Cytokinesis microtubule organisers at a glance

Journal of Cell Science

Volumn 125, Issue 15, 2012, Pages 3495-3500

  Lee, Kian Yong ^a   Davies, Tim ^a   Mishima, Masanori ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ACTININ; CLASP PROTEIN; GUANOSINE TRIPHOSPHATASE; KINESIN; KINESIN 4; MICROTUBULE ASSOCIATED PROTEIN; MITOTIC KINESIN LIKE PROTEIN 2; UNCLASSIFIED DRUG;

ANAPHASE; BLASTOMA; CELL PROLIFERATION; CELL STRUCTURE; CYTOKINESIS; MICROTUBULE; MOLECULAR DYNAMICS; NOTE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION;

CELL GROWTH PROCESSES; CYTOKINESIS; HUMANS; MICROTUBULES;

EID: 84869116731     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.094672     Document Type: Note

References (103)

1. Abaza, A., Soleilhac, J. M., Westendorf, J., Piel, M., Crevel, I., Roux, A. and Pirollet, F. (2003). M phase phosphoprotein 1 is a human plus-end-directed kinesinrelated protein required for cytokinesis. J. Biol. Chem. 278, 27844-27852.
2. Akhmanova, A. and Steinmetz, M. O. (2008). Tracking the ends: a dynamic protein network controls the fate of microtubule tips. Nat. Rev. Mol. Cell Biol. 9, 309-322.
3. Archambault, V. and Glover, D. M. (2009). Polo-like kinases: conservation and divergence in their functions and regulation. Nat. Rev. Mol. Cell Biol. 10, 265-275.
4. Arnaud, L., Pines, J. and Nigg, E. A. (1998). GFP tagging reveals human Polo-like kinase 1 at the kinetochore/centromere region of mitotic chromosomes. Chromosoma 107, 424-429.
5. Ban, R., Irino, Y., Fukami, K. and Tanaka, H. (2004). Human mitotic spindle-associated protein PRC1 inhibits MgcRacGAP activity toward Cdc42 during the metaphase. J. Biol. Chem. 279, 16394-16402.
6. Barr, F. A. and Gruneberg, U. (2007). Cytokinesis: placing and making the final cut. Cell 131, 847-860.
7. Bassi, Z. I., Verbrugghe, K. J., Capalbo, L., Gregory, S., Montembault, E., Glover, D. M. and D'Avino, P. P. (2011). Sticky/Citron kinase maintains proper RhoA localization at the cleavage site during cytokinesis. J. Cell Biol. 195, 595-603.
8. Bastos, R. N. and Barr, F. A. (2010). Plk1 negatively regulates Cep55 recruitment to the midbody to ensure orderly abscission. J. Cell Biol. 191, 751-760.
9. Bieling, P., Telley, I. A. and Surrey, T. (2010). A minimal midzone protein module controls formation and length of antiparallel microtubule overlaps. Cell 142, 420-432.
10. Bratman, S. V. and Chang, F. (2007). Stabilization of overlapping microtubules by fission yeast CLASP. Dev. Cell 13, 812-827.
11. Bringmann, H., Skiniotis, G., Spilker, A., Kandels-Lewis, S., Vernos, I. and Surrey, T. (2004). A kinesinlike motor inhibits microtubule dynamic instability. Science 303, 1519-1522.
12. Bringmann, H., Cowan, C. R., Kong, J. and Hyman, A. A. (2007). LET-99, GOA-1/GPA-16, and GPR-1/2 are required for aster-positioned cytokinesis. Curr. Biol. 17, 185-191.
13. Brown, K. D., Coulson, R. M., Yen, T. J. and Cleveland, D. W. (1994). Cyclin-like accumulation and loss of the putative kinetochore motor CENP-E results from coupling continuous synthesis with specific degradation at the end of mitosis. J. Cell Biol. 125, 1303-1312.
14. Buck, R. C. and Tisdale, J. M. (1962). The fine structure of the mid-body of the rat erythroblast. J. Cell Biol. 13, 109-115.
15. Caballe, A. and Martin-Serrano, J. (2011). ESCRT machinery and cytokinesis: the road to daughter cell separation. Traffic 12, 1318-1326.
16. Cai, S., Weaver, L. N., Ems-McClung, S. C. and Walczak, C. E. (2010). Proper organization of microtubule minus ends is needed for midzone stability and cytokinesis. Curr. Biol. 20, 880-885.
17. Canman, J. C., Lewellyn, L., Laband, K., Smerdon, S. J., Desai, A., Bowerman, B. and Oegema, K. (2008). Inhibition of Rac by the GAP activity of centralspindlin is essential for cytokinesis. Science 322, 1543-1546.
18. Cesario, J. M., Jang, J. K., Redding, B., Shah, N., Rahman, T. and McKim, K. S. (2006). Kinesin 6 family member Subito participates in mitotic spindle assembly and interacts with mitotic regulators. J. Cell Sci. 119, 4770-4780.
19. Chalamalasetty, R. B., Hümmer, S., Nigg, E. A. and Silljé, H. H. (2006). Influence of human Ect2 depletion and overexpression on cleavage furrow formation and abscission. J. Cell Sci. 119, 3008-3019.
20. D'Avino, P. P., Archambault, V., Przewloka, M. R., Zhang, W., Lilley, K. S., Laue, E. and Glover, D. M. (2007). Recruitment of Polo kinase to the spindle midzone during cytokinesis requires the Feo/Klp3A complex. PLoS ONE 2, e572.
21. D'Avino, P. P., Takeda, T., Capalbo, L., Zhang, W., Lilley, K. S., Laue, E. D. and Glover, D. M. (2008). Interaction between Anillin and RacGAP50C connects the actomyosin contractile ring with spindle microtubules at the cell division site. J. Cell Sci. 121, 1151-1158.
22. Douglas, M. E. and Mishima, M. (2010). Still entangled: assembly of the central spindle by multiple microtubule modulators. Semin. Cell Dev. Biol. 21, 899-908.
23. Douglas, M. E., Davies, T., Joseph, N. and Mishima, M. (2010). Aurora B and 14-3-3 coordinately regulate clustering of centralspindlin during cytokinesis. Curr. Biol. 20, 927-933.
24. Elad, N., Abramovitch, S., Sabanay, H. and Medalia, O. (2011). Microtubule organization in the final stages of cytokinesis as revealed by cryo-electron tomography. J. Cell Sci. 124, 207-215.
25. Fededa, J. P. and Gerlich, D. W. (2012). Molecular control of animal cell cytokinesis. Nat. Cell Biol. 14, 440-447.
26. Fu, C., Ward, J. J., Loiodice, I., Velve-Casquillas, G., Nedelec, F. J. and Tran, P. T. (2009). Phospho-regulated interaction between kinesin-6 Klp9p and microtubule bundler Ase1p promotes spindle elongation. Dev. Cell 17, 257-267.
27. Gai, M., Camera, P., Dema, A., Bianchi, F., Berto, G., Scarpa, E., Germena, G. and Di Cunto, F. (2011). Citron kinase controls abscission through RhoA and anillin. Mol. Biol. Cell 22, 3768-3778.
28. Ganem, N. J., Storchova, Z. and Pellman, D. (2007). Tetraploidy, aneuploidy and cancer. Curr. Opin. Genet. Dev. 17, 157-162.
29. Glotzer, M. (2009). The 3Ms of central spindle assembly: microtubules, motors and MAPs. Nat. Rev. Mol. Cell Biol. 10, 9-20.
30. Goodwin, S. S. and Vale, R. D. (2010). Patronin regulates the microtubule network by protecting microtubule minus ends. Cell 143, 263-274.
31. Goshima, G. and Vale, R. D. (2005). Cell cycledependent dynamics and regulation of mitotic kinesins in Drosophila S2 cells. Mol. Biol. Cell 16, 3896-3907.
32. Gregory, S. L., Ebrahimi, S., Milverton, J., Jones, W. M., Bejsovec, A. and Saint, R. (2008). Cell division requires a direct link between microtubule-bound RacGAP and Anillin in the contractile ring. Curr. Biol. 18, 25-29.
33. Gruneberg, U., Neef, R., Honda, R., Nigg, E. A. and Barr, F. A. (2004). Relocation of Aurora B from centromeres to the central spindle at the metaphase to anaphase transition requires MKlp2. J. Cell Biol. 166, 167-172.
34. Gruneberg, U., Neef, R., Li, X., Chan, E. H., Chalamalasetty, R. B., Nigg, E. A. and Barr, F. A. (2006). KIF14 and citron kinase act together to promote efficient cytokinesis. J. Cell Biol. 172, 363-372.
35. Guizetti, J. and Gerlich, D. W. (2010). Cytokinetic abscission in animal cells. Semin. Cell Dev. Biol. 21, 909-916.
36. Hamada, T. (2007). Microtubule-associated proteins in higher plants. J. Plant Res. 120, 79-98.
37. Hizlan, D., Mishima, M., Tittmann, P., Gross, H., Glotzer, M. and Hoenger, A. (2006). Structural analysis of the ZEN-4/CeMKLP1 motor domain and its interaction with microtubules. J. Struct. Biol. 153, 73-84.
38. Hu, C. K., Coughlin, M., Field, C. M. and Mitchison, T. J. (2011). KIF4 regulates midzone length during cytokinesis. Curr. Biol. 21, 815-824.
39. Hu, C. K., Coughlin, M. and Mitchison, T. J. (2012). Midbody assembly and its regulation during cytokinesis. Mol. Biol. Cell 23, 1024-1034.
40. Hümmer, S. and Mayer, T. U. (2009). Cdk1 negatively regulates midzone localization of the mitotic kinesin Mklp2 and the chromosomal passenger complex. Curr. Biol. 19, 607-612.
41. Hutterer, A., Glotzer, M. and Mishima, M. (2009). Clustering of centralspindlin is essential for its accumulation to the central spindle and the midbody. Curr. Biol. 19, 2043-2049.
42. Inoue, Y. H., do Carmo Avides, M., Shiraki, M., Deak, P., Yamaguchi, M., Nishimoto, Y., Matsukage, A. and Glover, D. M. (2000). Orbit, a novel microtubuleassociated protein essential for mitosis in Drosophila melanogaster. J. Cell Biol. 149, 153-166.
43. Inoue, Y. H., Savoian, M. S., Suzuki, T., Máthé, E., Yamamoto, M. T. and Glover, D. M. (2004). Mutations in orbit/mast reveal that the central spindle is comprised of two microtubule populations, those that initiate cleavage and those that propagate furrow ingression. J. Cell Biol. 166, 49-60.
44. Jantsch-Plunger, V., Gönczy, P., Romano, A., Schnabel, H., Hamill, D., Schnabel, R., Hyman, A. A. and Glotzer, M. (2000). CYK-4: A Rho family gtpase activating protein (GAP) required for central spindle formation and cytokinesis. J. Cell Biol. 149, 1391-1404.
45. Jiang, W., Jimenez, G., Wells, N. J., Hope, T. J., Wahl, G. M., Hunter, T. and Fukunaga, R. (1998). PRC1: a human mitotic spindle-associated CDK substrate protein required for cytokinesis. Mol. Cell 2, 877-885.
46. Joseph, N., Hutterer, A., Poser, I. and Mishima, M. (2012) ARF6 GTPase protects the post-mitotic midbody from 14-3-3-mediated disintegration. EMBO J. 31, 2604-2614.
47. Julian, M., Tollon, Y., Lajoie-Mazenc, I., Moisand, A., Mazarguil, H., Puget, A. and Wright, M. (1993). gamma-Tubulin participates in the formation of the midbody during cytokinesis in mammalian cells. J. Cell Sci. 105, 145-156.
48. Kamijo, K., Ohara, N., Abe, M., Uchimura, T., Hosoya, H., Lee, J. S. and Miki, T. (2006). Dissecting the role of Rho-mediated signaling in contractile ring formation. Mol. Biol. Cell 17, 43-55.
49. Kapitein, L. C., Janson, M. E., van den Wildenberg, S. M., Hoogenraad, C. C., Schmidt, C. F. and Peterman, E. J. (2008). Microtubule-driven multimerization recruits ase1p onto overlapping microtubules. Curr. Biol. 18, 1713-1717.
50. Kurasawa, Y., Earnshaw, W. C., Mochizuki, Y., Dohmae, N. and Todokoro, K. (2004). Essential roles of KIF4 and its binding partner PRC1 in organized central spindle midzone formation. EMBO J. 23, 3237-3248.
51. Lacroix, B. and Maddox, A. S. (2012). Cytokinesis, ploidy and aneuploidy. J. Pathol. 226, 338-351.
52. Li, H., Mao, T., Zhang, Z. and Yuan, M. (2007). The AtMAP65-1 cross-bridge between microtubules is formed by one dimer. Plant Cell Physiol. 48, 866-874.
53. Liu, J., Wang, Z., Jiang, K., Zhang, L., Zhao, L., Hua, S., Yan, F., Yang, Y., Wang, D., Fu, C. et al. (2009). PRC1 cooperates with CLASP1 to organize central spindle plasticity in mitosis. J. Biol. Chem. 284, 23059-23071.
54. Makyio, H., Ohgi, M., Takei, T., Takahashi, S., Takatsu, H., Katoh, Y., Hanai, A., Ueda, T., Kanaho, Y., Xie, Y. et al. (2012) Structural basis for Arf6-MKLP1 complex formation on the Flemming body responsible for cytokinesis. EMBO J. 31, 2590-2603.
55. 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.
56. Mazumdar, M., Sundareshan, S. and Misteli, T. (2004). Human chromokinesin KIF4A functions in chromosome condensation and segregation. J. Cell Biol. 166, 613-620.
57. Mazumdar, M., Lee, J. H., Sengupta, K., Ried, T., Rane, S. and Misteli, T. (2006). Tumor formation via loss of a molecular motor protein. Curr. Biol. 16, 1559-1564.
58. McIntosh, J. R. and Landis, S. C. (1971). The distribution of spindle microtubules during mitosis in cultured human cells. J. Cell Biol. 49, 468-497.
59. Miller, A. L. and Bement, W. M. (2009). Regulation of cytokinesis by Rho GTPase flux. Nat. Cell Biol. 11, 71-77.
60. Mishima, M., Kaitna, S. and Glotzer, M. (2002). Central spindle assembly and cytokinesis require a kinesin-like protein/RhoGAP complex with microtubule bundling activity. Dev. Cell 2, 41-54.
61. Mishima, M., Pavicic, V., Grüneberg, U., Nigg, E. A. and Glotzer, M. (2004). Cell cycle regulation of central spindle assembly. Nature 430, 908-913.
62. 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.
63. Montembault, E., Zhang, W., Przewloka, M. R., Archambault, V., Sevin, E. W., Laue, E. D., Glover, D. M. and D'Avino, P. P. (2010). Nessun Dorma, a novel centralspindlin partner, is required for cytokinesis in Drosophila spermatocytes. J. Cell Biol. 191, 1351-1365.
64. Murthy, K. and Wadsworth, P. (2008). Dual role for microtubules in regulating cortical contractility during cytokinesis. J. Cell Sci. 121, 2350-2359.
65. Neef, R., Preisinger, C., Sutcliffe, J., Kopajtich, R., Nigg, E. A., Mayer, T. U. and Barr, F. A. (2003). Phosphorylation of mitotic kinesin-like protein 2 by pololike kinase 1 is required for cytokinesis. J. Cell Biol. 162, 863-876.
66. Neef, R., Gruneberg, U., Kopajtich, R., Li, X., Nigg, E. A., Sillje, H. and Barr, F. A. (2007). Choice of Plk1 docking partners during mitosis and cytokinesis is controlled by the activation state of Cdk1. Nat. Cell Biol. 9, 436-444.
67. Neto, H. and Gould, G. W. (2011). The regulation of abscission by multi-protein complexes. J. Cell Sci. 124, 3199-3207.
68. Nishimura, Y. and Yonemura, S. (2006). Centralspindlin regulates ECT2 and RhoA accumulation at the equatorial cortex during cytokinesis. J. Cell Sci. 119, 104-114.
69. Nislow, C., Lombillo, V. A., Kuriyama, R. and McIntosh, J. R. (1992). A plus-end-directed motor enzyme that moves antiparallel microtubules in vitro localizes to the interzone of mitotic spindles. Nature 359, 543-547.
70. Paramasivam, M., Chang, Y. J. and LoTurco, J. J. (2007). ASPM and citron kinase co-localize to the midbody ring during cytokinesis. Cell Cycle 6, 1605-1612.
71. Pavicic-Kaltenbrunner, V., Mishima, M. and Glotzer, M. (2007). Cooperative assembly of CYK-4/MgcRacGAP and ZEN-4/MKLP1 to form the centralspindlin complex. Mol. Biol. Cell 18, 4992-5003.
72. Paweletz, N. (1967). Zur Funktion des "Flemming-Körpers"bei der Teilung tierischer Zellen Naturwissenschaften 54, 533-535.
73. Piekny, A., Werner, M. and Glotzer, M. (2005). Cytokinesis: welcome to the Rho zone. Trends Cell Biol. 15, 651-658.
74. Piekny, A. J. and Maddox, A. S. (2010). The myriad roles of Anillin during cytokinesis. Semin. Cell Dev. Biol. 21, 881-891.
75. Ruchaud, S., Carmena, M. and Earnshaw, W. C. (2007). Chromosomal passengers: conducting cell division. Nat. Rev. Mol. Cell Biol. 8, 798-812.
76. Sagona, A. P., Nezis, I. P., Pedersen, N. M., Liestøl, K., Poulton, J., Rusten, T. E., Skotheim, R. I., Raiborg, C. and Stenmark, H. (2010). PtdIns(3)P controls cytokinesis through KIF13A-mediated recruitment of FYVE-CENT to the midbody. Nat. Cell Biol. 12, 362-371.
77. Sasabe, M. and Machida, Y. (2006). MAP65: a bridge linking a MAP kinase to microtubule turnover. Curr. Opin. Plant Biol. 9, 563-570.
78. Savoian, M. S., Gatt, M. K., Riparbelli, M. G., Callaini, G. and Glover, D. M. (2004). Drosophila Klp67A is required for proper chromosome congression and segregation during meiosis I. J. Cell Sci. 117, 3669-3677.
79. Saxton, W. M. and McIntosh, J. R. (1987). Interzone microtubule behavior in late anaphase and telophase spindles. J. Cell Biol. 105, 875-886.
80. Schuyler, S. C., Liu, J. Y. and Pellman, D. (2003). The molecular function of Ase1p: evidence for a MAPdependent midzone-specific spindle matrix. J. Cell Biol. 160, 517-528.
81. Sekine, Y., Okada, Y., Noda, Y., Kondo, S., Aizawa, H., Takemura, R. and Hirokawa, N. (1994). A novel microtubule-based motor protein (KIF4) for organelle transports, whose expression is regulated developmentally. J. Cell Biol. 127, 187-201.
82. Severson, A. F., Hamill, D. R., Carter, J. C., Schumacher, J. and Bowerman, B. (2000). The aurorarelated kinase AIR-2 recruits ZEN-4/CeMKLP1 to the mitotic spindle at metaphase and is required for cytokinesis. Curr. Biol. 10, 1162-1171.
83. Shu, H. B., Li, Z., Palacios, M. J., Li, Q. and Joshi, H. C. (1995). A transient association of gamma-tubulin at the midbody is required for the completion of cytokinesis during the mammalian cell division. J. Cell Sci. 108, 2955-2962.
84. Simon, G. C., Schonteich, E., Wu, C. C., Piekny, A., Ekiert, D., Yu, X., Gould, G. W., Glotzer, M. and Prekeris, R. (2008). Sequential Cyk-4 binding to ECT2 and FIP3 regulates cleavage furrow ingression and abscission during cytokinesis. EMBO J. 27, 1791-1803.
85. Slep, K. C. (2009). The role of TOG domains in microtubule plus end dynamics. Biochem. Soc. Trans. 37, 1002-1006.
86. Somers, W. G. and Saint, R. (2003). A RhoGEF and Rho family GTPase-activating protein complex links the contractile ring to cortical microtubules at the onset of cytokinesis. Dev. Cell 4, 29-39.
87. Subramanian, R., Wilson-Kubalek, E. M., Arthur, C. P., Bick, M. J., Campbell, E. A., Darst, S. A., Milligan, R. A. and Kapoor, T. M. (2010). Insights into antiparallel microtubule crosslinking by PRC1, a conserved nonmotor microtubule binding protein. Cell 142, 433-443.
88. Uehara, R. and Goshima, G. (2010). Functional central spindle assembly requires de novo microtubule generation in the interchromosomal region during anaphase. J. Cell Biol. 191, 259-267.
89. Uehara, R., Nozawa, R. S., Tomioka, A., Petry, S., Vale, R. D., Obuse, C. and Goshima, G. (2009). The augmin complex plays a critical role in spindle microtubule generation for mitotic progression and cytokinesis in human cells. Proc. Natl. Acad. Sci. USA 106, 6998-7003.
90. Unno, K., Hanada, T. and Chishti, A. H. (2008). Functional involvement of human discs large tumor suppressor in cytokinesis. Exp. Cell Res. 314, 3118-3129.
91. Verbrugghe, K. J. and White, J. G. (2004). SPD-1 is required for the formation of the spindle midzone but is not essential for the completion of cytokinesis in C. elegans embryos. Curr. Biol. 14, 1755-1760.
92. Verní, F., Somma, M. P., Gunsalus, K. C., Bonaccorsi, S., Belloni, G., Goldberg, M. L. and Gatti, M. (2004). Feo, the Drosophila homolog of PRC1, is required for central-spindle formation and cytokinesis. Curr. Biol. 14, 1569-1575.
93. von Dassow, G., Verbrugghe, K. J., Miller, A. L., Sider, J. R. and Bement, W. M. (2009). Action at a distance during cytokinesis. J. Cell Biol. 187, 831-845.
94. Walczak, C. E. (2005). CLASP fluxes its mitotic muscles. Nat. Cell Biol. 7, 5-7.
95. Wang, S. Z. and Adler, R. (1995). Chromokinesin: a DNA-binding, kinesin-like nuclear protein. J. Cell Biol. 128, 761-768.
96. Williams, B. C., Riedy, M. F., Williams, E. V., Gatti, M. and Goldberg, M. L. (1995). The Drosophila kinesin-like protein KLP3A is a midbody component required for central spindle assembly and initiation of cytokinesis. J. Cell Biol. 129, 709-723.
97. Yamada, T., Hikida, M. and Kurosaki, T. (2006). Regulation of cytokinesis by mgcRacGAP in B lymphocytes is independent of GAP activity. Exp. Cell Res. 312, 3517-3525.
98. Yüce, O., Piekny, A. and Glotzer, M. (2005). An ECT2-centralspindlin complex regulates the localization and function of RhoA. J. Cell Biol. 170, 571-582.
99. Zavortink, M., Contreras, N., Addy, T., Bejsovec, A. and Saint, R. (2005). Tum/RacGAP50C provides a critical link between anaphase microtubules and the assembly of the contractile ring in Drosophila melanogaster. J. Cell Sci. 118, 5381-5392.
100. Zhao, W. M. and Fang, G. (2005). MgcRacGAP controls the assembly of the contractile ring and the initiation of cytokinesis. Proc. Natl. Acad. Sci. USA 102, 13158-13163.
101. Zhao, W. M., Seki, A. and Fang, G. (2006). Cep55, a microtubule-bundling protein, associates with centralspindlin to control the midbody integrity and cell abscission during cytokinesis. Mol. Biol. Cell 17, 3881-3896.
102. 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.
103. Zhu, C., Lau, E., Schwarzenbacher, R., Bossy-Wetzel, E. and Jiang, W. (2006). Spatiotemporal control of spindle midzone formation by PRC1 in human cells. Proc. Natl. Acad. Sci. USA 103, 6196-6201.