A kinetic test characterizes kinase intramolecular and intermolecular autophosphorylation mechanisms

Science Signaling

Volumn 6, Issue 282, 2013, Pages

  Dodson, Charlotte A ^a,b   Yeoh, Sharon ^c   Haq, Tamanna ^c   Bayliss, Richard ^a,c  

^a INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA A KINASE;

ARTICLE; AUTOPHOSPHORYLATION; CRYSTAL STRUCTURE; ENZYME ANALYSIS; ENZYME KINETICS; ENZYME MECHANISM; ENZYME PHOSPHORYLATION; ENZYME REACTIVATION; ENZYME STRUCTURE; MOLECULE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; SIGNAL NOISE RATIO;

AURORA KINASE A; BLOTTING, WESTERN; CHECKPOINT KINASE 2; HUMANS; KINETICS; MASS SPECTROMETRY; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MUTATION; PEPTIDES; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY; THREONINE;

EID: 84880895268     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2003910     Document Type: Article

References (33)

1. A. W. Oliver, A. Paul, K. J. Boxall, S. E. Barrie, G. W. Aherne, M. D. Garrett, S. Mittnacht, L. H. Pearl, Trans-activation of the DNA-damage signalling protein kinase Chk2 by T-loop exchange. EMBO J. 25, 3179-3190 (2006).
2. P. A. Lochhead, R. Kinstrie, G. Sibbet, T. Rawjee, N. Morrice, V. Cleghon, A chaperonedependent GSK3b transitional intermediate mediates activation-loop autophosphorylation. Mol. Cell 24, 627-633 (2006).
3. P. A. Lochhead, G. Sibbet, N.Morrice, V. Cleghon, Activation-loop autophosphorylation is mediated by a novel transitional intermediate form of DYRKs. Cell 121, 925-936 (2005).
4. A. C. Pike, P. Rellos, F. H. Niesen, A. Turnbull, A. W. Oliver, S. A. Parker, B. E. Turk, L. H. Pearl, S. Knapp, Activation segment dimerization: A mechanism for kinase autophosphorylation of non-consensus sites. EMBO J. 27, 704-714 (2008).
5. R. Bayliss, T. Sardon, I. Vernos, E. Conti, Structural basis of Aurora-A activation by TPX2 at the mitotic spindle. Mol. Cell 12, 851-862 (2003).
6. C. A. Dodson, M. Kosmopoulou, M.W. Richards, B. Atrash, V. Bavetsias, J. Blagg, R. Bayliss, Crystal structure of an Aurora-A mutant that mimics Aurora-B bound to MLN8054: Insights into selectivity and drug design. Biochem. J. 427, 19-28 (2010).
7. C. A. Dodson, R. Bayliss, Activation of Aurora-A kinase by protein partner binding and phosphorylation are independent and synergistic. J. Biol. Chem. 287, 1150-1157 (2012).
8. M. W. Richards, L. O'Regan, C. Mas-Droux, J. M. Blot, J. Cheung, S. Hoelder, A. M. Fry, R. Bayliss, An autoinhibitory tyrosine motif in the cell-cycle-regulated Nek7 kinase is released through binding of Nek9. Mol. Cell 36, 560-570 (2009).
9. A. S. Nikonova, I. Astsaturov, I. G. Serebriiskii, R. L. Dunbrack Jr., E. A. Golemis, Aurora A kinase (AURKA) in normal and pathological cell division. Cell. Mol. Life Sci. 70, 661-687 (2013).
10. A. O. Walter, W. Seghezzi, W. Korver, J. Sheung, E. Lees, The mitotic serine/threonine kinase Aurora2/AIK is regulated by phosphorylation and degradation. Oncogene 19, 4906-4916 (2000).
11. P. A. Eyers, E. Erikson, L. G. Chen, J. L. Maller, A novel mechanism for activation of the protein kinase Aurora A. Curr. Biol. 13, 691-697 (2003).
12. K. Zeng, R. N. Bastos, F. A. Barr, U. Gruneberg, 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 (2010).
13. V. Joukov, A. De Nicolo, A. Rodriguez, J. C. Walter, D. M. Livingston, Centrosomal protein of 192 kDa (Cep192) promotes centrosome-driven spindle assembly by engaging in organelle-specific Aurora A activation. Proc. Natl. Acad. Sci. U.S.A. 107, 21022-21027 (2010).
14. L. O'Regan, A. M. Fry, The Nek6 and Nek7 protein kinases are required for robust mitotic spindle formation and cytokinesis. Mol. Cell. Biol. 29, 3975-3990 (2009).
15. M. Capra, P. G. Nuciforo, S. Confalonieri, M. Quarto, M. Bianchi, M. Nebuloni, R. Boldorini, F. Pallotti, G. Viale, M. L. Gishizky, G. F. Draetta, P. P. Di Fiore, Frequent alterations in the expression of serine/threonine kinases in human cancers. Cancer Res. 66, 8147-8154 (2006).
16. C. Belham, J. Roig, J. A. Caldwell, Y. Aoyama, B. E. Kemp, M. Comb, J. Avruch, A mitotic cascade of NIMA family kinases. Nercc1/Nek9 activates the Nek6 and Nek7 kinases. J. Biol. Chem. 278, 34897-34909 (2003).
17. Y. J. Jeon, K. Y. Lee, Y. Y. Cho, A. Pugliese, H. G. Kim, C. H. Jeong, A. M. Bode, Z. Dong, Role of NEK6 in tumor promoter-induced transformation in JB6 C141 mouse skin epidermal cells. J. Biol. Chem. 285, 28126-28133 (2010).
18. T. Schindler, W. Bornmann, P. Pellicena, W. T. Miller, B. Clarkson, J. Kuriyan, Structural mechanism for STI-571 inhibition of Abelson tyrosine kinase. Science 289, 1938-1942 (2000).
19. G. Kontopidis, C. McInnes, S. R. Pandalaneni, I. McNae, D. Gibson, M. Mezna, M. Thomas, G. Wood, S. Wang, M. D. Walkinshaw, P. M. Fischer, Differential binding of inhibitors to active and inactive CDK2 provides insights for drug design. Chem. Biol. 13, 201-211 (2006).
20. J. Wu, W. Li, B. P. Craddock, K. W. Foreman, M. J. Mulvihill, Q. S. Ji, W. T. Miller, S. R. Hubbard, Small-molecule inhibition and activation-loop trans-phosphorylation of the IGF1 receptor. EMBO J. 27, 1985-1994 (2008).
21. H. Ma, S. Deacon, K. Horiuchi, The challenge of selecting protein kinase assays for lead discovery optimization. Expert Opin. Drug Discov. 3, 607-621 (2008).
22. H. Wu, Z. X. Wang, The mechanism of p21-activated kinase 2 autoactivation. J. Biol. Chem. 278, 41768-41778 (2003).
23. G. E. Benner, P. B. Dennis, R. A. Masaracchia, Activation of an S6/H4 kinase (PAK65) from human placenta by intramolecular and intermolecular autophosphorylation. J. Biol. Chem. 270, 21121-21128 (1995).
24. S. C. Barker, D. B. Kassel, D. Weigl, X. Huang, M. A. Luther, W. B. Knight, Characterization of pp60c-src tyrosine kinase activities using a continuous assay: Autoactivation of the enzyme is an intermolecular autophosphorylation process. Biochemistry 34, 14843-14851 (1995).
25. J. Wang, J. W. Wu, Z. X. Wang, Mechanistic studies of the autoactivation of PAK2: A two-step model of cis initiation followed by trans amplification. J. Biol. Chem. 286, 2689-2695 (2011).
26. H. R. Lawrence, M. P. Martin, Y. Luo, R. Pireddu, H. Yang, H. Gevariya, S. Ozcan, J. Y. Zhu, R. Kendig, M. Rodriguez, R. Elias, J. Q. Cheng, S. M. Sebti, E. Schonbrunn, N. J. Lawrence, Development of o-chlorophenyl substituted pyrimidines as exceptionally potent Aurora kinase inhibitors. J. Med. Chem. 55, 7392-7416 (2012).
27. R. Bayliss, A. M. Fry, T. Haq, S. Yeoh, On the molecular mechanisms of mitotic kinase activation. Open Biol. 2, 120136 (2012).
28. K. A. Pickin, S. Chaudhury, B. C. Dancy, J. J. Gray, P. A. Cole, Analysis of protein kinase autophosphorylation using expressed protein ligation and computational modeling. J. Am. Chem. Soc. 130, 5667-5669 (2008).
29. T. Hirota, N. Kunitoku, T. Sasayama, T. Marumoto, D. Zhang, M. Nitta, K. Hatakeyama, H. Saya, Aurora-A and an interacting activator, the LIM protein Ajuba, are required for mitotic commitment in human cells. Cell 114, 585-598 (2003).
30. Z. Cai, N. H. Chehab, N. P. Pavletich, Structure and activation mechanism of the CHK2 DNA damage checkpoint kinase. Mol. Cell 35, 818-829 (2009).
31. I. Westwood, D. M. Cheary, J. E. Baxter, M. W. Richards, R. L. van Montfort, A. M. Fry, R. Bayliss, Insights into the conformational variability and regulation of human Nek2 kinase. J. Mol. Biol. 386, 476-485 (2009).
32. P. Emsley, B. Lohkamp, W. G. Scott, K. Cowtan, Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).
33. 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, R.W. Grosse-Kunstleve, A. J. McCoy, N. W. Moriarty, R. Oeffner, R. J. Read, D. C. Richardson, J. S. Richardson, T. C. Terwilliger, P. H. Zwart, PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).