EB1 enables spindle microtubules to regulate centromeric recruitment of Aurora B

Journal of Cell Biology

Volumn 204, Issue 6, 2014, Pages 947-963

  Banerjee, Budhaditya ^a   Kestner, Cortney A ^a   Stukenberg, P Todd ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA B KINASE; EB1 PROTEIN; HISTONE H2A; HISTONE H3; MICROTUBULE PROTEIN; SURVIVIN; TUBULIN; UNCLASSIFIED DRUG;

ARTICLE; CELLULAR DISTRIBUTION; CENTROMERE; CHROMATIN; CONTROLLED STUDY; DEPOLYMERIZATION; ENZYME PHOSPHORYLATION; FEMALE; HELA CELL; HISTONE PHOSPHORYLATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IN VITRO STUDY; MICROTUBULE; PRIORITY JOURNAL; PROMETAPHASE; PROTEIN LOCALIZATION;

ANIMALS; AURORA KINASE B; CENTROMERE; CHROMATIN; HELA CELLS; HISTONES; HUMANS; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; PHOSPHORYLATION; PROMETAPHASE; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; SPINDLE APPARATUS; XENOPUS;

EID: 84896297809     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201307119     Document Type: Article

References (65)

1. 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
2. Brito, D.A., Z. Yang, and C.L. Rieder. 2008. Microtubules do not promote mitotic slippage when the spindle assembly checkpoint cannot be satisfied. J. Cell Biol. 182:623-629. http://dx.doi.org/10.1083/jcb.200805072
3. Cheeseman, I.M., J.S. Chappie, E.M. Wilson-Kubalek, and A. Desai. 2006. The conserved KMN network constitutes the core microtubule-binding site of the kinetochore. Cell. 127:983-997. http://dx.doi.org/10.1016/ j.cell.2006.09.039
4. Chu, Y., P.Y. Yao, W. Wang, D. Wang, Z. Wang, L. Zhang, Y. Huang, Y. Ke, X. Ding, and X. Yao. 2011. Aurora B kinase activation requires survivin priming phosphorylation by PLK1. J. Mol. Cell Biol. 3:260-267. http:// dx.doi.org/10.1093/jmcb/mjq037
5. Cimini, D., X. Wan, C.B. Hirel, and E.D. Salmon. 2006. Aurora kinase promotes turnover of kinetochore microtubules to reduce chromosome segregation errors. Curr. Biol. 16:1711-1718. http://dx.doi.org/10.1016/j.cub.2006 .07.022
6. De Antoni, A., S. Maffini, S. Knapp, A. Musacchio, and S. Santaguida. 2012. A small-molecule inhibitor of Haspin alters the kinetochore functions of Aurora B. J. Cell Biol. 199:269-284. http://dx.doi.org/10.1083/jcb.201205119
7. DeLuca, J.G., W.E. Gall, C. Ciferri, D. Cimini, A. Musacchio, and E.D. Salmon. 2006. Kinetochore microtubule dynamics and attachment stability are regulated by Hec1. Cell. 127:969-982. http://dx.doi.org/10.1016/j.cell .2006.09.047
8. Desai, A., A. Murray, T.J. Mitchison, and C.E. Walczak. 1999. The use of Xenopus egg extracts to study mitotic spindle assembly and function in vitro. Methods Cell Biol. 61:385-412. http://dx.doi.org/10.1016/S0091-679X(08)61991-3
9. Du, J., A.E. Kelly, H. Funabiki, and D.J. Patel. 2012. Structural basis for recognition of H3T3ph and Smac/DIABLO N-terminal peptides by human Survivin. Structure. 20:185-195. http://dx.doi.org/10.1016/j.str.2011.12.001
10. Dumont, S., E.D. Salmon, and T.J. Mitchison. 2012. Deformations within moving kinetochores reveal different sites of active and passive force generation. Science. 337:355-358. http://dx.doi.org/10.1126/science.1221886
11. Fischle, W., B.S. Tseng, H.L. Dormann, B.M. Ueberheide, B.A. Garcia, J. Shabanowitz, D.F. Hunt, H. Funabiki, and C.D. Allis. 2005. Regulation of HP1-chromatin binding by histone H3 methylation and phosphorylation. Nature. 438:1116-1122. http://dx.doi.org/10.1038/nature04219
12. 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
13. Hauf, S., R.W. Cole, S. LaTerra, C. Zimmer, G. Schnapp, R. Walter, A. Heckel, J. van Meel, C.L. Rieder, and J.-M. Peters. 2003. The small molecule Hesperadin reveals a role for Aurora B in correcting kinetochore-microtubule attachment and in maintaining the spindle assembly checkpoint. J. Cell Biol. 161:281-294. http://dx.doi.org/10.1083/jcb.200208092
14. Hayashi, I., and M. Ikura. 2003. Crystal structure of the amino-terminal microtubule-binding domain of end-binding protein 1 (EB1). J. Biol. Chem. 278:36430-36434. http://dx.doi.org/10.1074/jbc.M305773200
15. Hendzel, M.J., Y. Wei, M.A. Mancini, A. Van Hooser, T. Ranalli, B.R. Brinkley, D.P. Bazett-Jones, and C.D. Allis. 1997. Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma. 106:348-360. http://dx.doi.org/10 .1007/s004120050256
16. Hirota, T., J.J. Lipp, B.-H. Toh, and J.-M. Peters. 2005. Histone H3 serine 10 phosphorylation by Aurora B causes HP1 dissociation from heterochromatin. Nature. 438:1176-1180. http://dx.doi.org/10.1038/nature04254
17. Hsu, J.Y., Z.W. Sun, X. Li, M. Reuben, K. Tatchell, D.K. Bishop, J.M. Grushcow, C.J. Brame, J.A. Caldwell, D.F. Hunt, et al. 2000. Mitotic phosphorylation of histone H3 is governed by Ipl1/aurora kinase and Glc7/PP1 phosphatase in budding yeast and nematodes. Cell. 102:279-291. http:// dx.doi.org/10.1016/S0092-8674(00)00034-9
18. Jeyaprakash, A.A., C. Basquin, U. Jayachandran, and E. Conti. 2011. Structural basis for the recognition of phosphorylated histone h3 by the survivin subunit of the chromosomal passenger complex. Structure. 19:1625-1634. http://dx.doi.org/10.1016/j.str.2011.09.002
19. Joseph, J., S.-T. Liu, S.A. Jablonski, T.J. Yen, and M. Dasso. 2004. The RanGAP1-RanBP2 complex is essential for microtubule-kinetochore interactions in vivo. Curr. Biol. 14:611-617. http://dx.doi.org/10.1016/j .cub.2004.03.031
20. Kallio, M.J., M.L. McCleland, P.T. Stukenberg, and G.J. Gorbsky. 2002. Inhibition of aurora B kinase blocks chromosome segregation, overrides the spindle checkpoint, and perturbs microtubule dynamics in mitosis. Curr. Biol. 12:900-905. http://dx.doi.org/10.1016/S0960-9822(02)00887-4
21. Kelly, A.E., S.C. Sampath, T.A. Maniar, E.M. Woo, B.T. Chait, and H. Funabiki. 2007. Chromosomal enrichment and activation of the aurora B pathway are coupled to spatially regulate spindle assembly. Dev. Cell. 12:31-43. http://dx.doi.org/10.1016/j.devcel.2006.11.001
22. Kelly, A.E., C. Ghenoiu, J.Z. Xue, C. Zierhut, H. Kimura, and H. Funabiki. 2010. Survivin reads phosphorylated histone H3 threonine 3 to activate the mitotic kinase Aurora B. Science. 330:235-239. http://dx.doi.org/10 .1126/science.1189505
23. Khodjakov, A., L. Copenagle, M.B. Gordon, D.A. Compton, and T.M. Kapoor. 2003. Minus-end capture of preformed kinetochore fibers contributes to spindle morphogenesis. J. Cell Biol. 160:671-683. http://dx.doi.org/10 .1083/jcb.200208143
24. Knauer, S.K., C. Bier, N. Habtemichael, and R.H. Stauber. 2006. The Survivin-Crm1 interaction is essential for chromosomal passenger complex localization and function. EMBO Rep. 7:1259-1265. http://dx.doi.org/10.1038/ sj.embor.7400824
25. Knowlton, A.L., W. Lan, and P.T. Stukenberg. 2006. Aurora B is enriched at merotelic attachment sites, where it regulates MCAK. Curr. Biol. 16:1705-1710. http://dx.doi.org/10.1016/j.cub.2006.07.057
26. Lampson, M.A., K. Renduchitala, A. Khodjakov, and T.M. Kapoor. 2004. Correcting improper chromosome-spindle attachments during cell division. Nat. Cell Biol. 6:232-237. http://dx.doi.org/10.1038/ncb1102
27. 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. http://dx.doi.org/10.1016/j.cub.2004.01.055
28. Liu, D., G. Vader, M.J.M. Vromans, M.A. Lampson, and S.M.A. Lens. 2009. Sensing chromosome bi-orientation by spatial separation of aurora B kinase from kinetochore substrates. Science. 323:1350-1353. http://dx.doi.org/10 .1126/science.1167000
29. Losada, A., M. Hirano, and T. Hirano. 2002. Cohesin release is required for sister chromatid resolution, but not for condensin-mediated compaction, at the onset of mitosis. Genes Dev. 16:3004-3016. http://dx.doi.org/10 .1101/gad.249202
30. Mackay, A.M., A.M. Ainsztein, D.M. Eckley, and W.C. Earnshaw. 1998. A dominant mutant of inner centromere protein (INCENP), a chromosomal protein, disrupts prometaphase congression and cytokinesis. J. Cell Biol. 140:991-1002. http://dx.doi.org/10.1083/jcb.140.5.991
31. Matson, D.R., P.B. Demirel, P.T. Stukenberg, and D.J. Burke. 2012. A conserved role for COMA/CENP-H/I/N kinetochore proteins in the spindle checkpoint. Genes Dev. 26:542-547. http://dx.doi.org/10.1101/gad.184184 .111
32. Mishra, R.K., P. Chakraborty, A. Arnaoutov, B.M.A. Fontoura, and M. Dasso. 2010. The Nup107-160 complex and gamma-TuRC regulate microtubule polymerization at kinetochores. Nat. Cell Biol. 12:164-169. http://dx.doi .org/10.1038/ncb2016
33. Mitchison, T.J., and M.W. Kirschner. 1985. Properties of the kinetochore in vitro. I. Microtubule nucleation and tubulin binding. J. Cell Biol. 101:755-765. http://dx.doi.org/10.1083/jcb.101.3.755
34. Mollinari, C., C. Reynaud, S. Martineau-Thuillier, S. Monier, S. Kieffer, J. Garin, P.R. Andreassen, A. Boulet, B. Goud, J.-P. Kleman, and R.L. Margolis. 2003. The mammalian passenger protein TD-60 is an RCC1 family member with an essential role in prometaphase to metaphase progression. Dev. Cell. 5:295-307. http://dx.doi.org/10.1016/S1534-5807(03)00205-3
35. Morrison, E.E., B.N. Wardleworth, J.M. Askham, A.F. Markham, and D.M. Meredith. 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. http://dx.doi.org/10.1038/sj.onc.1202247
36. Niedzialkowska, E., F. Wang, P.J. Porebski, W. Minor, J.M.G. Higgins, and P.T. Stukenberg. 2012. Molecular basis for phosphospecific recognition of histone H3 tails by Survivin paralogues at inner centromeres. Mol. Biol. Cell. 23:1457-1466. http://dx.doi.org/10.1091/mbc.E11-11-0904
37. Orjalo, A.V., A. Arnaoutov, Z. Shen, Y. Boyarchuk, S.G. Zeitlin, B. Fontoura, S. Briggs, M. Dasso, and D.J. Forbes. 2006. The Nup107-160 nucleoporin complex is required for correct bipolar spindle assembly. Mol. Biol. Cell. 17:3806-3818. http://dx.doi.org/10.1091/mbc.E05-11-1061
38. Platani, M., R. Santarella-Mellwig, M. Posch, R. Walczak, J.R. Swedlow, and I.W. Mattaj. 2009. The Nup107-160 nucleoporin complex promotes mitotic events via control of the localization state of the chromosome passenger complex. Mol. Biol. Cell. 20:5260-5275. http://dx.doi.org/10.1091/mbc .E09-05-0377
39. Rosasco-Nitcher, S.E., W. Lan, S. Khorasanizadeh, and P.T. Stukenberg. 2008. Centromeric Aurora-B activation requires TD-60, microtubules, and substrate priming phosphorylation. Science. 319:469-472. http://dx.doi .org/10.1126/science.1148980
40. Ruchaud, S., M. Carmena, and W.C. Earnshaw. 2007. Chromosomal passengers: conducting cell division. Nat. Rev. Mol. Cell Biol. 8:798-812. http:// dx.doi.org/10.1038/nrm2257
41. Salimian, K.J., E.R. Ballister, E.M. Smoak, S. Wood, T. Panchenko, M.A. Lampson, and B.E. Black. 2011. Feedback control in sensing chromosome biorientation by the Aurora B kinase. Curr. Biol. 21:1158-1165. http://dx.doi.org/10.1016/j.cub.2011.06.015
42. Santaguida, S., A. Tighe, A.M. D'Alise, S.S. Taylor, and A. Musacchio. 2010. Dissecting the role of MPS1 in chromosome biorientation and the spindle checkpoint through the small molecule inhibitor reversine. J. Cell Biol. 190:73-87. http://dx.doi.org/10.1083/jcb.201001036
43. Santaguida, S., C. Vernieri, F. Villa, A. Ciliberto, and A. Musacchio. 2011. Evidence that Aurora B is implicated in spindle checkpoint signalling independently of error correction. EMBO J. 30:1508-1519. http://dx.doi .org/10.1038/emboj.2011.70
44. Saurin, A.T., M.S. van der Waal, R.H. Medema, S.M.A. Lens, and G.J.P.L. Kops. 2011. Aurora B potentiates Mps1 activation to ensure rapid checkpoint establishment at the onset of mitosis. Nat. Commun. 2:316. http://dx.doi .org/10.1038/ncomms1319
45. 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
46. Söderberg, O., M. Gullberg, M. Jarvius, K. Ridderstråle, K.-J. Leuchowius, J. Jarvius, K. Wester, P. Hydbring, F. Bahram, L.-G. Larsson, and U. Landegren. 2006. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods. 3:995-1000. http://dx.doi.org/10.1038/nmeth947
47. Stucke, V.M., C. Baumann, and E.A. Nigg. 2004. Kinetochore localization and microtubule interaction of the human spindle checkpoint kinase Mps1. Chromosoma. 113:1-15. http://dx.doi.org/10.1007/s00412-004-0288-2
48. Sun, L., J. Gao, X. Dong, M. Liu, D. Li, X. Shi, J.-T. Dong, X. Lu, C. Liu, and J. Zhou. 2008. EB1 promotes Aurora-B kinase activity through blocking its inactivation by protein phosphatase 2A. Proc. Natl. Acad. Sci. USA. 105:7153-7158. http://dx.doi.org/10.1073/pnas.0710018105
49. Terada, Y. 2001. Role of chromosomal passenger complex in chromosome segregation and cytokinesis. Cell Struct. Funct. 26:653-657. http://dx.doi .org/10.1247/csf.26.653
50. Tighe, A., O. Staples, and S. Taylor. 2008. Mps1 kinase activity restrains anaphase during an unperturbed mitosis and targets Mad2 to kinetochores. J. Cell Biol. 181:893-901. http://dx.doi.org/10.1083/jcb.200712028
51. Tirnauer, J.S., J.C. Canman, E.D. Salmon, and T.J. Mitchison. 2002. EB1 targets to kinetochores with attached, polymerizing microtubules. Mol. Biol. Cell. 13:4308-4316. http://dx.doi.org/10.1091/mbc.E02-04-0236
52. Tsai, M.-Y., C. Wiese, K. Cao, O. Martin, P. Donovan, J. Ruderman, C. Prigent, and Y. Zheng. 2003. A Ran signalling pathway mediated by the mitotic kinase Aurora A in spindle assembly. Nat. Cell Biol. 5:242-248. http:// dx.doi.org/10.1038/ncb936
53. Tseng, B.S., L. Tan, T.M. Kapoor, and H. Funabiki. 2010. Dual detection of chromosomes and microtubules by the chromosomal passenger complex drives spindle assembly. Dev. Cell. 18:903-912. http://dx.doi.org/10 .1016/j.devcel.2010.05.018
54. Tsukahara, T., Y. Tanno, and Y. Watanabe. 2010. Phosphorylation of the CPC by Cdk1 promotes chromosome bi-orientation. Nature. 467:719-723. http:// dx.doi.org/10.1038/nature09390
55. Tulu, U.S., C. Fagerstrom, N.P. Ferenz, and P. Wadsworth. 2006. Molecular requirements for kinetochore-associated microtubule formation in mammalian cells. Curr. Biol. 16:536-541. http://dx.doi.org/10.1016/j.cub .2006.01.060
56. van der Waal, M.S., A.T. Saurin, M.J.M. Vromans, M. Vleugel, C. Wurzenberger, D.W. Gerlich, R.H. Medema, G.J.P.L. Kops, and S.M.A. Lens. 2012. Mps1 promotes rapid centromere accumulation of Aurora B. EMBO Rep. 13:847-854. http://dx.doi.org/10.1038/embor.2012.93
57. Wang, E., E.R. Ballister, and M.A. Lampson. 2011a. Aurora B dynamics at centromeres create a diffusion-based phosphorylation gradient. J. Cell Biol. 194:539-549. http://dx.doi.org/10.1083/jcb.201103044
58. Wang, F., J. Dai, J.R. Daum, E. Niedzialkowska, B. Banerjee, P.T. Stukenberg, G.J. Gorbsky, and J.M. Higgins. 2010. Histone H3 Thr-3 phosphorylation by Haspin positions Aurora B at centromeres in mitosis. Science. 330:231-235. http://dx.doi.org/10.1126/science.1189435
59. Wang, F., N.P. Ulyanova, M.S. van der Waal, D. Patnaik, S.M.A. Lens, and J.M.G. Higgins. 2011b. A positive feedback loop involving Haspin and Aurora B promotes CPC accumulation at centromeres in mitosis. Curr. Biol. 21:1061-1069. http://dx.doi.org/10.1016/j.cub.2011.05.016
60. Wang, F., N.P. Ulyanova, J.R. Daum, D. Patnaik, A.V. Kateneva, G.J. Gorbsky, and J.M.G. Higgins. 2012. Haspin inhibitors reveal centromeric functions of Aurora B in chromosome segregation. J. Cell Biol. 199:251-268. http://dx.doi.org/10.1083/jcb.201205106
61. Welburn, J.P.I., M. Vleugel, D. Liu, J.R. Yates III, M.A. Lampson, T. Fukagawa, and I.M. Cheeseman. 2010. Aurora B phosphorylates spatially distinct targets to differentially regulate the kinetochore-microtubule interface. Mol. Cell. 38:383-392. http://dx.doi.org/10.1016/j.molcel.2010.02.034
62. Wheatley, S.P., A. Carvalho, P. Vagnarelli, and W.C. Earnshaw. 2001. INCENP is required for proper targeting of Survivin to the centromeres and the anaphase spindle during mitosis. Curr. Biol. 11:886-890. http://dx.doi.org/ 10.1016/S0960-9822(01)00238-X
63. Wheatley, S.P., A.J. Henzing, H. Dodson, W. Khaled, and W.C. Earnshaw. 2004. Aurora-B phosphorylation in vitro identifies a residue of survivin that is essential for its localization and binding to inner centromere protein (INCENP) in vivo. J. Biol. Chem. 279:5655-5660. http://dx.doi.org/10 .1074/jbc.M311299200
64. Yamagishi, Y., T. Honda, Y. Tanno, and Y. Watanabe. 2010. Two histone marks establish the inner centromere and chromosome bi-orientation. Science. 330:239-243. http://dx.doi.org/10.1126/science.1194498
65. Zimniak, T., K. Stengl, K. Mechtler, and S. Westermann. 2009. Phosphoregulation of the budding yeast EB1 homologue Bim1p by Aurora/Ipl1p. J. Cell Biol. 186:379-391. http://dx.doi.org/10.1083/jcb.200901036