ZAK: A MAP3Kinase that transduces Shiga toxin- and ricin-induced proinflammatory cytokine expression

Cellular Microbiology

Volumn 10, Issue 7, 2008, Pages 1468-1477

  Jandhyala, Dakshina M ^a   Ahluwalia, Amrita ^a   Obrig, Tom ^b   Thorpe, Cheleste M ^a  

^a TUFTS MEDICAL CENTER   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

7 [3 FLUORO 4 AMINOPHENYL[4 (2 PYRIDIN 2 YL 5,6 DIHYDRO 4H PYRROLO[1,2 B]PYRAZOL 3 YL)]]QUINOLINE; CYTOKINE; DHP 2; INTERLEUKIN 8; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; PROTEIN SERINE THREONINE KINASE; RICIN; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; VEROTOXIN 2; ZIPPER STERILE ALPHA MOTIF KINASE; ZIPPER STERILE BETA MOTIF KINASE;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; BACTERIAL INFECTION; CELL VIABILITY; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; ENZYME ACTIVATION; ESCHERICHIA COLI; HUMAN; HUMAN CELL; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; RIBOTOXIC STRESS RESPONSE; UPREGULATION;

AGED; ANIMALS; CELL LINE; CERCOPITHECUS AETHIOPS; CHILD; CYTOKINES; ENZYME ACTIVATION; ENZYME INHIBITORS; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; INTERLEUKIN-8; INTESTINAL MUCOSA; ISOENZYMES; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE SIGNALING SYSTEM; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN KINASES; PYRAZOLES; QUINOLINES; RICIN; RNA, SMALL INTERFERING; SHIGA TOXIN 2; SHIGA-TOXIGENIC ESCHERICHIA COLI; VERO CELLS;

ESCHERICHIA COLI;

EID: 45249123044     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2008.01139.x     Document Type: Article

References (46)

1. Acheson, D.W., Jacewicz, M., Kane, A.V., Donohue-Rolfe, A., and Keusch, G.T. (1993) One step high yield affinity purification of shiga-like toxin II variants and quantitation using enzyme linked immunosorbent assays. Microb Pathog 14: 57-66.
2. Berridge, M.V., and Tan, A.S. (1993) Characterization of the cellular reduction of 3-(4,5-dimethylthiazol-2-yl) -2,5-diphenyltetrazolium bromide (MTT): Subcellular localization, substrate dependence, and involvement of mitochondrial electron transport in MTT reduction. Arch Biochem Biophys 303: 474-482.
3. Bhattacharjee, R.N., Park, K.S., Uematsu, S., Okada, K., Hoshino, K., Takeda, K., et al. (2005) Escherichia coli verotoxin 1 mediates apoptosis in human HCT116 colon cancer cells by inducing overexpression of the GADD family of genes and S phase arrest. FEBS Lett 579: 6604-6610.
4. Bielaszewska, M., and Karch, H. (2005) Consequences of enterohaemorrhagic Escherichia coli infection for the vascular endothelium. Thromb Haemost 94: 312-318.
5. Bloem, L.J., Pickard, T.R., Acton, S., Donoghue, M., Beavis, R.C., Knierman, M.D., and Wang, X. (2001) Tissue distribution and functional expression of a cDNA encoding a novel mixed lineage kinase. J Mol Cell Cardiol 33: 1739-1750.
6. Cherla, R.P., Lee, S.Y., Mees, P.L., and Tesh, V.L. (2006) Shiga toxin 1-induced cytokine production is mediated by MAP kinase pathways and translation initiation factor eIF4E in the macrophage-like THP-1 cell line. J Leukoc Biol 79: 397-407.
7. Christe, M., Jin, N., Wang, X., Gould, K.E., Iversen, P.W., Yu, X., et al. (2004) Transgenic mice with cardiac-specific over-expression of MLK7 have increased mortality when exposed to chronic beta-adrenergic stimulation. J Mol Cell Cardiol 37: 705-715.
8. Church, G.M., and Gilbert, W. (1984) Genomic sequencing. Proc Natl Acad Sci USA 81: 1991-1995.
9. Dowling, T.C., Chavaillaz, P.A., Young, D.G., Melton-Celsa, A., O'Brien, A., Thuning-Roberson, C., et al. (2005) Phase 1 safety and pharmacokinetic study of chimeric murine-human monoclonal antibody c alpha Stx2 administered intravenously to healthy adult volunteers. Antimicrob Agents Chemother 49: 1808-1812.
10. Endo, Y., Mitsui, K., Motizuki, M., and Tsurugi, K. (1987) The mechanism of action of ricin and related toxic lectins on eukaryotic ribosomes. The site and the characteristics of the modification in 28S ribosomal RNA caused by the toxins. J Biol Chem 262: 5908-5912.
11. Endo, Y., Tsurugi, K., Yutsudo, T., Takeda, Y., Ogasawara, T., and Igarashi, K. (1988) Site of action of a Vero toxin (VT2) from Escherichia coli O157: H7 and of Shiga toxin on eukaryotic ribosomes. RNA N-glycosidase activity of the toxins. Eur J Biochem 171: 45-50.
12. Grollman, A.P. (1967) Inhibitors of protein biosynthesis. II. Mode of action of anisomycin. J Biol Chem 242: 3226-3233.
13. Hauck, C.R., Meyer, T.F., Lang, F., and Gulbins, E. (1998) CD66-mediated phagocytosis of Opa52 Neisseria gonorrhoeae requires a Src-like tyrosine kinase- and Rac1-dependent signalling pathway. Embo J 17: 443-454.
14. Heyderman, R.S., Soriani, M., and Hirst, T.R. (2001) Is immune cell activation the missing link in the pathogenesis of post-diarrhoeal HUS? Trends Microbiol 9: 262-266.
15. Higuchi, S., Tamura, T., and Oda, T. (2003) Cross-talk between the pathways leading to the induction of apoptosis and the secretion of tumor necrosis factor-alpha in ricin-treated RAW 264.7 cells. J Biochem (Tokyo) 134: 927-933.
16. Huang, Q., Yang, J., Lin, Y., Walker, C., Cheng, J., Liu, Z.G., and Su, B. (2004) Differential regulation of interleukin 1 receptor and Toll-like receptor signaling by MEKK3. Nat Immunol 5: 98-103.
17. Hurley, B.P., Thorpe, C.M., and Acheson, D.W. (2001) Shiga toxin translocation across intestinal epithelial cells is enhanced by neutrophil transmigration. Infect Immun 69: 6148-6155.
18. Igarashi, K., Ogasawara, T., Ito, K., Yutsudo T., and Takeda Y. (1987) Inhibition of elongaton factor 1-dependent aminoacyl-tRNA binding to ribosomes by Shiga-like toxin I (VT1) from Escherichia coli O157: H7 and by Shiga toxin. FEMS Microbiol Lett 44: 91-94.
19. Iordanov, M.S., Pribnow, D., Magun, J.L., Dinh, T.H., Pearson, J.A., Chen, S.L., and Magun, B.E. (1997) Ribotoxic stress response: Activation of the stress-activated protein kinase JNK1 by inhibitors of the peptidyl transferase reaction and by sequence-specific RNA damage to the alpha-sarcin/ricin loop in the 28S rRNA. Mol Cell Biol 17: 3373-3381.
20. Johnson, G.L., Dohlman, H.G., and Graves, L.M. (2005) MAPK kinase kinases (MKKKs) as a target class for small-molecule inhibition to modulate signaling networks and gene expression. Curr Opin Chem Biol 9: 325-331.
21. Keepers, T.R., Psotka, M.A., Gross, L.K., and Obrig, T.G. (2006) A murine model of HUS: Shiga toxin with lipopolysaccharide mimics the renal damage and physiologic response of human disease. J Am Soc Nephrol 17: 3404-3414.
22. Lauvrak, S.U., Walchli, S., Iversen, T.G., Slagsvold, H.H., Torgersen, M.L., Spilsberg, B., and Sandvig, K. (2006) Shiga toxin regulates its entry in a Syk-dependent manner. Mol Biol Cell 17: 1096-1109.
23. Lee, S.Y., Cherla, R.P., Caliskan, I., and Tesh, V.L. (2005) Shiga toxin 1 induces apoptosis in the human myelogenous leukemia cell line THP-1 by a caspase-8-dependent, tumor necrosis factor receptor-independent mechanism. Infect Immun 73: 5115-5126.
24. Mocsai, A., Jakus, Z., Vantus, T., Berton, G., Lowell, C.A., and Ligeti, E. (2000) Kinase pathways in chemoattractant-induced degranulation of neutrophils: The role of p38 mitogen-activated protein kinase activated by Src family kinases. J Immunol 164: 4321-4331.
25. Murata, K., Higuchi, T., Takada, K., Oida, K., Horie, S., and Ishii, H. (2006) Verotoxin-1 stimulation of macrophage-like THP-1 cells up-regulates tissue factor expression through activation of c-Yes tyrosine kinase: Possible signal transduction in tissue factor up-regulation. Biochim Biophys Acta 1762: 835-843.
26. Nilsson, L., and Nygard, O. (1986) The mechanism of the protein-synthesis elongation cycle in eukaryotes. Effect of ricin on the ribosomal interaction with elongation factors. Eur J Biochem 161: 111-117.
27. Ninomiya-Tsuji, J., Kishimoto, K., Hiyama, A., Inoue, J., Cao, Z., and Matsumoto, K. (1999) The kinase TAK1 can activate the NIK-I kappaB as well as the MAP kinase cascade in the IL-1 signalling pathway. Nature 398: 252-256.
28. Obrig, T.G., Moran, T.P., and Brown, J.E. (1987) The mode of action of Shiga toxin on peptide elongation of eukaryotic protein synthesis. Biochem J 244: 287-294.
29. Pestka, S. (1971) Inhibitors of ribosome functions. Annu Rev Microbiol 25: 487-562.
30. Rasband, W.S. (1997-2007) ImageJ. Bethesda, MD: US National Institutes of Health. http://rsb.info.nih.gov/ij/index.html
31. Ritchie, J.M., Thorpe, C.M., Rogers, A.B., and Waldor, M.K. (2003) Critical roles for stx2, eae, and tir in enterohemorrhagic Escherichia coli -induced diarrhea and intestinal inflammation in infant rabbits. Infect Immun 71: 7129-7139.
32. Saenz, J.B., Doggett, T.A., and Haslam, D.B. (2007) Identification and characterization of small molecules that inhibit intracellular toxin transport. Infect Immun 75: 4552-4561.
33. Sato, S., Sanjo, H., Takeda, K., Ninomiya-Tsuji, J., Yamamoto, M., Kawai, T., et al. (2005) Essential function for the kinase TAK1 in innate and adaptive immune responses. Nat Immunol 6: 1087-1095.
34. Shifrin, V.I., and Anderson, P. (1999) Trichothecene mycotoxins trigger a ribotoxic stress response that activates c-Jun N-terminal kinase and p38 mitogen-activated protein kinase and induces apoptosis. J Biol Chem 274: 13985-13992.
35. Smith, W.E., Kane, A.V., Campbell, S.T., Acheson, D.W., Cochran, B.H., and Thorpe, C.M. (2003) Shiga toxin 1 triggers a ribotoxic stress response leading to p38 and JNK activation and induction of apoptosis in intestinal epithelial cells. Infect Immun 71: 1497-1504.
36. Suntres, Z.E., Stone, W.L., and Smith, M.G. (2005) Ricin-induced toxicity: The role of oxidative stress. J Med CBR Defic 3: 1-21.
37. Thorpe, C.M., Hurley, B.P., Lincicome, L.L., Jacewicz, M.S., Keusch, G.T., and Acheson, D.W. (1999) Shiga toxins stimulate secretion of interleukin-8 from intestinal epithelial cells. Infect Immun 67: 5985-5993.
38. Thorpe, C.M., Ritchie, J.M., and Acheson, D.W.K., eds. (2002) Enterohemorrhagic and other Shiga toxin-producing Eschericia coli. In Donnenberg, M.S. (ed.). Escherichia coli: Virulance mechanisms of a versatile pathogen. San Diego, CA: Academic Press, pp. 119-154.
39. Tosti, E., Waldbaum, L., Warshaw, G., Gross, E.A., and Ruggieri, R. (2004) The stress kinase MRK contributes to regulation of DNA damage checkpoints through a p38gamma-independent pathway. J Biol Chem 279: 47652-47660.
40. Tzipori, S., Sheoran, A., Akiyoshi, D., Donohue-Rolfe, A., and Trachtman, H. (2004) Antibody therapy in the management of shiga toxin-induced hemolytic uremic syndrome. Clin Microbiol Rev 17: 926-941.
41. Vareille, M., de Sablet, T., Hindre, T., Martin, C., and Gobert, A.P. (2007) Nitric oxide inhibits Shiga-toxin synthesis by enterohemorrhagic Escherichia coli. Proc Natl Acad Sci USA 104: 10199-10204.
42. Wang, X., Mader, M.M., Toth, J.E., Yu, X., Jin, N., Campbell, R.M., et al. (2005) Complete inhibition of anisomycin and UV radiation but not cytokine induced JNK and p38 activation by an aryl-substituted dihydropyrrolopyrazole quinoline and mixed lineage kinase 7 small interfering RNA. J Biol Chem 280: 19298-19305.
43. Wool, I.G., Gluck, A., and Endo, Y. (1992) Ribotoxin recognition of ribosomal RNA and a proposal for the mechanism of translocation. Trends Biochem Sci 17: 266-269.
44. Yoder, J.M., Aslam, R.U., and Mantis, N.J. (2007) Evidence for widespread epithelial damage and coincident production of monocyte chemotactic protein 1 in a murine model of intestinal ricin intoxication. Infect Immun 75: 1745-1750.
45. Zhou, H.R., Lau, A.S., and Pestka, J.J. (2003) Role of double-stranded RNA-activated protein kinase R (PKR) in deoxynivalenol-induced ribotoxic stress response. Toxicol Sci 74: 335-344.
46. Zhou, H.R., Jia, Q., and Pestka, J.J. (2005) Ribotoxic stress response to the trichothecene deoxynivalenol in the macrophage involves the SRC family kinase Hck. Toxicol Sci 85: 916-926.