Quinone reductase 2 is an adventitious target of protein kinase CK2 inhibitors TBBz (TBI) and DMAT

Biochemistry

Volumn 54, Issue 1, 2015, Pages 47-59

  Leung, Kevin K K ^a   Shilton, Brian H ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEATH; ENZYMES; HYDROGEN; HYDROGEN BONDS; MOLECULES; OXIDATION; PROTEINS;

ACTIVITY PROFILE; CRYSTAL STRUCTURE ANALYSIS; FLUORESCENCE TITRATIONS; KINETIC ANALYSIS; PERIPHERAL REGIONS; PHARMACOLOGICAL EFFECTS; PROTEIN KINASE CK2; QUINONE REDUCTASE 2;

CRYSTAL STRUCTURE;

4,5,6,7 1H TETRABROMOBENZIMIDAZOLE; 4,5,6,7 TETRABROMO 2 DIMETHYLAMINO 1H BENZIMIDAZOLE; CASEIN KINASE II; HALOGEN; HYDROGEN; MENADIONE; PROTEIN SERINE THREONINE KINASE INHIBITOR; QUINONE REDUCTASE 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); UNCLASSIFIED DRUG; 2-DIMETHYLAMINO-4,5,6,7-TETRABROMO-1H-BENZIMIDAZOLE; 4,5,6,7-TETRABROMOBENZIMIDAZOLE; BENZIMIDAZOLE DERIVATIVE; NRH - QUINONE OXIDOREDUCTASE2; PROTEIN BINDING; PROTEIN KINASE INHIBITOR;

APOPTOSIS; ARTICLE; BINDING AFFINITY; BINDING SITE; COMPETITIVE INHIBITION; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; CRYSTALLIZATION; DISSOCIATION CONSTANT; ENZYMATIC ASSAY; ENZYME ACTIVITY; ENZYME INHIBITION; HYDROGEN BOND; IC50; INHIBITION CONSTANT; KINETICS; MICHAELIS CONSTANT; NONHUMAN; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; ANTAGONISTS AND INHIBITORS; CHEMISTRY; DOSE RESPONSE; DRUG DELIVERY SYSTEM; HUMAN; METABOLISM; PHYSIOLOGY; PROCEDURES; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

BENZIMIDAZOLES; CASEIN KINASE II; CRYSTALLOGRAPHY, X-RAY; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG DELIVERY SYSTEMS; HUMANS; PROTEIN BINDING; PROTEIN KINASE INHIBITORS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; QUINONE REDUCTASES;

EID: 84921024494     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi500959t     Document Type: Article

References (65)

1. Zhang, J., Yang, P. L., and Gray, N. S. (2009) Targeting cancer with small molecule kinase inhibitors Nat. Rev. Cancer 9, 28-39
2. Meggio, F. and Pinna, L. A. (2003) One-thousand-and-one substrates of protein kinase CK2? FASEB J. 17, 349-368
3. St-Denis, N. A. and Litchfield, D. W. (2009) Protein kinase CK2 in health and disease: From birth to death: The role of protein kinase CK2 in the regulation of cell proliferation and survival Cell. Mol. Life Sci. 66, 1817-1829
4. Filhol, O. and Cochet, C. (2011) Protein kinases curb cell death Sci. Signaling 4, pe26
5. Tawfic, S., Yu, S., Wang, H., Faust, R., Davis, A., and Ahmed, K. (2001) Protein kinase CK2 signal in neoplasia Histol. Histopathol. 16, 573-582
6. Battistutta, R. (2009) Protein kinase CK2 in health and disease: Structural bases of protein kinase CK2 inhibition Cell. Mol. Life Sci. 66, 1868-1889
7. Szyszka, R., Grankowski, N., Felczak, K., and Shugar, D. (1995) 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, 418-424
8. Szyszka, R., Boguszewska, A., Shugar, D., and Grankowski, N. (1996) Halogenated benzimidazole inhibitors of phosphorylation, in vitro and in vivo, of the surface acidic proteins of the yeast ribosomal 60S subunit by endogenous protein kinases CK-II and PK60S Acta Biochim. Pol. 43, 389-396
9. Sarno, S., Reddy, H., Meggio, F., Ruzzene, M., Davies, S. P., Donella-deana, A., Shugar, D., and Pinna, L. A. (2001) Selectivity of 4,5,6,7-tetrabromobenzotriazole, an ATP site-directed inhibitor of protein kinase CK2 (casein kinase-2) FEBS Lett. 496, 44-48
10. Ruzzene, M., Penzo, D., and Pinna, L. A. (2002) 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, 41-47
11. Zień, P., Bretner, M., Zastąpiło, K., Szyszka, R., and Shugar, D. (2003) 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, 129-133
12. Zień,P.,Abramczyk,O.,Domańska, K.,Bretner,M.,and Szyszka,R. (2003) TBBz but not TBBt discriminates between two molecular forms of CK2 in vivo and its implications Biochem. Biophys. Res. Commun. 312, 623-628
13. Pagano, M. A., Andrzejewska, M., Ruzzene, M., Sarno, S., Cesaro, L., Bain, J., Elliott, M., Meggio, F., Kazimierczuk, Z., and Pinna, L. A. (2004) Optimization of protein kinase CK2 inhibitors derived from 4,5,6,7-tetrabromobenzimidazole J. Med. Chem. 47, 6239-6247
14. Pagano, M. A., Meggio, F., Ruzzene, M., Andrzejewska, M., Kazimierczuk, Z., and Pinna, L. A. (2004) 2-Dimethylamino-4,5,6,7-tetrabromo-1H-benzimidazole: A novel powerful and selective inhibitor of protein kinase CK2 Biochem. Biophys. Res. Commun. 321, 1040-1044
15. Pagano, M. A., Bain, J., Kazimierczuk, Z., Sarno, S., Ruzzene, M., Di Maira, G., Elliott, M., Orzeszko, A., Cozza, G., Meggio, F., and Pinna, L. A. (2008) The selectivity of inhibitors of protein kinase CK2: An update Biochem. J. 415, 353-365
16. Gyenis, L., Kus̈, A., Bretner, M., and Litchfield, D. W. (2013) Functional proteomics strategy for validation of protein kinase inhibitors reveals new targets for a TBB-derived inhibitor of protein kinase CK2 J. Proteomics 81, 70-79
17. Duncan, J. S., Gyenis, L., Lenehan, J., Bretner, M., Graves, L. M., Haystead, T. A., and Litchfield, D. W. (2008) An unbiased evaluation of CK2 inhibitors by chemoproteomics: Characterization of inhibitor effects on CK2 and identification of novel inhibitor targets Mol. Cell. Proteomics 7, 1077-1088
18. Liao, S., Dulaney, J., and William-Ashman, H. (1962) Purification and properties of a flavoprotein catalyzing the oxidation of reduced ribosyl nicotinamide J. Biol. Chem. 237, 2981-2987
19. Wu, K., Knox, R., Sun, X. Z., Joseph, P., Jaiswal, A. K., Zhang, D., Deng, P. S., and Chen, S. (1997) Catalytic properties of NAD(P)H:quinone oxidoreductase-2 (NQO2), a dihydronicotinamide riboside dependent oxidoreductase Arch. Biochem. Biophys. 347, 221-228
20. Gong, X., Kole, L., Iskander, K., and Jaiswal, A. K. (2007) NRH:quinone oxidoreductase 2 and NAD(P)H:quinone oxidoreductase 1 protect tumor suppressor p53 against 20s proteasomal degradation leading to stabilization and activation of p53 Cancer Res. 67, 5380-5388
21. Khutornenko, A. A., Roudko, V. V., Chernyak, B. V., Vartapetian, A. B., Chumakov, P. M., and Evstafieva, A. G. (2010) Pyrimidine biosynthesis links mitochondrial respiration to the p53 pathway Proc. Natl. Acad. Sci. U.S.A. 107, 12828-12833
22. Leung, K. K. K. and Shilton, B. H. (2013) Chloroquine binding reveals flavin redox switch function of quinone reductase 2 J. Biol. Chem. 288, 11242-11251
23. Shen, J., Barrios, R. J., and Jaiswal, A. K. (2010) Inactivation of the quinone oxidoreductases NQO1 and NQO2 strongly elevates the incidence and multiplicity of chemically induced skin tumors Cancer Res. 70, 1006-1014
24. Bantscheff, M., Eberhard, D., Abraham, Y., Bastuck, S., Boesche, M., Hobson, S., Mathieson, T., Perrin, J., Raida, M., Rau, C., Reader, V., Sweetman, G., Bauer, A., Bouwmeester, T., Hopf, C., Kruse, U., Neubauer, G., Ramsden, N., Rick, J., Kuster, B., and Drewes, G. (2007) Quantitative chemical proteomics reveals mechanisms of action of clinical ABL kinase inhibitors Nat. Biotechnol. 25, 1035-1044
25. Rix, U., Hantschel, O., Dürnberger, G., Remsing Rix, L. L., Planyavsky, M., Fernbach, N. V., Kaupe, I., Bennett, K. L., Valent, P., Colinge, J., Köcher, T., and Superti-Furga, G. (2007) Chemical proteomic profiles of the BCR-ABL inhibitors imatinib, nilotinib, and dasatinib reveal novel kinase and nonkinase targets Blood 110, 4055-4063
26. Winger, J. A., Hantschel, O., Superti-Furga, G., and Kuriyan, J. (2009) The structure of the leukemia drug imatinib bound to human quinone reductase 2 (NQO2) BMC Struct. Biol. 9, 7
27. Brehmer, D., Godl, K., Zech, B., Wissing, J., and Daub, H. (2004) Proteome-wide identification of cellular targets affected by bisindolylmaleimide-type protein kinase C inhibitors Mol. Cell. Proteomics 3, 490-500
28. Leung, K. K. K., Litchfield, D. W., and Shilton, B. H. (2012) Flavin adenine dinucleotide content of quinone reductase 2: Analysis and optimization for structure-function studies Anal. Biochem. 420, 84-89
29. Kwiek, J. J., Haystead, T. A. J., and Rudolph, J. (2004) Kinetic mechanism of quinone oxidoreductase 2 and its inhibition by the antimalarial quinolines Biochemistry 43, 4538-4547
30. Leslie, A. G. W. and Powell, H. R. (2007) Evolving Methods for Macromolecular Crystallography. In Evolving Methods for Macromolecular Crystallography (Read, R. J. and Sussman, J. L., Eds.) Vol. 245, pp 41-51, Springer, Berlin.
31. Evans, P. (2006) Scaling and assessment of data quality Acta Crystallogr. D62, 72-82
32. Foster, C. E., Bianchet, M. A., Talalay, P., Zhao, Q., and Amzel, L. M. (1999) Crystal structure of human quinone reductase type 2, a metalloflavoprotein Biochemistry 38, 9881-9886
33. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L.-W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D66, 213-221
34. Politzer, P., Murray, J. S., and Clark, T. (2013) Halogen bonding and other σ-hole interactions: A perspective Phys. Chem. Chem. Phys. 15, 11178-11189
35. Levitt, M. and Perutz, M. (1988) Aromatic Rings Act as Hydrogen Bond Acceptors J. Mol. Biol. 201, 751-754
36. Hemmerich, P., Nagelschneider, G., and Veeger, C. (1970) Chemistry and molecular biology of flavins and flavoproteins FEBS Lett. 8, 69-83
37. Zien, P., Duncan, J. S., Skierski, J., Bretner, M., Litchfield, D. W., and Shugar, D. (2005) 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, 271-280
38. Sarno, S., Salvi, M., Battistutta, R., Zanotti, G., and Pinna, L. A. (2005) Features and potentials of ATP-site directed CK2 inhibitors Biochim. Biophys. Acta 1754, 263-270
39. Zanin, S., Borgo, C., Girardi, C., O'Brien, S. E., Miyata, Y., Pinna, L. A., Donella-Deana, A., and Ruzzene, M. (2012) Effects of the CK2 inhibitors CX-4945 and CX-5011 on drug-resistant cells PLoS One 7, e49193
40. Guo, C., Gasparian, A. V., Zhuang, Z., Bosykh, D. A., Komar, A. A., Gudkov, A. V., and Gurova, K. V. (2009) 9-Aminoacridine-based anticancer drugs target the PI3K/AKT/mTOR, NF-B and p53 pathways Oncogene 28, 1151-1161
41. Sarno, S., de Moliner, E., Ruzzene, M., Pagano, M. A., Battistutta, R., Bain, J., Fabbro, D., Schoepfer, J., Elliott, M., Furet, P., Meggio, F., Zanotti, G., and Pinna, L. A. (2003) Biochemical and three-dimensional-structural study of the specific inhibition of protein kinase CK2 by [5-oxo-5,6-dihydroindolo-(1,2-a)quinazolin-7-yl]acetic acid (IQA) Biochem. J. 374, 639-646
42. Battistutta, R., Mazzorana, M., Cendron, L., Bortolato, A., Sarno, S., Kazimierczuk, Z., Zanotti, G., Moro, S., and Pinna, L. A. (2007) The ATP-binding site of protein kinase CK2 holds a positive electrostatic area and conserved water molecules ChemBioChem 8, 1804-1809
43. Battistutta, R., Mazzorana, M., Sarno, S., Kazimierczuk, Z., Zanotti, G., and Pinna, L. A. (2005) Inspecting the structure-activity relationship of protein kinase CK2 inhibitors derived from tetrabromo-benzimidazole Chem. Biol. 12, 1211-1219
44. Cavelier, G. and Amzel, L. M. (2001) Mechanism of NAD(P)H:quinone reductase: Ab initio studies of reduced flavin Proteins 43, 420-432
45. Deininger, M., Buchdunger, E., and Druker, B. J. (2005) The development of imatinib as a therapeutic agent for chronic myeloid leukemia Blood 105, 2640-2653
46. Asher, G., Lotem, J., Cohen, B., Sachs, L., and Shaul, Y. (2001) Regulation of p53 stability and p53-dependent apoptosis by NADH quinone oxidoreductase 1 Proc. Natl. Acad. Sci. U.S.A. 98, 1188-1193
47. Huang, C., Ma, W. Y., Goranson, A., and Dong, Z. (1999) Resveratrol suppresses cell transformation and induces apoptosis through a p53-dependent pathway Carcinogenesis 20, 237-242
48. Kim, E. L., Wüstenberg, R., Rübsam, A., Schmitz-Salue, C., Warnecke, G., Bücker, E.-M., Pettkus, N., Speidel, D., Rohde, V., Schulz-Schaeffer, W., Deppert, W., and Giese, A. (2010) Chloroquine activates the p53 pathway and induces apoptosis in human glioma cells Neuro-Oncology (Cary, NC, U.S.) 12, 389-400
49. Wendel, H.-G., de Stanchina, E., Cepero, E., Ray, S., Emig, M., Fridman, J. S., Veach, D. R., Bornmann, W. G., Clarkson, B., McCombie, W. R., Kogan, S. C., Hochhaus, A., and Lowe, S. W. (2006) Loss of p53 impedes the antileukemic response to BCR-ABL inhibition Proc. Natl. Acad. Sci. U.S.A. 103, 7444-7449
50. Santoro, R., Marani, M., Blandino, G., Muti, P., and Strano, S. (2012) Melatonin triggers p53Ser phosphorylation and prevents DNA damage accumulation Oncogene 31, 2931-2942
51. Gurova, K. V., Hill, J. E., Guo, C., Prokvolit, A., Burdelya, L. G., Samoylova, E., Khodyakova, A. V., Ganapathi, R., Ganapathi, M., Tararova, N. D., Bosykh, D., Lvovskiy, D., Webb, T. R., Stark, G. R., and Gudkov, A. V. (2005) Small molecules that reactivate p53 in renal cell carcinoma reveal a NF-B-dependent mechanism of p53 suppression in tumors Proc. Natl. Acad. Sci. U.S.A. 102, 17448-17453
52. Moll, U. M., Wolff, S., Speidel, D., and Deppert, W. (2005) Transcription-independent pro-apoptotic functions of p53 Curr. Opin. Cell Biol. 17, 631-636
53. Nosjean, O., Ferro, M., Coge, F., Beauverger, P., Henlin, J. M., Lefoulon, F., Fauchere, J. L., Delagrange, P., Canet, E., and Boutin, J. A. (2000) Identification of the melatonin-binding site MT3 as the quinone reductase 2 J. Biol. Chem. 275, 31311-31317
54. Ferry, G., Hecht, S., Berger, S., Moulharat, N., Coge, F., Guillaumet, G., Leclerc, V., Yous, S., Delagrange, P., and Boutin, J. A. (2010) Old and new inhibitors of quinone reductase 2 Chem.-Biol. Interact. 186, 103-109
55. Reybier, K., Perio, P., Ferry, G., Bouajila, J., Delagrange, P., Boutin, J. A., and Nepveu, F. (2011) Insights into the redox cycle of human quinone reductase 2 Free Radical Res. 45, 1184-1195
56. Janda, E., Parafati, M., Aprigliano, S., Carresi, C., Visalli, V., Sacco, I., Ventrice, D., Mega, T., Vadalá, N., Rinaldi, S., Musolino, V., Palma, E., Gratteri, S., Rotiroti, D., and Mollace, V. (2013) The antidote effect of quinone oxidoreductase 2 inhibitor against paraquat-induced toxicity in vitro and in vivo Br. J. Pharmacol. 168, 46-59
57. Long, D. J., Iskander, K., Gaikwad, A., Arin, M., Roop, D. R., Knox, R., Barrios, R., and Jaiswal, A. K. (2002) Disruption of dihydronicotinamide riboside:quinone oxidoreductase 2 (NQO2) leads to myeloid hyperplasia of bone marrow and decreased sensitivity to menadione toxicity J. Biol. Chem. 277, 46131-46139
58. Dunstan, M. S., Barnes, J., Humphries, M., Whitehead, R. C., Bryce, R. A., Leys, D., Stratford, I. J., and Nolan, K. A. (2011) Novel inhibitors of NRH:quinone oxidoreductase 2 (NQO2): Crystal structures, biochemical activity, and intracellular effects of imidazoacridin-6-ones J. Med. Chem. 54, 6597-6611
59. Nolan, K. A., Humphries, M. P., Bryce, R. A., and Stratford, I. J. (2010) Imidazoacridin-6-ones as novel inhibitors of the quinone oxidoreductase NQO2 Bioorg. Med. Chem. Lett. 20, 2832-2836
60. Ahn, K. S., Gong, X., Sethi, G., Chaturvedi, M. M., Jaiswal, A. K., and Aggarwal, B. B. (2007) Deficiency of NRH:quinone oxidoreductase 2 differentially regulates TNF signaling in keratinocytes: Up-regulation of apoptosis correlates with down-regulation of cell survival kinases Cancer Res. 67, 10004-10011
61. Iskander, K., Paquet, M., Brayton, C., and Jaiswal, A. K. (2004) Deficiency of NRH:quinone oxidoreductase 2 increases susceptibility to 7,12-dimethylbenz(a)anthracene and benzo(a)pyrene-induced skin carcinogenesis Cancer Res. 64, 5925-5928
62. Battistutta, R., De Moliner, E., Sarno, S., Zanotti, G., and Pinna, L. A. (2001) Structural features underlying selective inhibition of protein kinase CK2 by ATP site-directed tetrabromo-2-benzotriazole Protein Sci. 10, 2200-2206
63. Baker, N. A., Sept, D., Joseph, S., Holst, M. J., and McCammon, J. A. (2001) Electrostatics of nanosystems: Application to microtubules and the ribosome Proc. Natl. Acad. Sci. U.S.A. 98, 10037-10041
64. Dolinsky, T. J., Czodrowski, P., Li, H., Nielsen, J. E., Jensen, J. H., Klebe, G., and Baker, N. A. (2007) PDB2PQR: Expanding and upgrading automated preparation of biomolecular structures for molecular simulations Nucleic Acids Res. 35 (Web Server Issue) W522-W525
65. Laskowski, R. A., MacArthur, M., Moss, D. S., and Thorton, J. M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures J. Appl. Cryst. 26, 283-291