Aurora B inhibits MCAK activity through a phosphoconformational switch that reduces microtubule association

Current Biology

Volumn 23, Issue 24, 2013, Pages 2491-2499

  Ems Mcclung, Stephanie C ^a   Hainline, Sarah G ^a   Devare, Jenna ^a   Zong, Hailing ^a   Cai, Shang ^a   Carnes, Stephanie K ^a   Shaw, Sidney L ^a   Walczak, Claire E ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA B KINASE; KINESIN;

ANIMAL; ARTICLE; CHEMISTRY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETIC PROCEDURES; HUMAN; METABOLISM; MICROTUBULE; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT;

ANIMALS; AURORA KINASE B; BIOSENSING TECHNIQUES; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMANS; KINESIN; MICROTUBULES; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT;

EID: 84890792731     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2013.10.054     Document Type: Article

References (42)

1. C.E. Walczak, S. Gayek, and R. Ohi Microtubule-depolymerizing kinesins Annu. Rev. Cell Dev. Biol. 29 2013 417 441
2. P.D. Andrews, Y. Ovechkina, N. Morrice, M. Wagenbach, K. Duncan, L. Wordeman, and J.R. Swedlow Aurora B regulates MCAK at the mitotic centromere Dev. Cell 6 2004 253 268
3. W. Lan, X. Zhang, S.L. Kline-Smith, S.E. Rosasco, G.A. Barrett-Wilt, J. Shabanowitz, D.F. Hunt, C.E. Walczak, and P.T. Stukenberg Aurora B phosphorylates centromeric MCAK and regulates its localization and microtubule depolymerization activity Curr. Biol. 14 2004 273 286
4. R. Ohi, T. Sapra, J. Howard, and T.J. Mitchison Differentiation of cytoplasmic and meiotic spindle assembly MCAK functions by Aurora B-dependent phosphorylation Mol. Biol. Cell 15 2004 2895 2906
5. X. Zhang, S.C. Ems-McClung, and C.E. Walczak Aurora A phosphorylates MCAK to control ran-dependent spindle bipolarity Mol. Biol. Cell 19 2008 2752 2765
6. K. Jiang, J. Wang, J. Liu, T. Ward, L. Wordeman, A. Davidson, F. Wang, and X. Yao TIP150 interacts with and targets MCAK at the microtubule plus ends EMBO Rep. 10 2009 857 865
7. A.T. Moore, K.E. Rankin, G. von Dassow, L. Peris, M. Wagenbach, Y. Ovechkina, A. Andrieux, D. Job, and L. Wordeman MCAK associates with the tips of polymerizing microtubules J. Cell Biol. 169 2005 391 397
8. D.S. Friedman, and R.D. Vale Single-molecule analysis of kinesin motility reveals regulation by the cargo-binding tail domain Nat. Cell Biol. 1 1999 293 297
9. D.D. Hackney, and M.F. Stock Kinesin's IAK tail domain inhibits initial microtubule-stimulated ADP release Nat. Cell Biol. 2 2000 257 260
10. M. Imanishi, N.F. Endres, A. Gennerich, and R.D. Vale Autoinhibition regulates the motility of the C. elegans intraflagellar transport motor OSM-3 J. Cell Biol. 174 2006 931 937
11. K.J. Verhey, and J.W. Hammond Traffic control: regulation of kinesin motors Nat. Rev. Mol. Cell Biol. 10 2009 765 777
12. D. Cai, A.D. Hoppe, J.A. Swanson, and K.J. Verhey Kinesin-1 structural organization and conformational changes revealed by FRET stoichiometry in live cells J. Cell Biol. 176 2007 51 63
13. J.W. Hammond, T.L. Blasius, V. Soppina, D. Cai, and K.J. Verhey Autoinhibition of the kinesin-2 motor KIF17 via dual intramolecular mechanisms J. Cell Biol. 189 2010 1013 1025
14. K.P. Wedaman, D.W. Meyer, D.J. Rashid, D.G. Cole, and J.M. Scholey Sequence and submolecular localization of the 115-kD accessory subunit of the heterotrimeric kinesin-II (KRP85/95) complex J. Cell Biol. 132 1996 371 380
15. J. Espeut, A. Gaussen, P. Bieling, V. Morin, S. Prieto, D. Fesquet, T. Surrey, and A. Abrieu Phosphorylation relieves autoinhibition of the kinetochore motor Cenp-E Mol. Cell 29 2008 637 643
16. A. Desai, S. Verma, T.J. Mitchison, and C.E. Walczak Kin I kinesins are microtubule-destabilizing enzymes Cell 96 1999 69 78
17. A.W. Hunter, M. Caplow, D.L. Coy, W.O. Hancock, S. Diez, L. Wordeman, and J. Howard The kinesin-related protein MCAK is a microtubule depolymerase that forms an ATP-hydrolyzing complex at microtubule ends Mol. Cell 11 2003 445 457
18. J. Helenius, G. Brouhard, Y. Kalaidzidis, S. Diez, and J. Howard The depolymerizing kinesin MCAK uses lattice diffusion to rapidly target microtubule ends Nature 441 2006 115 119
19. A. Moore, and L. Wordeman C-terminus of mitotic centromere-associated kinesin (MCAK) inhibits its lattice-stimulated ATPase activity Biochem. J. 383 2004 227 235
20. C.T. Friel, and J. Howard The kinesin-13 MCAK has an unconventional ATPase cycle adapted for microtubule depolymerization EMBO J. 30 2011 3928 3939
21. K.M. Hertzer, S.C. Ems-McClung, S.L. Kline-Smith, T.G. Lipkin, S.P. Gilbert, and C.E. Walczak Full-length dimeric MCAK is a more efficient microtubule depolymerase than minimal domain monomeric MCAK Mol. Biol. Cell 17 2006 700 710
22. C.A. Moores, M. Yu, J. Guo, C. Beraud, R. Sakowicz, and R.A. Milligan A mechanism for microtubule depolymerization by KinI kinesins Mol. Cell 9 2002 903 909
23. S.C. Ems-McClung, K.M. Hertzer, X. Zhang, M.W. Miller, and C.E. Walczak The interplay of the N- and C-terminal domains of MCAK control microtubule depolymerization activity and spindle assembly Mol. Biol. Cell 18 2007 282 294
24. T. Maney, M. Wagenbach, and L. Wordeman Molecular dissection of the microtubule depolymerizing activity of mitotic centromere-associated kinesin J. Biol. Chem. 276 2001 34753 34758
25. Y. Ovechkina, M. Wagenbach, and L. Wordeman K-loop insertion restores microtubule depolymerizing activity of a "neckless" MCAK mutant J. Cell Biol. 159 2002 557 562
26. J.R. Cooper, M. Wagenbach, C.L. Asbury, and L. Wordeman Catalysis of the microtubule on-rate is the major parameter regulating the depolymerase activity of MCAK Nat. Struct. Mol. Biol. 17 2010 77 82
27. T. Ogawa, R. Nitta, Y. Okada, and N. Hirokawa A common mechanism for microtubule destabilizers-M type kinesins stabilize curling of the protofilament using the class-specific neck and loops Cell 116 2004 591 602
28. T. Maney, A.W. Hunter, M. Wagenbach, and L. Wordeman Mitotic centromere-associated kinesin is important for anaphase chromosome segregation J. Cell Biol. 142 1998 787 801
29. L. Wordeman, M. Wagenbach, and T. Maney Mutations in the ATP-binding domain affect the subcellular distribution of mitotic centromere-associated kinesin (MCAK) Cell Biol. Int. 23 1999 275 286
30. D.D. Hackney, J.D. Levitt, and J. Suhan Kinesin undergoes a 9 S to 6 S conformational transition J. Biol. Chem. 267 1992 8696 8701
31. A. Gennerich, and R.D. Vale Walking the walk: how kinesin and dynein coordinate their steps Curr. Opin. Cell Biol. 21 2009 59 67
32. K.M. Hertzer, and C.E. Walczak The C-termini of tubulin and the specific geometry of tubulin substrates influence the depolymerization activity of MCAK Cell Cycle 7 2008 2727 2737
33. M. Wagenbach, S. Domnitz, L. Wordeman, and J. Cooper A kinesin-13 mutant catalytically depolymerizes microtubules in ADP J. Cell Biol. 183 2008 617 623
34. S.L. Kline-Smith, A. Khodjakov, P. Hergert, and C.E. Walczak Depletion of centromeric MCAK leads to chromosome congression and segregation defects due to improper kinetochore attachments Mol. Biol. Cell 15 2004 1146 1159
35. X. Zhang, W. Lan, S.C. Ems-McClung, P.T. Stukenberg, and C.E. Walczak Aurora B phosphorylates multiple sites on mitotic centromere-associated kinesin to spatially and temporally regulate its function Mol. Biol. Cell 18 2007 3264 3276
36. R.S. Rizk, K. Bohannon, L. Wetzel, J.A. Powers, S.L. Shaw, and C.E. Walczak MCAK and paclitaxel have differential effects on spindle microtubule organization and dynamics Mol. Biol. Cell 20 2009 1639 1651
37. L. Wordeman, M. Wagenbach, and G. von Dassow MCAK facilitates chromosome movement by promoting kinetochore microtubule turnover J. Cell Biol. 179 2007 869 879
38. 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
39. 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
40. 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
41. 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
42. C.E. Walczak, E.C. Gan, A. Desai, T.J. Mitchison, and S.L. Kline-Smith The microtubule-destabilizing kinesin XKCM1 is required for chromosome positioning during spindle assembly Curr. Biol. 12 2002 1885 1889