Coordination of adjacent domains mediates TACC3-ch-TOG-clathrin assembly and mitotic spindle binding

Journal of Cell Biology

Volumn 202, Issue 3, 2013, Pages 463-478

  Hood, Fiona E ^a   Williams, Samantha J ^a,e   Burgess, Selena G ^b   Richards, Mark W ^b   Roth, Daniel ^c   Straube, Anne ^c   Pfuhl, Mark ^d   Bayliss, Richard ^b   Royle, Stephen J ^a,c  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b UNIVERSITY OF LEICESTER   (United Kingdom)

^c UNIVERSITY OF WARWICK   (United Kingdom)

^d KING'S COLLEGE LONDON   (United Kingdom)

^e Centro Nacional de Investigations Oncológicas   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA A KINASE; CLATHRIN; PROTEIN; PROTEIN CH TOG; PROTEIN TACC3; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CENTROMERE; CROSS LINKING; HUMAN; HUMAN CELL; MICROTUBULE; MITOSIS SPINDLE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

ANIMALS; BINDING SITES; CARRIER PROTEINS; CLATHRIN; FETAL PROTEINS; HEK293 CELLS; HUMANS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; SPINDLE APPARATUS;

EID: 84883174686     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201211127     Document Type: Article

References (51)

1. Barr, A.R., and F. Gergely. 2007. Aurora-A: the maker and breaker of spindle poles. J. Cell Sci. 120:2987-2996. http://dx.doi.org/10.1242/jcs.013136
2. Barr, A.R., and F. Gergely. 2008. MCAK-independent functions of ch-Tog/XMAP215 in microtubule plus-end dynamics. Mol. Cell. Biol. 28:7199- 7211. http://dx.doi.org/10.1128/MCB.01040-08
3. Booth, D.G., F.E. Hood, I.A. Prior, and S.J. Royle. 2011. A TACC3/ch-TOG/clathrin complex stabilises kinetochore fibres by inter-microtubule bridging. EMBO J. 30:906-919. http://dx.doi.org/10.1038/emboj.2011.15
4. Brouhard, G.J., J.H. Stear, T.L. Noetzel, J. Al-Bassam, K. Kinoshita, S.C. Harrison, J. Howard, and A.A. Hyman. 2008. XMAP215 is a processive microtubule polymerase. Cell. 132:79-88. http://dx.doi.org/10.1016/j.cell.2007.11.043
5. Campbell, C., J. Squicciarini, M. Shia, P.F. Pilch, and R.E. Fine. 1984. Identification of a protein kinase as an intrinsic component of rat liver coated vesicles. Biochemistry. 23:4420-4426. http://dx.doi.org/10.1021/bi00314a028
6. Cassimeris, L., and J. Morabito. 2004. TOGp, the human homolog of XMAP215/Dis1, is required for centrosome integrity, spindle pole organization, and bipolar spindle assembly. Mol. Biol. Cell. 15:1580-1590. http://dx.doi.org/10.1091/mbc.E03-07-0544
7. Cassimeris, L., B. Becker, and B. Carney. 2009. TOGp regulates microtubule assembly and density during mitosis and contributes to chromosome directional instability. Cell Motil. Cytoskeleton. 66:535-545. http://dx.doi.org/10.1002/cm.20359
8. Charrasse, S., M. Schroeder, C. Gauthier-Rouviere, F. Ango, L. Cassimeris, D.L. Gard, and C. Larroque. 1998. The TOGp protein is a new human microtubule- associated protein homologous to the Xenopus XMAP215. J. Cell Sci. 111:1371-1383.
9. Cheeseman, L.P., D.G. Booth, F.E. Hood, I.A. Prior, and S.J. Royle. 2011. Aurora A kinase activity is required for localization of TACC3/ch-TOG/clathrin inter-microtubule bridges. Commun. Integr. Biol. 4: 409-412.
10. Cheeseman, L.P., E.F. Harry, A.D. McAinsh, I.A. Prior, and S.J. Royle. 2013. Specific removal of TACC3-ch-TOG-clathrin at metaphase deregulates kinetochore fiber tension. J. Cell Sci. 126:2102-2113. http://dx.doi.org/10.1242/jcs.124834
11. Conte, N., B. Delaval, C. Ginestier, A. Ferrand, D. Isnardon, C. Larroque, C. Prigent, B. Séraphin, J. Jacquemier, and D. Birnbaum. 2003. TACC1- chTOG-Aurora A protein complex in breast cancer. Oncogene. 22:8102- 8116. http://dx.doi.org/10.1038/sj.onc.1206972
12. De Luca, M., L. Brunetto, I.A. Asteriti, M. Giubettini, P. Lavia, and G. Guarguaglini. 2008. Aurora-A and ch-TOG act in a common pathway in control of spindle pole integrity. Oncogene. 27:6539-6549. http://dx.doi.org/10.1038/onc.2008.252
13. Edeling, M.A., S.K. Mishra, P.A. Keyel, A.L. Steinhauser, B.M. Collins, R. Roth, J.E. Heuser, D.J. Owen, and L.M. Traub. 2006. Molecular switches involving the AP-2 beta2 appendage regulate endocytic cargo selection and clathrin coat assembly. Dev. Cell. 10:329-342. http://dx.doi.org/10.1016/j.devcel.2006.01.016
14. Foraker, A.B., S.M. Camus, T.M. Evans, S.R. Majeed, C.Y. Chen, S.B. Taner, I.R. Corrêa Jr., S.J. Doxsey, and F.M. Brodsky. 2012. Clathrin promotes centrosome integrity in early mitosis through stabilization of centrosomal ch-TOG. J. Cell Biol. 198:591-605. http://dx.doi.org/10.1083/jcb.201205116
15. Fotin, A., Y. Cheng, P. Sliz, N. Grigorieff, S.C. Harrison, T. Kirchhausen, and T. Walz. 2004. Molecular model for a complete clathrin lattice from electron cryomicroscopy. Nature. 432:573-579. http://dx.doi.org/10.1038/nature03079
16. Fowler, C.A., F. Tian, H.M. Al-Hashimi, and J.H. Prestegard. 2000. Rapid determination of protein folds using residual dipolar couplings. J. Mol. Biol. 304:447-460. http://dx.doi.org/10.1006/jmbi.2000.4199
17. Fu, W., W. Tao, P. Zheng, J. Fu, M. Bian, Q. Jiang, P.R. Clarke, and C. Zhang. 2010. Clathrin recruits phosphorylated TACC3 to spindle poles for bipolar spindle assembly and chromosome alignment. J. Cell Sci. 123:3645-3651. http://dx.doi.org/10.1242/jcs.075911
18. Gell, C., C.T. Friel, B. Borgonovo, D.N. Drechsel, A.A. Hyman, and J. Howard. 2011. Purification of tubulin from porcine brain. Methods Mol. Biol. 777:15-28. http://dx.doi.org/10.1007/978-1-61779-252-6_2
19. Gergely, F., C. Karlsson, I. Still, J. Cowell, J. Kilmartin, and J.W. Raff. 2000a. The TACC domain identifies a family of centrosomal proteins that can interact with microtubules. Proc. Natl. Acad. Sci. USA. 97:14352-14357. http://dx.doi.org/10.1073/pnas.97.26.14352
20. Gergely, F., D. Kidd, K. Jeffers, J.G. Wakefield, and J.W. Raff. 2000b. D-TACC: a novel centrosomal protein required for normal spindle function in the early Drosophila embryo. EMBO J. 19:241-252. http://dx.doi.org/10.1093/emboj/19.2.241
21. 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. http://dx.doi.org/10.1101/gad.245603
22. Goode, B.L., J.J. Wong, A.C. Butty, M. Peter, A.L. McCormack, J.R. Yates, D.G. Drubin, and G. Barnes. 1999. Coronin promotes the rapid assembly and cross-linking of actin filaments and may link the actin and microtubule cytoskeletons in yeast. J. Cell Biol. 144:83-98. http://dx.doi.org/10.1083/jcb.144.1.83
23. Hawkins, T.L., D. Sept, B. Mogessie, A. Straube, and J.L. Ross. 2013. Mechanical properties of doubly stabilized microtubule filaments. Biophys. J. 104: 1517-1528. http://dx.doi.org/10.1016/j.bpj.2013.02.026
24. 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. http://dx.doi.org/10.1038/sj.emboj.7600076
25. Hood, F.E., and S.J. Royle. 2009. Functional equivalence of the clathrin heavy chains CHC17 and CHC22 in endocytosis and mitosis. J. Cell Sci. 122:2185-2190. http://dx.doi.org/10.1242/jcs.046177
26. Hubner, N.C., A.W. Bird, J. Cox, B. Splettstoesser, P. Bandilla, I. Poser, A. Hyman, and M. Mann. 2010. Quantitative proteomics combined with BAC TransgeneOmics reveals in vivo protein interactions. J. Cell Biol. 189:739-754. http://dx.doi.org/10.1083/jcb.200911091
27. Kinoshita, K., T.L. Noetzel, L. Pelletier, K. Mechtler, D.N. Drechsel, A. Schwager, M. Lee, J.W. Raff, and A.A. Hyman. 2005. Aurora A phosphorylation of TACC3/maskin is required for centrosome-dependent microtubule assembly in mitosis. J. Cell Biol. 170:1047-1055. http://dx.doi.org/10.1083/jcb.200503023
28. 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. http://dx.doi.org/10.1038/35083033
29. LeRoy, P.J., J.J. Hunter, K.M. Hoar, K.E. Burke, V. Shinde, J. Ruan, D. Bowman, K. Galvin, and J.A. Ecsedy. 2007. Localization of human TACC3 to mitotic spindles is mediated by phosphorylation on Ser558 by Aurora A: a novel pharmacodynamic method for measuring Aurora A activity. Cancer Res. 67:5362-5370. http://dx.doi.org/10.1158/0008-5472.CAN-07-0122
30. Lin, C.H., C.K. Hu, and H.M. Shih. 2010. Clathrin heavy chain mediates TACC3 targeting to mitotic spindles to ensure spindle stability. J. Cell Biol. 189:1097-1105. http://dx.doi.org/10.1083/jcb.200911120
31. Lupas, A., M. Van Dyke, and J. Stock. 1991. Predicting coiled coils from protein sequences. Science. 252:1162-1164. http://dx.doi.org/10.1126/science.252.5009.1162
32. Manning, A.L., and D.A. Compton. 2008. Structural and regulatory roles of nonmotor spindle proteins. Curr. Opin. Cell Biol. 20:101-106. http://dx.doi.org/10.1016/j.ceb.2007.11.004
33. McNicholas, S., E. Potterton, K.S. Wilson, and M.E. Noble. 2011. Presenting your structures: the CCP4mg molecular-graphics software. Acta Crystallogr. D Biol. Crystallogr. 67:386-394. http://dx.doi.org/10.1107/S0907444911007281
34. O'Brien, L.L., A.J. Albee, L. Liu, W. Tao, P. Dobrzyn, S.B. Lizarraga, and C. Wiese. 2005. The Xenopus TACC homologue, maskin, functions in mitotic spindle assembly. Mol. Biol. Cell. 16:2836-2847. http://dx.doi.org/10.1091/mbc.E04-10-0926
35. Peset, I., and I. Vernos. 2008. The TACC proteins: TACC-ling microtubule dynamics and centrosome function. Trends Cell Biol. 18:379-388. http://dx.doi.org/10.1016/j.tcb.2008.06.005
36. Peset, I., J. Seiler, T. Sardon, L.A. Bejarano, S. Rybina, and I. Vernos. 2005. Function and regulation of Maskin, a TACC family protein, in microtubule growth during mitosis. J. Cell Biol. 170:1057-1066. http://dx.doi.org/10.1083/jcb.200504037
37. Robinson, M.S., D.A. Sahlender, and S.D. Foster. 2010. Rapid inactivation of proteins by rapamycin-induced rerouting to mitochondria. Dev. Cell. 18:324-331. http://dx.doi.org/10.1016/j.devcel.2009.12.015
38. Royle, S.J. 2012. The role of clathrin in mitotic spindle organisation. J. Cell Sci. 125:19-28. http://dx.doi.org/10.1242/jcs.094607
39. Royle, S.J., and L. Lagnado. 2006. Trimerisation is important for the function of clathrin at the mitotic spindle. J. Cell Sci. 119:4071-4078. http://dx.doi.org/10.1242/jcs.03192
40. Royle, S.J., N.A. Bright, and L. Lagnado. 2005. Clathrin is required for the function of the mitotic spindle. Nature. 434:1152-1157. http://dx.doi.org/10.1038/nature03502
41. Singh, D., J.M. Chan, P. Zoppoli, F. Niola, R. Sullivan, A. Castano, E.M. Liu, J. Reichel, P. Porrati, S. Pellegatta, et al. 2012. Transforming fusions of FGFR and TACC genes in human glioblastoma. Science. 337:1231-1235. http://dx.doi.org/10.1126/science.1220834
42. Spittle, C., S. Charrasse, C. Larroque, and L. Cassimeris. 2000. The interaction of TOGp with microtubules and tubulin. J. Biol. Chem. 275: 20748-20753. http://dx.doi.org/10.1074/jbc.M002597200
43. Tjandra, N., and A. Bax. 1997. Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium. Science. 278:1111-1114. http://dx.doi.org/10.1126/science.278.5340.1111
44. Whitmore, L., and B.A. Wallace. 2004. DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res. 32:W668-W673.
45. Whitmore, L., and B.A. Wallace. 2008. Protein secondary structure analyses from circular dichroism spectroscopy: methods and reference databases. Biopolymers. 89:392-400. http://dx.doi.org/10.1002/bip.20853
46. Widlund, P.O., J.H. Stear, A. Pozniakovsky, M. Zanic, S. Reber, G.J. Brouhard, A.A. Hyman, and J. Howard. 2011. XMAP215 polymerase activity is built by combining multiple tubulin-binding TOG domains and a basic lattice-binding region. Proc. Natl. Acad. Sci. USA. 108:2741-2746. http://dx.doi.org/10.1073/pnas.1016498108
47. Willox, A.K., and S.J. Royle. 2012. Functional analysis of interaction sites on the N-terminal domain of clathrin heavy chain. Traffic. 13:70-81. http://dx.doi.org/10.1111/j.1600-0854.2011.01289.x
48. Woodland, H.R., and A.M. Fry. 2008. Pix proteins and the evolution of centrioles. PLoS ONE. 3:e3778. http://dx.doi.org/10.1371/journal.pone.0003778
49. Yao, R., Y. Natsume, Y. Saiki, H. Shioya, K. Takeuchi, T. Yamori, H. Toki, I. Aoki, T. Saga, and T. Noda. 2012. Disruption of Tacc3 function leads to in vivo tumor regression. Oncogene. 31:135-148. http://dx.doi.org/10.1038/onc.2011.235
50. Zhang, X., Q. Chen, J. Feng, J. Hou, F. Yang, J. Liu, Q. Jiang, and C. Zhang. 2009. Sequential phosphorylation of Nedd1 by Cdk1 and Plk1 is required for targeting of the gammaTuRC to the centrosome. J. Cell Sci. 122:2240-2251. http://dx.doi.org/10.1242/jcs.042747
51. Zweckstetter, M. 2008. NMR: prediction of molecular alignment from structure using the PALES software. Nat. Protoc. 3:679-690. http://dx.doi.org/10.1038/nprot.2008.36