Aurora A Kinase Contributes to a Pole-Based Error Correction Pathway

Current Biology

Volumn 25, Issue 14, 2015, Pages 1842-1851

  Ye, Anna A ^a   Deretic, Jovana ^b   Hoel, Christopher M ^a   Hinman, Albert W ^c   Cimini, Daniela ^c   Welburn, Julie P ^b   Maresca, Thomas J ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c VIRGINIA BIOINFORMATICS INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUR PROTEIN, DROSOPHILA; AURORA A KINASE; DROSOPHILA PROTEIN;

ANIMAL; CELL CULTURE; CELL POLARITY; CENTROMERE; CHROMOSOME POSITIONING; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; GENETICS; INSECT CHROMOSOME; METABOLISM; MICROTUBULE; ULTRASTRUCTURE;

ANIMALS; AURORA KINASE A; CELL POLARITY; CELLS, CULTURED; CHROMOSOME POSITIONING; CHROMOSOMES, INSECT; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION; KINETOCHORES; MICROTUBULES;

EID: 84937516391     PISSN: 09609822     EISSN: 18790445     Source Type: Journal    
DOI: 10.1016/j.cub.2015.06.021     Document Type: Article

References (54)

1. D. Cimini, B. Moree, J.C. Canman, and E.D. Salmon Merotelic kinetochore orientation occurs frequently during early mitosis in mammalian tissue cells and error correction is achieved by two different mechanisms J. Cell Sci. 116 2003 4213 4225
2. T.S. Kitajima, M. Ohsugi, and J. Ellenberg Complete kinetochore tracking reveals error-prone homologous chromosome biorientation in mammalian oocytes Cell 146 2011 568 581
3. D. Cimini, X. Wan, C.B. Hirel, and E.D. Salmon Aurora kinase promotes turnover of kinetochore microtubules to reduce chromosome segregation errors Curr. Biol. 16 2006 1711 1718
4. A.E. Kelly, and H. Funabiki Correcting aberrant kinetochore microtubule attachments: an Aurora B-centric view Curr. Opin. Cell Biol. 21 2009 51 58
5. T.U. Tanaka, N. Rachidi, C. Janke, G. Pereira, M. Galova, E. Schiebel, M.J. Stark, and K. Nasmyth Evidence that the Ipl1-Sli15 (Aurora kinase-INCENP) complex promotes chromosome bi-orientation by altering kinetochore-spindle pole connections Cell 108 2002 317 329
6. M.A. Lampson, K. Renduchitala, A. Khodjakov, and T.M. Kapoor Correcting improper chromosome-spindle attachments during cell division Nat. Cell Biol. 6 2004 232 237
7. K. Ke, J. Cheng, and A.J. Hunt The distribution of polar ejection forces determines the amplitude of chromosome directional instability Curr. Biol. 19 2009 807 815
8. S. Cane, A.A. Ye, S.J. Luks-Morgan, and T.J. Maresca Elevated polar ejection forces stabilize kinetochore-microtubule attachments J. Cell Biol. 200 2013 203 218
9. R.B. Nicklas, and C.A. Koch Chromosome micromanipulation. 3. Spindle fiber tension and the reorientation of mal-oriented chromosomes J. Cell Biol. 43 1969 40 50
10. I.M. Cheeseman, J.S. Chappie, E.M. Wilson-Kubalek, and A. Desai The conserved KMN network constitutes the core microtubule-binding site of the kinetochore Cell 127 2006 983 997
11. C. Ciferri, S. Pasqualato, E. Screpanti, G. Varetti, S. Santaguida, G. Dos Reis, A. Maiolica, J. Polka, J.G. De Luca, P. De Wulf, and et al. Implications for kinetochore-microtubule attachment from the structure of an engineered Ndc80 complex Cell 133 2008 427 439
12. J.G. DeLuca, W.E. Gall, C. Ciferri, D. Cimini, A. Musacchio, and E.D. Salmon Kinetochore microtubule dynamics and attachment stability are regulated by Hec1 Cell 127 2006 969 982
13. T.J. Maresca, and E.D. Salmon Intrakinetochore stretch is associated with changes in kinetochore phosphorylation and spindle assembly checkpoint activity J. Cell Biol. 184 2009 373 381
14. K.S. Uchida, K. Takagaki, K. Kumada, Y. Hirayama, T. Noda, and T. Hirota Kinetochore stretching inactivates the spindle assembly checkpoint J. Cell Biol. 184 2009 383 390
15. D. Liu, G. Vader, M.J. Vromans, M.A. Lampson, and S.M. Lens Sensing chromosome bi-orientation by spatial separation of aurora B kinase from kinetochore substrates Science 323 2009 1350 1353
16. A. Suzuki, B.L. Badger, X. Wan, J.G. DeLuca, and E.D. Salmon The architecture of CCAN proteins creates a structural integrity to resist spindle forces and achieve proper Intrakinetochore stretch Dev. Cell 30 2014 717 730
17. J.P. Welburn, M. Vleugel, D. Liu, J.R. Yates 3rd, M.A. Lampson, T. Fukagawa, and I.M. Cheeseman Aurora B phosphorylates spatially distinct targets to differentially regulate the kinetochore-microtubule interface Mol. Cell 38 2010 383 392
18. T.J. Maresca, and E.D. Salmon Welcome to a new kind of tension: translating kinetochore mechanics into a wait-anaphase signal J. Cell Sci. 123 2010 825 835
19. L. Cassimeris, C.L. Rieder, and E.D. Salmon Microtubule assembly and kinetochore directional instability in vertebrate monopolar spindles: implications for the mechanism of chromosome congression J. Cell Sci. 107 1994 285 297
20. C.S. Campbell, and A. Desai Tension sensing by Aurora B kinase is independent of survivin-based centromere localization Nature 497 2013 118 121
21. M. Carmena, and W.C. Earnshaw The cellular geography of aurora kinases Nat. Rev. Mol. Cell Biol. 4 2003 842 854
22. I.M. Cheeseman, S. Anderson, M. Jwa, E.M. Green, Js. Kang, J.R. Yates 3rd, C.S. Chan, D.G. Drubin, and G. Barnes Phospho-regulation of kinetochore-microtubule attachments by the Aurora kinase Ipl1p Cell 111 2002 163 172
23. S. Li, Z. Deng, J. Fu, C. Xu, G. Xin, Z. Wu, J. Luo, G. Wang, S. Zhang, B. Zhang, and et al. Spatial compartmentalization specializes function of Aurora-A and Aurora-B J. Biol. Chem. 2015 10.1074/jbc.M115.652453 Published online May 18, 2015
24. W.E. Theurkauf, and R.S. Hawley Meiotic spindle assembly in Drosophila females: behavior of nonexchange chromosomes and the effects of mutations in the nod kinesin-like protein J. Cell Biol. 116 1992 1167 1180
25. D.L. Stenoien, S. Sen, M.A. Mancini, and B.R. Brinkley Dynamic association of a tumor amplified kinase, Aurora-A, with the centrosome and mitotic spindle Cell Motil. Cytoskeleton 55 2003 134 146
26. J.D. Violin, J. Zhang, R.Y. Tsien, and A.C. Newton A genetically encoded fluorescent reporter reveals oscillatory phosphorylation by protein kinase C J. Cell Biol. 161 2003 899 909
27. B.G. Fuller, M.A. Lampson, E.A. Foley, S. Rosasco-Nitcher, K.V. Le, P. Tobelmann, D.L. Brautigan, P.T. Stukenberg, and T.M. Kapoor Midzone activation of aurora B in anaphase produces an intracellular phosphorylation gradient Nature 453 2008 1132 1136
28. B.S. Tseng, L. Tan, T.M. Kapoor, and H. Funabiki Dual detection of chromosomes and microtubules by the chromosomal passenger complex drives spindle assembly Dev. Cell 18 2010 903 912
29. U.S. Eggert, A.A. Kiger, C. Richter, Z.E. Perlman, N. Perrimon, T.J. Mitchison, and C.M. Field Parallel chemical genetic and genome-wide RNAi screens identify cytokinesis inhibitors and targets PLoS Biol. 2 2004 e379
30. Y. Smurnyy, A.V. Toms, G.R. Hickson, M.J. Eck, and U.S. Eggert Binucleine 2, an isoform-specific inhibitor of Drosophila Aurora B kinase, provides insights into the mechanism of cytokinesis ACS Chem. Biol. 5 2010 1015 1020
31. J.K. Yucel, J.D. Marszalek, J.R. McIntosh, L.S. Goldstein, D.W. Cleveland, and A.V. Philp CENP-meta, an essential kinetochore kinesin required for the maintenance of metaphase chromosome alignment in Drosophila J. Cell Biol. 150 2000 1 11
32. F.R. Putkey, T. Cramer, M.K. Morphew, A.D. Silk, R.S. Johnson, J.R. McIntosh, and D.W. Cleveland Unstable kinetochore-microtubule capture and chromosomal instability following deletion of CENP-E Dev. Cell 3 2002 351 365
33. J.V. Shah, E. Botvinick, Z. Bonday, F. Furnari, M. Berns, and D.W. Cleveland Dynamics of centromere and kinetochore proteins; implications for checkpoint signaling and silencing Curr. Biol. 14 2004 942 952
34. J.R. Pollard, and M. Mortimore Discovery and development of aurora kinase inhibitors as anticancer agents J. Med. Chem. 52 2009 2629 2651
35. M. Barisic, P. Aguiar, S. Geley, and H. Maiato Kinetochore motors drive congression of peripheral polar chromosomes by overcoming random arm-ejection forces Nat. Cell Biol. 16 2014 1249 1256
36. R. Giet, D. McLean, S. Descamps, M.J. Lee, J.W. Raff, C. Prigent, and D.M. Glover Drosophila Aurora A kinase is required to localize D-TACC to centrosomes and to regulate astral microtubules J. Cell Biol. 156 2002 437 451
37. T.M. Kapoor, M.A. Lampson, P. Hergert, L. Cameron, D. Cimini, E.D. Salmon, B.F. McEwen, and A. Khodjakov Chromosomes can congress to the metaphase plate before biorientation Science 311 2006 388 391
38. M.G. Manfredi, J.A. Ecsedy, K.A. Meetze, S.K. Balani, O. Burenkova, W. Chen, K.M. Galvin, K.M. Hoar, J.J. Huck, P.J. LeRoy, and et al. Antitumor activity of MLN8054, an orally active small-molecule inhibitor of Aurora A kinase Proc. Natl. Acad. Sci. USA 104 2007 4106 4111
39. G.M. Alushin, V.H. Ramey, S. Pasqualato, D.A. Ball, N. Grigorieff, A. Musacchio, and E. Nogales The Ndc80 kinetochore complex forms oligomeric arrays along microtubules Nature 467 2010 805 810
40. R.R. Wei, J. Al-Bassam, and S.C. Harrison The Ndc80/HEC1 complex is a contact point for kinetochore-microtubule attachment Nat. Struct. Mol. Biol. 14 2007 54 59
41. G.J. Guimaraes, Y. Dong, B.F. McEwen, and J.G. Deluca Kinetochore-microtubule attachment relies on the disordered N-terminal tail domain of Hec1 Curr. Biol. 18 2008 1778 1784
42. S.A. Miller, M.L. Johnson, and P.T. Stukenberg Kinetochore attachments require an interaction between unstructured tails on microtubules and Ndc80(Hec1) Curr. Biol. 18 2008 1785 1791
43. A.N. Kettenbach, D.K. Schweppe, B.K. Faherty, D. Pechenick, A.A. Pletnev, and S.A. Gerber Quantitative phosphoproteomics identifies substrates and functional modules of Aurora and Polo-like kinase activities in mitotic cells Sci. Signal. 4 2011 rs5
44. K.W. Wood, L. Lad, L. Luo, X. Qian, S.D. Knight, N. Nevins, K. Brejc, D. Sutton, A.G. Gilmartin, P.R. Chua, and et al. Antitumor activity of an allosteric inhibitor of centromere-associated protein-E Proc. Natl. Acad. Sci. USA 107 2010 5839 5844
45. K.M. Godek, L. Kabeche, and D.A. Compton Regulation of kinetochore-microtubule attachments through homeostatic control during mitosis Nat. Rev. Mol. Cell Biol. 16 2015 57 64
46. Y. Kim, A.J. Holland, W. Lan, and D.W. Cleveland Aurora kinases and protein phosphatase 1 mediate chromosome congression through regulation of CENP-E Cell 142 2010 444 455
47. X. Wan, R.P. O'Quinn, H.L. Pierce, A.P. Joglekar, W.E. Gall, J.G. DeLuca, C.W. Carroll, S.T. Liu, T.J. Yen, B.F. McEwen, and et al. Protein architecture of the human kinetochore microtubule attachment site Cell 137 2009 672 684
48. G. Goshima Identification of a TPX2-like microtubule-associated protein in Drosophila PLoS ONE 6 2011 e28120
49. T.A. Kufer, H.H. Silljé, R. Körner, O.J. Gruss, P. Meraldi, and E.A. Nigg Human TPX2 is required for targeting Aurora-A kinase to the spindle J. Cell Biol. 158 2002 617 623
50. P.A. Eyers, E. Erikson, L.G. Chen, and J.L. Maller A novel mechanism for activation of the protein kinase Aurora A Curr. Biol. 13 2003 691 697
51. M.Y. Tsai, C. Wiese, K. Cao, O. Martin, P. Donovan, J. Ruderman, C. Prigent, and Y. Zheng A Ran signalling pathway mediated by the mitotic kinase Aurora A in spindle assembly Nat. Cell Biol. 5 2003 242 248
52. G. Greenan, C.P. Brangwynne, S. Jaensch, J. Gharakhani, F. Jülicher, and A.A. Hyman Centrosome size sets mitotic spindle length in Caenorhabditis elegans embryos Curr. Biol. 20 2010 353 358
53. L. Chmátal, K. Yang, R.M. Schultz, and M.A. Lampson Spatial regulation of kinetochore microtubule attachments by destabilization at spindle poles in meiosis I Curr. Biol. 25 2015 1835 1841 this issue
54. S.L. Thompson, and D.A. Compton Chromosome missegregation in human cells arises through specific types of kinetochore-microtubule attachment errors Proc. Natl. Acad. Sci. USA 108 2011 17974 17978