Aurora-A-Dependent Control of TACC3 Influences the Rate of Mitotic Spindle Assembly

1. Meunier S, Vernos I (2012) Microtubule assembly during mitosis—from distinct origins to distinct functions? J Cell Sci 125: 2805–2814. doi: 10.1242/jcs.092429 22736044

2. Gatlin JC, Bloom K (2010) Microtubule motors in eukaryotic spindle assembly and maintenance. Semin Cell Dev Biol 21: 248–254. doi: 10.1016/j.semcdb.2010.01.015 20109569

3. Walczak CE, Heald R (2008) Mechanisms of mitotic spindle assembly and function. Int Rev Cytol 265: 111–158. doi: 10.1016/S0074-7696(07)65003-7 18275887

4. O'Connell CB, Khodjakov AL (2007) Cooperative mechanisms of mitotic spindle formation. J Cell Sci 120: 1717–1722. 17502482

5. Barr AR, Gergely F (2007) Aurora-A: the maker and breaker of spindle poles. J Cell Sci 120: 2987–2996. 17715155

6. Nikonova AS, Astsaturov I, Serebriiskii IG, Dunbrack RL Jr., Golemis EA (2012) Aurora A kinase (AURKA) in normal and pathological cell division. Cell Mol Life Sci 70: 661–687. doi: 10.1007/s00018-012-1073-7 22864622

7. Manfredi MG, Ecsedy JA, Meetze KA, Balani SK, Burenkova O, et al. (2007) Antitumor activity of MLN8054, an orally active small-molecule inhibitor of Aurora A kinase. Proc Natl Acad Sci U S A 104: 4106–4111. 17360485

8. Hegarat N, Smith E, Nayak G, Takeda S, Eyers PA, et al. (2011) Aurora A and Aurora B jointly coordinate chromosome segregation and anaphase microtubule dynamics. J Cell Biol 195: 1103–1113. doi: 10.1083/jcb.201105058 22184196

9. Cowley DO, Rivera-Perez JA, Schliekelman M, He YJ, Oliver TG, et al. (2009) Aurora-A kinase is essential for bipolar spindle formation and early development. Mol Cell Biol 29: 1059–1071. doi: 10.1128/MCB.01062-08 19075002

10. Kesisova IA, Nakos KC, Tsolou A, Angelis D, Lewis J, et al. (2013) Tripolin A, a novel small-molecule inhibitor of aurora A kinase, reveals new regulation of HURP's distribution on microtubules. PLoS One 8: e58485. doi: 10.1371/journal.pone.0058485 23516487

11. Asteriti IA, Giubettini M, Lavia P, Guarguaglini G (2011) Aurora-A inactivation causes mitotic spindle pole fragmentation by unbalancing microtubule-generated forces. Mol Cancer 10: 131. doi: 10.1186/1476-4598-10-131 22011530

12. Marumoto T, Honda S, Hara T, Nitta M, Hirota T, et al. (2003) Aurora-A kinase maintains the fidelity of early and late mitotic events in HeLa cells. J Biol Chem 278: 51786–51795. 14523000

13. Foley EA, Kapoor TM (2013) Microtubule attachment and spindle assembly checkpoint signalling at the kinetochore. Nat Rev Mol Cell Biol 14: 25–37. doi: 10.1038/nrm3494 23258294

14. Sardon T, Pache RA, Stein A, Molina H, Vernos I, et al. (2010) Uncovering new substrates for Aurora A kinase. EMBO Rep 11: 977–984. doi: 10.1038/embor.2010.171 21072059

15. Sardon T, Peset I, Petrova B, Vernos I (2008) Dissecting the role of Aurora A during spindle assembly. EMBO J 27: 2567–2579. doi: 10.1038/emboj.2008.173 18756265

16. Peset I, Vernos I (2008) The TACC proteins: TACC-ling microtubule dynamics and centrosome function. Trends Cell Biol 18: 379–388. doi: 10.1016/j.tcb.2008.06.005 18656360

17. Piekorz RP, Hoffmeyer A, Duntsch CD, McKay C, Nakajima H, et al. (2002) The centrosomal protein TACC3 is essential for hematopoietic stem cell function and genetically interfaces with p53-regulated apoptosis. EMBO J 21: 653–664. 11847113

18. Ayaz P, Ye X, Huddleston P, Brautigam CA, Rice LM (2012) A TOG:alphabeta-tubulin complex structure reveals conformation-based mechanisms for a microtubule polymerase. Science 337: 857–860. doi: 10.1126/science.1221698 22904013

19. Brouhard GJ, Stear JH, Noetzel TL, Al-Bassam J, Kinoshita K, et al. (2008) XMAP215 is a processive microtubule polymerase. Cell 132: 79–88. doi: 10.1016/j.cell.2007.11.043 18191222

20. Lee MJ, Gergely F, Jeffers K, Peak-Chew SY, Raff JW (2001) Msps/XMAP215 interacts with the centrosomal protein D-TACC to regulate microtubule behaviour. Nat Cell Biol 3: 643–649. 11433296

21. Bucciarelli E, Pellacani C, Naim V, Palena A, Gatti M, et al. (2009) Drosophila Dgt6 interacts with Ndc80, Msps/XMAP215, and gamma-tubulin to promote kinetochore-driven MT formation. Curr Biol 19: 1839–1845. doi: 10.1016/j.cub.2009.09.043 19836241

22. Fu W, Chen H, Wang G, Luo J, Deng Z, et al. (2013) Self-assembly and sorting of acentrosomal microtubules by TACC3 facilitate kinetochore capture during the mitotic spindle assembly. Proc Natl Acad Sci U S A 110: 15295–15300. doi: 10.1073/pnas.1312382110 24003142

23. Cullen CF, Ohkura H (2001) Msps protein is localized to acentrosomal poles to ensure bipolarity of Drosophila meiotic spindles. Nat Cell Biol 3: 637–642. 11433295

24. Gergely F, Karlsson C, Still I, Cowell J, Kilmartin J, et al. (2000) The TACC domain identifies a family of centrosomal proteins that can interact with microtubules. Proc Natl Acad Sci U S A 97: 14352–14357. 11121038

25. Gergely F, Kidd D, Jeffers K, Wakefield JG, Raff JW (2000) D-TACC: a novel centrosomal protein required for normal spindle function in the early Drosophila embryo. EMBO J 19: 241–252. 10637228

26. Peset I, Seiler J, Sardon T, Bejarano LA, Rybina S, et al. (2005) Function and regulation of Maskin, a TACC family protein, in microtubule growth during mitosis. J Cell Biol 170: 1057–1066. 16172207

27. Kinoshita K, Noetzel TL, Pelletier L, Mechtler K, Drechsel DN, et al. (2005) Aurora A phosphorylation of TACC3/maskin is required for centrosome-dependent microtubule assembly in mitosis. J Cell Biol 170: 1047–1055. 16172205

28. Sato M, Toda T (2007) Alp7/TACC is a crucial target in Ran-GTPase-dependent spindle formation in fission yeast. Nature 447: 334–337. 17476213

29. Sato M, Vardy L, Angel Garcia M, Koonrugsa N, 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. 14742702

30. Barros TP, Kinoshita K, Hyman AA, Raff JW (2005) Aurora A activates D-TACC-Msps complexes exclusively at centrosomes to stabilize centrosomal microtubules. J Cell Biol 170: 1039–1046. 16186253

31. Hubner NC, Bird AW, Cox J, Splettstoesser B, Bandilla P, et al. (2010) Quantitative proteomics combined with BAC TransgeneOmics reveals in vivo protein interactions. J Cell Biol 189: 739–754. doi: 10.1083/jcb.200911091 20479470

32. Fu W, Tao W, Zheng P, Fu J, Bian M, et al. (2010) Clathrin recruits phosphorylated TACC3 to spindle poles for bipolar spindle assembly and chromosome alignment. J Cell Sci 123: 3645–3651. doi: 10.1242/jcs.075911 20923838

33. Lin CH, Hu CK, Shih HM (2010) Clathrin heavy chain mediates TACC3 targeting to mitotic spindles to ensure spindle stability. J Cell Biol 189: 1097–1105. doi: 10.1083/jcb.200911120 20566684

34. Cheeseman LP, Booth DG, Hood FE, Prior IA, Royle SJ (2011) Aurora A kinase activity is required for localization of TACC3/ch-TOG/clathrin inter-microtubule bridges. Commun Integr Biol 4: 409–412. doi: 10.4161/cib.4.4.15250 21966557

35. Booth DG, Hood FE, Prior IA, Royle SJ (2011) A TACC3/ch-TOG/clathrin complex stabilises kinetochore fibres by inter-microtubule bridging. EMBO J 30: 906–919. doi: 10.1038/emboj.2011.15 21297582

36. Hood FE, Williams SJ, Burgess SG, Richards MW, Roth D, et al. (2013) Coordination of adjacent domains mediates TACC3-ch-TOG-clathrin assembly and mitotic spindle binding. J Cell Biol 202: 463–478. doi: 10.1083/jcb.201211127 23918938

37. Gard DL, Kirschner MW (1987) A microtubule-associated protein from Xenopus eggs that specifically promotes assembly at the plus-end. J Cell Biol 105: 2203–2215. 2890645

38. Thakur HC, Singh M, Nagel-Steger L, Kremer J, Prumbaum D, et al. (2014) The centrosomal adaptor TACC3 and the microtubule polymerase chTOG interact via defined C-terminal subdomains in an Aurora-A kinase-independent manner. J Biol Chem 289: 74–88. doi: 10.1074/jbc.M113.532333 24273164

39. Ha GH, Kim JL, Breuer EK (2013) Transforming acidic coiled-coil proteins (TACCs) in human cancer. Cancer Lett 336: 24–33. doi: 10.1016/j.canlet.2013.04.022 23624299

40. Capelletti M, Dodge ME, Ercan D, Hammerman PS, Park SI, et al. (2014) Identification of recurrent FGFR3-TACC3 fusion oncogenes from lung adenocarcinoma. Clin Cancer Res 20: 6551–6558. doi: 10.1158/1078-0432.CCR-14-1337 25294908

41. Guo G, Sun X, Chen C, Wu S, Huang P, et al. (2013) Whole-genome and whole-exome sequencing of bladder cancer identifies frequent alterations in genes involved in sister chromatid cohesion and segregation. Nat Genet 45: 1459–1463. doi: 10.1038/ng.2798 24121792

42. Singh D, Chan JM, Zoppoli P, Niola F, Sullivan R, et al. (2012) Transforming fusions of FGFR and TACC genes in human glioblastoma. Science 337: 1231–1235. doi: 10.1126/science.1220834 22837387

43. Williams SV, Hurst CD, Knowles MA (2013) Oncogenic FGFR3 gene fusions in bladder cancer. Hum Mol Genet 22: 795–803. doi: 10.1093/hmg/dds486 23175443

44. Yuan L, Liu ZH, Lin ZR, Xu LH, Zhong Q, et al. (2014) Recurrent FGFR3-TACC3 fusion gene in nasopharyngeal carcinoma. Cancer Biol Ther 15: 1613–1621. doi: 10.4161/15384047.2014.961874 25535896

45. Walter AO, Seghezzi W, Korver W, Sheung J, Lees E (2000) The mitotic serine/threonine kinase Aurora2/AIK is regulated by phosphorylation and degradation. Oncogene 19: 4906–4916. 11039908

46. Littlepage LE, Wu H, Andresson T, Deaneham JKA, L T, Ruderman JV (2002) Identification of phosphorylated residues that affect the activity of the mitotic kinase Aurora-A. Proc Natl Acad Sci U S A 99: 15440–15445. 12422018

47. Eyers PA, Erikson E, Chen LG, Maller JL (2003) A novel mechanism for activation of the protein kinase Aurora A. Curr Biol 13: 691–697. 12699628

48. Bayliss R, Sardon T, Vernos I, Conti E (2003) Structural basis of Aurora-A activation by TPX2 at the mitotic spindle. Mol Cell 12: 851–862. 14580337

49. Dodson CA, Bayliss R (2012) Activation of Aurora-A kinase by protein partner binding and phosphorylation are independent and synergistic. J Biol Chem 287: 1150–1157. doi: 10.1074/jbc.M111.312090 22094468

50. Vranken WF, Boucher W, Stevens TJ, Fogh RH, Pajon A, et al. (2005) The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins 59: 687–696. 15815974

51. Brinda KV, Kannan N, Vishveshwara S (2002) Analysis of homodimeric protein interfaces by graph-spectral methods. Protein Eng 15: 265–277. 11983927

52. Espinoza-Fonseca LM (2012) Aromatic residues link binding and function of intrinsically disordered proteins. Mol Biosyst 8: 237–246. doi: 10.1039/c1mb05239j 21863198

53. Ma B, Elkayam T, Wolfson H, Nussinov R (2003) Protein-protein interactions: structurally conserved residues distinguish between binding sites and exposed protein surfaces. Proc Natl Acad Sci U S A 100: 5772–5777. 12730379

54. Rowan FC, Richards M, Bibby RA, Thompson A, Bayliss R, et al. (2013) Insights into Aurora-A Kinase Activation Using Unnatural Amino Acids Incorporated by Chemical Modification. ACS Chem Biol.

55. Burgess SG, Bayliss R (2015) The structure of C290A:C393A Aurora A provides structural insights into kinase regulation. Acta Crystallogr F Struct Biol Commun 71: 315–319. doi: 10.1107/S2053230X15002290 25760707

56. Bachman M, Uribe-Lewis S, Yang X, Williams M, Murrell A, et al. (2014) 5-Hydroxymethylcytosine is a predominantly stable DNA modification. Nat Chem 6: 1049–1055. doi: 10.1038/nchem.2064 25411882

57. Gergely F, Draviam VM, Raff JW (2003) The ch-TOG/XMAP215 protein is essential for spindle pole organization in human somatic cells. Genes Dev 17: 336–341. 12569123

58. Kufer TA, Sillje HH, Korner R, Gruss OJ, Meraldi P, et al. (2002) Human TPX2 is required for targeting Aurora-A kinase to the spindle. J Cell Biol 158: 617–623. 12177045

59. Cheeseman LP, Harry EF, McAinsh AD, Prior IA, Royle SJ (2013) Specific removal of TACC3-ch-TOG-clathrin at metaphase deregulates kinetochore fiber tension. J Cell Sci 126: 2102–2113. doi: 10.1242/jcs.124834 23532825

60. Meraldi P, Draviam VM, Sorger PK (2004) Timing and checkpoints in the regulation of mitotic progression. Dev Cell 7: 45–60. 15239953

61. Gomez-Baldo L, Schmidt S, Maxwell CA, Bonifaci N, Gabaldon T, et al. (2010) TACC3-TSC2 maintains nuclear envelope structure and controls cell division. Cell Cycle 9: 1143–1155. 20237422

62. Kaseda K, McAinsh AD, Cross RA (2012) Dual pathway spindle assembly increases both the speed and the fidelity of mitosis. Biol Open 1: 12–18. doi: 10.1242/bio.2011012 23213363

63. McHedlishvili N, Wieser S, Holtackers R, Mouysset J, Belwal M, et al. (2012) Kinetochores accelerate centrosome separation to ensure faithful chromosome segregation. J Cell Sci 125: 906–918. doi: 10.1242/jcs.091967 22399803

64. Silkworth WT, Nardi IK, Paul R, Mogilner A, Cimini D (2012) Timing of centrosome separation is important for accurate chromosome segregation. Mol Biol Cell 23: 401–411. doi: 10.1091/mbc.E11-02-0095 22130796

65. Nwagbara BU, Faris AE, Bearce EA, Erdogan B, Ebbert PT, et al. (2014) TACC3 is a microtubule plus end-tracking protein that promotes axon elongation and also regulates microtubule plus end dynamics in multiple embryonic cell types. Mol Biol Cell 25: 3350–3362. doi: 10.1091/mbc.E14-06-1121 25187649

66. Gutierrez-Caballero C, Burgess SG, Bayliss R, Royle SJ (2015) TACC3-ch-TOG track the growing tips of microtubules independently of clathrin and Aurora-A phosphorylation. Biol Open.

67. Pascreau G, Delcros JG, Cremet JY, Prigent C, Arlot-Bonnemains Y (2005) Phosphorylation of maskin by Aurora-A participates in the control of sequential protein synthesis during Xenopus laevis oocyte maturation. J Biol Chem 280: 13415–13423. 15687499

68. Zeng K, Bastos RN, Barr FA, Gruneberg U (2010) Protein phosphatase 6 regulates mitotic spindle formation by controlling the T-loop phosphorylation state of Aurora A bound to its activator TPX2. J Cell Biol 191: 1315–1332. doi: 10.1083/jcb.201008106 21187329

69. Giet R, McLean D, Descamps S, Lee MJ, Raff JW, et al. (2002) Drosophila Aurora A kinase is required to localize D-TACC to centrosomes and to regulate astral microtubules. J Cell Biol 156: 437–451. 11827981

70. Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, et al. (2012) The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov 2: 401–404. doi: 10.1158/2159-8290.CD-12-0095 22588877

71. Westwood I, Cheary DM, Baxter JE, Richards MW, van Montfort RL, et al. (2009) Insights into the conformational variability and regulation of human Nek2 kinase. J Mol Biol 386: 476–485. doi: 10.1016/j.jmb.2008.12.033 19124027

72. Marley J, Lu M, Bracken C (2001) A method for efficient isotopic labeling of recombinant proteins. J Biomol NMR 20: 71–75. 11430757

73. Zhang AJ, Bai G, Deans-Zirattu S, Browner MF, Lee EY (1992) Expression of the catalytic subunit of phosphorylase phosphatase (protein phosphatase-1) in Escherichia coli. J Biol Chem 267: 1484–1490. 1730696

74. Team RC (2013) R: A language and environment for statistical computing: R Foundation for Statistical Computing, Vienna, Austria.

75. Jerabek-Willemsen M, Wienken CJ, Braun D, Baaske P, Duhr S (2011) Molecular interaction studies using microscale thermophoresis. Assay Drug Dev Technol 9: 342–353. doi: 10.1089/adt.2011.0380 21812660

76. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947–2948. 17846036

77. Faisal A, Vaughan L, Bavetsias V, Sun C, Atrash B, et al. (2011) The aurora kinase inhibitor CCT137690 downregulates MYCN and sensitizes MYCN-amplified neuroblastoma in vivo. Mol Cancer Ther 10: 2115–2123. doi: 10.1158/1535-7163.MCT-11-0333 21885865

78. Barr AR, Kilmartin JV, Gergely F (2010) CDK5RAP2 functions in centrosome to spindle pole attachment and DNA damage response. J Cell Biol 189: 23–39. doi: 10.1083/jcb.200912163 20368616

79. Sir JH, Putz M, Daly O, Morrison CG, Dunning M, et al. (2013) Loss of centrioles causes chromosomal instability in vertebrate somatic cells. J Cell Biol 203: 747–756. doi: 10.1083/jcb.201309038 24297747

80. Zyss D, Ebrahimi H, Gergely F (2011) Casein kinase I delta controls centrosome positioning during T cell activation. J Cell Biol 195: 781–797. doi: 10.1083/jcb.201106025 22123863