Aurora B suppresses microtubule dynamics and limits central spindle size by locally activating KIF4A

Journal of Cell Biology

Volumn 202, Issue 4, 2013, Pages 605-621

  Bastos, Ricardo Nunes ^a   Gandhi, Sapan R ^a   Baron, Ryan D ^a,b   Gruneberg, Ulrike ^a   Nigg, Erich A ^c   Barr, Francis A ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA B KINASE; KIF4A PROTEIN; KINESIN; MOLECULAR MOTOR; POLYCOMB GROUP PROTEIN; UNCLASSIFIED DRUG;

ANAPHASE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IN VITRO STUDY; MICROTUBULE; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; SPINDLE CELL;

ANIMALS; CELLS, CULTURED; HELA CELLS; HUMANS; KINESIN; MICROTUBULES; MITOTIC SPINDLE APPARATUS; PROTEIN-SERINE-THREONINE KINASES; SPODOPTERA;

EID: 84884249418     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201301094     Document Type: Article

References (69)

1. Akhmanova, A., and M.O. Steinmetz. 2008. Tracking the ends: a dynamic protein network controls the fate of microtubule tips. Nat. Rev. Mol. Cell Biol. 9:309-322. http://dx.doi.org/10.1038/nrm2369
2. Akhmanova, A., and M.O. Steinmetz 2010. Microtubule +TIPs at a glance. J. Cell Sci. 123:3415-3419. http://dx.doi.org/10.1242/jcs.062414
3. Alexander, J., D. Lim, B.A. Joughin, B. Hegemann, J.R. Hutchins, T. Ehrenberger, F. Ivins, F. Sessa, O. Hudecz, E.A. Nigg, et al. 2011. Spatial exclusivity combined with positive and negative selection of phosphorylation motifs is the basis for context-dependent mitotic signaling. Sci. Signal. 4:ra42. http://dx.doi.org/10.1126/scisignal.2001796
4. Andrews, P.D., Y. Ovechkina, N. Morrice, M. Wagenbach, K. Duncan, L. Wordeman, and J.R. Swedlow. 2004. Aurora B regulates MCAK at the mitotic centromere. Dev. Cell. 6:253-268. http://dx.doi.org/10.1016/S1534-5807(04)00025-5
5. Bastos, R.N., and F.A. Barr. 2010. Plk1 negatively regulates Cep55 recruitment to the midbody to ensure orderly abscission. J. Cell Biol. 191:751-760. http://dx.doi.org/10.1083/jcb.201008108
6. Bastos, R.N., X. Penate, M. Bates, D. Hammond, and F.A. Barr. 2012. CYK4 inhibits Rac1-dependent PAK1 and ARHGEF7 effector pathways during cytokinesis. J. Cell Biol. 198:865-880. http://dx.doi.org/10.1083/jcb.201204107
7. Bayliss, R., T. Sardon, I. Vernos, and E. Conti. 2003. Structural basis of Aurora-A activation by TPX2 at the mitotic spindle. Mol. Cell. 12:851-862. http://dx.doi.org/10.1016/S1097-2765(03)00392-7
8. Bieling, P., I.A. Telley, and T. Surrey. 2010. A minimal midzone protein module controls formation and length of antiparallel microtubule overlaps. Cell. 142:420-432. http://dx.doi.org/10.1016/j.cell.2010.06.033
9. Blangy, A., H.A. Lane, P. d'Hérin, M. Harper, M. Kress, and E.A. Nigg. 1995. Phosphorylation by p34cdc2 regulates spindle association of human Eg5, a kinesin-related motor essential for bipolar spindle formation in vivo. Cell. 83:1159-1169. http://dx.doi.org/10.1016/0092-8674(95)90142-6
10. Bringmann, H., G. Skiniotis, A. Spilker, S. Kandels-Lewis, I. Vernos, and T. Surrey. 2004. A kinesin-like motor inhibits microtubule dynamic instability. Science. 303:1519-1522. http://dx.doi.org/10.1126/science.1094838
11. Castoldi, M., and A.V. Popov. 2003. Purification of brain tubulin through two cycles of polymerization-depolymerization in a high-molarity buffer. Protein Expr. Purif. 32:83-88. http://dx.doi.org/10.1016/S1046-5928(03)00218-3
12. Cox, J., and M. Mann. 2008. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26:1367-1372. http://dx.doi.org/10.1038/nbt.1511
13. Cox, J., I. Matic, M. Hilger, N. Nagaraj, M. Selbach, J.V. Olsen, and M. Mann. 2009. A practical guide to the MaxQuant computational platform for SILACbased quantitative proteomics. Nat. Protoc. 4:698-705. http://dx.doi.org/10.1038/nprot.2009.36
14. Desai, A., and T.J. Mitchison. 1997. Microtubule polymerization dynamics. Annu. Rev. Cell Dev. Biol. 13:83-117. http://dx.doi.org/10.1146/annurev .cellbio.13.1.83
15. Douglas, M.E., T. Davies, N. Joseph, and M. Mishima. 2010. Aurora B and 14-3-3 coordinately regulate clustering of centralspindlin during cytokinesis. Curr. Biol. 20:927-933. http://dx.doi.org/10.1016/j.cub.2010.03.055
16. Eggert, U.S., T.J. Mitchison, and C.M. Field. 2006. Animal cytokinesis: from parts list to mechanisms. Annu. Rev. Biochem. 75:543-566. http://dx.doi.org/10.1146/annurev.biochem.74.082803.133425
17. Elad, N., S. Abramovitch, H. Sabanay, and O. Medalia. 2011. Microtubule organization in the final stages of cytokinesis as revealed by cryo-electron tomography. J. Cell Sci. 124:207-215. http://dx.doi.org/10.1242/jcs .073486
18. Fabbro, M., B.B. Zhou, M. Takahashi, B. Sarcevic, P. Lal, M.E. Graham, B.G. Gabrielli, P.J. Robinson, E.A. Nigg, Y. Ono, and K.K. Khanna. 2005. Cdk1/Erk2-and Plk1-dependent phosphorylation of a centrosome protein, Cep55, is required for its recruitment to midbody and cytokinesis. Dev. Cell. 9:477-488. http://dx.doi.org/10.1016/j.devcel.2005.09.003
19. Friel, C.T., and J. Howard. 2012. Coupling of kinesin ATP turnover to translocation and microtubule regulation: one engine, many machines. J. Muscle Res. Cell Motil. 33:377-383. http://dx.doi.org/10.1007/s10974-012-9289-6
20. Fuller, B.G., M.A. Lampson, E.A. Foley, S. Rosasco-Nitcher, K.V. Le, P. Tobelmann, D.L. Brautigan, P.T. Stukenberg, and T.M. Kapoor. 2008. Midzone activation of aurora B in anaphase produces an intracellular phosphorylation gradient. Nature. 453:1132-1136. http://dx.doi.org/10.1038/nature06923
21. Gell, C., V. Bormuth, G.J. Brouhard, D.N. Cohen, S. Diez, C.T. Friel, J. Helenius, B. Nitzsche, H. Petzold, J. Ribbe, et al. 2010. Microtubule dynamics reconstituted in vitro and imaged by single-molecule fluorescence microscopy. Methods Cell Biol. 95:221-245. http://dx.doi.org/10.1016/S0091-679X(10)95013-9
22. Glotzer, M. 2009. The 3Ms of central spindle assembly: microtubules, motors and MAPs. Nat. Rev. Mol. Cell Biol. 10:9-20. http://dx.doi.org/10 .1038/nrm2609
23. Gruneberg, U., R. Neef, R. Honda, E.A. Nigg, and F.A. Barr. 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. http://dx.doi.org/10.1083/jcb.200403084
24. Gruneberg, U., R. Neef, X. Li, E.H. Chan, R.B. Chalamalasetty, E.A. Nigg, and F.A. Barr. 2006. KIF14 and citron kinase act together to promote efficient cytokinesis. J. Cell Biol. 172:363-372. http://dx.doi.org/10 .1083/jcb.200511061
25. Guse, A., M. Mishima, and M. Glotzer. 2005. Phosphorylation of ZEN-4/MKLP1 by aurora B regulates completion of cytokinesis. Curr. Biol. 15:778-786. http://dx.doi.org/10.1016/j.cub.2005.03.041
26. Hackney, D.D. 2007. Jump-starting kinesin. J. Cell Biol. 176:7-9. http://dx.doi.org/10.1083/jcb.200611082
27. Howard, J., and A.A. Hyman. 2009. Growth, fluctuation and switching at microtubule plus ends. Nat. Rev. Mol. Cell Biol. 10:569-574. http://dx.doi.org/10.1038/nrm2713
28. Hu, C.K., M. Coughlin, C.M. Field, and T.J. Mitchison. 2011. KIF4 regulates midzone length during cytokinesis. Curr. Biol. 21:815-824. http://dx.doi.org/10.1016/j.cub.2011.04.019
29. Hu, C.K., N. Ozlü, M. Coughlin, J.J. Steen, and T.J. Mitchison. 2012. Plk1 negatively regulates PRC1 to prevent premature midzone formation before cytokinesis. Mol. Biol. Cell. 23:2702-2711. http://dx.doi.org/10.1091/mbc.E12-01-0058
30. Hümmer, S., and T.U. Mayer. 2009. Cdk1 negatively regulates midzone localization of the mitotic kinesin Mklp2 and the chromosomal passenger complex. Curr. Biol. 19:607-612. http://dx.doi.org/10.1016/j.cub.2009.02.046
31. Jiang, W., G. Jimenez, N.J. Wells, T.J. Hope, G.M. Wahl, T. Hunter, and R. Fukunaga. 1998. PRC1: a human mitotic spindle-associated CDK substrate protein required for cytokinesis. Mol. Cell. 2:877-885. http://dx.doi.org/10.1016/S1097-2765(00)80302-0
32. Kaan, H.Y., D.D. Hackney, and F. Kozielski. 2011. The structure of the kinesin-1 motor-tail complex reveals the mechanism of autoinhibition. Science. 333:883-885. http://dx.doi.org/10.1126/science.1204824
33. Kettenbach, A.N., D.K. Schweppe, B.K. Faherty, D. Pechenick, A.A. Pletnev, and S.A. Gerber. 2011. Quantitative phosphoproteomics identifies substrates and functional modules of Aurora and Polo-like kinase activities in mitotic cells. Sci. Signal. 4:rs5. http://dx.doi.org/10.1126/scisignal.2001497
34. Klein, U.R., E.A. Nigg, and U. Gruneberg. 2006. Centromere targeting of the chromosomal passenger complex requires a ternary subcomplex of Borealin, Survivin, and the N-terminal domain of INCENP. Mol. Biol. Cell. 17:2547-2558. http://dx.doi.org/10.1091/mbc.E05-12-1133
35. Kurasawa, Y., W.C. Earnshaw, Y. Mochizuki, N. Dohmae, and K. Todokoro. 2004. Essential roles of KIF4 and its binding partner PRC1 in organized central spindle midzone formation. EMBO J. 23:3237-3248. http://dx.doi.org/10.1038/sj.emboj.7600347
36. Lan, W., X. Zhang, S.L. Kline-Smith, S.E. Rosasco, G.A. Barrett-Wilt, J. Shabanowitz, D.F. Hunt, C.E. Walczak, and P.T. Stukenberg. 2004. Aurora B phosphorylates centromeric MCAK and regulates its localization and microtubule depolymerization activity. Curr. Biol. 14:273-286.
37. Lee, S.H., F. McCormick, and H. Saya. 2010. Mad2 inhibits the mitotic kinesin MKlp2. J. Cell Biol. 191:1069-1077. http://dx.doi.org/10.1083/jcb.201003095
38. Lee, Y.M., and W. Kim. 2004. Kinesin superfamily protein member 4 (KIF4) is localized to midzone and midbody in dividing cells. Exp. Mol. Med. 36:93-97. http://dx.doi.org/10.1038/emm.2004.13
39. Mirchenko, L., and F. Uhlmann. 2010. Sli15(INCENP) dephosphorylation prevents mitotic checkpoint reengagement due to loss of tension at anaphase onset. Curr. Biol. 20:1396-1401. http://dx.doi.org/10.1016/j.cub.2010.06.023
40. Mishima, M., S. Kaitna, and M. Glotzer. 2002. Central spindle assembly and cytokinesis require a kinesin-like protein/RhoGAP complex with microtubule bundling activity. Dev. Cell. 2:41-54. http://dx.doi.org/10.1016/S1534-5807(01)00110-1
41. Mishima, M., V. Pavicic, U. Grüneberg, E.A. Nigg, and M. Glotzer. 2004. Cell cycle regulation of central spindle assembly. Nature. 430:908-913. http://dx.doi.org/10.1038/nature02767
42. Mollinari, C., J.P. Kleman, W. Jiang, G. Schoehn, T. Hunter, and R.L. Margolis. 2002. PRC1 is a microtubule binding and bundling protein essential to maintain the mitotic spindle midzone. J. Cell Biol. 157:1175-1186. http://dx.doi.org/10.1083/jcb.200111052
43. Neef, R., C. Preisinger, J. Sutcliffe, R. Kopajtich, E.A. Nigg, T.U. Mayer, and F.A. Barr. 2003. Phosphorylation of mitotic kinesin-like protein 2 by polo-like kinase 1 is required for cytokinesis. J. Cell Biol. 162:863-875. http://dx.doi.org/10.1083/jcb.200306009
44. Neef, R., U.R. Klein, R. Kopajtich, and F.A. Barr. 2006. Cooperation between mitotic kinesins controls the late stages of cytokinesis. Curr. Biol. 16:301-307. http://dx.doi.org/10.1016/j.cub.2005.12.030
45. Neef, R., U. Gruneberg, R. Kopajtich, X. Li, E.A. Nigg, H. Sillje, and F.A. Barr. 2007. Choice of Plk1 docking partners during mitosis and cytokinesis is controlled by the activation state of Cdk1. Nat. Cell Biol. 9:436-444. http://dx.doi.org/10.1038/ncb1557
46. Niiya, F., T. Tatsumoto, K.S. Lee, and T. Miki. 2006. Phosphorylation of the cytokinesis regulator ECT2 at G2/M phase stimulates association of the mitotic kinase Plk1 and accumulation of GTP-bound RhoA. Oncogene. 25:827-837. http://dx.doi.org/10.1038/sj.onc.1209124
47. Nislow, C., V.A. Lombillo, R. Kuriyama, and J.R. McIntosh. 1992. A plusend-directed motor enzyme that moves antiparallel microtubules in vitro localizes to the interzone of mitotic spindles. Nature. 359:543-547. http://dx.doi.org/10.1038/359543a0
48. Ohi, R., T. Sapra, J. Howard, and T.J. Mitchison. 2004. Differentiation of cytoplasmic and meiotic spindle assembly MCAK functions by Aurora Bdependent phosphorylation. Mol. Biol. Cell. 15:2895-2906. http://dx.doi.org/10.1091/mbc.E04-02-0082
49. Ozlü, N., F. Monigatti, B.Y. Renard, C.M. Field, H. Steen, T.J. Mitchison, and J.J. Steen. 2010. Binding partner switching on microtubules and aurora-B in the mitosis to cytokinesis transition. Mol. Cell. Proteomics. 9:336-350. http://dx.doi.org/10.1074/mcp.M900308-MCP200
50. Pavicic-Kaltenbrunner, V., M. Mishima, and M. Glotzer. 2007. Cooperative assembly of CYK-4/MgcRacGAP and ZEN-4/MKLP1 to form the centralspindlin complex. Mol. Biol. Cell. 18:4992-5003. http://dx.doi.org/10.1091/mbc.E07-05-0468
51. Petronczki, M., M. Glotzer, N. Kraut, and J.M. Peters. 2007. Polo-like kinase 1 triggers the initiation of cytokinesis in human cells by promoting recruitment of the RhoGEF Ect2 to the central spindle. Dev. Cell. 12:713-725. http://dx.doi.org/10.1016/j.devcel.2007.03.013
52. Samejima, K., I. Samejima, P. Vagnarelli, H. Ogawa, G. Vargiu, D.A. Kelly, F. de Lima Alves, A. Kerr, L.C. Green, D.F. Hudson, et al. 2012. Mitotic chromosomes are compacted laterally by KIF4 and condensin and axially by topoisomerase II?. J. Cell Biol. 199:755-770. http://dx.doi.org/10.1083/jcb.201202155
53. Santamaria, A., R. Neef, U. Eberspächer, K. Eis, M. Husemann, D. Mumberg, S. Prechtl, V. Schulze, G. Siemeister, L. Wortmann, et al. 2007. Use of the novel Plk1 inhibitor ZK-thiazolidinone to elucidate functions of Plk1 in early and late stages of mitosis. Mol. Biol. Cell. 18:4024-4036. http://dx.doi.org/10.1091/mbc.E07-05-0517
54. Sawin, K.E., and T.J. Mitchison. 1995. Mutations in the kinesin-like protein Eg5 disrupting localization to the mitotic spindle. Proc. Natl. Acad. Sci. USA. 92:4289-4293. http://dx.doi.org/10.1073/pnas.92.10.4289
55. Sekine, Y., Y. Okada, Y. Noda, S. Kondo, H. Aizawa, R. Takemura, and N. Hirokawa. 1994. A novel microtubule-based motor protein (KIF4) for organelle transports, whose expression is regulated developmentally. J. Cell Biol. 127:187-201. http://dx.doi.org/10.1083/jcb.127.1.187
56. Sellitto, C., and R. Kuriyama. 1988. Distribution of a matrix component of the midbody during the cell cycle in Chinese hamster ovary cells. J. Cell Biol. 106:431-439. http://dx.doi.org/10.1083/jcb.106.2.431
57. Sessa, F., M. Mapelli, C. Ciferri, C. Tarricone, L.B. Areces, T.R. Schneider, P.T. Stukenberg, and A. Musacchio. 2005. Mechanism of Aurora B activation by INCENP and inhibition by hesperadin. Mol. Cell. 18:379-391. http://dx.doi.org/10.1016/j.molcel.2005.03.031
58. Subramanian, R., E.M. Wilson-Kubalek, C.P. Arthur, M.J. Bick, E.A. Campbell, S.A. Darst, R.A. Milligan, and T.M. Kapoor. 2010. Insights into antiparallel microtubule crosslinking by PRC1, a conserved nonmotor microtubule binding protein. Cell. 142:433-443. http://dx.doi.org/10.1016/j.cell.2010.07.012
59. Tanenbaum, M.E., L. Macurek, B. van der Vaart, M. Galli, A. Akhmanova, and R.H. Medema. 2011. A complex of Kif18b and MCAK promotes microtubule depolymerization and is negatively regulated by Aurora kinases. Curr. Biol. 21:1356-1365. http://dx.doi.org/10.1016/j.cub.2011.07.017
60. Vázquez-Novelle, M.D., and M. Petronczki. 2010. Relocation of the chromosomal passenger complex prevents mitotic checkpoint engagement at anaphase. Curr. Biol. 20:1402-1407. http://dx.doi.org/10.1016/j.cub.2010.06.036
61. Walczak, C.E., T.J. Mitchison, and A. Desai. 1996. XKCM1: a Xenopus kinesin-related protein that regulates microtubule dynamics during mitotic spindle assembly. Cell. 84:37-47. http://dx.doi.org/10.1016/S0092-8674(00)80991-5
62. Walczak, C.E., E.C. Gan, A. Desai, T.J. Mitchison, and S.L. Kline-Smith. 2002. The microtubule-destabilizing kinesin XKCM1 is required for chromosome positioning during spindle assembly. Curr. Biol. 12:1885-1889. http://dx.doi.org/10.1016/S0960-9822(02)01227-7
63. Wandke, C., M. Barisic, R. Sigl, V. Rauch, F. Wolf, A.C. Amaro, C.H. Tan, A.J. Pereira, U. Kutay, H. Maiato, et al. 2012. Human chromokinesins promote chromosome congression and spindle microtubule dynamics during mitosis. J. Cell Biol. 198:847-863. http://dx.doi.org/10.1083/jcb.201110060
64. Wilm, M., A. Shevchenko, T. Houthaeve, S. Breit, L. Schweigerer, T. Fotsis, and M. Mann. 1996. Femtomole sequencing of proteins from polyacrylamide gels by nano-electrospray mass spectrometry. Nature. 379:466-469. http://dx.doi.org/10.1038/379466a0
65. Wittmann, T., A. Hyman, and A. Desai. 2001. The spindle: a dynamic assembly of microtubules and motors. Nat. Cell Biol. 3:E28-E34. http://dx.doi.org/10.1038/35050669
66. Wolfe, B.A., T. Takaki, M. Petronczki, and M. Glotzer. 2009. Polo-like kinase 1 directs assembly of the HsCyk-4 RhoGAP/Ect2 RhoGEF complex to initiate cleavage furrow formation. PLoS Biol. 7:e1000110. http://dx.doi.org/10.1371/journal.pbio.1000110
67. Zhu, C., and W. Jiang. 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. http://dx.doi.org/10.1073/pnas.0408438102
68. Zhu, C., J. Zhao, M. Bibikova, J.D. Leverson, E. Bossy-Wetzel, J.B. Fan, R.T. Abraham, and W. Jiang. 2005. Functional analysis of human microtubulebased motor proteins, the kinesins and dyneins, in mitosis/cytokinesis using RNA interference. Mol. Biol. Cell. 16:3187-3199. http://dx.doi.org/10.1091/mbc.E05-02-0167
69. Zhu, C., E. Lau, R. Schwarzenbacher, E. Bossy-Wetzel, and W. Jiang. 2006. Spatiotemporal control of spindle midzone formation by PRC1 in human cells. Proc. Natl. Acad. Sci. USA. 103:6196-6201. http://dx.doi.org/10.1073/pnas.0506926103