Chemical proteomics and functional proteomics strategies for protein kinase inhibitor validation and protein kinase substrate identification: Applications to protein kinase CK2

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1834, Issue 7, 2013, Pages 1352-1358

  Gyenis, Laszlo ^a   Turowec, Jacob P ^a   Bretner, Maria ^b,c   Litchfield, David W ^a  

^a WESTERN UNIVERSITY   (Canada)

^b WARSAW UNIVERSITY OF TECHNOLOGY   (Poland)

^c INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

Author keywords

Chemoproteomics; CK2; Functional proteomics; Inhibitor profiling; Protein kinase inhibitor; TBB

Indexed keywords

4,5,6,7 TETRABROMO 1H BENZOTRIAZOLE; ADENOSINE TRIPHOSPHATASE INHIBITOR; CASEIN KINASE II; CELL EXTRACT; PROTEIN KINASE; PROTEIN KINASE INHIBITOR; PROTEIN SERINE THREONINE KINASE INHIBITOR; SEPHAROSE; TRIAZOLE DERIVATIVE; UNCLASSIFIED DRUG;

BINDING AFFINITY; CANCER THERAPY; CHEMICAL PROTEOMIC; CONTROLLED STUDY; FUNCTIONAL PROTEOMIC; MASS SPECTROMETRY; MOLECULAR INTERACTION; MUTANT; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEOMICS; REVIEW; VALIDATION PROCESS;

ADENOSINE TRIPHOSPHATE; CASEIN KINASE II; HUMANS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN KINASE INHIBITORS; PROTEIN KINASES; PROTEOMICS; SUBSTRATE SPECIFICITY; TRIAZOLES;

EID: 84878845087     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2013.02.006     Document Type: Review

References (72)

1. P. Cohen Protein kinases - the major drug targets of the twenty-first century? Nat. Rev. Drug Discov. 1 2002 309 315 (Pubitemid 37361447)
2. A.C. Dar, and K.M. Shokat The evolution of protein kinase inhibitors from antagonists to agonists of cellular signaling Annu. Rev. Biochem. 80 2011 769 795
3. P. Lahiry, A. Torkamani, N.J. Schork, and R.A. Hegele Kinase mutations in human disease: interpreting genotype-phenotype relationships Nat. Rev. Genet. 11 2010 60 74
4. W.R. Sellers A blueprint for advancing genetics-based cancer therapy Cell 147 2011 26 31
5. J. Zhang, P.L. Yang, and N.S. Gray Targeting cancer with small molecule kinase inhibitors Nat. Rev. Cancer 9 2009 28 39
6. B.J. Druker, C.L. Sawyers, H. Kantarjian, D.J. Resta, S.F. Reese, J.M. Ford, R. Capdeville, and M. Talpaz Activity of a specific inhibitor of the BCR-ABL tyrosine kinase in the blast crisis of chronic myeloid leukemia and acute lymphoblastic leukemia with the Philadelphia chromosome N. Engl. J. Med. 344 2001 1038 1042 (Pubitemid 32267973)
7. B.J. Druker, M. Talpaz, D.J. Resta, B. Peng, E. Buchdunger, J.M. Ford, N.B. Lydon, H. Kantarjian, R. Capdeville, S. Ohno-Jones, and C.L. Sawyers Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia N. Engl. J. Med. 344 2001 1031 1037 (Pubitemid 32267972)
8. A.L. Hopkins, and C.R. Groom The druggable genome Nat. Rev. Drug Discov. 1 2002 727 730 (Pubitemid 37361545)
9. J. Bain, L. Plater, M. Elliott, N. Shpiro, C.J. Hastie, H. McLauchlan, I. Klevernic, J.S. Arthur, D.R. Alessi, and P. Cohen The selectivity of protein kinase inhibitors: a further update Biochem. J. 408 2007 297 315
10. J. Bain, H. McLauchlan, M. Elliott, and P. Cohen The specificities of protein kinase inhibitors: an update Biochem. J. 371 2003 199 204 (Pubitemid 36458094)
11. S.P. Davies, H. Reddy, M. Caivano, and P. Cohen Specificity and mechanism of action of some commonly used protein kinase inhibitors Biochem. J. 351 2000 95 105
12. M.P. Patricelli, T.K. Nomanbhoy, J. Wu, H. Brown, D. Zhou, J. Zhang, S. Jagannathan, A. Aban, E. Okerberg, C. Herring, B. Nordin, H. Weissig, Q. Yang, J.D. Lee, N.S. Gray, and J.W. Kozarich In situ kinase profiling reveals functionally relevant properties of native kinases Chem. Biol. 18 2011 699 710
13. L. Gyenis, J.S. Duncan, J.P. Turowec, M. Bretner, and D.W. Litchfield Unbiased functional proteomics strategy for protein kinase inhibitor validation and identification of bona fide protein kinase substrates: application to identification of EEF1D as a substrate for CK2 J. Proteome Res. 10 2011 4887 4901
14. J.S. Duncan, L. Gyenis, J. Lenehan, M. Bretner, L.M. Graves, T.A. Haystead, and D.W. Litchfield An unbiased evaluation of CK2 inhibitors by chemo-proteomics: characterization of inhibitor effects on CK2 and identification of novel inhibitor targets Mol. Cell Proteomics 7 2008 1077 1088 (Pubitemid 351943955)
15. J.S. Duncan, T.A. Haystead, and D.W. Litchfield Chemoproteomic characterization of protein kinase inhibitors using immobilized ATP Methods Mol. Biol. 795 2012 119 134
16. L. Gyenis, A. Kus, M. Bretner, and D.W. Litchfield Functional proteomics strategy for validation of protein kinase inhibitors reveals new targets for a TBB-derived inhibitor of protein kinase CK2 J. Proteomics 2012 http://dx.doi.org/10.1016/j.jprot.2012.09.017 (pii: S1874-3919(12)00661-6)
17. K. Bettayeb, O.M. Tirado, S. Marionneau-Lambot, Y. Ferandin, O. Lozach, J.C. Morris, S. Mateo-Lozano, P. Drueckes, C. Schachtele, M.H. Kubbutat, F. Liger, B. Marquet, B. Joseph, A. Echalier, J.A. Endicott, V. Notario, and L. Meijer Meriolins, a new class of cell death inducing kinase inhibitors with enhanced selectivity for cyclin-dependent kinases Cancer Res. 67 2007 8325 8334 (Pubitemid 47395171)
18. M.A. Pagano, J. Bain, Z. Kazimierczuk, S. Sarno, M. Ruzzene, G. Di Maira, M. Elliott, A. Orzeszko, G. Cozza, F. Meggio, and L.A. Pinna The selectivity of inhibitors of protein kinase CK2: an update Biochem. J. 415 2008 353 365
19. M.A. Pagano, F. Meggio, M. Ruzzene, M. Andrzejewska, Z. Kazimierczuk, and L.A. Pinna 2-Dimethylamino-4,5,6,7-tetrabromo-1H-benzimidazole: a novel powerful and selective inhibitor of protein kinase CK2 Biochem. Biophys. Res. Commun. 321 2004 1040 1044 (Pubitemid 39044414)
20. S. Sarno, H. Reddy, F. Meggio, M. Ruzzene, S.P. Davies, A. Donella-Deana, D. Shugar, and L.A. Pinna Selectivity of 4,5,6,7-tetrabromobenzotriazole, an ATP site-directed inhibitor of protein kinase CK2 ('casein kinase-2') FEBS Lett. 496 2001 44 48 (Pubitemid 32436419)
21. G. Di Maira, F. Brustolon, J. Bertacchini, K. Tosoni, S. Marmiroli, L.A. Pinna, and M. Ruzzene Pharmacological inhibition of protein kinase CK2 reverts the multidrug resistance phenotype of a CEM cell line characterized by high CK2 level Oncogene 26 2007 6915 6926 (Pubitemid 47609076)
22. J.S. Duncan, and D.W. Litchfield Too much of a good thing: the role of protein kinase CK2 in tumorigenesis and prospects for therapeutic inhibition of CK2 Biochim. Biophys. Acta 1784 2008 33 47
23. J.S. Duncan, J.P. Turowec, K.E. Duncan, G. Vilk, C. Wu, B. Luscher, S.S. Li, G.B. Gloor, and D.W. Litchfield A peptide-based target screen implicates the protein kinase CK2 in the global regulation of caspase signaling Sci. Signal. 4 2011 ra30
24. J.P. Turowec, J.S. Duncan, A.C. French, L. Gyenis, N.A. St Denis, G. Vilk, and D.W. Litchfield Protein kinase CK2 is a constitutively active enzyme that promotes cell survival: strategies to identify CK2 substrates and manipulate its activity in mammalian cells Methods Enzymol. 484 2010 471 493
25. P. Zien, J.S. Duncan, J. Skierski, M. Bretner, D.W. Litchfield, and D. Shugar Tetrabromobenzotriazole (TBBt) and tetrabromobenzimidazole (TBBz) as selective inhibitors of protein kinase CK2: evaluation of their effects on cells and different molecular forms of human CK2 Biochim. Biophys. Acta 1754 2005 271 280 (Pubitemid 41797708)
26. F. Meggio, and L.A. Pinna One-thousand-and-one substrates of protein kinase CK2? FASEB J. 17 2003 349 368 (Pubitemid 36292951)
27. R. Prudent, and C. Cochet New protein kinase CK2 inhibitors: jumping out of the catalytic box Chem. Biol. 16 2009 112 120
28. S. Sarno, E. Papinutto, C. Franchin, J. Bain, M. Elliott, F. Meggio, Z. Kazimierczuk, A. Orzeszko, G. Zanotti, R. Battistutta, and L.A. Pinna ATP site-directed inhibitors of protein kinase CK2: an update Curr. Top. Med. Chem. 11 2011 1340 1351
29. S. Sarno, M. Ruzzene, P. Frascella, M.A. Pagano, F. Meggio, A. Zambon, M. Mazzorana, G. Di Maira, V. Lucchini, and L.A. Pinna Development and exploitation of CK2 inhibitors Mol. Cell. Biochem. 274 2005 69 76 (Pubitemid 41001502)
30. R. Szyszka, N. Grankowski, K. Felczak, and D. Shugar Halogenated benzimidazoles and benzotriazoles as selective inhibitors of protein kinases CK I and CK II from Saccharomyces cerevisiae and other sources Biochem. Biophys. Res. Commun. 208 1995 418 424
31. M. Zhao, J. Ma, H.Y. Zhu, X.H. Zhang, Z.Y. Du, Y.J. Xu, and X.D. Yu Apigenin inhibits proliferation and induces apoptosis in human multiple myeloma cells through targeting the trinity of CK2, Cdc37 and Hsp90 Mol. Cancer 10 2011 104
32. P. Zien, M. Bretner, K. Zastapilo, R. Szyszka, and D. Shugar Selectivity of 4,5,6,7-tetrabromobenzimidazole as an ATP-competitive potent inhibitor of protein kinase CK2 from various sources Biochem. Biophys. Res. Commun. 306 2003 129 133 (Pubitemid 36629415)
33. P.V. Hornbeck, J.M. Kornhauser, S. Tkachev, B. Zhang, E. Skrzypek, B. Murray, V. Latham, and M. Sullivan PhosphoSitePlus: a comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse Nucleic Acids Res. 40 2012 D261 D270
34. F. Gnad, S. Ren, J. Cox, J.V. Olsen, B. Macek, M. Oroshi, and M. Mann PHOSIDA (phosphorylation site database): management, structural and evolutionary investigation, and prediction of phosphosites Genome Biol. 8 2007 R250
35. H. Dinkel, C. Chica, A. Via, C.M. Gould, L.J. Jensen, T.J. Gibson, and F. Diella Phospho.ELM: a database of phosphorylation sites - update 2011 Nucleic Acids Res. 39 2011 D261 D267
36. K. Gevaert, A. Staes, J. Van Damme, S. De Groot, K. Hugelier, H. Demol, L. Martens, M. Goethals, and J. Vandekerckhove Global phosphoproteome analysis on human HepG2 hepatocytes using reversed-phase diagonal LC Proteomics 5 2005 3589 3599 (Pubitemid 41393292)
37. R. Linding, L.J. Jensen, G.J. Ostheimer, M.A. van Vugt, C. Jorgensen, I.M. Miron, F. Diella, K. Colwill, L. Taylor, K. Elder, P. Metalnikov, V. Nguyen, A. Pasculescu, J. Jin, J.G. Park, L.D. Samson, J.R. Woodgett, R.B. Russell, P. Bork, M.B. Yaffe, and T. Pawson Systematic discovery of in vivo phosphorylation networks Cell 129 2007 1415 1426 (Pubitemid 46962092)
38. R. Linding, L.J. Jensen, A. Pasculescu, M. Olhovsky, K. Colwill, P. Bork, M.B. Yaffe, and T. Pawson NetworKIN: a resource for exploring cellular phosphorylation networks Nucleic Acids Res. 36 2008 D695 D699
39. J.V. Olsen, B. Blagoev, F. Gnad, B. Macek, C. Kumar, P. Mortensen, and M. Mann Global, in vivo, and site-specific phosphorylation dynamics in signaling networks Cell 127 2006 635 648 (Pubitemid 44647421)
40. J.V. Olsen, M. Vermeulen, A. Santamaria, C. Kumar, M.L. Miller, L.J. Jensen, F. Gnad, J. Cox, T.S. Jensen, E.A. Nigg, S. Brunak, and M. Mann Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis Sci. Signal. 3 2010 ra3
41. D.W. Litchfield, F.J. Lozeman, C. Piening, J. Sommercorn, K. Takio, K.A. Walsh, and E.G. Krebs Subunit structure of casein kinase II from bovine testis. Demonstration that the alpha and alpha′ subunits are distinct polypeptides J. Biol. Chem. 265 1990 7638 7644
42. T.E. Thingholm, O.N. Jensen, and M.R. Larsen Analytical strategies for phosphoproteomics Proteomics 9 2009 1451 1468
43. S. Morandell, T. Stasyk, K. Grosstessner-Hain, E. Roitinger, K. Mechtler, G.K. Bonn, and L.A. Huber Phosphoproteomics strategies for the functional analysis of signal transduction Proteomics 6 2006 4047 4056
44. R.C. Hengeveld, N.T. Hertz, M.J. Vromans, C. Zhang, A.L. Burlingame, K.M. Shokat, and S.M. Lens Development of a chemical genetic approach for human aurora B kinase identifies novel substrates of the chromosomal passenger complex Mol. Cell Proteomics 11 2012 47 59
45. S.T. Eblen, N.V. Kumar, K. Shah, M.J. Henderson, C.K. Watts, K.M. Shokat, and M.J. Weber Identification of novel ERK2 substrates through use of an engineered kinase and ATP analogs J. Biol. Chem. 278 2003 14926 14935 (Pubitemid 36799822)
46. J.D. Blethrow, J.S. Glavy, D.O. Morgan, and K.M. Shokat Covalent capture of kinase-specific phosphopeptides reveals Cdk1-cyclin B substrates Proc. Natl. Acad. Sci. U. S. A. 105 2008 1442 1447 (Pubitemid 351346533)
47. P. Cohen Guidelines for the effective use of chemical inhibitors of protein function to understand their roles in cell regulation Biochem. J. 425 2010 53 54
48. T.A. Haystead The purinome, a complex mix of drug and toxicity targets Curr. Top. Med. Chem. 6 2006 1117 1127 (Pubitemid 44110924)
49. M.A. Fabian, W.H. Biggs III, D.K. Treiber, C.E. Atteridge, M.D. Azimioara, M.G. Benedetti, T.A. Carter, P. Ciceri, P.T. Edeen, M. Floyd, J.M. Ford, M. Galvin, J.L. Gerlach, R.M. Grotzfeld, S. Herrgard, D.E. Insko, M.A. Insko, A.G. Lai, J.M. Lelias, S.A. Mehta, Z.V. Milanov, A.M. Velasco, L.M. Wodicka, H.K. Patel, P.P. Zarrinkar, and D.J. Lockhart A small molecule-kinase interaction map for clinical kinase inhibitors Nat. Biotechnol. 23 2005 329 336 (Pubitemid 41094421)
50. M.W. Karaman, S. Herrgard, D.K. Treiber, P. Gallant, C.E. Atteridge, B.T. Campbell, K.W. Chan, P. Ciceri, M.I. Davis, P.T. Edeen, R. Faraoni, M. Floyd, J.P. Hunt, D.J. Lockhart, Z.V. Milanov, M.J. Morrison, G. Pallares, H.K. Patel, S. Pritchard, L.M. Wodicka, and P.P. Zarrinkar A quantitative analysis of kinase inhibitor selectivity Nat. Biotechnol. 26 2008 127 132
51. L.M. Graves, and D.W. Litchfield "Going KiNativ": probing the Native Kinome Chem. Biol. 18 2011 683 684
52. M. Ruzzene, D. Penzo, and L.A. Pinna Protein kinase CK2 inhibitor 4,5,6,7-tetrabromobenzotriazole (TBB) induces apoptosis and caspase-dependent degradation of haematopoietic lineage cell-specific protein 1 (HS1) in Jurkat cells Biochem. J. 364 2002 41 47 (Pubitemid 34538944)
53. G. Fritz, O.G. Issinger, and B.B. Olsen Selectivity analysis of protein kinase CK2 inhibitors DMAT, TBB and resorufin in cisplatin-induced stress responses Int. J. Oncol. 35 2009 1151 1157
54. A. Hessenauer, C.C. Schneider, C. Gotz, and M. Montenarh CK2 inhibition induces apoptosis via the ER stress response Cell. Signal. 23 2011 145 151
55. P.R. Graves, J.J. Kwiek, P. Fadden, R. Ray, K. Hardeman, A.M. Coley, M. Foley, and T.A. Haystead Discovery of novel targets of quinoline drugs in the human purine binding proteome Mol. Pharmacol. 62 2002 1364 1372 (Pubitemid 35403831)
56. C.M. Haystead, P. Gregory, T.W. Sturgill, and T.A. Haystead Gamma-phosphate-linked ATP-sepharose for the affinity purification of protein kinases. Rapid purification to homogeneity of skeletal muscle mitogen-activated protein kinase kinase Eur. J. Biochem. 214 1993 459 467 (Pubitemid 23173796)
57. U. Rix, O. Hantschel, G. Durnberger, L.L. Remsing Rix, M. Planyavsky, N.V. Fernbach, I. Kaupe, K.L. Bennett, P. Valent, J. Colinge, T. Kocher, and G. Superti-Furga Chemical proteomic profiles of the BCR-ABL inhibitors imatinib, nilotinib, and dasatinib reveal novel kinase and nonkinase targets Blood 110 2007 4055 4063 (Pubitemid 350248462)
58. C. Pan, J.V. Olsen, H. Daub, and M. Mann Global effects of kinase inhibitors on signaling networks revealed by quantitative phosphoproteomics Mol. Cell Proteomics 8 2009 2796 2808
59. F.S. Oppermann, F. Gnad, J.V. Olsen, R. Hornberger, Z. Greff, G. Keri, M. Mann, and H. Daub Large-scale proteomics analysis of the human kinome Mol. Cell Proteomics 8 2009 1751 1764
60. U. Kruse, C.P. Pallasch, M. Bantscheff, D. Eberhard, L. Frenzel, S. Ghidelli, S.K. Maier, T. Werner, C.M. Wendtner, and G. Drewes Chemoproteomics-based kinome profiling and target deconvolution of clinical multi-kinase inhibitors in primary chronic lymphocytic leukemia cells Leukemia 25 2011 89 100
61. M. Bantscheff, D. Eberhard, Y. Abraham, S. Bastuck, M. Boesche, S. Hobson, T. Mathieson, J. Perrin, M. Raida, C. Rau, V. Reader, G. Sweetman, A. Bauer, T. Bouwmeester, C. Hopf, U. Kruse, G. Neubauer, N. Ramsden, J. Rick, B. Kuster, and G. Drewes Quantitative chemical proteomics reveals mechanisms of action of clinical ABL kinase inhibitors Nat. Biotechnol. 25 2007 1035 1044 (Pubitemid 47517638)
62. J.S. Duncan, M.C. Whittle, K. Nakamura, A.N. Abell, A.A. Midland, J.S. Zawistowski, N.L. Johnson, D.A. Granger, N.V. Jordan, D.B. Darr, J. Usary, P.F. Kuan, D.M. Smalley, B. Major, X. He, K.A. Hoadley, B. Zhou, N.E. Sharpless, C.M. Perou, W.Y. Kim, S.M. Gomez, X. Chen, J. Jin, S.V. Frye, H.S. Earp, L.M. Graves, and G.L. Johnson Dynamic reprogramming of the kinome in response to targeted MEK inhibition in triple-negative breast cancer Cell 149 2012 307 321
63. N. Bischoff, J. Raaf, B. Olsen, M. Bretner, O.G. Issinger, and K. Niefind Enzymatic activity with an incomplete catalytic spine: insights from a comparative structural analysis of human CK2alpha and its paralogous isoform CK2alpha′ Mol. Cell. Biochem. 356 2011 57 65
64. T. Geiger, A. Wehner, C. Schaab, J. Cox, and M. Mann Comparative proteomic analysis of eleven common cell lines reveals ubiquitous but varying expression of most proteins Mol. Cell Proteomics 11 2012 10.1074/mcp.M111.014050
65. B.J. Ryu, S.H. Baek, J. Kim, S.J. Bae, S.Y. Chang, J.N. Heo, H. Lee, S.Y. Lee, and S.H. Kim Anti-androgen receptor activity of apoptotic CK2 inhibitor CX4945 in human prostate cancer LNCap cells Bioorg. Med. Chem. Lett. 22 2012 5470 5474
66. G. Cozza, L.A. Pinna, and S. Moro Protein kinase CK2 inhibitors: a patent review Expert Opin. Ther. Pat 22 2012 1081 1097
67. S. Zanin, C. Borgo, C. Girardi, S.E. O'Brien, Y. Miyata, L.A. Pinna, A. Donella-Deana, and M. Ruzzene Effects of the CK2 inhibitors CX-4945 and CX-5011 on drug-resistant cells PLoS One 7 2012 e49193
68. G. Cozza, L.A. Pinna, and S. Moro Kinase Ck2 inhibition: an update Curr. Med. Chem. 2012
69. Y. Miyata, and E. Nishida CK2 controls multiple protein kinases by phosphorylating a kinase-targeting molecular chaperone, Cdc37 Mol. Cell. Biol. 24 2004 4065 4074 (Pubitemid 38496182)
70. M. Taipale, I. Krykbaeva, M. Koeva, C. Kayatekin, K.D. Westover, G.I. Karras, and S. Lindquist Quantitative analysis of HSP90-client interactions reveals principles of substrate recognition Cell 150 2012 987 1001
71. Y. Miyata Protein kinase CK2 in health and disease: CK2: the kinase controlling the Hsp90 chaperone machinery Cell Mol. Life Sci. 66 2009 1840 1849
72. Y. Miyata, and E. Nishida Supervision of multiple signaling protein kinases by the CK2-Cdc37 couple, a possible novel cancer therapeutic target Ann. N. Y. Acad. Sci. 1030 2004 150 157 (Pubitemid 40378908)