Temporal changes in Hec1 phosphorylation control kinetochore - Microtubule attachment stability during mitosis

Journal of Cell Science

Volumn 124, Issue 4, 2011, Pages 622-634

  DeLuca, Keith F ^a   Lens, Susanne M A ^b   DeLuca, Jennifer G ^a  

^a Veterinary Dentistry and Oral Surgery   (United States)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Aurora B; Hec1; Kinetochore; Microtubule; NDC80

Indexed keywords

AURORA B KINASE; CHROMOSOME PROTEIN; HEC1 PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL DIVISION; CENTROMERE; CONTROLLED STUDY; HUMAN; HUMAN CELL; KINETOCHORE MICROTUBULE ATTACHMENT STABILITY; MICROTUBULE; MITOSIS; MOLECULAR DYNAMICS; MOLECULAR STABILITY; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; TENSION;

HELA CELLS; HUMANS; KINETOCHORES; MICROTUBULES; MITOSIS; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN-SERINE-THREONINE KINASES;

EID: 79951833036     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.072629     Document Type: Article

References (44)

1. Andrews, P. D., Ovechkina, Y., Morrice, N., Wagenbach, M., Duncan, K., Wordeman, L. and Swedlow, J. R. (2004). Aurora B regulates MCAK at the mitotic centromere. Dev. Cell 6, 253-268.
2. Akiyoshi, B., Nelson, C.R., Ranish, J.A. and Biggins, S. (2009) Analysis of Ipl1- mediated phosphorylation of the Ndc80 kinetochore protein in Saccharomyces cerevisiae. Genetics 183,1591-1595.
3. Bakhoum, S. F., Thompson, S. L., Manning, A. L. and Compton, D. A. (2009). Genome stability is ensured by temporal control of kinetochore- microtubule dynamics. Nat. Cell Biol. 11, 27-35.
4. Biggins, S. and Murray, A. W. (2001). The budding yeast protein kinase Ipl1/Aurora allows the absence of tension to activate the spindle checkpoint. Genes Dev. 15, 3118-3129.
5. Brill, L. M., Xiong, W., Lee, K. B., Ficarro, S. B., Crain, A., Xu, Y., Terskikh, A., Snyder, E. Y. and Ding, S. (2009). Phosphoproteomic analysis of human embryonic stem cells. Cell Stem Cell 5, 204-213.
6. Cheeseman, I. M., Anderson, S., Jwa, M., Green, E. M., Kang, J., Yates, J. R., III, Chan, C. S., Drubin, D. G. and Barnes, G. (2002). Phospho-regulation of kinetochore-microtubule attachments by the Aurora kinase Ipl1p. Cell 111, 163-172. (Pubitemid 35292437)
7. Cheeseman, I. M., Chappie, J. S., Wilson-Kubalek, E. M. and Desai, A. (2006). The conMcserved KMN network constitutes the core microtubule-binding site of the kinetochore. Cell 127, 983-997. (Pubitemid 44792248)
8. Chen, R. H., Waters, J. C., Salmon, E. D. and Murray, A. W. (1996). Association of spindle assembly checkpoint component XMAD2 with unattached kinetochores. Science 274, 242-246.
9. Chen, Y., Riley, D. J., Chen, P. L. and Lee, W. H. (1997). HEC, a novel nuclear protein rich in leucine heptad repeats specifically involved in mitosis. Mol. Cell. Biol. 17, 6049-6056.
10. Ciferri, C., Pasqualato, S., Screpanti, E., Varetti, G., Santaguida, S., Dos Reis, G., Maiolica, A., Polka, J., DeLuca, J. G., De Wulf, P. et al. (2008). Implications for kinetochore-microtubule attachment from the structure of an engineered Ndc80 complex. Cell 133, 427-439. (Pubitemid 351622013)
11. Cimini, D. (2008). Merotelic kinetochore orientation, aneuploidy, and cancer. Biochim. Biophys. Acta 1786, 32-40.
12. Cimini, D., Cameron, L. A. and Salmon, E. D. (2004). Anaphase spindle mechanics prevent mis-segregation of merotelically oriented chromosomes. Curr. Biol. 14, 2149-2155.
13. Cimini, D., Wan, X., Hirel, C. B. and Salmon, E. D. (2006). Aurora kinase promotes turnover of kinetochore microtubules to reduce chromosome segregation errors. Curr. Biol. 16, 1711-1718.
14. Cohen, P. and Nimmo, G. A. (1978). The purification and characterization of protein phosphatase inhibitor-1 from rabbit skeletal muscle. Biochem. Soc. Trans. 6, 17-20.
15. DeLuca, J. G., Moree, B., Hickey, J. M., Kilmartin, J. V. and Salmon, E. D. (2002). hNuf2 inhibition blocks stable kinetochore-microtubule attachment and induces mitotic cell death in HeLa cells. J. Cell Biol. 159, 549-555.
16. DeLuca, J. G., Gall, W. E., Ciferri, C., Cimini, D., Musacchio, A. and Salmon, E. D. (2006). Kinetochore microtubule dynamics and attachment stability are regulated by Hec1. Cell 127, 969-982.
17. Ditchfield, C., Johnson, V. L., Tighe, A., Ellston, R., Haworth, C., Johnson, T., Mortlock, A., Keen, N. and Taylor, S. S. (2003). Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores. J. Cell Biol. 161, 267-280.
18. Guimaraes, G., Dong, Y., McEwen, B. F. and DeLuca, J. G. (2008). Kinetochore-microtubule attachment relies on the disordered N-terminal tail domain of Hec1. Curr. Biol. 18, 1778-1784.
19. Hauf, S., Cole, R. W., LaTerra, S., Zimmer, C., Schnapp, G., Walter, R., Heckel, A., van Meel, J., Rieder, C. L. and Peters, J. M. (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.
20. 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.
21. Knowlton, A. L., Lan, W. and Stukenberg, P. T. (2006). Aurora B is enriched at merotelic attachment sites, where it regulates MCAK. Curr. Biol. 16, 1705-1710.
22. Lampson, M. A. and Kapoor, T. M. (2005). The human mitotic checkpoint protein BubR1 regulates chromosome-spindle attachments. Nat. Cell Biol. 7, 93-98.
23. Li, Y. and Benezra, R. (1996). Identification of a human mitotic checkpoint gene: hsMAD2. Science 274, 246-248.
24. Liu, D., Vader, G., Vromans, M. J., Lampson, M. A. and Lens, S. M. (2009). Sensing chromosome bi-orientation by spatial separation of aurora B kinase from kinetochore substrates. Science 323, 1350-1353.
25. Liu, D., Vleugel, M., Backer, C. B., Hori, T., Fukagawa, T., Cheeseman, I. M. and Lampson, M. A. (2010). Regulated targeting of protein phosphatase 1 to the outer kinetochore by KNL1 opposes Aurora B kinase. J. Cell Biol. 188, 809-820.
26. Malik, R., Lenobel, R., Santamaria, A., Ries, A., Nigg, E. A. and Körner, R. (2009). Quantitative analysis of the human spindle phosphoproteome at distinct mitotic stages. J. Proteome Res. 8, 4553-4563.
27. Martin-Lluesma, S., Stucke, V. M. and Nigg, E. A. (2002). Role of Hec1 in spindle checkpoint signaling and kinetochore recruitment of Mad1/Mad2. Science 297, 2267-2270.
28. 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.
29. McCleland, M. L., Kallio, M. J., Barrett-Wilt, G. A., Kestner, C. A., Shabanowitz, J., Hunt, D. F., Gorbsky, G. J. and Stukenberg, P. T. (2004). The vertebrate Ndc80 complex contains Spc24 and Spc25 homologs, which are required to establish and maintain kinetochore-microtubule attachment. Curr. Biol. 14, 131-137.
30. Miller, S. A., Johnson, M. L. and Stukenberg, P. T. (2008). Kinetochore attachments require an interaction between unstructured tails on microtubules and Ndc80(Hec1). Curr. Biol. 18, 1785-1791.
31. Nousiainen, M., Sillje, H. H., Sauer, G., Nigg, E. A. and Korner, R. (2006). Phosphoproteome analysis of the human mitotic spindle. Proc. Natl. Acad. Sci. USA 103, 5391-5396.
32. Olsen, J. V., Vermeulen, M., Santamaria, A., Kumar, C., Miller, M. L., Jensen, L. J., Gnad, F., Cox, J., Jensen, T. S., Nigg, E. A. et al. (2010). Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci. Signal. 3, ra3.
33. Pinsky, B. A., Kung, C., Shokat, K. M. and Biggins, S. (2006). The Ipl1-Aurora protein kinase activates the spindle checkpoint by creating unattached kinetochores. Nat. Cell Biol. 8, 78-83.
34. Sessa, F., Mapelli, M., Ciferri, C., Tarricone, C., Areces, L. B., Schneider, T. R., Stukenberg, P. T. and Musacchio, A. (2005). Mechanism of Aurora B activation by INCENP and inhibition by hesperadin. Mol. Cell 18, 379-391. (Pubitemid 41350542)
35. Stumpff, J., von Dassow, G., Wagenbach, M., Asbury, C. and Wordeman, L. (2008). The kinesin-8 motor Kif18A suppresses kinetochore movements to control mitotic chromosome alignment. Dev. Cell 14, 252-262. (Pubitemid 351189173)
36. Tanaka, T. U., Rachidi, N., Janke, C., Pereira, G., Galova, M., Schiebel, E., Stark, M. J. and Nasmyth, K. (2002). Evidence that the Ipl1-Sli15 (Aurora kinase-INCENP) complex promotes chromosome bi-orientation by altering kinetochore-spindle pole connections. Cell 108, 317-329. (Pubitemid 34178397)
37. Tien, A. C., Lin, M. H., Su, L. J., Hong, Y. R., Cheng, T. S., Lee, Y. C., Lin, W. J., Still, I. H. and Huang, C. Y. (2004). Identification of the substrates and interaction proteins of aurora kinases from a protein-protein interaction model. Mol. Cell. Proteomics 3, 93-104.
38. Trinkle-Mulcahy, L. and Lamond, A. I. (2006). Mitotic phosphatases: no longer silent partners. Curr. Opin. Cell Biol. 18, 623-631.
39. Vader, G., Maia, A. F. and Lens, S. M. (2008). The chromosomal passenger complex and the spindle assembly checkpoint: kinetochore-microtubule error correction and beyond. Cell Div. 3, 10-19.
40. Wei, R. R., Al-Bassam, J., Harrison, S. C. (2007). The Ndc80/HEC1 complex is a contact point for kinetochore-microtubule attachment. Nat. Struct. Mol. Biol. 14, 54-59.
41. Welburn, J. P., Vleugel, M., Liu, D., Yates, J. R., III, Lampson, M. A., Fukagawa, T. and Cheeseman, I. M. (2010). Aurora B phosphorylates spatially distinct targets to differentially regulate the kinetochore-microtubule interface. Mol. Cell 38, 383-392.
42. Wigge, P. A. and Kilmartin, J. V. (2001). The Ndc80p complex from Saccharomyces cerevisiae contains conserved centromere components and has a function in chromosome segregation. J. Cell Biol. 152, 349-360.
43. Yasui, Y., Urano, T., Kawajiri, A., Nagata, K., Tatsuka, M., Saya, H., Furukawa, K., Takahashi, T., Izawa, I. and Inagaki, M. (2004). Autophosphorylation of a newly identified site of Aurora-B is indispensable for cytokinesis. J. Biol. Chem. 279, 12997-3003.
44. Zhai, Y., Kronebusch, P. J. and Borisy, G. G. (1995). Kinetochore microtubule dynamics and the metaphase-anaphase transition. J. Cell Biol. 131, 721-734.