Molecular distinctions between Aurora A and B: A single residue change transforms Aurora A into correctly localized and functional Aurora B

Molecular Biology of the Cell

Volumn 20, Issue 15, 2009, Pages 3491-3502

  Hans, Fabienne ^a   Skoufias, Dimitrios A ^b   Dimitrov, Stefan ^a   Margolis, Robert L ^c  

^a INSERM   (France)

^b INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^c SIDNEY KIMMEL CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARAGINE; AURORA A KINASE; AURORA B KINASE; GLYCINE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; CELL STRAIN HCT116; CELLULAR DISTRIBUTION; CENTROMERE; CENTROSOME; CONTROLLED STUDY; ENZYME LOCALIZATION; HELA CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; BINDING SITES; CELL CYCLE PROTEINS; CHROMOSOMAL PROTEINS, NON-HISTONE; HCT116 CELLS; HELA CELLS; HISTONES; HUMANS; IMMUNOPRECIPITATION; MICROTUBULE-ASSOCIATED PROTEINS; MITOSIS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; RNA INTERFERENCE; SEQUENCE HOMOLOGY, AMINO ACID; TRANSFECTION; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 68249114474     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E09-05-0370     Document Type: Article

References (55)

1. 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.
2. Anand, S., Penrhyn-Lowe, S., and Venkitaraman, A. R. (2003). AURORA-A amplification overrides the mitotic spindle assembly checkpoint, inducing resistance to Taxol. Cancer Cell 3, 51-62. (Pubitemid 37443890)
3. Andrews, P. D., Knatko, E., Moore, W. J., and Swedlow, J. R. (2003). Mitotic mechanics: the auroras come into view. Curr. Opin. Cell Biol. 15, 672-683.
4. Barr, A. R., and Gergely, F. (2007). Aurora-A: the maker and breaker of spindle poles. J. Cell Sci. 120, 2987-2996.
5. Bayliss, R., Sardon, T., Ebert, J., Lindner, D., Vernos, I., and Conti, E. (2004). Determinants for Aurora-A activation and Aurora-B discrimination by TPX2. Cell Cycle 3, 404-407. (Pubitemid 40278221)
6. Bayliss, R., Sardon, T., Vernos, I., and Conti, E. (2003). Structural basis of Aurora-A activation by TPX2 at the mitotic spindle. Mol. Cell 12, 851-862. (Pubitemid 37352779)
7. Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., Shindyalov, I. N., and Bourne, P. E. (2000). The Protein Data Bank. Nucleic Acids Res. 28, 235-242.
8. Bischoff, J. R., et al. (1998). A homologue of Drosophila aurora kinase is oncogenic and amplified in human colorectal cancers. EMBO J. 17, 3052-3065.
9. Bischoff, J. R., and Plowman, G. D. (1999). The Aurora/Ipl1p kinase family: regulators of chromosome segregation and cytokinesis. Trends Cell Biol. 9, 454-459.
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. 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.
12. Carmena, M., and Earnshaw, W. C. (2003). The cellular geography of aurora kinases. Nat. Rev. Mol. Cell Biol. 4, 842-854.
13. Ciferri, C., et al. (2008). Implications for kinetochore-microtubule attachment from the structure of an engineered Ndc80 complex. Cell 133, 427-439. (Pubitemid 351622013)
14. Cooke, C. A., Heck, M. M., and Earnshaw, W. C. (1987). The inner centromere protein (INCENP) antigens: movement from inner centromere to midbody during mitosis. J. Cell Biol. 105, 2053-2067.
15. Dutertre, S., Descamps, S., and Prigent, C. (2002). On the role of aurora-A in centrosome function. Oncogene 21, 6175-6183.
16. Eyers, P. A., Churchill, M. E., and Maller, J. L. (2005). The Aurora A and Aurora B protein kinases: a single amino acid difference controls intrinsic activity and activation by TPX2. Cell Cycle 4, 784-789. ]
17. Eyers, P. A., and Maller, J. L. (2004). Regulation of Xenopus Aurora A activation by TPX2. J. Biol. Chem. 279, 9008-9015.
18. Fu, J., Bian, M., Jiang, Q., and Zhang, C. (2007). Roles of Aurora kinases in mitosis and tumorigenesis. Mol. Cancer Res. 5, 1-10.
19. Fuller, B. G., Lampson, M. A., Foley, E. A., Rosasco-Nitcher, S., Le, K. V., Tobelmann, P., Brautigan, D. L., Stukenberg, P. T., and Kapoor, T. M. (2008). Midzone activation of aurora B in anaphase produces an intracellular phosphorylation gradient. Nature 453, 1132-1136. (Pubitemid 351871729)
20. Giet, R., Petretti, C., and Prigent, C. (2005). Aurora kinases, aneuploidy and cancer, a coincidence or a real link? Trends Cell Biol. 15, 241-250.
21. Giet, R., and Prigent, C. (1999). Aurora/Ipl1p-related kinases, a new oncogenic family of mitotic serine-threonine kinases. J. Cell Sci. 112, 3591-3601. (Pubitemid 129783931)
22. Giet, R., and Prigent, C. (2001). The non-catalytic domain of the Xenopus laevis auroraA kinase localises the protein to the centrosome. J. Cell Sci. 114, 2095-2104.
23. Goto, H., Yasui, Y., Nigg, E. A., and Inagaki, M. (2002). Aurora-B phosphorylates Histone H3 at serine28 with regard to the mitotic chromosome condensation. Genes Cells 7, 11-17. (Pubitemid 34121301)
24. Hagemeier, C., Caswell, R., Hayhurst, G., Sinclair, J., and Kouzarides, T. (1994). Functional interaction between the HCMV IE2 transactivator and the retinoblastoma protein. EMBO J. 13, 2897-2903. (Pubitemid 24191700)
25. Hannak, E., Kirkham, M., Hyman, A. A., and Oegema, K. (2001). Aurora-A kinase is required for centrosome maturation in Caenorhabditis elegans. J. Cell Biol. 155, 1109-1116.
26. Hirota, T., Kunitoku, N., Sasayama, T., Marumoto, T., Zhang, D., Nitta, M., Hatakeyama, K., and Saya, H. (2003). Aurora-A and an interacting activator, the LIM protein Ajuba, are required for mitotic commitment in human cells. Cell 114, 585-598. (Pubitemid 37159255)
27. Honda, R., Korner, R., and Nigg, E. A. (2003). Exploring the functional interactions between Aurora B, INCENP, and survivin in mitosis. Mol. Biol. Cell 14, 3325-3341.
28. Jelluma, N., Brenkman, A. B., van den Broek, N. J., Cruijsen, C. W., van Osch, M. H., Lens, S. M., Medema, R. H., and Kops, G. J. (2008). Mps1 phosphorylates Borealin to control Aurora B activity and chromosome alignment. Cell 132, 233-246. (Pubitemid 351172430)
29. 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. (Pubitemid 47576137)
30. Kabsch, W., and Sander, C. (1983). Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22, 2577-2637.
31. Kaitna, S., Mendoza, M., Jantsch-Plunger, V., and Glotzer, M. (2000). Incenp and an aurora-like kinase form a complex essential for chromosome segregation and efficient completion of cytokinesis. Curr. Biol. 10, 1172-1181.
32. Kang, D., Chen, J., Wong, J., and Fang, G. (2002). The checkpoint protein Chfr is a ligase that ubiquitinates Plk1 and inhibits Cdc2 at the G2 to M transition. J. Cell Biol. 156, 249-259. (Pubitemid 34839907)
33. Keniry, M. E., and Sprague, G. F., Jr. (2003). Identification of p21-activated kinase specificity determinants in budding yeast: a single amino acid substitution imparts Ste20 specificity to Cla4. Mol. Cell Biol. 23, 1569-1580.
34. Klein, U. R., Nigg, E. A., Gruneberg, U., and Zheng, Y. (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.
35. Kufer, T. A., Sillje, H. H., Korner, R., Gruss, O. J., Meraldi, P., and Nigg, E. A. (2002). Human TPX2 is required for targeting Aurora-A kinase to the spindle. J. Cell Biol. 158, 617-623. (Pubitemid 34920101)
36. Kunitoku, N., Sasayama, T., Marumoto, T., Zhang, D., Honda, S., Kobayashi, O., Hatakeyama, K., Ushio, Y., Saya, H., and Hirota, T. (2003). CENP-A phosphorylation by Aurora-A in prophase is required for enrichment of Aurora-B at inner centromeres and for kinetochore function. Dev. Cell 5, 853-864. (Pubitemid 37527686)
37. Liu, Q., and Ruderman, J. V. (2006). Aurora A, mitotic entry, and spindle bipolarity. Proc. Natl. Acad. Sci. USA 103, 5811-5816.
38. Luger, K., Rechsteiner, T. J., and Richmond, T. J. (1999). Expression and purification of recombinant histones and nucleosome reconstitution. Methods Mol. Biol. 119, 1-16.
39. Macurek, L., Lindqvist, A., Lim, D., Lampson, M. A., Klompmaker, R., Freire, R., Clouin, C., Taylor, S. S., Yaffe, M. B., and Medema, R. H. (2008). Polo-like kinase-1 is activated by aurora A to promote checkpoint recovery. Nature 455, 119-123.
40. Meraldi, P., Honda, R., and Nigg, E. A. (2002). Aurora-A overexpression reveals tetraploidization as a major route to centrosome amplification in p53-/- cells. EMBO J. 21, 483-492. (Pubitemid 34174030)
41. 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.
42. Nowakowski, J., et al. (2002). Structures of the cancer-related Aurora-A, FAK, and EphA2 protein kinases from nanovolume crystallography. Structure 10, 1659-1667. (Pubitemid 35452573)
43. Ohashi, S., Sakashita, G., Ban, R., Nagasawa, M., Matsuzaki, H., Murata, Y., Taniguchi, H., Shima, H., Furukawa, K., and Urano, T. (2006). Phosphoregulation of human protein kinase Aurora-A: analysis using anti-phospho-Thr288 monoclonal antibodies. Oncogene 25, 7691-7702. (Pubitemid 44967964)
44. Pan, X., and Heitman, J. (1999). Cyclic AMP-dependent protein kinase regulates pseudohyphal differentiation in Saccharomyces cerevisiae. Mol. Cell Biol. 19, 4874-4887.
45. 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. (Pubitemid 351160581)
46. Roussel, A., Fontecilla-Camps, J. C., and Cambillau, C. (1990). CRYStallize: a crystallographic symmetry display and handling subpackage in TOM/ FRODO. J. Mol. Graph. 8, 86-88, 91.
47. Ruchaud, S., Carmena, M., and Earnshaw, W. C. (2007). Chromosomal passengers: conducting cell division. Nat. Rev. Mol. Cell Biol. 8, 798-812.
48. Satinover, D. L., Leach, C. A., Stukenberg, P. T., and Brautigan, D. L. (2004). Activation of Aurora-A kinase by protein phosphatase inhibitor-2, a bifunctional signaling protein. Proc. Natl. Acad. Sci. USA 101, 8625-8630.
49. Scrittori, L., Skoufias, D. A., Hans, F., Gerson, V., Sassone-Corsi, P., Dimitrov, S., and Margolis, R. L. (2005). A small C-terminal sequence of Aurora B is responsible for localization and function. Mol. Biol. Cell 16, 292-305.
50. 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)
51. Shulz, G. E., and Schirmer, R. H. (1979). Principles of Protein Structure, New York: Springer-Verlag.
52. Soncini, C., et al. (2006). PHA-680632, a novel Aurora kinase inhibitor with potent antitumoral activity. Clin. Cancer Res. 12, 4080-4089.
53. 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. (Pubitemid 38697108)
54. Vader, G., Kauw, J. J., Medema, R. H., and Lens, S. M. (2006). Survivin mediates targeting of the chromosomal passenger complex to the centromere and midbody. EMBO Rep. 7, 85-92.
55. Zhou, H., Kuang, J., Zhong, L., Kuo, W. L., Gray, J. W., Sahin, A., Brinkley, B. R., and Sen, S. (1998). Tumour amplified kinase STK15/BTAK induces centrosome amplification, aneuploidy and transformation. Nat. Genet. 20, 189-193.