Kinetic characterization of human JNK2α2 reaction mechanism using substrate competitive inhibitors

Biochemistry

Volumn 46, Issue 16, 2007, Pages 4775-4784

  Niu, Linghao ^a   Chang, Kung Ching ^a   Wilson, Stacy ^a   Tran, Patricia ^a   Zuo, Fengrong ^a   Swinney, David C ^a  

^a ROCHE BIOSCIENCE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

JUN N-TERMINAL KINASE (JNK); KINETIC MECHANISM; PEPTIDE INHIBITOR; STRESS ACTIVATED SERINE;

ADENOSINETRIPHOSPHATE; BINDING ENERGY; CELLS; ENZYMES; PEPTIDES; PHOSPHORYLATION;

REACTION KINETICS;

ACTIVATING TRANSCRIPTION FACTOR 2; AMINO ACID; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; C JUN N TERMINAL KINASE 2ALPHA2; DOCKING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 9; PROTEIN SERINE THREONINE KINASE; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ALLOSTERISM; AMINO ACID SEQUENCE; ARTICLE; CHEMICAL REACTION; COMPETITIVE INHIBITION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INHIBITION; ENZYME KINETICS; ENZYME MECHANISM; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE COMPLEX; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REACTION ANALYSIS; SEQUENCE HOMOLOGY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANTHRACENES; BINDING, COMPETITIVE; ENZYME INHIBITORS; HUMANS; KINETICS; MITOGEN-ACTIVATED PROTEIN KINASE 9; PEPTIDE FRAGMENTS; PHOSPHORYLATION;

EID: 34247517344     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi602423e     Document Type: Article

References (56)

1. Derijard, B., Hibi, M., Wu, I. H., Barrett, T., Su, B., Deng, T., Karin, M., and Davis, R. J. (1994) JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain, Cell 76, 1025-1037.
2. Kyriakis, J. M., Banerjee, P., Nikolakaki, E., Dai, T., Rubie, E. A., Ahmad, M. F., Avruch, J., and Woodgett, J. R. (1994) The stress-activated protein kinase subfamily of c-Jun kinases, Nature 369, 156-160.
3. Minden, A., Lin, A., Smeal, T., Derijard, B., Cobb, M., Davis, R., and Karin, M. (1994) c-Jun N-terminal phosphorylation correlates with activation of the JNK subgroup but not the ERK subgroup of mitogen-activated protein kinases, Mol. Cell. Biol. 14, 6683-6688.
4. Adler, V., Schaffer, A., Kim, J., Dolan, L., and Ronai, Z. (1995) UV irradiation and heat shock mediate JNK activation via alternate pathways, J. Biol. Chem. 270, 26071-26077.
5. Cano, E., Hazzalin, C. A., and Mahadevan, L. C. (1994) Anisomycin-activated protein kinases p45 and p55 but not mitogen-activated protein kinases ERK-1 and -2 are implicated in the induction of c-fos and c-jun, Mol. Cell. Biol. 14, 7352-7362.
6. Westwick, J. K., Weitzel, C., Minden, A., Karin, M., and Brenner, D. A. (1994) Tumor necrosis factor alpha stimulates AP-1 activity through prolonged activation of the c-Jun kinase, J. Biol. Chem. 269, 26396-26401.
7. Gupta, S., Barrett, T., Whitmarsh, A. J., Cavanagh, J., Sluss, H. K., Derijard, B., and Davis, R. J. (1996) Selective interaction of JNK protein kinase isoforms with transcription factors, EMBO J. 15, 2760-2770.
8. Martin, J. H., Mohit, A. A., and Miller, C. A. (1996) Developmental expression in the mouse nervous system of the p493F12 SAP kinase, Brain Res. Mol. Brain Res. 35, 47-57.
9. Chen, N., She, Q. B., Bode, A. M., and Dong, Z. (2002) Differential gene expression profiles of Jnk1- and Jnk2-deficient murine fibroblast cells, Cancer Res. 62, 1300-1304.
10. Kallunki, T., Su, B., Tsigelny, I., Sluss, H. K., Derijard, B., Moore, G., Davis, R., and Karin, M. (1994) JNK2 contains a specificity-determining region responsible for efficient c-Jun binding and phosphorylation, Genes Dev. 8, 2996-3007.
11. Xie, X., Gu, Y., Fox, T., Coll, J. T., Fleming, M. A., Markland, W., Caron, P. R., Wilson, K. P., and Su, M. S. (1998) Crystal structure of JNK3: a kinase implicated in neuronal apoptosis, Structure 6, 983-991.
12. Davis, R. J. (1999) Signal transduction by the c-Jun N-terminal kinase, Biochem. Soc. Symp. 64, 1-12.
13. Cuenda, A. (2000) Mitogen-activated protein kinase kinase 4 (MKK4), Int. J. Biochem. Cell Biol. 32, 581-587.
14. Hirai, S., Noda, K., Moriguchi, T., Nishida, E., Yamashita, A., Deyama, T., Fukuyama, K., and Ohno, S. (1998) Differential activation of two JNK activators, MKK7 and SEK1, by MKN28-derived nonreceptor serine/threonine kinase/mixed lineage kinase 2, J. Biol. Chem. 273, 7406-7412.
15. Tanoue, T., Adachi, M., Moriguchi, T., and Nishida, E. (2000) A conserved docking motif in MAP kinases common to substrates, activators and regulators, Nat. Cell Biol. 2, 110-116.
16. Enslen, H., and Davis, R. J. (2001) Regulation of MAP kinases by docking domains, Biol. Cell. 93, 5-14.
17. Minden, A., and Karin, M. (1997) Regulation and function of the JNK subgroup of MAP kinases, Biochim. Biophys. Acta 1333, F85-F104.
18. Jain, J., Valge-Archer, V. E., and Rao, A. (1992) Analysis of the AP-1 sites in the IL-2 promoter, J. Immunol. 148, 1240-1250.
19. Foletta, V. C., Segal, D. H., and Cohen, D. R. (1998) Transcriptional regulation in the immune system: all roads lead to AP-1, J. Leukocyte Biol. 63, 139-152.
20. Pendas, A. M., Balbin, M., Llano, E., Jimenez, M. G., and Lopez-Otin, C. (1997) Structural analysis and promoter characterization of the human collagenase-3 gene (MMP13), Genomics 40, 222-233.
21. Manning, A. M., and Mercurio, F. (1997) Transcription inhibitors in inflammation, Expert Opin. Invest. Drugs 6, 555-567.
22. Adjei, A. A. (2001) Blocking oncogenic Ras signaling for cancer therapy, J. Natl. Cancer Inst. 93, 1062-1074.
23. Bruckner, S. R., Tammariello, S. P., Kuan, C. Y., Flavell, R. A., Rakic, P., and Estus, S. (2001) JNK3 contributes to c-Jun activation and apoptosis but not oxidative stress in nerve growth factor-deprived sympathetic neurons, J. Neurochem. 78, 298-303.
24. Hirosumi, J., Tuncman, G., Chang, L., Gorgun, C. Z., Uysal, K. T., Maeda, K., Karin, M., and Hotamisligil, G. S. (2002) A central role for JNK in obesity and insulin resistance, Nature 420, 333-336.
25. Waetzig, V., and Herdegen, T. (2005) Context-specific inhibition of JNKs: overcoming the dilemma of protection and damage, Trends Pharmacol. Sci. 26, 455-461.
26. Manning, A. M., and Davis, R. J. (2003) Targeting JNK for therapeutic benefit: from junk to gold? Nat. Rev. Drug Discovery 2, 554-565.
27. Ito, M., Yoshioka, K., Akechi, M., Yamashita, S., Takamatsu, N., Sugiyama, K., Hibi, M., Nakabeppu, Y., Shiba, T., and Yamamoto, K. I. (1999) JSAP1, a novel jun N-terminal protein kinase (JNK)-binding protein that functions as a Scaffold factor in the JNK signaling pathway, Mol. Cell. Biol. 19, 7539-7548.
28. Whitmarsh, A. J., Cavanagh, J., Tournier, C., Yasuda, J., and Davis, R. J. (1998) A mammalian scaffold complex that selectively mediates MAP kinase activation, Science 281, 1671-1674.
29. Yasuda, J., Whitmarsh, A. J., Cavanagh, J., Sharma, M., and Davis, R. J. (1999) The JIP group of mitogen-activated protein kinase scaffold proteins, Mol. Cell. Biol. 19, 7245-7254.
30. Morrison, D. K., and Davis, R. J. (2003) Regulation of MAP kinase signaling modules by scaffold proteins in mammals, Annu. Rev. Cell Dev. Biol. 19, 91-118.
31. Barr, R. K., Kendrick, T. S., and Bogoyevitch, M. A. (2002) Identification of the critical features of a small peptide inhibitor of JNK activity, J. Biol. Chem. 277, 10987-10997.
32. Heo, Y. S., Kim, S. K., Seo, C. I., Kim, Y. K., Sung, B. J., Lee, H. S., Lee, J. I., Park, S. Y., Kim, J. H., Hwang, K. Y., Hyun, Y. L., Jeon, Y. H., Ro, S., Cho, J. M., Lee, T. G., and Yang, C. H. (2004) Structural basis for the selective inhibition of JNK1 by the scaffolding protein JIP1 and SP600125, EMBO J. 23, 2185-2195.
33. Bennett, B. L., Sasaki, D. T., Murray, B. W., O'Leary, E. C., Sakata, S. T., Xu, W., Leisten, J. C., Motiwala, A., Pierce, S., Satoh, Y., Bhagwat, S. S., Manning, A. M., and Anderson, D. W. (2001) SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase, Proc. Natl. Acad. Sci. U.S.A. 98, 13681-13686.
34. Copeland, R. A. (2000) Enzymes: A Practical Introduction to Structure, Mechanism, and Data Analysis, 2nd ed., Wiley & Sons, New York.
35. Palmer, T. (1995) Understanding Enzymes, 4th ed., Prentice Hall, London.
36. Fromm, H. J. (1979) Use of competitive inhibitors to study substrate binding order, Methods Enzymol. 63, 467-486.
37. Khokhlatchev, A., Xu, S., English, J., Wu, P., Schaefer, E., and Cobb, M. H. (1997) Reconstitution of mitogen-activated protein kinase phosphorylation cascades in bacteria. Efficient synthesis of active protein kinases, J. Biol. Chem. 272, 11057-11062.
38. Barr, R. K., Boehm, I., Attwood, P. V., Watt, P. M., and Bogoyevitch, M. A. (2004) The critical features and the mechanism of inhibition of a kinase interaction motif-based peptide inhibitor of JNK, J. Biol. Chem. 279, 36327-36338.
39. Hawkins, J., Zheng, S., Frantz, B., and LoGrasso, P. (2000) p38 map kinase substrate specificity differs greatly for protein and peptide substrates, Arch. Biochem. Biophys. 382, 310-313.
40. Schulman, B. A., Lindstrom, D. L., and Harlow, E. (1998) Substrate recruitment to cyclin-dependent kinase 2 by a multi-purpose docking site on cyclin A, Proc. Natl. Acad. Sci. U.S.A. 95, 10453-10458.
41. Brown, N. R., Noble, M. E., Endicott, J. A., and Johnson, L. N. (1999) The structural basis for specificity of substrate and recruitment peptides for cyclin-dependent kinases, Nat. Cell Biol. 1, 438-443.
42. Sharrocks, A. D., Yang, S. H., and Galanis, A. (2000) Docking domains and substrate-specificity determination for MAP kinases, Trends Biochem. Sci. 25, 448-453.
43. Marangoni, A. G. (2003) Enzyme Kinetics: A Modern Approach, Wiley-Interscience, Hoboken, NJ.
44. Huynh, Q. K., Kishore, N., Mathialagan, S., Donnelly, A. M., and Tripp, C. S. (2002) Kinetic mechanisms of IkappaB-related kinases (IKK) inducible IKK and TBK-1 differ from IKK-1/IKK-2 heterodimer, J. Biol. Chem. 277, 12550-12558.
45. Burke, J. R., Miller, K. R., Wood, M. K., and Meyers, C. A. (1998) The multisubunit IkappaB kinase complex shows random sequential kinetics and is activated by the C-terminal domain of IkappaB alpha, J. Biol. Chem. 273, 12041-12046.
46. Peet, G. W., and Li, J. (1999) IkappaB kinases alpha and beta show a random sequential kinetic mechanism and are inhibited by staurosporine and quercetin, J. Biol. Chem. 274, 32655-32661.
47. Gold, M. H., and Segel, I. H. (1974) Neurospora crassa protein kinase. Purification, properties, and kinetic mechanism, J. Biol. Chem. 249, 2417-2423.
48. Cole, P. A., Burn, P., Takacs, B., and Walsh, C. T. (1994) Evaluation of the catalytic mechanism of recombinant human Csk (C-terminal Src kinase) using nucleotide analogs and viscosity effects, J. Biol. Chem. 269, 30880-30887.
49. Boerner, R. J., Barker, S. C., and Knight, W. B. (1995) Kinetic mechanisms of the forward and reverse pp60c-src tyrosine kinase reactions, Biochemistry 34, 16419-16423.
50. Cook, P. F., Neville, M. E., Jr., Vrana, K. E., Hartl, F. T., and Roskoski, R., Jr. (1982) Adenosine cyclic 3′,5′-monophosphate dependent protein kinase: kinetic mechanism for the bovine skeletal muscle catalytic subunit, Biochemistry 21, 5794-5799.
51. Horiuchi, K. Y., Scherle, P. A., Trzaskos, J. M., and Copeland, R. A. (1998) Competitive inhibition of MAP kinase activation by a peptide representing the alpha C helix of ERK, Biochemistry 37, 8879-8885.
52. Chen, G., Porter, M. D., Bristol, J. R., Fitzgibbon, M. J., and Pazhanisamy, S. (2000) Kinetic mechanism of the p38-alpha MAP kinase: phosphoryl transfer to synthetic peptides, Biochemistry 39, 2079-2087.
53. LoGrasso, P. V., Frantz, B., Rolando, A. M., O'Keefe, S. J., Hermes, J. D., and O'Neill, E. A. (1997) Kinetic mechanism for p38 MAP kinase, Biochemistry 36, 10422-10427.
54. Whitehouse, S., and Walsh, D. A. (1983) Mg X ATP2-dependent interaction of the inhibitor protein of the cAMP-dependent protein kinase with the catalytic subunit, J. Biol. Chem. 258, 3682-3692.
55. Erneux, C., Cohen, S., and Garbers, D. L. (1983) The kinetics of tyrosine phosphorylation by the purified epidermal growth factorreceptor kinase of A-431 cells, J. Biol. Chem. 258, 4137-4142.
56. Posner, I., Engel, M., and Levitzki, A. (1992) Kinetic model of the epidermal growth factor (EGF) receptor tyrosine kinase and a possible mechanism of its activation by EGF, J. Biol. Chem. 267, 20638-20647.