Anthrax lethal factor-cleavage products of MAPK (mitogen-activated protein kinase) kinases exhibit reduced binding to their cognate MAPKs

Biochemical Journal

Volumn 378, Issue 2, 2004, Pages 569-577

  Bardwell, A Jane ^a   Abdollahi, Mahsa ^a   Bardwell, Lee ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Anthrax lethal factor protease; Docking site; MAPK kinase (MKK); MAPK ERK kinase (MEK); Mitogen activated protein kinase (MAPK); Molecular pathogenesis

Indexed keywords

ANTIGENS; CELLS; ENZYME INHIBITION; SUBSTRATES; TOXICITY;

CELL SURFACE RECEPTORS; TOXINS;

ENZYMES;

ANTHRAX TOXIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; MITOGEN ACTIVATED PROTEIN KINASE KINASE 6; MITOGEN ACTIVATED PROTEIN KINASE KINASE 7; UNCLASSIFIED DRUG;

ANTHRAX; ARTICLE; CAUSE OF DEATH; ENZYME BINDING; ENZYME DEGRADATION; ENZYME SUBSTRATE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL TOXINS; BINDING SITES; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE KINASE 1; MAP KINASE KINASE 2; MAP KINASE KINASE 3; MAP KINASE KINASE 4; MAP KINASE KINASE 6; MAP KINASE KINASE 7; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MITOGEN-ACTIVATED PROTEIN KINASES; MOLECULAR SEQUENCE DATA; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN-TYROSINE KINASES; RATS; SEQUENCE ALIGNMENT;

ANTHRAX;

EID: 1642349448     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20031382     Document Type: Article

References (45)

1. Dixon, T. C., Meselson, M., Guillemin, J. and Hanna, P. C. (1999) Anthrax. N. Engl. J. Med. 341, 815-826
2. Friedlander, A. M. (2001) Tackling anthrax. Nature (London) 414, 160-161
3. Ezzell, J. W., Ivins, B. E. and Leppla, S. H. (1984) Immunoelectrophoretic analysis, toxicity, and kinetics of in vitro production of the protective antigen and lethal factor components of Bacillus anthracis toxin. Infect. Immun. 45, 761-767
4. Agrawal, A., Lingappa, J., Leppla, S. H., Agrawal, S., Jabbar, A., Quinn, C. and Pulendran, B. (2003) Impairment of dendritic cells and adaptive immunity by anthrax lethal toxin. Nature (London) 424, 329-334
5. Pellizzari, R., Guidi-Rontani, C., Vitale, G., Mock, M. and Montecucco, C. (1999) Anthrax lethal factor cleaves MKK3 in macrophages and inhibits the LPS/IFNγ-induced release of NO and TNFα. FEBS Lett. 462, 199-204
6. Park, J. M., Greten, F. R., Li, Z. W. and Karin, M. (2002) Macrophage apoptosis by anthrax lethal factor through p38 MAP kinase inhibition. Science 297, 2048-2051
7. Popov, S. G., Villasmil, R., Bernardi, J., Grene, E., Cardwell, J., Wu, A., Alibek, D., Bailey, C. and Alibek, K. (2002) Lethal toxin of Bacillus anthracis causes apoptosis of macrophages. Biochem. Biophys. Res. Commun. 293, 349-355
8. Popov, S. G., Villasmil, R., Bernardi, J., Grene, E., Cardwell, J., Popova, T., Wu, A., Alibek, D., Bailey, C. and Alibek, K. (2002) Effect of Bacillus anthracis lethal toxin on human peripheral blood mononuclear cells. FEBS Lett. 527, 211-215
9. Bradley, K. A., Mogridge, J., Mourez, M., Collier, R. J. and Young, J. A. (2001) Identification of the cellular receptor for anthrax toxin. Nature (London) 414, 225-229
10. Kochi, S. K., Schiavo, G., Mock, M. and Montecucco, C. (1994) Zinc content of the Bacillus anthracis lethal factor. FEMS Microbiol. Lett. 124, 343-348
11. Klimpel, K. R., Arora, N. and Leppla, S. H. (1994) Anthrax toxin lethal factor contains a zinc metalloprotease consensus sequence which is required for lethal toxin activity. Mol. Microbiol. 13, 1093-1100
12. Bragg, T. S. and Robertson, D. L. (1989) Nucleotide sequence and analysis of the lethal factor gene (lef) from Bacillus anthracis. Gene 81, 45-54
13. Vitale, G., Bernardi, L., Napolitani, G., Mock, M. and Montecucco, C. (2000) Susceptibility of mitogen-activated protein kinase kinase family members to proteolysis by anthrax lethal factor. Biochem. J. 352, 739-745
14. Vitale, G., Pellizzari, R., Recchi, C., Napolitani, G., Mock, M. and Montecucco, C. (1998) Anthrax lethal factor cleaves the N-terminus of MAPKKs and induces tyrosine/threonine phosphorylation of MAPKs in cultured macrophages. Biochem. Biophys. Res. Commun. 248, 706-711
15. Duesbery, N. S., Webb, C. P., Leppla, S. H., Gordon, V. M., Klimpel, K. R., Copeland, T. D., Ahn, N. G., Oskarsson, M. K., Fukasawa, K., Paull, K. D. and Vande Woude, G. F. (1998) Proteolytic inactivation of MAP-kinase-kinase by anthrax lethal factor. Science 280, 734-737
16. Dong, C., Davis, R. J. and Flavell, R. A. (2002) MAP kinases in the immune response. Annu. Rev. Immunol. 20, 55-72
17. Johnson, G. L. and Lapadat, R. (2002) Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science 298, 1911-1912
18. Chang, L and Karin, M. (2001) Mammalian MAP kinase signalling cascades. Nature (London) 410, 37-40
19. Pannifer, A. D., Wong, T. Y., Schwarzenbacher, R., Renatus, M., Petosa, C., Bienkowska, J., Lacy, D. B., Collier, R. J., Park, S., Leppia, S. H. et al. (2001) Crystal structure of the anthrax lethal factor. Nature (London) 414, 229-233
20. Xu, B., Stippec, S., Robinson, F. L. and Cobb, M. H. (2001) Hydrophobic as well as charged residues in both MEK1 and ERK2 are important for their proper docking. J. Biol. Chem. 276, 26509-26515
21. Bardwell, A. J., Flatauer, L. J., Matsukuma, K., Thorner, J. and Bardwell, L. (2001) A conserved docking site in MEKs mediates high-affinity binding to MAP kinases and cooperates with a scaffold protein to enhance signal transmission. J. Biol. Chem. 276, 10374-10385
22. Enslen, H., Brancho, D. M. and Davis, R. J. (2000) Molecular determinants that mediate selective activation of p38 MAP kinase isoforms. EMBO J. 19, 1301-1311
23. Ho, D. T., Bardwell, A. J., Abdollahi, M. and Bardwell, L. (2003) A docking site in MKK4 rrediates high affinity binding to JNK MAPKs and competes with similar docking sites in JNKsubstrates. J. Biol. Chem. 278, 32662-32672
24. Bardwell, A. J., Abdollahi, M. and Bardwell, L. (2003) Docking sites on mitogen-activated protein kinase (MAPK) kinases, MAPK phosphatases and the Elk-1 transcription factor compete for MAPK binding and are crucial for enzymic activity. Biochem. J. 370, 1077-1085
25. Chopra, A. P., Boone, S. A., Liang, X. and Duesbery, N. S. (2003) Anthrax lethal factor proteolysis and inactivation of MAPK kinase. J. Biol. Chem. 278, 9402-9406
26. Duesbery, N. S., Resau, J., Webb, C. P., Koochekpour, S., Koo, H. M., Leppla, S. H. and Vande Woude, G. F. (2001) Suppression of ras-mediated transformation and inhibition of tu nor growth and angiogenesis by anthrax lethal factor, a proteolytic inhibitor of multiple MEK pathways. Proc. Natl. Acad. Sci. U.S.A. 98, 4089-4094
27. Koo, H. M., VanBrocklin, M., McWilliams, M. J., Leppla, S. H., Duesbery, N. S. and Woude, G. F. (2002) Apoptosis and melanogenesis in human melanoma cells induced by anthrax lethal factor inactivation of mitogen-activated protein kinase kinase. Proc. Natl. Acad. Sci. U.S.A. 99, 3052-3057
28. Liu, S., Netzel-Arnett, S., Birkedal-Hansen, H. and Leppla, S. H. (2000) Tumor cell-selective cytotoxicity of matrix metalloproteinase-activated anthrax toxin. Cancer Res. 60, 6061-6067
29. Liu, S., Schubert, R. L., Bugge, T. H. and Leppla, S. H. (2003) Anthrax toxin: structures, functions and tumour targeting. Expert Opin. Biol. Ther. 3, 843-853
30. Zheng, C.-F. and Guan, K.-L. (1993) Properties of MEKs, the kinases that phosphorylate and activate the extracellular signal-regulated kinases. J. Biol. Chem. 268, 23933-23939
31. Lennon, G., Auffray, C., Polymeropoulos, M. and Soares, M. B. (1996) The I.M.A.G.E. consortium: an integrated molecular analysis of genomes and their expression. Genomics 33, 151-152
32. Charest, D. L., Mordret, G., Harder, K. W., Jirik, F. and Pelech, S. L. (1993) Molecular cloning, expression, and characterization of the human mitogen-activated protein kinase p44erk1. Mol. Cell. Biol. 13, 4679-4690
33. Bardwell, L., Cook, J. G., Chang, E. C., Cairns, B. R. and Thorner, J. (1996) Signaling in the yeast pheromone response pathway: specific and high-affinity interaction of the mitogen-activated protein (MAP) kinases Kss1 and Fus3 with the upstream MAP kinase kinase Ste7. Mol. Cell. Biol. 16, 3637-3650
34. 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
35. Chang, C. I., Xu, B., Akella, R., Cobb, M. and Goldsmith, E. J. (2002) Crystal structure of MAP kinase p38 complexed to the docking sites on its nuclear substrate MEF2A and activator MKK3b. Mol. Cell 9, 1241-1249
36. Guidi-Rontani, C. (2002) The alveolar macrophage: the Trojan horse of Bacillus anthracis. Trends Microbiol. 10, 405-409
37. Hanna, P. C. and Ireland, J. A. (1999) Understanding Bacillus anthracis pathogenesis. Trends Microbiol. 7, 180-182
38. Struhl, K. (1991) Reverse biochemistry: methods and applications for synthesizing yeast proteins in vitro. Methods Enzymol. 194, 520-535
39. Hale, K. K., Trollinger, D., Rihanek, M. and Manthey, C. L. (1999) Differential expression and activation of p38 mitogen-activated protein kinase alpha, beta, gamma, and delta in inflammatory cell lineages. J. Immunol. 162, 4246-4252
40. Davis, R. J. (2000) Signal transduction by the JNK group of MAP kinases. Cell 103, 239-252
41. Tournier, C., Whitmarsh, A. J., Cavanagh, J., Barrett, T. and Davis, R. J. (1999) The MKK7 gene encodes a group of c-Jun NH2-terminal kinase kinases. Mol. Cell. Biol. 19, 1569-1581
42. Xia, Y., Wu, Z., Su, B., Murray, B. and Karin, M. (1998) JNKK1 organizes a MAP kinase module through specific and sequential interactions with upstream and downstream components mediated by its amino-terminal extension. Genes Dev. 12, 3369-3381
43. Manning, G., Whyte, D. B., Martinez, R., Hunter, T. and Sudarsanam, S. (2002) The protein kinase complement of the human genome. Science 298, 1912-1934
44. Enslen, H. and Davis, R. J. (2001) Regulation of MAP kinases by docking domains. Biol. Cell 93, 5-14
45. 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