Aurora A phosphorylation of TACC3/maskin is required for centrosome-dependent microtubule assembly in mitosis

Journal of Cell Biology

Volumn 170, Issue 7, 2005, Pages 1047-1055

  Kinoshita, Kazuhisa ^a   Noetzel, Tim L ^a   Pelletier, Laurence ^a   Mechtler, Karl ^b   Drechsel, David N ^a   Schwager, Anne ^a   Lee, Mike ^c   Raff, Jordan W ^c   Hyman, Anthony A ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^b RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA A PROTEIN KINASE; MASKIN PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; PROTEIN; PROTEIN KINASE; TRANSFORMING ACIDIC COILED COIL 3 PROTEIN; UNCLASSIFIED DRUG; XENOPUS MICROTUBLE ASSOCIATED PROTEIN 215;

ANIMAL CELL; ARTICLE; CENTROSOME; COMPLEX FORMATION; CONTROLLED STUDY; EGG; ENZYME PHOSPHORYLATION; ENZYME REGULATION; EXTRACT; HUMAN; HUMAN CELL; IN VITRO STUDY; MICROTUBULE; MICROTUBULE ASSEMBLY; MITOSIS; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PURIFICATION; REGULATORY MECHANISM; XENOPUS LAEVIS;

ANIMALS; CELL CYCLE PROTEINS; CELL EXTRACTS; CENTROSOME; KINESIN; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MITOSIS; OOCYTES; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; TRANSCRIPTION FACTORS; XENOPUS LAEVIS; XENOPUS PROTEINS;

XENOPUS LAEVIS;

EID: 25444493845     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200503023     Document Type: Article

References (50)

1. Ashford, A.J., S.S. Andersen, and A.A. Hyman. 1998. Preparation of tubulin from bovine brain. In Cell Biology: A Laboratory Handbook. Vol. 2. 2nd ed. J.E. Celis, editor. Academic Press/UK, London. 205-212.
2. Bellanger, J.M., and P. Gönczy. 2003. TAC-1 and ZYG-9 form a complex that promotes microtubule assembly in C. elegans embryos. Curr. Biol. 13:1488-1498.
3. Belmont, L.D., A.A. Hyman, K.E. Sawin, and T.J. Mitchison. 1990. Real-time visualization of cell cycle-dependent changes in microtubule dynamics in cytoplasmic extracts. Cell. 62:579-589.
4. 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.
5. Cheeseman, I.M., S. Anderson, M. Jwa, E.M. Green, J. Kang, J.R. Yates, C.S. Chan, D.G. Drubin, and G. Barnes. 2002. Phospho-regulation of kinetochore-microtubule attachments by the Aurora kinase Ipl1p. Cell. 111:163-172.
6. Cullen, C.F., and H. Ohkura. 2001. Msps protein is localized to acentrosomal poles to ensure bipolarity of Drosophila meiotic spindles. Nat. Cell Biol. 3:637-642.
7. Desai, A., S. Verma, T.J. Mitchison, and C.E. Walczak. 1999a. Kin I kinesins are microtubule-destabilizing enzymes. Cell. 96:69-78.
8. Desai, A., A. Murray, T.J. Mitchison, and C.E. Walczak. 1999b. The use of Xenopus egg extracts to study mitotic spindle assembly and function in vitro. Methods Cell Biol. 61:385-412.
9. Field, C.M., K. Oegema, Y. Zheng, T.J. Mitchison, and C.E. Walczak. 1998. Purification of cytoskeletal proteins using peptide antibodies. Methods Enzymol. 298:525-541.
10. Funabiki, H., and A.W. Murray. 2000. The Xenopus chromokinesin Xkid is essential for metaphase chromosome alignment and must be degraded to allow anaphase chromosome movement. Cell. 102:411-424.
11. Gard, D.L., B.E. Becker, and S. Josh Romney. 2004. MAPping the eukaryotic tree of life: structure, function, and evolution of the MAP215/Dis1 family of microtubule-associated proteins. Int. Rev. Cytol. 239:179-272.
12. Gergely, F., C. Karlsson, I. Still, J. Cowell, J. Kilmartin, and J.W. Raff. 2000. The TACC domain identifies a family of centrosomal proteins that can interact with microtubules. Proc. Natl. Acad. Sci. USA. 97:14352-14357.
13. Gergely, F., V.M. Draviam, and J.W. Raff. 2003. The ch-TOG/XMAP215 protein is essential for spindle pole organization in human somatic cells. Genes Dev. 17:336-341.
14. Giet, R., D. McLean, S. Descamps, M.J. Lee, J.W. Raff, C. Prigent, and D.M. Glover. 2002. Drosophila Aurora A kinase is required to localize D-TACC to centrosomes and to regulate astral microtubules. J. Cell Biol. 156:437-451.
15. Glotzer, M., A.W. Murray, and M.W. Kirschner. 1991. Cyclin is degraded by the ubiquitin pathway. Nature. 349:132-138.
16. Gräf, R., C. Daunderer, and I. Schulz. 2004. Molecular and functional analysis of the dictyostelium centrosome. Int. Rev. Cytol. 241:155-202.
17. Hannak, E., M. Kirkham, A.A. Hyman, and K. Oegema. 2001. Aurora-A kinase is required for centrosome maturation in Caenorhabditis elegans. J. Cell Biol. 155:1109-1116.
18. Hannak, E., K. Oegema, M. Kirkham, P. Gönczy, B. Habermann, and A.A. Hyman. 2002. The kinetically dominant assembly pathway for centrosomal asters in Caenorhabditis elegans is γ-tubulin dependent. J. Cell Biol. 157:591-602.
19. Heald, R., R. Tournebize, T. Blank, R. Sandaltzopoulos, P. Becker, A. Hyman, and E. Karsenti. 1996. Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature. 382:420-425.
20. Hirota, T., N. Kunitoku, T. Sasayama, T. Marumoto, D. Zhang, M. Nitta, K. Hatakeyama, and H. Saya. 2003. Aurora-A and an interacting activator, the LIM protein Ajuba, are required for mitotic commitment in human cells. Cell. 114:585-598.
21. Holmfeldt, P., S. Stenmark, and M. Gullberg. 2004. Differential functional interplay of TOGp/XMAP215 and the KinI kinesin MCAK during interphase and mitosis. EMBO J. 23:627-637.
22. Howard, J., and A.A. Hyman. 2003. Dynamics and mechanics of the microtubule plus end. Nature. 422:753-758.
23. Hyman, A., D. Drechsel, D. Kellogg, S. Salser, K. Sawin, P. Steffen, L. Wordeman, and T. Mitchison. 1991. Preparation of modified tubulins. Methods Enzymol. 196:478-485.
24. Job, D., O. Valiron, and B. Oakley. 2003. Microtubule nucleation. Curr. Opin. Cell Biol. 15:111-117.
25. Karsenti, E., and I. Vernos. 2001. The mitotic spindle: a self-made machine. Science. 294:543-547.
26. Khodjakov, A., and C.L. Rieder. 1999. The sudden recruitment of γ-tubulin to the centrosome at the onset of mitosis and its dynamic exchange throughout the cell cycle, do not require microtubules. J. Cell Biol. 146:585-596.
27. Kinoshita, K., I. Arnal, A. Desai, D.N. Drechsel, and A.A. Hyman. 2001. Reconstitution of physiological microtubule dynamics using purified components. Science. 294:1340-1343.
28. Kinoshita, K., B. Habermann, and A.A. Hyman. 2002. XMAP215: a key component of the dynamic microtubule cytoskeleton. Trends Cell Biol. 12:267-273.
29. Kline-Smith, S.L., and C.E. Walczak. 2004. Mitotic spindle assembly and chromosome segregation: refocusing on microtubule dynamics. Mol. Cell. 15:317-327.
30. Kraft, C., F. Herzog, C. Gieffers, K. Mechtler, A. Hagting, J. Pines, and J.M. Peters. 2003. Mitotic regulation of the human anaphase-promoting complex by phosphorylation. EMBO J. 22:6598-6609.
31. Le Bot, N., M.C. Tsai, R.K. Andrews, and J. Ahringer. 2003. TAC-1, a regulator of microtubule length in the C. elegans embryo. Curr. Biol. 13:1499-1505.
32. Lee, M.J., F. Gergely, K. Jeffers, S.Y. Peak-Chew, and J.W. Raff. 2001. Msps/XMAP215 interacts with the centrosomal protein D-TACC to regulate microtubule behaviour. Nat. Cell Biol. 3:643-649.
33. Moudjou, M., and M. Bornens. 1998. Method of centrosome isolation from cultured animal cells. In Cell Biology: A Laboratory Handbook. Vol. 2. 2nd ed. J.E. Celis, editor. Academic Press/UK, London. 111-119.
34. Murray, A.W. 1991. Cell cycle extracts. Methods Cell Biol. 36:581-605.
35. Noetzel, T.L., D.N. Drechsel, A.A. Hyman, and K. Kinoshita. 2005. A comparison of the ability of XMAP215 and tau to inhibit the microtubule destabilizing activity of XKCM1. Philos. Trans. R. Soc. Lond. B Biol. Sci. 360:591-594.
36. Oegema, K., A. Desai, S. Rybina, M. Kirkham, and A.A. Hyman. 2001. Functional analysis of kinetochore assembly in Caenorhabditis elegans. J. Cell Biol. 153:1209-1226.
37. Pascreau, G., J.G. Delcros, J.Y. Cremet, C. Prigent, and Y. Arlot-Bonnemains. 2005. Phosphorylation of maskin by Aurora-A participates to the control of sequential protein synthesis during Xenopus laevis oocyte maturation. J. Biol. Chem. 280:13415-13423.
38. Piehl, M., U.S. Tulu, P. Wadsworth, and L. Cassimeris. 2004. Centrosome maturation: measurement of microtubule nucleation throughout the cell cycle by using GFP-tagged EB1. Proc. Natl. Acad. Sci. USA. 101:1584-1588.
39. Raff, J.W. 2002. Centrosomes and cancer: lessons from a TACC. Trends Cell Biol. 12:222-225.
40. Sampath, S.C., R. Ohi, O. Leismann, A. Salic, A. Pozniakovski, and H. Funabiki. 2004. The chromosomal passenger complex is required for chromatin-induced microtubule stabilization and spindle assembly. Cell. 118:187-202.
41. Sato, M., L. Vardy, M. Angel Garcia, N. Koonrugsa, and T. Toda. 2004. Interdependency of fission yeast Alp14/TOG and coiled coil protein Alp7 in microtubule localization and bipolar spindle formation. Mol. Biol. Cell. 15:1609-1622.
42. Srayko, M., S. Quintin, A. Schwager, and A.A. Hyman. 2003. Caenorhabditis elegans TAC-1 and ZYG-9 form a complex that is essential for long astral and spindle microtubules. Curr. Biol. 13:1506-1511.
43. Stebbins-Boaz, B., Q. Cao, C.H. de Moor, R. Mendez, and J.D. Richter. 1999. Maskin is a CPEB-associated factor that transiently interacts with elF-4E. Mol. Cell. 4:1017-1027.
44. Still, I.H., A.K. Vettaikkorumakankauv, A. DiMatteo, and P. Liang. 2004. Structure-function evolution of the transforming acidic coiled coil genes revealed by analysis of phylogenetically diverse organisms. BMC Evol. Biol. 4:16.
45. Tien, A.C., M.H. Lin, L.J. Su, Y.R. Hong, T.S. Cheng, Y.C. Lee, W.J. Lin, I.H. Still, and C.Y. Huang. 2004. Identification of the substrates and interaction proteins of aurora kinases from a protein-protein interaction model. Mol. Cell. Proteomics. 3:93-104.
46. Tournebize, R., A. Popov, K. Kinoshita, A.J. Ashford, S. Rybina, A. Pozniakovsky, T.U. Mayer, C.E. Walczak, E. Karsenti, and A.A. Hyman. 2000. Control of microtubule dynamics by the antagonistic activities of XMAP215 and XKCM1 in Xenopus egg extracts. Nat. Cell Biol. 2:13-19.
47. Usui, T., H. Maekawa, G. Pereira, and E. Schiebel. 2003. The XMAP215 homologue Stu2 at yeast spindle pole bodies regulates microtubule dynamics and anchorage. EMBO J. 22:4779-4793.
48. Vorlaufer, E., and J.M. Peters. 1998. Regulation of the cyclin B degradation system by an inhibitor of mitotic proteolysis. Mol. Biol. Cell. 9:1817-1831.
49. Walczak, C.E., T.J. Mitchison, and A. Desai. 1996. XKCM1: a Xenopus kinesin-related protein that regulates microtubule dynamics during mitotic spindle assembly. Cell. 84:37-47.
50. Walker, R.A., E.T. O'Brien, N.K. Pryer, M.F. Soboeiro, W.A. Voter, H.P. Erickson, and E.D. Salmon. 1988. Dynamic instability of individual microtubules analyzed by video light microscopy: rate constants and transition frequencies. J. Cell Biol. 107:1437-1448.