Anthrax lethal toxin increases superoxide production in murine neutrophils via differential effects on MAPK signaling pathways

Journal of Immunology

Volumn 180, Issue 6, 2008, Pages 4139-4147

  Xu, Lixin ^a   Fang, Hui ^a   Frucht, David M ^a  

^a CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRAX TOXIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE 4; MITOGEN ACTIVATED PROTEIN KINASE 6; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE P38; STRESS ACTIVATED PROTEIN KINASE; SUPEROXIDE; AUTACOID; BACTERIAL ANTIGEN; BACTERIAL TOXIN; PROTEIN KINASE INHIBITOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTHRAX; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DOSE RESPONSE; DRUG INHIBITION; ENZYME BINDING; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NEUTROPHIL COUNT; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELL CULTURE; COMPARATIVE STUDY; DRUG ANTAGONISM; DRUG DELIVERY SYSTEM; ENZYMOLOGY; IMMUNOLOGY; METABOLISM; NEUTROPHIL; PATHOLOGY; PHYSIOLOGY; UPREGULATION;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL TOXINS; CELLS, CULTURED; DRUG DELIVERY SYSTEMS; INFLAMMATION MEDIATORS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEUTROPHILS; PROTEIN KINASE INHIBITORS; SUPEROXIDES; UP-REGULATION;

EID: 44849106935     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.6.4139     Document Type: Article

References (50)

1. Turnbull, P. C. 2002. Introduction: anthrax history, disease, and ecology. Curr. Top. Microbiol. Immunol. 271: 1-19.
2. Spencer, R. C. 2003. Bacillus anthracis. J. Clin. Pathol. 56: 182-187.
3. Abrami, L., N. Reig, and F. G. van der Goot. 2005. Anthrax toxin: the long and winding road that leads to the kill. Trends Microbiol. 13: 72-78.
4. Collier, R. J., and J. A. Young. 2003. Anthrax toxin. Annu. Rev. Cell. Dev. Biol. 19: 45-70.
5. Xu, L., and D. M. Frucht. 2007. Bacillus anthracis: a multi-faceted role for anthrax lethal toxin in thwarting host immune defenses. Int J. Biochem. Cell Biol. 39: 20-24.
6. Beall, F. A., M. J. Taylor, and C. B. Thorne. 1962. Rapid lethal effect in rats of a third component found upon fractionating the toxin of Bacillus anthracis. J. Bacteriol. 83: 1274-1280.
7. Beall, F. A., and F. G. Dalldorf. 1966. The pathogenesis of the lethal effect of anthrax toxin in the rat. J. Infect. Dis. 116: 377-389.
8. + T cells. J. Immunol. 174: 4966-4971.
9. Cordoba-Rodriguez, R., H. Fang, C. S. Lankford, and D. M. Frucht. 2004. Anthrax lethal toxin rapidly activates caspase-1/ICE and induces extracellular release of interleukin (IL)-1β and IL-18. J. Biol. Chem. 279: 20563-20566.
10. Fang, H., L. Xu, T. Y. Chen, J. M. Cyr, and D. M. Frucht. 2006. Anthrax lethal toxin has direct and potent inhibitory effects on B cell proliferation and immunoglobulin production. J. Immunol. 176: 6155-6161.
11. Paccani, S. R., F. Tonello, R. Ghittoni, M. Natale, L. Muraro, M. M. D'Elios, W. J. Tang, C. Montecucco, and C. T. Baldari. 2005. Anthrax toxins suppress T lymphocyte activation by disrupting antigen receptor signaling. J. Exp. Med. 201: 325-331.
12. Comer, J. E., A. K. Chopra, J. W. Peterson, and R. Konig. 2005. Direct inhibition of T-lymphocyte activation by anthrax toxins in vivo. Infect. Immun. 73: 8275-8281.
13. Warfel, J. M., A. D. Steele, and F. D'Agnillo. 2005. Anthrax lethal toxin induces endothelial barrier dysfunction. Am. J. Pathol. 166: 1871-1881.
14. Kirby, J. E. 2004. Anthrax lethal toxin induces human endothelial cell apoptosis. Infect. Immun. 72: 430-439.
15. Pellizzari, R., C. Guidi-Rontani, G. Vitale, M. Mock, and C. Montecucco. 1999. Anthrax lethal factor cleaves MKK3 in macrophages and inhibits the LPS/IFNγ-induced release of NO and TNFα. FEBS Lett. 462: 199-204.
16. Agrawal, A., J. Lingappa, S. H. Leppla, S. Agrawal, A. Jabbar, C. Quinn, and B. Pulendran. 2003. Impairment of dendritic cells and adaptive immunity by anthrax lethal toxin. Nature 424: 329-334.
17. Moayeri, M., D. Haines, H. A. Young, and S. H. Leppla. 2003. Bacillus anthracis lethal toxin induces TNF-α-independent hypoxia-mediated toxicity in mice. J. Clin. Invest. 112: 670-682.
18. Boyden, E. D., and W. F. Dietrich. 2006. Nalp1b controls mouse macrophage susceptibility to anthrax lethal toxin. Nat. Genet. 38: 240-244.
19. Moayeri, M., and S. H. Leppla. 2004. The roles of anthrax toxin in pathogenesis. Curr. Opin. Microbiol. 7: 19-24.
20. Jaeschke, H., and T. Hasegawa. 2006. Role of neutrophils in acute inflammatory liver injury. Liver Int. 26: 912-919.
21. Moraes, T. J., J. H. Zurawska, and G. P. Downey. 2006. Neutrophil granule contents in the pathogenesis of lung injury. Curr. Opin. Hematol. 13: 21-27.
22. O'Brien, J., A. Friedlander, T. Dreier, J. Ezzell, and S. Leppla. 1985. Effects of anthrax toxin components on human neutrophils. Infect. Immun. 47: 306-310.
23. Wade, B. H., G. G. Wright, E. L. Hewlett, S. H. Leppla, and G. L. Mandell. 1985. Anthrax toxin components stimulate chemotaxis of human polymorphonuclear neutrophils. Proc. Soc. Exp. Biol. Med. 179: 159-162.
24. Wright, G. G., and G. L. Mandell. 1986. Anthrax toxin blocks priming of neutrophils by lipopolysaccharide and by muramyl dipeptide. J. Exp. Med. 164: 1700-1709.
25. Wu, A. G., D. Alibek, Y. L. Li, C. Bradburne, C. L. Bailey, and K. Alibek. 2003. Anthrax toxin induces hemolysis: an indirect effect through polymorphonuclear cells. J. Infect. Dis. 188: 1138-1141.
26. During, R. L., W. Li, B. Hao, J. M. Koenig, D. S. Stephens, C. P. Quinn, and F. S. Southwick. 2005. Anthrax lethal toxin paralyzes neutrophil actin-based motility. J. Infect. Dis. 192: 837-845.
27. During, R. L., B. G. Gibson, W. Li, E. A. Bishai, G. S. Sidhu, J. Landry, and F. S. Southwick. 2007. Anthrax lethal toxin paralyzes actin-based motility by blocking Hsp27 phosphorylation. EMBO J. 26: 2240-2250.
28. Crawford, M. A., C. V. Aylott, R. W. Bourdeau, and G. M. Bokoch. 2006. Bacillus anthracis toxins inhibit human neutrophil NADPH oxidase activity. J. Immunol. 176: 7557-7565.
29. Kim, C., N. Gajendran, H. W. Mittrucker, M. Weiwad, Y. H. Song, R. Hurwitz, M. Wilmanns, G. Fischer, and S. H. Kaufmann. 2005. Human α-defensins neutralize anthrax lethal toxin and protect against its fatal consequences. Proc. Natl. Acad. Sci. USA 102: 4830-4835.
30. Eisenhauer, P. B., and R. I. Lehrer. 1992. Mouse neutrophils lack defensins. Infect. Immun. 60: 3446-3447.
31. Park, J. M., F. R. Greten, Z. W. Li, and M. Karin. 2002. Macrophage apoptosis by anthrax lethal factor through p38 MAP kinase inhibition. Science 297: 2048-2051.
32. Duesbery, N. S., C. P. Webb, S. H. Leppla, V. M. Gordon, K. R. Klimpel, T. D. Copeland, N. G. Ahn, M. K. Oskarsson, K. Fukasawa, K. D. Paull, and G. F. Vande Woude. 1998. Proteolytic inactivation of MAP-kinase-kinase by anthrax lethal factor. Science 280: 734-737.
33. Vitale, G., L. Bernardi, G. Napolitani, M. Mock, and C. Montecucco. 2000. Susceptibility of mitogen-activated protein kinase kinase family members to proteolysis by anthrax lethal factor. Biochem. J. 352: 739-745.
34. Bardwell, A. J., M. Abdollahi, and L. Bardwell. 2004. Anthrax lethal factor-cleavage products of MAPK (mitogen-activated protein kinase) kinases exhibit reduced binding to their cognate MAPKs. Biochem. J. 378: 569-577.
35. Dong, C., R. J. Davis, and R. A. Flavell. 2002. MAP kinases in the immune response. Annu. Rev. Immunol. 20: 55-72.
36. Wong, C. K., P. F. Cheung, W. K. Ip, and C. W. Lam. 2007. Intracellular signaling mechanisms regulating Toll-like receptor-mediated activation of eosinophils. Am. J. Respir. Cell Mol. Biol. 37: 85-96.
37. Sakamoto, K., F. Kuribayashi, M. Nakamura, and K. Takeshige. 2006. Involvement of p38 MAP kinase in not only activation of the phagocyte NADPH oxidase induced by formyl-methionyl-leucyl-phenylalanine but also determination of the extent of the activity. J. Biochem. 140: 739-745.
38. Watanabe, I., M. Ichiki, A. Shiratsuchi, and Y. Nakanishi. 2007. TLR2-mediated survival of Staphylococcus aureus in macrophages: a novel bacterial strategy against host innate immunity. J. Immunol. 178: 4917-4925.
39. Ventura, J. J., P. Cogswell, R. A. Flavell, A. S. Baldwin, Jr., and R. J. Davis. 2004. JNK potentiates TNF-stimulated necrosis by increasing the production of cytotoxic reactive oxygen species. Genes Dev. 18: 2905-2915.
40. Favata, M. F., K. Y. Horiuchi, E. J. Manos, A. J. Daulerio, D. A. Stradley, W. S. Feeser, D. E. Van Dyk, W. J. Pitts, R. A. Earl, F. Hobbs, et al. 1998. Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J. Biol. Chem. 273: 18623-18632.
41. Abalakin, V. A., E. G. Sirina, and T. D. Cherkasova. 1990. The effect of lethal anthrax toxin on the functional activity of peritoneal mononuclear phagocytes and polymorphonuclear neutrophils in mice. Zh. Mikrobiol. Epidemiol. Immunobiol. 2: 62-67.
42. Herwig, S., Q. Su, W. Zhang, Y. Ma, and P. Tempst. 1996. Distinct temporal patterns of defensin mRNA regulation during drug-induced differentiation of human myeloid leukemia cells. Blood 87: 350-364.
43. Nakajima, A., S. Komazawa-Sakon, M. Takekawa, T. Sasazuki, W. C. Yeh, H. Yagita, K. Okumura, and H. Nakano. 2006. An antiapoptotic protein, c-FLIPL, directly binds to MKK7 and inhibits the JNK pathway. EMBO J. 25: 5549-5559.
44. Fleming, Y., C. G. Armstrong, N. Morrice, A. Paterson, M. Goedert, and P. Cohen. 2000. Synergistic activation of stress-activated protein kinase 1/c-Jun N-terminal kinase (SAPK1/JNK) isoforms by mitogen-activated protein kinase kinase 4 (MKK4) and MKK7. Biochem. J. 352: 145-154.
45. Davis, R. J. 1999. Signal transduction by the c-Jun N-terminal kinase. Biochem. Soc. Symp. 64: 1-12.
46. Steichen, C., P. Chen, J. F. Kearney, and C. L. Turnbough, Jr. 2003. Identification of the immunodominant protein and other proteins of the Bacillus anthracis exosporium. J. Bacteriol. 185: 1903-1910.
47. Baillie, L., S. Hibbs, P. Tsai, G. L. Cao, and G. M. Rosen. 2005. Role of superoxide in the germination of Bacillus anthracis endospores. FEMS Microb. Lett. 245: 33-38.
48. Flora, S. J. 2007. Role of free radicals and antioxidants in health and disease. Cell. Mol. Biol. 53: 1-2.
49. Jackson, S. H., J. I. Gallin, and S. M. Holland. 1995. The p47phox mouse knockout model of chronic granulomatous disease. J. Exp. Med. 182: 751-758.
50. Cui, X., M. Moayeri, Y. Li, X. Li, M. Haley, Y. Fitz, R. Correa-Araujo, S. M. Banks, S. H. Leppla, and P. Q. Eichacker. 2004. Lethality during continuous anthrax lethal toxin infusion is associated with circulatory shock but not inflammatory cytokine or nitric oxide release in rats. Am. J. Physiol. 286: R699-R709.