Phosphorylation regulates kinase and microtubule binding activities of the budding yeast chromosomal passenger complex in vitro

Journal of Biological Chemistry

Volumn 288, Issue 32, 2013, Pages 23203-23211

  Cormier, Anthony ^a   Drubin, David G ^a   Barnes, Georjana ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ACTIVITIES; BUDDING YEASTS; IN-VITRO; KINASE ACTIVITY; MICROTUBULES; STRUCTURAL STUDIES;

BINDING SITES; CHROMOSOMES; PHOSPHORYLATION;

ENZYMES;

AURORA B KINASE; CHROMOSOMAL PASSENGER COMPLEX; FUNGAL PROTEIN; INCENP PROTEIN; IPL1 PROTEIN; REGULATOR PROTEIN; SLI15 PROTEIN; TUBULIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CHROMOSOME SEGREGATION; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; ENZYME PURIFICATION; ENZYME REGULATION; IN VITRO STUDY; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN SUBUNIT; REGULATORY MECHANISM; SACCHAROMYCES CEREVISIAE; STATIC ELECTRICITY; YEAST;

CANCER BIOLOGY; CELL BIOLOGY; CELL CYCLE; ENZYME PURIFICATION; KINASE; MITOTIC SPINDLE; TUBULIN;

INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MULTIPROTEIN COMPLEXES; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84881448321     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.491480     Document Type: Article

References (33)

1. Meraldi, P., Honda, R., and Nigg, E. A. (2004) Aurora kinases link chromosome segregation and cell division to cancer susceptibility. Curr. Opin. Genet. Dev. 14, 29-36
2. Musacchio, A. (2011) Spindle assembly checkpoint: the third decade. Philos. Trans. R. Soc. Lond. B Biol. Sci. 366, 3595-3604
3. Ruchaud, S., Carmena, M., and Earnshaw, W. C. (2007) Chromosomal passengers: conducting cell division. Nat. Rev. Mol. Cell Biol. 8, 798-812
4. Carmena, M. (2008) Cytokinesis: the final stop for the chromosomal passengers. Biochem. Soc. Trans. 36, 367-370
5. 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
6. Kitzen, J. J., de Jonge, M. J., and Verweij, J. (2010) Aurora kinase inhibitors. Crit. Rev. Oncol. Hematol. 73, 99-110
7. Carmena, M., and Earnshaw, W. C. (2003) The cellular geography of Aurora kinases. Nat. Rev. Mol. Cell Biol. 4, 842-854
8. Cheeseman, I. M., Anderson, S., Jwa, M., Green, E. M., Kang, J. S., Yates, J. R., 3rd, Chan, C. S., Drubin, D. G., and Barnes, G. (2002) Phosphoregulation of kinetochore-microtubule attachments by the Aurora kinase Ipl1p. Cell 111, 163-172
9. Nakajima, Y., Tyers, R. G., Wong, C. C., Yates, J. R., 3rd, Drubin, D. G., and Barnes, G. (2009) Nbl1p: a Borealin/Dasra/CSC-1-like protein essential for Aurora/Ipl1 complex function and integrity in Saccharomyces cerevisiae. Mol. Biol. Cell 20, 1772-1784
10. Bishop, J. D., and Schumacher, J. M. (2002) Phosphorylation of the carboxyl terminus of inner centromere protein (INCENP) by the Aurora B kinase stimulates Aurora B kinase activity. J. Biol. Chem. 277, 27577-27580
11. Honda, R., Körner, R., and Nigg, E. A. (2003) Exploring the functional interactions between Aurora B, INCENP, and Survivin in mitosis. Mol. Biol. Cell 14, 3325-3341
12. 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
13. Yang, J., Zappacosta, F., Annan, R. S., Nurse, K., Tummino, P. J., Copeland, R. A., and Lai, Z. (2009) The catalytic role of INCENP in Aurora B activation and the kinetic mechanism of Aurora B/INCENP. Biochem. J. 417, 355-360
14. Adams, R. R., Wheatley, S. P., Gouldsworthy, A. M., Kandels-Lewis, S. E., Carmena, M., Smythe, C., Gerloff, D. L., and Earnshaw, W. C. (2000) INCENP binds the Aurora-related kinase AIRK2 and is required to target it to chromosomes, the central spindle and cleavage furrow. Curr. Biol. 10, 1075-1078
15. 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
16. Jeyaprakash, A. A., Klein, U. R., Lindner, D., Ebert, J., Nigg, E. A., and Conti, E. (2007) Structure of a Survivin-Borealin-INCENP core complex reveals how chromosomal passengers travel together. Cell 131, 271-285
17. van der Waal, M. S., Hengeveld, R. C., van der Horst, A., and Lens, S. M. (2012) Cell division control by the chromosomal passenger complex. Exp. Cell Res. 318, 1407-1420
18. Tan, S. (2001) A modular polycistronic expression system for overexpressing protein complexes in Escherichia coli. Protein Expression Purification 21, 224-234
19. Nakajima, Y., Cormier, A., Tyers, R. G., Pigula, A., Peng, Y., Drubin, D. G., and Barnes, G. (2011) Ipl1/Aurora-dependent phosphorylation of Sli15/ INCENP regulates CPC-spindle interaction to ensure proper microtubule dynamics. J. Cell Biol. 194, 137-153
20. Robichon, C., Luo, J., Causey, T. B., Benner, J. S., and Samuelson, J. C. (2011) Engineering Escherichia coli BL21(DE3) derivative strains to minimize E. coli protein contamination after purification by immobilized metal affinity chromatography. Appl. Environ. Microbiol. 77, 4634-4646
21. Westermann, S., Avila-Sakar, A., Wang, H. W., Niederstrasser, H., Wong, J., Drubin, D. G., Nogales, E., and Barnes, G. (2005) Formation of a dynamic kinetochore-microtubule interface through assembly of the Dam1 ring complex. Mol. Cell 17, 277-290
22. Kang, J., Cheeseman, I. M., Kallstrom, G., Velmurugan, S., Barnes, G., and Chan, C. S. (2001) Functional cooperation of Dam1, Ipl1, and the inner centromere protein (INCENP)-related protein Sli15 during chromosome segregation. J. Cell Biol. 155, 763-774
23. Biggins, S., Severin, F. F., Bhalla, N., Sassoon, I., Hyman, A. A., and Murray, A. W. (1999) The conserved protein kinase Ipl1 regulates microtubule binding to kinetochores in budding yeast. Genes Dev. 13, 532-544
24. Serrano, L., Avila, J., and Maccioni, R. B. (1984) Controlled proteolysis of tubulin by subtilisin: localization of the site for MAP2 interaction. Biochemistry 23, 4675-4681
25. Campbell, C. S., and Desai, A. (2013) Tension sensing by Aurora B kinase is independent of Survivin-based centromere localization. Nature 497, 118-121
26. Rosasco-Nitcher, S. E., Lan, W., Khorasanizadeh, S., and Stukenberg, P. T. (2008) Centromeric Aurora-B activation requires TD-60, microtubules, and substrate priming phosphorylation. Science 319, 469-472
27. Woodruff, J. B., Drubin, D. G., and Barnes, G. (2010) Mitotic spindle disassembly occurs via distinct subprocesses driven by the anaphase-promoting complex, Aurora B kinase, and kinesin-8. J. Cell Biol. 191, 795-808
28. Pereira, G., and Schiebel, E. (2003) Separase regulates INCENP-Aurora B anaphase spindle function through Cdc14. Science 302, 2120-2124
29. Cooper, J. R., and Wordeman, L. (2009) The diffusive interaction of microtubule-binding proteins. Curr. Opin. Cell Biol. 21, 68-73
30. Ramey, V. H., Wang, H. W., Nakajima, Y., Wong, A., Liu, J., Drubin, D., Barnes, G., and Nogales, E. (2011) The Dam1 ring binds to the E-hook of tubulin and diffuses along the microtubule. Mol. Biol. Cell 22, 457-466
31. Alushin, G. M., Ramey, V. H., Pasqualato, S., Ball, D. A, Grigorieff, N., Musacchio, A., and Nogales, E. (2010) The Ndc80 kinetochore complex forms oligomeric arrays along microtubules. Nature 467, 805-810
32. Zimmermann, D., Abdel Motaal, B., Voith von Voithenberg, L., Schliwa, M., and Ökten, Z. (2011) Diffusion of myosin V on microtubules: a finetuned interaction for which E-hooks are dispensable. PloS One 6, e25473
33. Bolton, M. A., Lan, W., Powers, S. E., McCleland, M. L., Kuang, J., and Stukenberg, P. T. (2002) Aurora B kinase exists in a complex with Survivin and INCENP and its kinase activity is stimulated by Survivin binding and phosphorylation. Mol. Biol. Cell 13, 3064-3077