Home Role of centrosomal adaptor proteins of the TACC family in the regulation of microtubule dynamics during mitotic cell division
Article
Licensed
Unlicensed Requires Authentication

Role of centrosomal adaptor proteins of the TACC family in the regulation of microtubule dynamics during mitotic cell division

  • Harish C. Thakur , Madhurendra Singh , Luitgard Nagel-Steger , Daniel Prumbaum , Eyad Kalawy Fansa , Lothar Gremer , Hakima Ezzahoini , André Abts , Lutz Schmitt , Stefan Raunser , Mohammad R. Ahmadian and Roland P. Piekorz EMAIL logo
Published/Copyright: June 20, 2013

Abstract

During the mitotic division cycle, cells pass through an extensive microtubule rearrangement process where microtubules forming the mitotic spindle apparatus are dynamically instable. Several centrosomal- and microtubule-associated proteins are involved in the regulation of microtubule dynamics and stability during mitosis. Here, we focus on members of the transforming acidic coiled coil (TACC) family of centrosomal adaptor proteins, in particular TACC3, in which their subcellular localization at the mitotic spindle apparatus is controlled by Aurora-A kinase-mediated phosphorylation. At the effector level, several TACC-binding partners have been identified and characterized in greater detail, in particular, the microtubule polymerase XMAP215/ch-TOG/CKAP5 and clathrin heavy chain (CHC). We summarize the recent progress in the molecular understanding of these TACC3 protein complexes, which are crucial for proper mitotic spindle assembly and dynamics to prevent faulty cell division and aneuploidy. In this regard, the (patho)biological role of TACC3 in development and cancer will be discussed.


Corresponding author: Roland P. Piekorz, Institut für Biochemie und Molekularbiologie II, Medizinische Fakultät der Heinrich-Heine-Universität, D-40225 Düsseldorf, Germany, e-mail:

We thank our colleagues Astrid Hoeppner, Cordula Kruse, Klaus Schulze-Osthoff, Reiner Jänicke, Jürgen Scheller, and all former and current members of the Institute for Biochemistry and Molecular Biology II for support and discussions. We gratefully acknowledge financial support by a Ph.D. fellowship of the NRW graduate school ‘BioStruct – Biological Structures in Molecular Medicine and Biotechnology’ (to H.C.T.), the DFG (SFB 728 to R.P.P.), and the research commission of the medical faculty of the Heinrich-Heine-University (to R.P.P. and M.R.A). E.K.F. and M.R.A. thank the BMBF (NGFNplus program, grant 01GS08100) for their financial support.

References

Al-Bassam, J. and Chang, F. (2011). Regulation of microtubule dynamics by TOG-domain proteins XMAP215/Dis1 and CLASP. Trends Cell Biol. 21, 604–614.10.1016/j.tcb.2011.06.007Search in Google Scholar

Andersen, J.S., Wilkinson, C.J., Mayor, T., Mortensen, P., Nigg, E.A., and Mann, M. (2003). Proteomic characterization of the human centrosome by protein correlation profiling. Nature 426, 570–574.10.1038/nature02166Search in Google Scholar

Azimzadeh, J. and Bornens, M. (2005). The centrosome in evolution. In Centrosomes in Development and Disease (Weinheim, Germany: Wiley-VCH Verlag GmbH & Co. KGaA), pp. 93–122.10.1002/3527603808.ch6Search in Google Scholar

Barr, A.R. and Gergely, F. (2008). MCAK-independent functions of ch-Tog/XMAP215 in microtubule plus-end dynamics. Mol. Cell Biol. 28, 7199–7211.10.1128/MCB.01040-08Search in Google Scholar

Barros, T.P., Kinoshita, K., Hyman, A.A., and Raff, J.W. (2005). Aurora A activates D-TACC-Msps complexes exclusively at centrosomes to stabilize centrosomal microtubules. J. Cell Biol. 170, 1039–1046.10.1083/jcb.200504097Search in Google Scholar

Bellanger, J.M. and Gonczy, P. (2003). TAC-1 and ZYG-9 form a complex that promotes microtubule assembly in C. elegans embryos. Curr. Biol. 13, 1488–1498.10.1016/S0960-9822(03)00582-7Search in Google Scholar

Booth, D.G., Hood, F.E., Prior, I.A., and Royle, S.J. (2011). A TACC3/ch-TOG/clathrin complex stabilises kinetochore fibres by inter-microtubule bridging. EMBO J. 30, 906–919.10.1038/emboj.2011.15Search in Google Scholar

Bornens, M. (2002). Centrosome composition and microtubule anchoring mechanisms. Curr. Opin. Cell Biol. 14, 25–34.10.1016/S0955-0674(01)00290-3Search in Google Scholar

Bornens, M. (2012). The centrosome in cells and organisms. Science 335, 422–426.10.1126/science.1209037Search in Google Scholar PubMed

Brouhard, G.J., Stear, J.H., Noetzel, T.L., Al-Bassam, J., Kinoshita, K., Harrison, S.C., Howard, J., and Hyman, A.A. (2008). XMAP215 is a processive microtubule polymerase. Cell 132, 79–88.10.1016/j.cell.2007.11.043Search in Google Scholar PubMed PubMed Central

Cappell, K.M., Sinnott, R., Taus, P., Maxfield, K., Scarbrough, M., and Whitehurst, A.W. (2012). Multiple cancer testis antigens function to support tumor cell mitotic fidelity. Mol. Cell Biol. 32, 4131–4140.10.1128/MCB.00686-12Search in Google Scholar PubMed PubMed Central

Charrasse, S., Mazel, M., Taviaux, S., Berta, P., Chow, T., and Larroque, C. (1995). Characterization of the cDNA and pattern of expression of a new gene over-expressed in human hepatomas and colonic tumors. Eur. J. Biochem. 234, 406–413.10.1111/j.1432-1033.1995.406_b.xSearch in Google Scholar PubMed

Cheeseman, L.P., Harry, E.F., McAinsh, A.D., Prior, I.A., and Royle, S.J. (2013). Specific removal of TACC3/ch-TOG/clathrin at metaphase deregulates kinetochore fiber tension. J. Cell Sci. 126, 2102–2113.10.1242/jcs.124834Search in Google Scholar PubMed PubMed Central

Chen, X.P., Yin, H., and Huffaker, T.C. (1998). The yeast spindle pole body component Spc72p interacts with Stu2p and is required for proper microtubule assembly. J. Cell Biol. 141, 1169–1179.10.1083/jcb.141.5.1169Search in Google Scholar PubMed PubMed Central

Compton, D.A. (2000). Spindle assembly in animal cells. Annu. Rev. Biochem. 69, 95–114.10.1146/annurev.biochem.69.1.95Search in Google Scholar PubMed

Conte, N., Charafe-Jauffret, E., Delaval, B., Adelaide, J., Ginestier, C., Geneix, J., Isnardon, D., Jacquemier, J., and Birnbaum, D. (2002). Carcinogenesis and translational controls: TACC1 is down-regulated in human cancers and associates with mRNA regulators. Oncogene 21, 5619–5630.10.1038/sj.onc.1205658Search in Google Scholar PubMed

Conte, N., Delaval, B., Ginestier, C., Ferrand, A., Isnardon, D., Larroque, C., Prigent, C., Seraphin, B., Jacquemier, J., and Birnbaum, D. (2003). TACC1-chTOG-Aurora A protein complex in breast cancer. Oncogene 22, 8102–8116.10.1038/sj.onc.1206972Search in Google Scholar PubMed

Cully, M., Shiu, J., Piekorz, R.P., Muller, W.J., Done, S.J., and Mak, T.W. (2005). Transforming acidic coiled coil 1 promotes transformation and mammary tumorigenesis. Cancer Res. 65, 10363–10370.10.1158/0008-5472.CAN-05-1633Search in Google Scholar PubMed

DeLuca, J.G. and Musacchio, A. (2012). Structural organization of the kinetochore-microtubule interface. Curr. Opin. Cell Biol. 24, 48–56.10.1016/j.ceb.2011.11.003Search in Google Scholar PubMed PubMed Central

Desai, A. and Mitchison, T.J. (1997). Microtubule polymerization dynamics. Annu. Rev. Cell Dev. Biol. 13, 83–117.10.1146/annurev.cellbio.13.1.83Search in Google Scholar PubMed

Duncan, C.G., Killela, P.J., Payne, C.A., Lampson, B., Chen, W.C., Liu, J., Solomon, D., Waldman, T., Towers, A.J., Gregory, S.G., et al. (2010). Integrated genomic analyses identify ERRFl1 and TACC3 as glioblastoma-targeted genes. Oncotarget 1, 265–277.10.18632/oncotarget.137Search in Google Scholar PubMed PubMed Central

Eslinger, M.R., Lauffart, B., and Still, I.H. (2010). TACC3 (transforming, acidic coiled-coil containing protein 3). Atlas Genet. Cytogenet. Oncol. Haematol. 14, 527–553Search in Google Scholar

Foraker, A.B., Camus, S.M., Evans, T.M., Majeed, S.R., Chen, C.Y., Taner, S.B., Correa, I.R., Jr., Doxsey, S.J., and Brodsky, F.M. (2012). Clathrin promotes centrosome integrity in early mitosis through stabilization of centrosomal ch-TOG. J. Cell Biol. 198, 591–605.10.1083/jcb.201205116Search in Google Scholar PubMed PubMed Central

Fu, W., Jiang, Q., and Zhang, C. (2011). Novel functions of endocytic player clathrin in mitosis. Cell Res. 21, 1655–1661.10.1038/cr.2011.106Search in Google Scholar PubMed PubMed Central

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, 3645–3651.10.1242/jcs.075911Search in Google Scholar PubMed

Gardner, M.K., Zanic, M., and Howard, J. (2013). Microtubule catastrophe and rescue. Curr. Opin. Cell Biol. 25, 14–22.10.1016/j.ceb.2012.09.006Search in Google Scholar PubMed PubMed Central

Garriga-Canut, M. and Orkin, S.H. (2004). Transforming acidic coiled-coil protein 3 (TACC3) controls friend of GATA-1 (FOG-1) subcellular localization and regulates the association between GATA-1 and FOG-1 during hematopoiesis. J. Biol. Chem. 279, 23597–23605.10.1074/jbc.M313987200Search in Google Scholar PubMed

Gergely, F. (2002). Centrosomal TACCtics. Bioessays 24, 915–925.10.1002/bies.10162Search in Google Scholar PubMed

Gergely, F., Draviam, V.M., and Raff, J.W. (2003). The ch-TOG/XMAP215 protein is essential for spindle pole organization in human somatic cells. Genes Dev. 17, 336–341.10.1101/gad.245603Search in Google Scholar PubMed PubMed Central

Gergely, F., Karlsson, C., Still, I., Cowell, J., Kilmartin, J., and Raff, J.W. (2000a). The TACC domain identifies a family of centrosomal proteins that can interact with microtubules. Proc. Natl. Acad. Sci. USA 97, 14352–14357.10.1073/pnas.97.26.14352Search in Google Scholar PubMed PubMed Central

Gergely, F., Kidd, D., Jeffers, K., Wakefield, J.G., and Raff, J.W. (2000b). D-TACC: a novel centrosomal protein required for normal spindle function in the early Drosophila embryo. EMBO J. 19, 241–252.10.1093/emboj/19.2.241Search in Google Scholar PubMed PubMed Central

Giet, R., McLean, D., Descamps, S., Lee, M.J., Raff, J.W., Prigent, C., and Glover, D.M. (2002). Drosophila Aurora A kinase is required to localize D-TACC to centrosomes and to regulate astral microtubules. J. Cell Biol. 156, 437–451.10.1083/jcb.200108135Search in Google Scholar PubMed PubMed Central

Gomez-Baldo, L., Schmidt, S., Maxwell, C.A., Bonifaci, N., Gabaldon, T., Vidalain, P.O., Senapedis, W., Kletke, A., Rosing, M., Barnekow, A., et al. (2010). TACC3-TSC2 maintains nuclear envelope structure and controls cell division. Cell Cycle 9, 1143–1155.10.4161/cc.9.6.11018Search in Google Scholar PubMed

Ha, G.H., Kim, J.L., and Breuer, E.K. (2013a). Transforming acidic coiled-coil proteins (TACCs) in human cancer. Cancer Lett. DOI: 10.1016/j.canlet.2013.04.022. Epub April 23, 2013.10.1016/j.canlet.2013.04.022Search in Google Scholar PubMed

Ha, G.H., Park, J.S., and Breuer, E.K. (2013b). TACC3 promotes epithelial-mesenchymal transition (EMT) through the activation of PI3K/Akt and ERK signaling pathways. Cancer Lett. 332, 63–73.10.1016/j.canlet.2013.01.013Search in Google Scholar PubMed

Hao, Z., Stoler, M.H., Sen, B., Shore, A., Westbrook, A., Flickinger, C.J., Herr, J.C., and Coonrod, S.A. (2002). TACC3 expression and localization in the murine egg and ovary. Mol. Reprod. Dev. 63, 291–299.10.1002/mrd.90012Search in Google Scholar PubMed

Hodis, E., Watson, I.R., Kryukov, G.V., Arold, S.T., Imielinski, M., Theurillat, J.P., Nickerson, E., Auclair, D., Li, L., Place, C., et al. (2012). A landscape of driver mutations in melanoma. Cell 150, 251–263.10.1016/j.cell.2012.06.024Search in Google Scholar PubMed PubMed Central

Hood, F.E. and Royle, S.J. (2011). Pulling it together: the mitotic function of TACC3. BioArchitecture 1, 105–109.10.4161/bioa.1.3.16518Search in Google Scholar PubMed PubMed Central

Hubner, N.C., Bird, A.W., Cox, J., Splettstoesser, B., Bandilla, P., Poser, I., Hyman, A., and Mann, M. (2010). Quantitative proteomics combined with BAC TransgeneOmics reveals in vivo protein interactions. J. Cell Biol. 189, 739–754.10.1083/jcb.200911091Search in Google Scholar PubMed PubMed Central

Hutchins, J.R., Toyoda, Y., Hegemann, B., Poser, I., Heriche, J.K., Sykora, M.M., Augsburg, M., Hudecz, O., Buschhorn, B.A., Bulkescher, J., et al. (2010). Systematic analysis of human protein complexes identifies chromosome segregation proteins. Science 328, 593–599.10.1126/science.1181348Search in Google Scholar PubMed PubMed Central

Jeng, J.-C., Lin, Y.-M., Lin, C.-H., and Shih, H.-M. (2009a). Cdh1 controls the stability of TACC3. Cell Cycle 8, 3537–3544.10.4161/cc.8.21.9935Search in Google Scholar PubMed

Jeng, J.C., Lin, Y.M., Lin, C.H., and Shih, H.M. (2009b). Cdh1 controls the stability of TACC3. Cell Cycle 8, 3529–3536.10.4161/cc.8.21.9935Search in Google Scholar

Jung, C.K., Jung, J.H., Park, G.S., Lee, A., Kang, C.S., and Lee, K.Y. (2006). Expression of transforming acidic coiled-coil containing protein 3 is a novel independent prognostic marker in non-small cell lung cancer. Pathol. Int. 56, 503–509.10.1111/j.1440-1827.2006.01998.xSearch in Google Scholar

Kay, B.K., Williamson, M.P., and Sudol, M. (2000). The importance of being proline: the interaction of proline-rich motifs in signaling proteins with their cognate domains. FASEB J. 14, 231–241.10.1096/fasebj.14.2.231Search in Google Scholar

Khodjakov, A. and Rieder, C.L. (2009). The nature of cell-cycle checkpoints: facts and fallacies. J. Biol. 8, 88.10.1186/jbiol195Search in Google Scholar

Kiemeney, L.A., Sulem, P., Besenbacher, S., Vermeulen, S.H., Sigurdsson, A., Thorleifsson, G., Gudbjartsson, D.F., Stacey, S.N., Gudmundsson, J., Zanon, C., et al. (2010). A sequence variant at 4p16.3 confers susceptibility to urinary bladder cancer. Nat. Genet. 42, 415–419.10.1038/ng.558Search in Google Scholar

Kinoshita, K., Habermann, B., and Hyman, A.A. (2002). XMAP215: a key component of the dynamic microtubule cytoskeleton. Trends Cell Biol. 12, 267–273.10.1016/S0962-8924(02)02295-XSearch in Google Scholar

Kinoshita, K., Noetzel, T.L., Pelletier, L., Mechtler, K., Drechsel, D.N., Schwager, A., Lee, M., Raff, J.W., and Hyman, A.A. (2005). Aurora A phosphorylation of TACC3/maskin is required for centrosome-dependent microtubule assembly in mitosis. J. Cell Biol. 170, 1047–1055.10.1083/jcb.200503023Search in Google Scholar PubMed PubMed Central

Klein, S.L., Strausberg, R.L., Wagner, L., Pontius, J., Clifton, S.W., and Richardson, P. (2002). Genetic and genomic tools for Xenopus research: the NIH Xenopus initiative. Dev. Dyn. 225, 384–391.10.1002/dvdy.10174Search in Google Scholar PubMed

Kobayashi, T., Minowa, O., Kuno, J., Mitani, H., Hino, O., and Noda, T. (1999). Renal carcinogenesis, hepatic hemangiomatosis, and embryonic lethality caused by a germ-line Tsc2 mutation in mice. Cancer Res. 59, 1206–1211.Search in Google Scholar

Lauffart, B., Dimatteo, A., Vaughan, M.M., Cincotta, M.A., Black, J.D., and Still, I.H. (2006). Temporal and spatial expression of TACC1 in the mouse and human. Dev. Dyn. 235, 1638–1647.10.1002/dvdy.20724Search in Google Scholar PubMed

Lauffart, B., Vaughan, M., Eddy, R., Chervinsky, D., DiCioccio, R., Black, J., and Still, I. (2005). Aberrations of TACC1 and TACC3 are associated with ovarian cancer. BMC Women’s Health 5, 8.10.1186/1472-6874-5-8Search in Google Scholar PubMed PubMed Central

LeRoy, P.J., Hunter, J.J., Hoar, K.M., Burke, K.E., Shinde, V., Ruan, J., Bowman, D., Galvin, K., and Ecsedy, J.A. (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, 5362–5370.10.1158/0008-5472.CAN-07-0122Search in Google Scholar PubMed

Lin, C.H., Hu, C.K., and Shih, H.M. (2010). Clathrin heavy chain mediates TACC3 targeting to mitotic spindles to ensure spindle stability. J. Cell Biol. 189, 1097–1105.10.1083/jcb.200911120Search in Google Scholar PubMed PubMed Central

Mikolajka, A., Yan, X., Popowicz, G.M., Smialowski, P., Nigg, E.A., and Holak, T.A. (2006). Structure of the N-terminal domain of the FOP (FGFR1OP) protein and implications for its dimerization and centrosomal localization. J. Mol. Biol. 359, 863–875.10.1016/j.jmb.2006.03.070Search in Google Scholar PubMed

Mitchison, T. and Kirschner, M. (1984). Dynamic instability of microtubule growth. Nature 312, 237–242.10.1038/312237a0Search in Google Scholar PubMed

Musacchio, A. (2011). Spindle assembly checkpoint: the third decade. Philos. Trans. R. Soc. Lond. B Biol. Sci. 366, 3595–3604.10.1098/rstb.2011.0072Search in Google Scholar PubMed PubMed Central

Neumann, B., Walter, T., Heriche, J.K., Bulkescher, J., Erfle, H., Conrad, C., Rogers, P., Poser, I., Held, M., Liebel, U., et al. (2010). Phenotypic profiling of the human genome by time-lapse microscopy reveals cell division genes. Nature 464, 721–727.10.1038/nature08869Search in Google Scholar PubMed PubMed Central

Nigg, E.A. and Raff, J.W. (2009). Centrioles, centrosomes, and cilia in health and disease. Cell 139, 663–678.10.1016/j.cell.2009.10.036Search in Google Scholar PubMed

O’Brien, L.L., Albee, A.J., Liu, L., Tao, W., Dobrzyn, P., Lizarraga, S.B., and Wiese, C. (2005). The Xenopus TACC homologue, maskin, functions in mitotic spindle assembly. Mol. Biol. Cell 16, 2836–2847.10.1091/mbc.e04-10-0926Search in Google Scholar PubMed PubMed Central

Parker, B.C., Annala, M.J., Cogdell, D.E., Granberg, K.J., Sun, Y., Ji, P., Li, X., Gumin, J., Zheng, H., Hu, L., et al. (2011). Coactivators necessary for transcriptional output of the hypoxia inducible factor, HIF, are directly recruited by ARNT PAS-B. Proc. Natl. Acad. Sci. USA 108, 7739–7744.10.1073/pnas.1101357108Search in Google Scholar PubMed PubMed Central

Peset, I., Seiler, J., Sardon, T., Bejarano, L.A., Rybina, S., and Vernos, I. (2005). Function and regulation of Maskin, a TACC family protein, in microtubule growth during mitosis. J. Cell Biol. 170, 1057–1066.10.1083/jcb.200504037Search in Google Scholar PubMed PubMed Central

Peset, I. and Vernos, I. (2008). The TACC proteins: TACC-ling microtubule dynamics and centrosome function. Trends Cell Biol. 18, 379–388.10.1016/j.tcb.2008.06.005Search in Google Scholar

Piekorz, R.P., Hoffmeyer, A., Duntsch, C.D., McKay, C., Nakajima, H., Sexl, V., Snyder, L., Rehg, J., and 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, 653–664.10.1093/emboj/21.4.653Search in Google Scholar

Popov, A.V., Pozniakovsky, A., Arnal, I., Antony, C., Ashford, A.J., Kinoshita, K., Tournebize, R., Hyman, A.A., and Karsenti, E. (2001). XMAP215 regulates microtubule dynamics through two distinct domains. EMBO J. 20, 397–410.10.1093/emboj/20.3.397Search in Google Scholar

Raff, J.W. (2002). Centrosomes and cancer: lessons from a TACC. Trends Cell Biol. 12, 222–225.10.1016/S0962-8924(02)02268-7Search in Google Scholar

Rieder, C.L. (2011). Mitosis in vertebrates: the G2/M and M/A transitions and their associated checkpoints. Chromosome Res. 19, 291–306.10.1007/s10577-010-9178-zSearch in Google Scholar

Rieder, C.L. and Maiato, H. (2004). Stuck in division or passing through: what happens when cells cannot satisfy the spindle assembly checkpoint. Dev. Cell 7, 637–51.10.1016/j.devcel.2004.09.002Search in Google Scholar

Royle, S.J. (2012). The role of clathrin in mitotic spindle organisation. J. Cell Sci. 125, 19–28.10.1242/jcs.094607Search in Google Scholar

Sadek, C.M., Jalaguier, S., Feeney, E.P., Aitola, M., Damdimopoulos, A.E., Pelto-Huikko, M., and Gustafsson, J.A. (2000). Isolation and characterization of AINT: a novel ARNT interacting protein expressed during murine embryonic development. Mech. Dev. 97, 13–26.10.1016/S0925-4773(00)00415-9Search in Google Scholar

Samereier, M., Baumann, O., Meyer, I., and Graf, R. (2011). Analysis of Dictyostelium TACC reveals differential interactions with CP224 and unusual dynamics of Dictyostelium microtubules. Cell. Mol. Life Sci. 68, 275–287.10.1007/s00018-010-0453-0Search in Google Scholar PubMed

Sato, M., Koonrugsa, N., Toda, T., Vardy, L., Tournier, S., and Millar, J.B. (2003). Deletion of Mia1/Alp7 activates Mad2-dependent spindle assembly checkpoint in fission yeast. Nat. Cell Biol. 5, 764–766; author reply 766.10.1038/ncb0903-764Search in Google Scholar PubMed

Sato, M., Vardy, L., Angel Garcia, M., Koonrugsa, N., and Toda, T. (2004). Interdependency of fission yeast Alp14/TOG and coiled coil protein Alp7 in microtubule localization and bipolar spindle formation. Mol. Biol. Cell 15, 1609–1622.10.1091/mbc.e03-11-0837Search in Google Scholar

Schmidt, S., Essmann, F., Cirstea, I.C., Kuck, F., Thakur, H.C., Singh, M., Kletke, A., Jänicke, R.U., Wiek, C., Hanenberg, H., et al. (2010a). The centrosome and mitotic spindle apparatus in cancer and senescence. Cell Cycle 9, 4469–4473.10.4161/cc.9.22.13684Search in Google Scholar

Schmidt, S., Schneider, L., Essmann, F., Cirstea, I.C., Kuck, F., Kletke, A., Jänicke, R.U., Wiek, C., Hanenberg, H., Ahmadian, et al. (2010b). The centrosomal protein TACC3 controls paclitaxel sensitivity by modulating a premature senescence program. Oncogene 29, 6184–6192.10.1038/onc.2010.354Search in Google Scholar

Schneider, L., Essmann, F., Kletke, A., Rio, P., Hanenberg, H., Schulze-Osthoff, K., Nürnberg, B., and Piekorz, R.P. (2008). TACC3 depletion sensitizes to paclitaxel-induced cell death and overrides p21WAF-mediated cell cycle arrest. Oncogene 27, 116–125.10.1038/sj.onc.1210628Search in Google Scholar

Schneider, L., Essmann, F., Kletke, A., Rio, P., Hanenberg, H., Wetzel, W., Schulze-Osthoff, K., Nürnberg, B., and 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, 29273–29283.10.1074/jbc.M704151200Search in Google Scholar

Schuendeln, M.M., Piekorz, R.P., Wichmann, C., Lee, Y., McKinnon, P.J., Boyd, K., Takahashi, Y., and Ihle, J.N. (2004). The centrosomal, putative tumor suppressor protein TACC2 is dispensable for normal development, and deficiency does not lead to cancer. Mol. Cell. Biol. 24, 6403–6409.10.1128/MCB.24.14.6403-6409.2004Search in Google Scholar

Sillje, H.H., Nagel, S., Korner, R., and Nigg, E.A. (2006). HURP is a Ran-importin beta-regulated protein that stabilizes kinetochore microtubules in the vicinity of chromosomes. Curr. Biol. 16, 731–742.10.1016/j.cub.2006.02.070Search in Google Scholar

Singh, D., Chan, J.M., Zoppoli, P., Niola, F., Sullivan, R., Castano, A., Liu, E.M., Reichel, J., Porrati, P., Pellegatta, S., et al. (2012). Transforming fusions of FGFR and TACC genes in human glioblastoma. Science 337, 1231–1235.10.1126/science.1220834Search in Google Scholar

Srayko, M., Quintin, S., Schwager, A., and Hyman, A.A. (2003). Caenorhabditis elegans TAC-1 and ZYG-9 form a complex that is essential for long astral and spindle microtubules. Curr. Biol. 13, 1506–1511.10.1016/S0960-9822(03)00597-9Search in Google Scholar

Still, I., Vettaikkorumakankauv, A., DiMatteo, A., and Liang, P. (2004). Structure-function evolution of the transforming acidic coiled coil genes revealed by analysis of phylogenetically diverse organisms. BMC Evol. Biol. 4, 16.10.1186/1471-2148-4-16Search in Google Scholar PubMed PubMed Central

Still, I.H., Hamilton, M., Vince, P., Wolfman, A., and Cowell, J.K. (1999a). Cloning of TACC1, an embryonically expressed, potentially transforming coiled coil containing gene, from the 8p11 breast cancer amplicon. Oncogene 18, 4032–4038.10.1038/sj.onc.1202801Search in Google Scholar PubMed

Still, I.H., Vince, P., and Cowell, J.K. (1999b). The third member of the transforming acidic coiled coil-containing gene family, TACC3, maps in 4p16, close to translocation breakpoints in multiple myeloma, and is upregulated in various cancer cell lines. Genomics 58, 165–170.10.1006/geno.1999.5829Search in Google Scholar PubMed

Takayama, K., Horie-Inoue, K., Suzuki, T., Urano, T., Ikeda, K., Fujimura, T., Takahashi, S., Homma, Y., Ouchi, Y., and Inoue, S. (2012). TACC2 is an androgen-responsive cell cycle regulator promoting androgen-mediated and castration-resistant growth of prostate cancer. Mol. Endocrinol. 26, 748–761.10.1210/me.2011-1242Search in Google Scholar PubMed PubMed Central

Tan, S., Lyulcheva, E., Dean, J., and Bennett, D. (2008). Mars promotes dTACC dephosphorylation on mitotic spindles to ensure spindle stability. J. Cell Biol. 182, 27–33.10.1083/jcb.200712080Search in Google Scholar PubMed PubMed Central

Thakur, H.C. (2012). Biochemical and biophysical characterization of the centrosomal protein TACC3. Dissertation (Faculty of Mathematics and Natural Sciences of the Heinrich Heine University, Düsseldorf, Germany), November 2012.Search in Google Scholar

Tsou, A.P., Yang, C.W., Huang, C.Y., Yu, R.C., Lee, Y.C., Chang, C.W., Chen, B.R., Chung, Y.F., Fann, M.J., Chi, C.W., et al. (2003). Identification of a novel cell cycle regulated gene, HURP, overexpressed in human hepatocellular carcinoma. Oncogene 22, 298–307.10.1038/sj.onc.1206129Search in Google Scholar PubMed

Widlund, P.O., Stear, J.H., Pozniakovsky, A., Zanic, M., Reber, S., Brouhard, G.J., Hyman, A.A., and Howard, J. (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, 2741–2746.10.1073/pnas.1016498108Search in Google Scholar PubMed PubMed Central

Williams, S.V., Hurst, C.D., and Knowles, M.A. (2012). Oncogenic FGFR3 gene fusions in bladder cancer. Hum. Mol. Genet. 22, 795–803.10.1093/hmg/dds486Search in Google Scholar PubMed PubMed Central

Wong, J., Lerrigo, R., Jang, C.Y., and Fang, G. (2008). Aurora A regulates the activity of HURP by controlling the accessibility of its microtubule-binding domain. Mol. Biol. Cell 19, 2083–2091.10.1091/mbc.e07-10-1088Search in Google Scholar PubMed PubMed Central

Wurdak, H., Zhu, S., Min, K.H., Aimone, L., Lairson, L.L., Watson, J., Chopiuk, G., Demas, J., Charette, B., Halder, R., et al. (2010). A small molecule accelerates neuronal differentiation in the adult rat. Proc. Natl. Acad. Sci. USA 107, 16542–16547.10.1073/pnas.1010300107Search in Google Scholar PubMed PubMed Central

Yao, R., Natsume, Y., and Noda, T. (2007). TACC3 is required for the proper mitosis of sclerotome mesenchymal cells during formation of the axial skeleton. Cancer Sci. 98, 555–562.10.1111/j.1349-7006.2007.00433.xSearch in Google Scholar PubMed

Yao, R., Natsume, Y., Saiki, Y., Shioya, H., Takeuchi, K., Yamori, T., Toki, H., Aoki, I., Saga, T., and Noda, T. (2011). Disruption of Tacc3 function leads to in vivo tumor regression. Oncogene 31, 135–148.10.1038/onc.2011.235Search in Google Scholar PubMed

Yu, C.T., Hsu, J.M., Lee, Y.C., Tsou, A.P., Chou, C.K., and 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, 5789–5800.10.1128/MCB.25.14.5789-5800.2005Search in Google Scholar PubMed PubMed Central

Zyss, D. and Gergely, F. (2009). Centrosome function in cancer: guilty or innocent? Trends Cell Biol. 19, 334–346.Search in Google Scholar

Received: 2013-5-16
Accepted: 2013-6-18
Published Online: 2013-06-20
Published in Print: 2013-11-01

©2013 by Walter de Gruyter Berlin Boston

Articles in the same Issue

  1. Masthead
  2. Masthead
  3. Guest Editorial
  4. Highlight: NRW Research School BioStruct – Biological Structures in Molecular Medicine and Biotechnology
  5. Highlight: NRW Research School Biostruct – Biological Structures in Molecular Medicine and Biotechnology
  6. Structural features of antiviral DNA cytidine deaminases
  7. Molecular insights into type I secretion systems
  8. Structural comparison of the transport units of type V secretion systems
  9. Rho-kinase: regulation, (dys)function, and inhibition
  10. Role of centrosomal adaptor proteins of the TACC family in the regulation of microtubule dynamics during mitotic cell division
  11. Revisiting Disrupted-in-Schizophrenia 1 as a scaffold protein
  12. Structural snapshot of cyclic nucleotide binding domains from cyclic nucleotide-sensitive ion channels
  13. Full-length Vpu and human CD4(372–433) in phospholipid bilayers as seen by magic angle spinning NMR
  14. Membrane protein stability depends on the concentration of compatible solutes – a single molecule force spectroscopic study
  15. Expression and characterisation of fully posttranslationally modified cellular prion protein in Pichia pastoris
  16. Contribution of distinct platelet integrins to binding, unfolding, and assembly of fibronectin
  17. Shear-related fibrillogenesis of fibronectin
  18. Enzyme-substrate complexes of the quinate/shikimate dehydrogenase from Corynebacterium glutamicum enable new insights in substrate and cofactor binding, specificity, and discrimination
  19. The amino acids surrounding the flavin 7a-methyl group determine the UVA spectral features of a LOV protein
  20. Determinants of the species selectivity of oxazolidinone antibiotics targeting the large ribosomal subunit
  21. NSR from Streptococcus agalactiae confers resistance against nisin and is encoded by a conserved nsr operon
Downloaded on 4.11.2025 from https://www.degruyterbrill.com/document/doi/10.1515/hsz-2013-0184/html
Scroll to top button