of cytokinesis with a myosin II Inhibitor. Science 299, 1743-1747.
58. Tirnauer, J. S., Canman, J. C., Salmon, E. D., and Mitchison, T. J. (2002). EB1 targets to kinetochores with attached, polymerizing microtubules. Mol. Biol. Cell 13, 4308-4316.
59. Tolliday, N., VerPlank, L., and Li, R. (2002). Rho1 directs formin-mediated actin ring assembly during budding yeast cytokinesis. Curr. Biol. 12, 1864-1870.
60. Waterman-Storer, C. M., Desai, A., Bulinski, J. C., and Salmon, E. D. (1998). Fluorescent speckle microscopy, a method to visualize the dynamics of protein assemblies in living cells. Curr. Biol. 8, 1227-1230.
61. Waterman-Storer, C. M., Worthylake, R. A., Liu, B. P., Burridge, K., and Salmon, E. D. (1999). Microtubule growth activates Rac1 to promote lamellipodial protrusion in fibroblasts. Nat. Cell Biol. 1, 45-50.
62. Waters, J. C., Mitchison, T. J., Rieder, C. L., and Salmon, E. D. (1996). The kinetochore microtubule minus-end disassembly associated with poleward flux produces a force that can do work. Mol. Biol. Cell 7, 1547-1558.
63. Wheatley, S. P., Kandels-Lewis, S. E., Adams, R. R., Ainsztein, A. M., and Earnshaw, W. C. (2001). INCENP binds directly to tubulin and requires dynamic microtubules to target to the cleavage furrow. Exp. Cell Res. 262, 122-127.
64. Wheatley, S. P., and Wang, Y. (1996). Midzone microtubule bundles are continuously required for cytokinesis in cultured epithelial cells. J. Cell Biol. 135, 981-989.
65. Yvon, A. M., Wadsworth, P., and Jordan, M. A. (1999). Taxol suppresses dynamics of individual microtubules in living human tumor cells. Mol. Biol. Cell 10, 947-959.
66. Zhu, C., and Jiang, W. (2005). Cell cycle-dependent translocation of PRC1 on the spindle by Kif4 is essential for midzone formation and cytokinesis. Proc. Natl. Acad. Sci. USA 102, 343-348.