Specific removal of TACC3-ch-TOG-clathrin at metaphase deregulates kinetochore fiber tension

Journal of Cell Science

Volumn 126, Issue 9, 2013, Pages 2102-2113

  Cheeseman, Liam P ^a   Harry, Edward F ^b,c   McAinsh, Andrew D ^b   Prior, Ian A ^a   Royle, Stephen J ^a,b  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b UNIVERSITY OF WARWICK   (United Kingdom)

^c UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

Checkpoint; Knocksideways; Microtubule; Mitotic spindle; Rapid inactivation

Indexed keywords

CLATHRIN; MEMBRANE PROTEIN; PROTEIN TACC3 CH TOG CLATHRIN; UNCLASSIFIED DRUG;

ANAPHASE; ARTICLE; CELL NUCLEUS MEMBRANE; CENTROMERE; COMPLEX FORMATION; HELA CELL; METAPHASE; MICROTUBULE; MITOCHONDRION; MITOSIS; MITOSIS SPINDLE; PRIORITY JOURNAL; PROMETAPHASE; PROTEIN CROSS LINKING; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

CHECKPOINT; KNOCKSIDEWAYS; MICROTUBULE; MITOTIC SPINDLE; RAPID INACTIVATION;

CHROMOSOMES, HUMAN; CLATHRIN; HELA CELLS; HUMANS; KINETOCHORES; METAPHASE; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MITOTIC SPINDLE APPARATUS; MULTIPROTEIN COMPLEXES;

EID: 84878628957     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.124834     Document Type: Article

References (40)

1. Barr, A. R. and Gergely, F. (2008). MCAK-independent functions of ch-Tog/ XMAP215 in microtubule plus-end dynamics. Mol. Cell. Biol. 28, 7199-7211.
2. Booth, D. G., Hood, F. E., Prior, I. A., Royle, S. J. (2011). A TACC3/ch-TOG/ clathrin complex stabilises kinetochore fibres by inter-microtubule bridging. EMBO J. 30, 906-919.
3. Borner, G. H., Antrobus, R., Hirst, J., Bhumbra, G. S., Kozik, P., Jackson, L. P., Sahlender, D. A., Robinson, M. S. (2012). Multivariate proteomic profiling identifies novel accessory proteins of coated vesicles. J. Cell Biol. 197, 141-160.
4. Brodsky, F. M. (2012). Diversity of clathrin function: new tricks for an old protein. Annu. Rev. Cell Dev. Biol. 28, 309-336.
5. Cassimeris, L., Becker, B., Carney, B. (2009). TOGp regulates microtubule assembly and density during mitosis and contributes to chromosome directional instability. Cell Motil. Cytoskeleton 66, 535-545.
6. Charlebois, B. D., Kollu, S., Schek, H. T., Compton, D. A., Hunt, A. J. (2011). Spindle pole mechanics studied in mitotic asters: dynamic distribution of spindle forces through compliant linkages. Biophys. J. 100, 1756-1764.
7. Cheeseman, L. P., Booth, D. G., Hood, F. E., Prior, I. A., Royle, S. J. (2011). Aurora A kinase activity is required for localization of TACC3/ch-TOG/clathrin intermicrotubule bridges. Commun. Integr. Biol. 4, 409-412.
8. Dumont, S., Mitchison, T. J. (2009). Compression regulates mitotic spindle length by a mechanochemical switch at the poles. Curr. Biol. 19, 1086-1095.
9. Fu, W., Tao, W., Zheng, P., Fu, J., Bian, M., Jiang, Q., Clarke, P. R., Zhang, C. (2010). Clathrin recruits phosphorylated TACC3 to spindle poles for bipolar spindle assembly and chromosome alignment. J. Cell Sci. 123, 3645-3651.
10. Fu, W., Jiang, Q., Zhang, C. (2011). Novel functions of endocytic player clathrin in mitosis. Cell Res. 21, 1655-1661.
11. Gergely, F., Karlsson, C., Still, I., Cowell, J., Kilmartin, J., Raff, J. W. (2000a). The TACC domain identifies a family of centrosomal proteins that can interact with microtubules. Proc. Natl. Acad. Sci. USA 97, 14352-14357.
12. Gergely, F., Kidd, D., Jeffers, K., Wakefield, J. G., Raff, J. W. (2000b). DTACC: a novel centrosomal protein required for normal spindle function in the early Drosophila embryo. EMBO J. 19, 241-252.
13. Gergely, F., Draviam, V. M., Raff, J. W. (2003). The ch-TOG/XMAP215 protein is essential for spindle pole organization in human somatic cells. Genes Dev. 17, 336- 341.
14. Giet, R., Uzbekov, R., Cubizolles, F., Le Guellec, K., 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.
15. Hepler, P. K., McIntosh, J. R., Cleland, S. (1970). Intermicrotubule bridges in mitotic spindle apparatus. J. Cell Biol. 45, 438-444.
16. Hirst, J., Borner, G. H., Antrobus, R., Peden, A. A., Hodson, N. A., Sahlender, D. A., Robinson, M. S. (2012). Distinct and overlapping roles for AP-1 and GGAs revealed by the "knocksideways" system. Curr. Biol. 22, 1711-1716.
17. Hubner, N. C., Bird, A. W., Cox, J., Splettstoesser, B., Bandilla, P., Poser, I., Hyman, A., Mann, M. (2010). Quantitative proteomics combined with BAC TransgeneOmics reveals in vivo protein interactions. J. Cell Biol. 189, 739-754.
18. Jaqaman, K., King, E. M., Amaro, A. C., Winter, J. R., Dorn, J. F., Elliott, H. L., McHedlishvili, N., McClelland, S. E., Porter, I. M., Posch, M. et al. (2010). Kinetochore alignment within the metaphase plate is regulated by centromere stiffness and microtubule depolymerases. J. Cell Biol. 188, 665-679.
19. Kettenbach, A. N., Schweppe, D. K., Faherty, B. K., Pechenick, D., Pletnev, A. A., Gerber, S. A. (2011). Quantitative phosphoproteomics identifies substrates and functional modules of Aurora and Polo-like kinase activities in mitotic cells. Sci. Signal. 4, rs5.
20. Khodjakov, A., Pines, J. (2010). Centromere tension: a divisive issue. Nat. Cell Biol. 12, 919-923.
21. Kinoshita, K., Noetzel, T. L., Pelletier, L., Mechtler, K., Drechsel, D. N., Schwager, A., Lee, M., Raff, J. W., Hyman, A. A. (2005). Aurora A phosphorylation of TACC3/maskin is required for centrosome-dependent microtubule assembly in mitosis. J. Cell Biol. 170, 1047-1055.
22. Lee, M. J., Gergely, F., Jeffers, K., Peak-Chew, S. Y., Raff, J. W. (2001). Msps/ XMAP215 interacts with the centrosomal protein D-TACC to regulate microtubule behaviour. Nat. Cell Biol. 3, 643-649.
23. Lin, C. H., Hu, C. K., Shih, H. M. (2010). Clathrin heavy chain mediates TACC3 targeting to mitotic spindles to ensure spindle stability. J. Cell Biol. 189, 1097-1105.
24. McDonald, K. L., O"Toole, E. T., Mastronarde, D. N., McIntosh, J. R. (1992). Kinetochore microtubules in PTK cells. J. Cell Biol. 118, 369-383.
25. McEwen, B. F., Heagle, A. B., Cassels, G. O., Buttle, K. F., Rieder, C. L. (1997). Kinetochore fiber maturation in PtK1 cells and its implications for the mechanisms of chromosome congression and anaphase onset. J. Cell Biol. 137, 1567-1580.
26. Murray, A. W. (2011). A brief history of error. Nat. Cell Biol. 13, 1178-1182.
27. Nicklas, R. B., Kubai, D. F., Hays, T. S. (1982). Spindle microtubules and their mechanical associations after micromanipulation in anaphase. J. Cell Biol. 95, 91- 104.
28. Nishimura, K., Fukagawa, T., Takisawa, H., Kakimoto, T., Kanemaki, M. (2009). An auxin-based degron system for the rapid depletion of proteins in nonplant cells. Nat. Methods 6, 917-922.
29. Peset, I., Vernos, I. (2008). The TACC proteins: TACC-ling microtubule dynamics and centrosome function. Trends Cell Biol. 18, 379-388.
30. Peterman, E. J., Scholey, J. M. (2009). Mitotic microtubule crosslinkers: insights from mechanistic studies. Curr. Biol. 19, R1089-R1094.
31. Piekorz, R. P., Hoffmeyer, A., Duntsch, C. D., McKay, C., Nakajima, H., Sexl, V., Snyder, L., Rehg, J., Ihle, J. N. (2002). The centrosomal protein TACC3 is essential for hematopoietic stem cell function and genetically interfaces with p53- regulated apoptosis. EMBO J. 21, 653-664.
32. Robinson, M. S., Sahlender, D. A., Foster, S. D. (2010). Rapid inactivation of proteins by rapamycin-induced rerouting to mitochondria. Dev. Cell 18, 324-331.
33. Royle, S. J. (2011). Mitotic moonlighting functions for membrane trafficking proteins. Traffic 12, 791-798.
34. Royle, S. J. (2012). The role of clathrin in mitotic spindle organisation. J. Cell Sci. 125, 19-28.
35. Royle, S. J., Bright, N. A., Lagnado, L. (2005). Clathrin is required for the function of the mitotic spindle. Nature 434, 1152-1157.
36. Schneider, L., Essmann, F., Kletke, A., Rio, P., Hanenberg, H., Wetzel, W., Schulze-Osthoff, K., Nü rnberg, B., Piekorz, R. P. (2007). The transforming acidic coiled coil 3 protein is essential for spindle-dependent chromosome alignment and mitotic survival. J. Biol. Chem. 282, 29273-29283.
37. Toso, A., Winter, J. R., Garrod, A. J., Amaro, A. C., Meraldi, P., McAinsh, A. D. (2009). Kinetochore-generated pushing forces separate centrosomes during bipolar spindle assembly. J. Cell Biol. 184, 365-372.
38. Waters, J. C., Chen, R. H., Murray, A. W., Salmon, E. D. (1998). Localization of Mad2 to kinetochores depends on microtubule attachment, not tension. J. Cell Biol. 141, 1181-1191.
39. Willox, A. K., Royle, S. J. (2012). Stonin 2 is a major adaptor protein for clathrinmediated synaptic vesicle retrieval. Curr. Biol. 22, 1435-1439.
40. Yu, C. T., Hsu, J. M., Lee, Y. C., Tsou, A. P., Chou, C. K., Huang, C. Y. (2005). Phosphorylation and stabilization of HURP by Aurora-A: implication of HURP as a transforming target of Aurora-A. Mol. Cell. Biol. 25, 5789-5800.