Substrate-Specific Activation of the Mitotic Kinase Bub1 through Intramolecular Autophosphorylation and Kinetochore Targeting

Structure

Volumn 22, Issue 11, 2014, Pages 1616-1627

  Lin, Zhonghui ^a,b   Jia, Luying ^a,b   Tomchick, Diana R ^a   Luo, Xuelian ^b   Yu, Hongtao ^a,b  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID; BUB1 KINASE; CELL CYCLE PROTEIN 20; PHOSPHOTRANSFERASE; UNCLASSIFIED DRUG; BUB1 PROTEIN, HUMAN; CDC20 PROTEIN, HUMAN; HISTONE; PROTEIN SERINE THREONINE KINASE; SERINE;

ARTICLE; AUTOPHOSPHORYLATION; CENTROMERE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; HUMAN; HUMAN CELL; MITOSIS; MOLECULAR MECHANICS; PROTEIN DOMAIN; CELL CYCLE; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; HELA CELL LINE; METABOLISM; PHOSPHORYLATION; PROTEIN SECONDARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

CATALYTIC DOMAIN; CDC20 PROTEINS; CELL CYCLE; CRYSTALLOGRAPHY, X-RAY; HELA CELLS; HISTONES; HUMANS; MODELS, MOLECULAR; PHOSPHORYLATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN-SERINE-THREONINE KINASES; SERINE; SUBSTRATE SPECIFICITY;

EID: 84908548650     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2014.08.020     Document Type: Article

References (33)

1. P.D. Adams, P.V. Afonine, G. Bunkóczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.W. Hung, G.J. Kapral, and R.W. Grosse-Kunstleve PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D Biol. Crystallogr. 66 2010 213 221
2. V.B. Chen, W.B. Arendall 3rd, J.J. Headd, D.A. Keedy, R.M. Immormino, G.J. Kapral, L.W. Murray, J.S. Richardson, and D.C. Richardson MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr. D Biol. Crystallogr. 66 2010 12 21
3. C.A. Dodson, S. Yeoh, T. Haq, and R. Bayliss A kinetic test characterizes kinase intramolecular and intermolecular autophosphorylation mechanisms Sci. Signal. 6 2013 ra54
4. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132
5. E.A. Foley, and T.M. Kapoor Microtubule attachment and spindle assembly checkpoint signalling at the kinetochore Nat. Rev. Mol. Cell Biol. 14 2013 25 37
6. J. Hu, E.C. Stites, H. Yu, E.A. Germino, H.S. Meharena, P.J. Stork, A.P. Kornev, S.S. Taylor, and A.S. Shaw Allosteric activation of functionally asymmetric RAF kinase dimers Cell 154 2013 1036 1046
7. L. Jia, S. Kim, and H. Yu Tracking spindle checkpoint signals from kinetochores to APC/C Trends Biochem. Sci. 38 2013 302 311
8. J. Kang, M. Yang, B. Li, W. Qi, C. Zhang, K.M. Shokat, D.R. Tomchick, M. Machius, and H. Yu Structure and substrate recruitment of the human spindle checkpoint kinase Bub1 Mol. Cell 32 2008 394 405
9. S.A. Kawashima, Y. Yamagishi, T. Honda, K. Ishiguro, and Y. Watanabe Phosphorylation of H2A by Bub1 prevents chromosomal instability through localizing shugoshin Science 327 2010 172 177
10. T.S. Kitajima, S. Hauf, M. Ohsugi, T. Yamamoto, and Y. Watanabe Human Bub1 defines the persistent cohesion site along the mitotic chromosome by affecting Shugoshin localization Curr. Biol. 15 2005 353 359
11. T.S. Kitajima, T. Sakuno, K. Ishiguro, S. Iemura, T. Natsume, S.A. Kawashima, and Y. Watanabe Shugoshin collaborates with protein phosphatase 2A to protect cohesin Nature 441 2006 46 52
12. T. Kiyomitsu, C. Obuse, and M. Yanagida Human Blinkin/AF15q14 is required for chromosome alignment and the mitotic checkpoint through direct interaction with Bub1 and BubR1 Dev. Cell 13 2007 663 676
13. V. Krenn, A. Wehenkel, X. Li, S. Santaguida, and A. Musacchio Structural analysis reveals features of the spindle checkpoint kinase Bub1-kinetochore subunit Knl1 interaction J. Cell Biol. 196 2012 451 467
14. V. Krenn, K. Overlack, I. Primorac, S. van Gerwen, and A. Musacchio KI motifs of human Knl1 enhance assembly of comprehensive spindle checkpoint complexes around MELT repeats Curr. Biol. 24 2014 29 39
15. P. Lara-Gonzalez, F.G. Westhorpe, and S.S. Taylor The spindle assembly checkpoint Curr. Biol. 22 2012 R966 R980
16. H. Liu, L. Jia, and H. Yu Phospho-H2A and cohesin specify distinct tension-regulated Sgo1 pools at kinetochores and inner centromeres Curr. Biol. 23 2013 1927 1933
17. H. Liu, S. Rankin, and H. Yu Phosphorylation-enabled binding of SGO1-PP2A to cohesin protects sororin and centromeric cohesion during mitosis Nat. Cell Biol. 15 2013 40 49
18. A.J. McCoy Solving structures of protein complexes by molecular replacement with Phaser Acta Crystallogr. D Biol. Crystallogr. 63 2007 32 41
19. W. Minor, M. Cymborowski, Z. Otwinowski, and M. Chruszcz HKL-3000: the integration of data reduction and structure solution - from diffraction images to an initial model in minutes Acta Crystallogr. D Biol. Crystallogr. 62 2006 859 866
20. L. Ni, S. Li, J. Yu, J. Min, C.A. Brautigam, D.R. Tomchick, D. Pan, and X. Luo Structural basis for autoactivation of human Mst2 kinase and its regulation by RASSF5 Structure 21 2013 1757 1768
21. B. Nolen, S. Taylor, and G. Ghosh Regulation of protein kinases; controlling activity through activation segment conformation Mol. Cell 15 2004 661 675
22. I. Primorac, J.R. Weir, E. Chiroli, F. Gross, I. Hoffmann, S. van Gerwen, A. Ciliberto, and A. Musacchio Bub3 reads phosphorylated MELT repeats to promote spindle assembly checkpoint signaling eLife 2 2013 e01030
23. R.M. Ricke, K.B. Jeganathan, L. Malureanu, A.M. Harrison, and J.M. van Deursen Bub1 kinase activity drives error correction and mitotic checkpoint control but not tumor suppression J. Cell Biol. 199 2012 931 949
24. C.G. Riedel, V.L. Katis, Y. Katou, S. Mori, T. Itoh, W. Helmhart, M. Gálová, M. Petronczki, J. Gregan, and B. Cetin Protein phosphatase 2A protects centromeric sister chromatid cohesion during meiosis I Nature 441 2006 53 61
25. Cdc20 by the mitotic checkpoint protein BubR1 Dev. Cell 1 2001 227 237
26. Z. Tang, H. Shu, D. Oncel, S. Chen, and H. Yu Phosphorylation of Cdc20 by Bub1 provides a catalytic mechanism for APC/C inhibition by the spindle checkpoint Mol. Cell 16 2004 387 397
27. Z. Tang, Y. Sun, S.E. Harley, H. Zou, and H. Yu Human Bub1 protects centromeric sister-chromatid cohesion through Shugoshin during mitosis Proc. Natl. Acad. Sci. USA 101 2004 18012 18017
28. Z. Tang, H. Shu, W. Qi, N.A. Mahmood, M.C. Mumby, and H. Yu PP2A is required for centromeric localization of Sgo1 and proper chromosome segregation Dev. Cell 10 2006 575 585
29. S.S. Taylor, and A.P. Kornev Protein kinases: evolution of dynamic regulatory proteins Trends Biochem. Sci. 36 2011 65 77
30. M. Vleugel, E. Tromer, M. Omerzu, V. Groenewold, W. Nijenhuis, B. Snel, and G.J. Kops Arrayed BUB recruitment modules in the kinetochore scaffold KNL1 promote accurate chromosome segregation J. Cell Biol. 203 2013 943 955
31. Y. Yamagishi, C.H. Yang, Y. Tanno, and Y. Watanabe MPS1/Mph1 phosphorylates the kinetochore protein KNL1/Spc7 to recruit SAC components Nat. Cell Biol. 14 2012 746 752
32. H. Yu Cdc20: a WD40 activator for a cell cycle degradation machine Mol. Cell 27 2007 3 16
33. G. Zhang, T. Lischetti, and J. Nilsson A minimal number of MELT repeats supports all the functions of KNL1 in chromosome segregation J. Cell Sci. 127 2014 871 884