Nucleophosmin/B23 activates aurora a at the centrosome through phosphorylation of serine 89

Journal of Cell Biology

Volumn 197, Issue 1, 2012, Pages 19-26

  Reboutier, David ^a   Troadec, Marie Bérengère ^a   Cremet, Jean Yves ^a   Fukasawa, Kenji ^b   Prigent, Claude ^a  

^a UNIVERSITÉ DE RENNES 1   (France)

^b H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA A KINASE; NUCLEOPHOSMIN; SERINE; SERINE 89; THREONINE; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE G2 PHASE; CENTROSOME; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RNA INTERFERENCE;

CENTROSOME; HELA CELLS; HUMANS; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; SERINE;

EID: 84860284549     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201107134     Document Type: Article

References (36)

1. Amin, M.A., S. Matsunaga, S. Uchiyama, and K. Fukui. 2008a. Depletion of nucleophosmin leads to distortion of nucleolar and nuclear structures in HeLa cells. Biochem. J. 415:345-351. http://dx.doi.org/10.1042/BJ20081411
2. Amin, M.A., S. Matsunaga, S. Uchiyama, and K. Fukui. 2008b. Nucleophosmin is required for chromosome congression, proper mitotic spindle formation, and kinetochore-microtubule attachment in HeLa cells. FEBS Lett. 582:3839-3844. http://dx.doi.org/10.1016/j.febslet.2008.10.023
3. Anthis, N.J., J.R. Haling, C.L. Oxley, M. Memo, K.L. Wegener, C.J. Lim, M.H. Ginsberg, and I.D. Campbell. 2009. Beta integrin tyrosine phosphorylation is a conserved mechanism for regulating talin-induced integrin activation. J. Biol. Chem. 284:36700-36710. http://dx.doi.org/10.1074/jbc.M109.061275
4. 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
5. Bischoff, J.R., L. Anderson, Y. Zhu, K. Mossie, L. Ng, B. Souza, B. Schryver, P. Flanagan, F. Clairvoyant, C. Ginther, et al. 1998. A homologue of Drosophila aurora kinase is oncogenic and amplified in human colorectal cancers. EMBO J. 17:3052-3065. http://dx.doi.org/10.1093/emboj/17.11.3052
6. Boutros, R., V. Lobjois, and B. Ducommun. 2007. CDC25B involvement in the centrosome duplication cycle and in microtubule nucleation. Cancer Res. 67:11557-11564. http://dx.doi.org/10.1158/0008-5472.CAN-07-2415
7. Cazales, M., E. Schmitt, E. Montembault, C. Dozier, C. Prigent, and B. Ducommun. 2005. CDC25B phosphorylation by Aurora-A occurs at the G2/M transition and is inhibited by DNA damage. Cell Cycle. 4:1233-1238. http://dx.doi.org/10.4161/cc.4.9.1964
8. Cremet, J.Y., S. Descamps, F. Vérite, A. Martin, and C. Prigent. 2003. Preparation and characterization of a human aurora-A kinase monoclonal antibody. Mol. Cell. Biochem. 243:123-131. http://dx.doi.org/10.1023/A:1021608012253
9. Dodson, C.A., and R. Bayliss. 2012. Activation of Aurora-A kinase by protein partner binding and phosphorylation are independent and synergistic. J. Biol. Chem. 287:1150-1157. http://dx.doi.org/10.1074/jbc.M111.312090
10. Dutertre, S., M. Cazales, M. Quaranta, C. Froment, V. Trabut, C. Dozier, G. Mirey, J.P. Bouché, N. Theis-Febvre, E. Schmitt, et al. 2004. Phosphorylation of CDC25B by Aurora-A at the centrosome contributes to the G2-M transition. J. Cell Sci. 117:2523-2531. http://dx.doi.org/10.1242/jcs.01108
11. Eyers, P.A., and J.L. Maller. 2004. Regulation of Xenopus Aurora A activation by TPX2. J. Biol. Chem. 279:9008-9015. http://dx.doi.org/10.1074/jbc.M312424200
12. Eyers, P.A., E. Erikson, L.G. Chen, and J.L. Maller. 2003. A novel mechanism for activation of the protein kinase Aurora A. Curr. Biol. 13:691-697. http://dx.doi.org/10.1016/S0960-9822(03)00166-0
13. Gabrielli, B.G., C.P. De Souza, I.D. Tonks, J.M. Clark, N.K. Hayward, and K.A. Ellem. 1996. Cytoplasmic accumulation of cdc25B phosphatase in mitosis triggers centrosomal microtubule nucleation in HeLa cells. J. Cell Sci. 109:1081-1093.
14. Ganem, N.J., S.A. Godinho, and D. Pellman. 2009. A mechanism linking extra centrosomes to chromosomal instability. Nature. 460:278-282. http://dx.doi.org/10.1038/nature08136
15. Gopalan, G., C.S. Chan, and P.J. Donovan. 1997. A novel mammalian, mitotic spindle-associated kinase is related to yeast and fly chromosome segregation regulators. J. Cell Biol. 138:643-656. http://dx.doi.org/10.1083/jcb .138.3.643
16. Haydon, C.E., P.A. Eyers, L.D. Aveline-Wolf, K.A. Resing, J.L. Maller, and N.G. Ahn. 2003. Identification of novel phosphorylation sites on Xenopus laevis Aurora A and analysis of phosphopeptide enrichment by immobilized metal-affinity chromatography. Mol. Cell. Proteomics. 2:1055-1067. http://dx.doi.org/10.1074/mcp.M300054-MCP200
17. Hutterer, A., D. Berdnik, F. Wirtz-Peitz, M. Zigman, A. Schleiffer, and J.A. Knoblich. 2006. Mitotic activation of the kinase Aurora-A requires its binding partner Bora. Dev. Cell. 11:147-157. http://dx.doi.org/10.1016/j.devcel.2006.06.002
18. Joukov, V. 2011. Aurora kinases and spindle assembly: Variations on a common theme? Cell Cycle. 10:895-903. http://dx.doi.org/10.4161/cc.10.6.14909
19. Joukov, V., A. De Nicolo, A. Rodriguez, J.C. Walter, and D.M. Livingston. 2010. Centrosomal protein of 192 kDa (Cep192) promotes centrosomedriven spindle assembly by engaging in organelle-specific Aurora A activation. Proc. Natl. Acad. Sci. USA. 107:21022-21027. http://dx.doi.org/10.1073/pnas.1014664107
20. Krystyniak, A., C. Garcia-Echeverria, C. Prigent, and S. Ferrari. 2006. Inhibition of Aurora A in response to DNA damage. Oncogene. 25:338-348.
21. Macůrek, L., A. Lindqvist, D. Lim, M.A. Lampson, R. Klompmaker, R. Freire, C. Clouin, S.S. Taylor, M.B. Yaffe, and R.H. Medema. 2008. Polo-like kinase-1 is activated by aurora A to promote checkpoint recovery. Nature. 455:119-123. http://dx.doi.org/10.1038/nature07185
22. Molli, P.R., D.Q. Li, R. Bagheri-Yarmand, S.B. Pakala, H. Katayama, S. Sen, J. Iyer, J. Chernoff, M.Y. Tsai, S.S. Nair, and R. Kumar. 2010. Arpc1b, a centrosomal protein, is both an activator and substrate of Aurora A. J. Cell Biol. 190:101-114. http://dx.doi.org/10.1083/jcb.200908050
23. Okuda, M., H.F. Horn, P. Tarapore, Y. Tokuyama, A.G. Smulian, P.K. Chan, E.S. Knudsen, I.A. Hofmann, J.D. Snyder, K.E. Bove, and K. Fukasawa. 2000. Nucleophosmin/B23 is a target of CDK2/cyclin E in centrosome duplication. Cell. 103:127-140. http://dx.doi.org/10.1016/S0092-8674(00)00093-3
24. Paleologou, K.E., A.W. Schmid, C.C. Rospigliosi, H.Y. Kim, G.R. Lamberto, R.A. Fredenburg, P.T. Lansbury Jr., C.O. Fernandez, D. Eliezer, M. Zweckstetter, and H.A. Lashuel. 2008. Phosphorylation at Ser-129 but not the phosphomimics S129E/D inhibits the fibrillation of alpha-synuclein. J. Biol. Chem. 283:16895-16905. http://dx.doi.org/10.1074/jbc.M800747200
25. Pascreau, G., J.G. Delcros, N. Morin, C. Prigent, and Y. Arlot-Bonnemains. 2008. Aurora-A kinase Ser349 phosphorylation is required during Xenopus laevis oocyte maturation. Dev. Biol. 317:523-530. http://dx.doi.org/10.1016/j.ydbio.2008.02.053
26. Pugacheva, E.N., and E.A. Golemis. 2005. The focal adhesion scaffolding protein HEF1 regulates activation of the Aurora-A and Nek2 kinases at the centrosome. Nat. Cell Biol. 7:937-946. http://dx.doi.org/10.1038/ncb1309
27. Rannou, Y., M.B. Troadec, C. Petretti, F. Hans, S. Dutertre, S. Dimitrov, and C. Prigent. 2008. Localization of aurora A and aurora B kinases during interphase: Role of the N-terminal domain. Cell Cycle. 7:3012-3020. http://dx.doi.org/10.4161/cc.7.19.6718
28. Roghi, C., R. Giet, R. Uzbekov, N. Morin, I. Chartrain, R. Le Guellec, A. Couturier, M. Dorée, M. Philippe, and C. Prigent. 1998. The Xenopus protein kinase pEg2 associates with the centrosome in a cell cycle-dependent manner, binds to the spindle microtubules and is involved in bipolar mitotic spindle assembly. J. Cell Sci. 111:557-572.
29. Sabino, D., N.H. Brown, and R. Basto. 2011. Drosophila Ajuba is not an Aurora-A activator but is required to maintain Aurora-A at the centrosome. J. Cell Sci. 124:1156-1166. http://dx.doi.org/10.1242/jcs.076711
30. Saskova, A., P. Solc, V. Baran, M. Kubelka, R.M. Schultz, and J. Motlik. 2008. Aurora kinase A controls meiosis I progression in mouse oocytes. Cell Cycle. 7:2368-2376.
31. Satinover, D.L., C.A. Leach, P.T. Stukenberg, and D.L. Brautigan. 2004. Activation of Aurora-A kinase by protein phosphatase inhibitor-2, a bifunctional signaling protein. Proc. Natl. Acad. Sci. USA. 101:8625-8630. http://dx.doi.org/10.1073/pnas.0402966101
32. Scrittori, L., F. Hans, D. Angelov, M. Charra, C. Prigent, and S. Dimitrov. 2001. pEg2 aurora-A kinase, histone H3 phosphorylation, and chromosome assembly in Xenopus egg extract. J. Biol. Chem. 276:30002-30010. http://dx.doi.org/10.1074/jbc.M102701200
33. Seki, A., J.A. Coppinger, C.Y. Jang, J.R. Yates, and G. Fang. 2008. Bora and the kinase Aurora a cooperatively activate the kinase Plk1 and control mitotic entry. Science. 320:1655-1658. http://dx.doi.org/10.1126/science.1157425
34. Shinmura, K., P. Tarapore, Y. Tokuyama, K.R. George, and K. Fukasawa. 2005. Characterization of centrosomal association of nucleophosmin/B23 linked to Crm1 activity. FEBS Lett. 579:6621-6634. http://dx.doi.org/10.1016/j.febslet.2005.10.057
35. Tong, Y., A. Ben-Shlomo, C. Zhou, K. Wawrowsky, and S. Melmed. 2008. Pituitary tumor transforming gene 1 regulates Aurora kinase A activity. Oncogene. 27:6385-6395. http://dx.doi.org/10.1038/onc.2008.234
36. Zatsepina, O.V., N.Zh. Zhelev, and G.J. Jordan. 1995. [Immunolocalization of nucleolar protein B23 in mitotic centrosomes]. Mol. Biol. (Mosk.). 29: 1359-1367.