Generation and characterization of ATP analog-specific protein kinase Cδ

Journal of Biological Chemistry

Volumn 290, Issue 4, 2015, Pages 1936-1951

  Kumar, Varun ^a   Weng, Yi Chinn ^a   Geldenhuys, Werner J ^b   Wang, Dan ^c   Han, Xiqian ^a   Messing, Robert O ^c,d   Chou, Wen Hai ^a,c  

^a KENT STATE UNIVERSITY   (United States)

^b NORTHEAST OHIO MEDICAL UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CELL SIGNALING; CRYSTAL STRUCTURE;

BINDING POCKETS; HIGHER EFFICIENCY; HOMOLOGY MODELING; KINASE INHIBITORS; PHOSPHORYL TRANSFER; PYRAZOLO[3 ,4-D]PYRIMIDINE; SELECTIVE INHIBITION; STRUCTURAL BASIS;

ENZYMES;

4 AMINO 7 TERT BUTYL 5 (4 METHYLPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; ADENINE; ADENOSINE TRIPHOSPHATE; GLYCINE; PROTEIN KINASE C DELTA; PURINE; SUPEROXIDE; GLUTAMINE; LEUCINE; LYSINE; PHENYLALANINE; PROTEIN BINDING; PURINE DERIVATIVE;

ARTICLE; CATALYSIS; COMPUTER MODEL; CONTROLLED STUDY; COS 7 CELL LINE; CRYSTAL STRUCTURE; ENZYME ANALYSIS; ENZYME BINDING; ENZYME SPECIFICITY; ENZYME SUBSTRATE; HUMAN; IMMUNOFLUORESCENCE; MOLECULAR DOCKING; NONHUMAN; PROTEIN FUNCTION; PROTEIN INTERACTION; WILD TYPE; AMINO ACID SEQUENCE; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; CHEMISTRY; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; METABOLISM; MOLECULAR GENETICS; MOUSE; NEUTROPHIL; PHOSPHORYLATION; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

RUMEX;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; ANIMALS; CATALYSIS; CERCOPITHECUS AETHIOPS; COS CELLS; GLUTAMINE; HUMANS; LEUCINE; LYSINE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; NEUTROPHILS; PHENYLALANINE; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN KINASE C-DELTA; PURINES; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY; SUPEROXIDES;

EID: 84921716432     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.598698     Document Type: Article

References (53)

1. Steinberg, S. F. (2008) Structural basis of protein kinase C isoform function. Physiol. Rev. 88, 1341-1378
2. Newton, A. C. (2010) Protein kinase C: poised to signal. Am. J. Physiol. Endocrinol. Metab. 298, E395-E402
3. Choi, D. S., Wei, W., Deitchman, J. K., Kharazia, V. N., Lesscher, H. M., McMahon, T., Wang, D., Qi, Z. H., Sieghart, W., Zhang, C., Shokat, K. M., Mody, I., and Messing, R. O. (2008) Protein kinase Cδ regulates ethanol intoxication and enhancement of GABA-stimulated tonic current. J. Neurosci. 28, 11890-11899
4. Chou, W. H., Choi, D. S., Zhang, H., Mu, D., McMahon, T., Kharazia, V. N., Lowell, C. A., Ferriero, D. M., and Messing, R. O. (2004) Neutrophil protein kinase Cδ as a mediator of stroke-reperfusion injury. J. Clin. Invest. 114, 49-56
5. Bishop, A. C., Buzko, O., and Shokat, K. M. (2001) Magic bullets for protein kinases. Trends Cell Biol. 11, 167-172
6. Zhang, C., Lopez, M. S., Dar, A. C., Ladow, E., Finkbeiner, S., Yun, C. H., Eck, M. J., and Shokat, K. M. (2013) Structure-guided inhibitor design expands the scope of analog-sensitive kinase technology. ACS Chem. Biol. 8, 1931-1938
7. Allen, J. J., Lazerwith, S. E., and Shokat, K. M. (2005) Bio-orthogonal affinity purification of direct kinase substrates. J. Am. Chem. Soc. 127, 5288-5289
8. Habelhah, H., Shah, K., Huang, L., Burlingame, A. L., Shokat, K. M., and Ronai, Z. (2001) Identification of new JNK substrate using ATP pocket mutant JNK and a corresponding ATP analogue. J. Biol. Chem. 276, 18090-18095
9. Shah, K., and Shokat, K. M. (2002) A chemical genetic screen for direct v-Src substrates reveals ordered assembly of a retrograde signaling pathway. Chem. Biol. 9, 35-47
10. Eblen, S. T., Kumar, N. V., Shah, K., Henderson, M. J., Watts, C. K., Shokat, K. M., and Weber, M. J. (2003) Identification of novel ERK2 substrates through use of an engineered kinase and ATP analogs. J. Biol. Chem. 278, 14926-14935
11. Ubersax, J. A., Woodbury, E. L., Quang, P. N., Paraz, M., Blethrow, J. D., Shah, K., Shokat, K. M., and Morgan, D. O. (2003) Targets of the cyclin-dependent kinase Cdk1. Nature 425, 859-864
12. Hindley, A. D., Park, S., Wang, L., Shah, K., Wang, Y., Hu, X., Shokat, K. M., Kolch, W., Sedivy, J. M., and Yeung, K. C. (2004) Engineering the serine/threonine protein kinase Raf-1 to utilise an orthogonal analogue of ATP substituted at the N6 position. FEBS Lett. 556, 26-34
13. Larochelle, S., Batliner, J., Gamble, M. J., Barboza, N. M., Kraybill, B. C., Blethrow, J. D., Shokat, K. M., and Fisher, R. P. (2006) Dichotomous but stringent substrate selection by the dual-function Cdk7 complex revealed by chemical genetics. Nat. Struct. Mol. Biol. 13, 55-62
14. Chou, W. H., Wang, D., McMahon, T., Qi, Z. H., Song, M., Zhang, C., Shokat, K. M., and Messing, R. O. (2010) GABAA receptor trafficking is regulated by protein kinase Cε and the N-ethylmaleimide-sensitive factor. J. Neurosci. 30, 13955-13965
15. Wu, D. F., Chandra, D., McMahon, T., Wang, D., Dadgar, J., Kharazia, V. N., Liang, Y. J., Waxman, S. G., Dib-Hajj, S. D., and Messing, R. O. (2012) PKCepsilon phosphorylation of the sodium channel NaV1.8 increases channel function and produces mechanical hyperalgesia in mice. J. Clin. Invest. 122, 1306-1315
16. Hanke, J. H., Gardner, J. P., Dow, R. L., Changelian, P. S., Brissette, W. H., Weringer, E. J., Pollok, B. A., and Connelly, P. A. (1996) Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and FynT-dependent T cell activation. J. Biol. Chem. 271, 695-701
17. Allen, J. J., Li, M., Brinkworth, C. S., Paulson, J. L., Wang, D., Hübner, A., Chou, W. H., Davis, R. J., Burlingame, A. L., Messing, R. O., Katayama, C. D., Hedrick, S. M., and Shokat, K. M. (2007) A semisynthetic epitope for kinase substrates. Nat. Methods 4, 511-516
18. Bell, R. M. (1986) Protein kinase C activation by diacylglycerol second messengers. Cell 45, 631-632
19. Lowell, C. A., Fumagalli, L., and Berton, G. (1996) Deficiency of Src family kinases p59/61hck and p58c-fgr results in defective adhesion-dependent neutrophil functions. J. Cell Biol. 133, 895-910
20. Qi, Z. H., Song, M., Wallace, M. J., Wang, D., Newton, P. M., McMahon, T., Chou, W. H., Zhang, C., Shokat, K. M., and Messing, R. O. (2007) Protein kinase C epsilon regulates γ-aminobutyrate type A receptor sensitivity to ethanol and benzodiazepines through phosphorylation of γ2 subunits. J. Biol. Chem. 282, 33052-33063
21. Pongracz, J., Webb, P., Wang, K., Deacon, E., Lunn, O. J., and Lord, J. M. (1999) Spontaneous neutrophil apoptosis involves caspase 3-mediated activation of protein kinase C-δ. J. Biol. Chem. 274, 37329-37334
22. Takimura, T., Kamata, K., Fukasawa, K., Ohsawa, H., Komatani, H., Yoshizumi, T., Takahashi, I., Kotani, H., and Iwasawa, Y. (2010) Structures of the PKC-ι kinase domain in its ATP-bound and apo forms reveal defined structures of residues 533-551 in the C-terminal tail and their roles in ATP binding. Acta Crystallogr. D Biol. Crystallogr. 66, 577-583
23. Zheng, J., Knighton, D. R., ten Eyck, L. F., Karlsson, R., Xuong, N., Taylor, S. S., and Sowadski, J. M. (1993) Crystal structure of the catalytic subunit of cAMP-dependent protein kinase complexed with MgATP and peptide inhibitor. Biochemistry 32, 2154-2161
24. Zheng, J., Trafny, E. A., Knighton, D. R., Xuong, N. H., Taylor, S. S., Ten Eyck, L. F., and Sowadski, J. M. (1993) 2.2 Å refined crystal structure of the catalytic subunit of cAMP-dependent protein kinase complexed with MnATP and a peptide inhibitor. Acta Crystallogr. D Biol. Crystallogr. 49, 362-365
25. Trott, O., and Olson, A. J. (2010) AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J. Comput. Chem. 31, 455-461
26. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera: a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612
27. Mou, T. C., Gille, A., Fancy, D. A., Seifert, R., and Sprang, S. R. (2005) Structural basis for the inhibition of mammalian membrane adenylyl cyclase by 2′(3′)-O-(N-Methylanthraniloyl)-guanosine 5′-triphosphate. J. Biol. Chem. 280, 7253-7261
28. Carugo, O., and Pongor, S. (2001) A normalized root-mean-square distance for comparing protein three-dimensional structures. Protein Sci. 10, 1470-1473
29. Kornev, A. P., Haste, N. M., Taylor, S. S., and Eyck, L. F. (2006) Surface comparison of active and inactive protein kinases identifies a conserved activation mechanism. Proc. Natl. Acad. Sci. U.S.A. 103, 17783-17788
30. Taylor, S. S., Zhang, P., Steichen, J. M., Keshwani, M. M., and Kornev, A. P. (2013) PKA: lessons learned after twenty years. Biochim. Biophys. Acta 1834, 1271-1278
31. Leonard, T. A., Różycki, B., Saidi, L. F., Hummer, G., and Hurley, J. H. (2011) Crystal structure and allosteric activation of protein kinase C βII. Cell 144, 55-66
32. Witucki, L. A., Huang, X., Shah, K., Liu, Y., Kyin, S., Eck, M. J., and Shokat, K. M. (2002) Mutant tyrosine kinases with unnatural nucleotide specificity retain the structure and phospho-acceptor specificity of the wild-type enzyme. Chem. Biol. 9, 25-33
33. Niswender, C. M., Ishihara, R. W., Judge, L. M., Zhang, C., Shokat, K. M., and McKnight, G. S. (2002) Protein engineering of protein kinase A catalytic subunits results in the acquisition of novel inhibitor sensitivity. J. Biol. Chem. 277, 28916-28922
34. Burley, S. K., and Petsko, G. A. (1985) Aromatic-aromatic interaction: a mechanism of protein structure stabilization. Science 229, 23-28
35. Boehr, D. D., Farley, A. R., Wright, G. D., and Cox, J. R. (2002) Analysis of the π-π stacking interactions between the aminoglycoside antibiotic kinase APH(3′)-IIIa and its nucleotide ligands. Chem. Biol. 9, 1209-1217
36. Banko, M. R., Allen, J. J., Schaffer, B. E., Wilker, E. W., Tsou, P., White, J. L., Villén, J., Wang, B., Kim, S. R., Sakamoto, K., Gygi, S. P., Cantley, L. C., Yaffe, M. B., Shokat, K. M., and Brunet, A. (2011) Chemical genetic screen for AMPKα2 substrates uncovers a network of proteins involved in mitosis. Mol. Cell 44, 878-892
37. Moffat, L. D., Brown, S. B., Grassie, M. E., Ulke-Lemé, A., Williamson, L. M., Walsh, M. P., and MacDonald, J. A. (2011) Chemical genetics of zipper-interacting protein kinase reveal myosin light chain as a bona fide substrate in permeabilized arterial smooth muscle. J. Biol. Chem. 286, 36978-36991
38. Mayadas, T. N., Cullere, X., and Lowell, C. A. (2014) The multifaceted functions of neutrophils. Annu. Rev. Pathol. 9, 181-218
39. DeChatelet, L. R., Shirley, P. S., and Johnston, R. B., Jr. (1976) Effect of phorbol myristate acetate on the oxidative metabolism of human polymorphonuclear leukocytes. Blood 47, 545-554
40. Brown, G. E., Stewart, M. Q., Liu, H., Ha, V. L., and Yaffe, M. B. (2003) A novel assay system implicates PtdIns(3,4)P(2), PtdIns(3)P, and PKCδ in intracellular production of reactive oxygen species by the NADPH oxidase. Mol. Cell 11, 35-47
41. Kilpatrick, L. E., Sun, S., Li, H., Vary, T. C., and Korchak, H. M. (2010) Regulation of TNF-induced oxygen radical production in human neutrophils: role of δ-PKC. J. Leukoc. Biol. 87, 153-164
42. Chen, L., Hahn, H., Wu, G., Chen, C. H., Liron, T., Schechtman, D., Cavallaro, G., Banci, L., Guo, Y., Bolli, R., Dorn, G. W., 2nd, and Mochly-Rosen, D. (2001) Opposing cardioprotective actions and parallel hypertrophic effects of δ PKC and ε PKC. Proc. Natl. Acad. Sci. U.S.A. 98, 11114-11119
43. Mochly-Rosen, D., Das, K., and Grimes, K. V. (2012) Protein kinase C, an elusive therapeutic target? Nat. Rev. Drug Discov. 11, 937-957
44. Chen, X., Ye, H., Kuruvilla, R., Ramanan, N., Scangos, K. W., Zhang, C., Johnson, N. M., England, P. M., Shokat, K. M., and Ginty, D. D. (2005) A chemical-genetic approach to studying neurotrophin signaling. Neuron 46, 13-21
45. Jaeschke, A., Karasarides, M., Ventura, J. J., Ehrhardt, A., Zhang, C., Flavell, R. A., Shokat, K. M., and Davis, R. J. (2006) JNK2 is a positive regulator of the cJun transcription factor. Mol. Cell 23, 899-911
46. Seifert, R., Lushington, G. H., Mou, T. C., Gille, A., and Sprang, S. R. (2012) Inhibitors of membranous adenylyl cyclases. Trends Pharmacol. Sci. 33, 64-78
47. Dar, A. C., and Shokat, K. M. (2011) The evolution of protein kinase inhibitors from antagonists to agonists of cellular signaling. Annu. Rev. Biochem. 80, 769-795
48. Emrick, M. A., Lee, T., Starkey, P. J., Mumby, M. C., Resing, K. A., and Ahn, N. G. (2006) The gatekeeper residue controls autoactivation of ERK2 via a pathway of intramolecular connectivity. Proc. Natl. Acad. Sci. U.S.A. 103, 18101-18106
49. Schauble, S., King, C. C., Darshi, M., Koller, A., Shah, K., and Taylor, S. S. (2007) Identification of ChChd3 as a novel substrate of the cAMP-dependent protein kinase (PKA) using an analog-sensitive catalytic subunit. J. Biol. Chem. 282, 14952-14959
50. Karaman, M. W., Herrgard, S., Treiber, D. K., Gallant, P., Atteridge, C. E., Campbell, B. T., Chan, K. W., Ciceri, P., Davis, M. I., Edeen, P. T., Faraoni, R., Floyd, M., Hunt, J. P., Lockhart, D. J., Milanov, Z. V., Morrison, M. J., Pallares, G., Patel, H. K., Pritchard, S., Wodicka, L. M., and Zarrinkar, P. P. (2008) A quantitative analysis of kinase inhibitor selectivity. Nat. Biotechnol. 26, 127-132
51. Tanramluk, D., Schreyer, A., Pitt, W. R., and Blundell, T. L. (2009) On the origins of enzyme inhibitor selectivity and promiscuity: a case study of protein kinase binding to staurosporine. Chem. Biol. Drug Des. 74, 16-24
52. Carter, T. A., Wodicka, L. M., Shah, N. P., Velasco, A. M., Fabian, M. A., Treiber, D. K., Milanov, Z. V., Atteridge, C. E., Biggs, W. H., 3rd, Edeen, P. T., Floyd, M., Ford, J. M., Grotzfeld, R. M., Herrgard, S., Insko, D. E., Mehta, S. A., Patel, H. K., Pao, W., Sawyers, C. L., Varmus, H., Zarrinkar, P. P., and Lockhart, D. J. (2005) Inhibition of drug-resistant mutants of ABL, KIT, and EGF receptor kinases. Proc. Natl. Acad. Sci. U.S.A. 102, 11011-11016
53. Zhang, J., Yang, P. L., and Gray, N. S. (2009) Targeting cancer with small molecule kinase inhibitors. Nat. Rev. Cancer 9, 28-39