Spatial compartmentalization specializes the function of Aurora A and Aurora B

Journal of Biological Chemistry

Volumn 290, Issue 28, 2015, Pages 17546-17558

  Li, Si ^a,b   Deng, Zhaoxuan ^b   Fu, Jingyan ^b   Xu, Caiyue ^b   Xin, Guangwei ^b   Wu, Zhige ^b   Luo, Jia ^b   Wang, Gang ^b   Zhang, Shuli ^b   Zhang, Boyan ^b   Zou, Fangdong ^a   Jiang, Qing ^b   Zhang, Chuanmao ^b  

^a SICHUAN UNIVERSITY   (China)

^b Peking University   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOLOGY;

AURORA KINASE;

ENZYMES;

AURORA A KINASE; AURORA B KINASE; HISTONE H3; AURKA PROTEIN, HUMAN; AURKB PROTEIN, HUMAN; CHROMATIN; HISTONE; HYBRID PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL COMPARTMENTALIZATION; CENTROSOME; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; PRIORITY JOURNAL; PROTEIN EXPRESSION; AMINO ACID SEQUENCE; ANIMAL; BIOLOGICAL MODEL; CELL CYCLE CHECKPOINT; CENTROMERE; CHEMISTRY; CHROMATIN; GENETICS; HELA CELL LINE; HUMAN; METABOLISM; MITOSIS; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PHOSPHORYLATION; SEQUENCE HOMOLOGY; SPINDLE APPARATUS;

AMINO ACID SEQUENCE; ANIMALS; AURORA KINASE A; AURORA KINASE B; CELL COMPARTMENTATION; CELL CYCLE CHECKPOINTS; CENTROSOME; CHROMATIN; EVOLUTION, MOLECULAR; HELA CELLS; HISTONES; HUMANS; KINETOCHORES; MITOSIS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; RECOMBINANT FUSION PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SPINDLE APPARATUS;

EID: 84937537279     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.652453     Document Type: Article

References (48)

1. Carmena, M., and Earnshaw, W. C. (2003) The cellular geography of aurora kinases. Nat. Rev. Mol. Cell Biol. 4, 842-854
2. Fu, J., Bian, M., Jiang, Q., and Zhang, C. (2007) Roles of aurora kinases in mitosis and tumorigenesis. Mol Cancer Res. 5, 1-10
3. Carmena, M., Wheelock, M., Funabiki, H., and Earnshaw, W. C. (2012) The chromosomal passenger complex (CPC): from easy rider to the godfather of mitosis. Nat. Rev. Mol. Cell Biol. 13, 789-803
4. Fu, J., Bian, M., Liu, J., Jiang, Q., and Zhang, C. (2009) A single amino acid change converts Aurora A into Aurora B-like kinase in terms of partner specificity and cellular function. Proc. Natl. Acad. Sci. U.S.A. 106, 6939-6944
5. Reboutier, D., Troadec, M. B., Cremet, J. Y., Chauvin, L., Guen, V., Salaun, P., and Prigent, C. (2013) Aurora A is involved in central spindle assembly through phosphorylation of Ser-19 in P150Glued. J. Cell Biol. 201, 65-79
6. Stenoien, D. L., Sen, S., Mancini, M. A., and Brinkley, B. R. (2003) Dynamic association of a tumor amplified kinase, Aurora A, with the centrosome and mitotic spindle. Cell Motil. Cytoskeleton 55, 134-146
7. Fu, W., Tao, W., Zheng, P., Fu, J., Bian, M., Jiang, Q., Clarke, P. R., and Zhang, C. (2010) Clathrin recruits phosphorylated TACC3 to spindle poles for bipolar spindle assembly and chromosome alignment. J. Cell Sci. 123, 3645-3651
8. Fu, W., Chen, H., Wang, G., Luo, J., Deng, Z., Xin, G., Xu, N., Guo, X., Lei, J., Jiang, Q., and Zhang, C. (2013) Self-assembly and sorting of acentrosomal microtubules by TACC3 facilitate kinetochore capture during the mitotic spindle assembly. Proc. Natl. Acad. Sci. U.S.A. 110, 15295-15300
9. Giet, R., Uzbekov, R., Cubizolles, F., Le Guellec, K., and Prigent, C. (1999) The Xenopus laevis aurora-related protein kinase pEg2 associates with and phosphorylates the kinesin-related protein XlEg5. J. Biol. Chem. 274, 15005-15013
10. 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
11. Wang, G., Jiang, Q., and Zhang, C. (2014) The role of mitotic kinases in coupling the centrosome cycle with the assembly of the mitotic spindle. J. Cell Sci. 127, 4111-4122
12. 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
13. 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
14. Glover, D. (2003) Aurora A on the mitotic spindle is activated by the way it holds its partner. Mol. Cell 12, 797-799.
15. Eyers, P. A., Erikson, E., Chen, L. G., and Maller, J. L. (2003) A novel mechanism for activation of the protein kinase Aurora A. Curr. Biol. 13, 691-697
16. Hutterer, A., Berdnik, D., Wirtz-Peitz, F., Zigman, M., Schleiffer, A., and Knoblich, J. A. (2006) Mitotic activation of the kinase Aurora A requires its binding partner Bora. Dev. Cell 11, 147-157
17. Zhao, Z. S., Lim, J. P., Ng, Y. W., Lim, L., and Manser, E. (2005) The GIT-associated kinase PAK targets to the centrosome and regulates Aurora A. Mol. Cell 20, 237-249
18. Abe, Y., Okumura, E., Hosoya, T., Hirota, T., and Kishimoto, T. (2010) A single starfish Aurora kinase performs the combined functions of Aurora A and Aurora B in human cells. J. Cell Sci. 123, 3978-3988
19. Hebras, C., and McDougall, A. (2012) Urochordate ascidians possess a single isoform of Aurora kinase that localizes to the midbody via TPX2 in eggs and cleavage stage embryos. PLoS ONE 7, e45431
20. Li, H., Chen, Q., Kaller, M., Nellen, W., Gräf, R., and De Lozanne, A. (2008) Dictyostelium Aurora kinase has properties of both Aurora A and Aurora B kinases. Eukaryot. Cell 7, 894-905
21. Brown, J. R., Koretke, K. K., Birkeland, M. L., Sanseau, P., and Patrick, D. R. (2004) Evolutionary relationships of Aurora kinases: implications for model organism studies and the development of anti-cancer drugs. BMC Evol. Biol. 4, 39
22. Capra, E. J., Perchuk, B. S., Skerker, J. M., and Laub, M. T. (2012) Adaptive mutations that prevent crosstalk enable the expansion of paralogous signaling protein families. Cell 150, 222-232
23. Rausell, A., Juan, D., Pazos, F., and Valencia, A. (2010) Protein interactions and ligand binding: from protein subfamilies to functional specificity. Proc. Natl. Acad. Sci. U.S.A. 107, 1995-2000
24. Alexander, J., Lim, D., Joughin, B. A., Hegemann, B., Hutchins, J. R., Ehrenberger, T., Ivins, F., Sessa, F., Hudecz, O., Nigg, E. A., Fry, A. M., Musacchio, A., Stukenberg, P. T., Mechtler, K., Peters, J. M., Smerdon, S. J., and Yaffe, M. B. (2011) Spatial exclusivity combined with positive and negative selection of phosphorylation motifs is the basis for context-dependent mitotic signaling. Sci. Signal. 4, ra42
25. Kim, Y., Holland, A. J., Lan, W., and Cleveland, D. W. (2010) Aurora kinases and protein phosphatase 1 mediate chromosome congression through regulation of CENP-E. Cell 142, 444-455
26. Tanenbaum, M. E., Macurek, L., van der Vaart, B., Galli, M., Akhmanova, A., and Medema, R. H. (2011) A complex of Kif18b and MCAK promotes microtubule depolymerization and is negatively regulated by Aurora kinases. Curr. Biol. 21, 1356-1365
27. Knowlton, A. L., Vorozhko, V. V., Lan, W., Gorbsky, G. J., and Stukenberg, P. T. (2009) ICIS and Aurora B coregulate the microtubule depolymerase Kif2a. Curr. Biol. 19, 758-763
28. Jang, C. Y., Coppinger, J. A., Seki, A., Yates, J. R., 3rd, and Fang, G. (2009) Plk1 and Aurora A regulate the depolymerase activity and the cellular localization of Kif2a. J. Cell Sci. 122, 1334-1341
29. Song, S. J., Song, M. S., Kim, S. J., Kim, S. Y., Kwon, S. H., Kim, J. G., Calvisi, D. F., Kang, D., and Lim, D. S. (2009) Aurora A regulates prometaphase progression by inhibiting the ability of RASSF1A to suppress APC-Cdc20 activity. Cancer Res. 69, 2314-2323
30. Hochegger, H., Hégarat, N., and Pereira-Leal, J. B. (2013) Aurora at the pole and equator: overlapping functions of Aurora kinases in the mitotic spindle. Open Biol. 3, 120185
31. Carmena, M., Ruchaud, S., and Earnshaw, W. C. (2009) Making the Auroras glow: regulation of Aurora A and B kinase function by interacting proteins. Curr. Opin. Cell Biol. 21, 796-805
32. 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
33. Wang, E., Ballister, E. R., and Lampson, M. A. (2011) Aurora B dynamics at centromeres create a diffusion-based phosphorylation gradient. J. Cell Biol. 194, 539-549
34. Lampson, M. A., and Cheeseman, I. M. (2011) Sensing centromere tension: Aurora B and the regulation of kinetochore function. Trends Cell Biol. 21, 133-140
35. Przewloka, M. R., and Glover, D. M. (2009) The Kinetochore and the centromere: a working long distance relationship. Ann. Rev. Genet. 43, 439-465
36. Santaguida, S., Vernieri, C., Villa, F., Ciliberto, A., and Musacchio, A. (2011) Evidence that Aurora B is implicated in spindle checkpoint signalling independently of error correction. EMBO J. 30, 1508-1519
37. Saurin, A. T., van der Waal, M. S., Medema, R. H., Lens, S. M., and Kops, G. J. (2011) Aurora B potentiates Mps1 activation to ensure rapid checkpoint establishment at the onset of mitosis. Nat. Commun. 2, 316
38. DeBonis, S., Skoufias, D. A., Lebeau, L., Lopez, R., Robin, G., Margolis, R. L., Wade, R. H., and Kozielski, F. (2004) In vitro screening for inhibitors of the human mitotic kinesin Eg5 with antimitotic and antitumor activities. Mol Cancer Ther. 3, 1079-1090
39. Skoufias, D. A., DeBonis, S., Saoudi, Y., Lebeau, L., Crevel, I., Cross, R., Wade, R. H., Hackney, D., and Kozielski, F. (2006) S-trityl-L-cysteine is a reversible, tight binding inhibitor of the human kinesin Eg5 that specifically blocks mitotic progression. J. Biol. Chem. 281, 17559-17569
40. 2-M transition. J. Cell Sci. 117, 2523-2531
41. Seki, A., Coppinger, J. A., Jang, C. Y., Yates, J. R., and Fang, G. (2008) Bora and the kinase Aurora a cooperatively activate the kinase Plk1 and control mitotic entry. Science 320, 1655-1658
42. Sonnen, K. F., Gabryjonczyk, A.-M., Anselm, E., Stierhof, Y.-D., and Nigg, E. A. (2013) Human Cep192 and Cep152 cooperate in Plk4 recruitment and centriole duplication. J. Cell Sci. 126, 3223-3233
43. Li, J., Meyer, A. N., and Donoghue, D. J. (1997) Nuclear localization of cyclin B1 mediates its biological activity and is regulated by phosphorylation. Proc. Natl. Acad. Sci. U.S.A. 94, 502-507
44. Hans, F., Skoufias, D. A., Dimitrov, S., and Margolis, R. L. (2009) Molecular distinctions between Aurora A and B: a single residue change transforms aurora A into correctly localized and functional Aurora B. Mol. Biol. Cell 20, 3491-3502
45. Giet, R., and Prigent, C. (2001) The non-catalytic domain of the Xenopus laevis Aurora A kinase localises the protein to the centrosome. J. Cell Sci. 114, 2095-2104
46. 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
47. Marumoto, T., Honda, S., Hara, T., Nitta, M., Hirota, T., Kohmura, E., and Saya, H. (2003) Aurora A kinase maintains the fidelity of early and late mitotic events in HeLa cells. J. Biol. Chem. 278, 51786-51795
48. Bian, M., Fu, J., Yan, Y., Chen, Q., Yang, C., Shi, Q., Jiang, Q., and Zhang, C. (2010) Short exposure to paclitaxel induces multipolar spindle formation and aneuploidy through promotion of acentrosomal pole assembly. Sci. China Life Sci. 53, 1322-1329