Contribution of lethal toxin and edema toxin to the pathogenesis of anthrax meningitis

Infection and Immunity

Volumn 79, Issue 7, 2011, Pages 2510-2518

  Ebrahimi, Celia M ^a   Sheen, Tamsin R ^a   Renken, Christian W ^b   Gottlieb, Roberta A ^a,c   Doran, Kelly S ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

^b Applied BioPhysics Inc   (United States)

^c SAN DIEGO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRAX TOXIN; EDEMA TOXIN; LETHAL TOXIN; PROTEIN ZO1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGY; BACILLUS ANTHRACIS; BACTERIAL LOAD; BLOOD BRAIN BARRIER; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; HOST CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; MENINGITIS; MORTALITY; MOUSE; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SPECIES INVASION;

ANIMALS; ANTHRAX; ANTIGENS, BACTERIAL; AUTOPHAGY; BACILLUS ANTHRACIS; BACTERIAL TOXINS; BLOOD-BRAIN BARRIER; BRAIN; ENDOTHELIAL CELLS; HUMANS; MEMBRANE PROTEINS; MENINGITIS, BACTERIAL; MICE; MICROVESSELS; MUTATION; PHOSPHOPROTEINS; TIGHT JUNCTIONS;

EID: 79959426377     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00006-11     Document Type: Article

References (61)

1. Abramova, F. A., L. M. Grinberg, O. V. Yampolskaya, and D. H. Walker. 1993. Pathology of inhalational anthrax in 42 cases from the Sverdlovsk outbreak of 1979. Proc. Natl. Acad. Sci. U. S. A. 90:2291-2294.
2. Agrawal, A., et al. 2003. Impairment of dendritic cells and adaptive immunity by anthrax lethal toxin. Nature 424:329-334.
3. Ballabh, P., A. Braun, and M. Nedergaard. 2004. The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiol. Dis. 16:1-13.
4. Bardwell, A. J., M. Abdollahi, and L. Bardwell. 2004. Anthrax lethal factorcleavage products of MAPK (mitogen-activated protein kinase) kinases exhibit reduced binding to their cognate MAPKs. Biochem. J. 378:569-577.
5. 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.
6. Betz, A. L. 1985. Epithelial properties of brain capillary endothelium. Fed. Proc. 44:2614-2615.
7. Betz, A. L. 1992. An overview of the multiple functions of the blood-brain barrier. NIDA Res. Monogr. 120:54-72.
8. Coombes, B. K., B. Chiu, I. W. Fong, and J. B. Mahony. 2002. Chlamydia pneumoniae infection of endothelial cells induces transcriptional activation of platelet-derived growth factor-B: a potential link to intimal thickening in a rabbit model of atherosclerosis. J. Infect. Dis. 185:1621-1630.
9. Dalldorf, F. G., and F. A. Beall. 1967. Capillary thrombosis as a cause of death in experimental anthrax. Arch. Pathol. 83:154-161.
10. Dejana, E. 2004. Endothelial cell-cell junctions: happy together. Nat. Rev. Mol. Cell Biol. 5:261-270.
11. Deretic, V., and B. Levine. 2009. Autophagy, immunity, and microbial adaptations. Cell Host Microbe 5:527-549.
12. Dixon, T. C., M. Meselson, J. Guillemin, and P. C. Hanna. 1999. Anthrax. N. Engl. J. Med. 341:815-826.
13. Doran, K. S., et al. 2005. Blood-brain barrier invasion by group B Streptococcus depends upon proper cell-surface anchoring of lipoteichoic acid. J. Clin. Invest. 115:2499-2507.
14. Doran, K. S., G. Y. Liu, and V. Nizet. 2003. Group B streptococcal betahemolysin/ cytolysin activates neutrophil signaling pathways in brain endothelium and contributes to development of meningitis. J. Clin. Invest. 112: 736-744.
15. Duesbery, N. S., et al. 1998. Proteolytic inactivation of MAP-kinase-kinase by anthrax lethal factor. Science 280:734-737.
16. Ebrahimi, C. M., et al. 2009. Penetration of the blood-brain barrier by Bacillus anthracis requires the pXO1-encoded BslA protein. J. Bacteriol. 191:7165-7173.
17. Evans, D. J., I. A. Maltseva, J. Wu, and S. M. Fleiszig. 2002. Pseudomonas aeruginosa internalization by corneal epithelial cells involves MEK and ERK signal transduction proteins. FEMS Microbiol. Lett. 213:73-79.
18. Firoved, A. M., et al. 2005. Bacillus anthracis edema toxin causes extensive tissue lesions and rapid lethality in mice. Am. J. Pathol. 167:1309-1320.
19. Fritz, D. L., et al. 1995. Pathology of experimental inhalation anthrax in the rhesus monkey. Lab. Invest. 73:691-702.
20. Giaever, I., and C. R. Keese. 1991. Micromotion of mammalian cells measured electrically. Proc. Natl. Acad. Sci. U. S. A. 88:7896-7900.
21. Giaever, I., and C. R. Keese. 1984. Monitoring fibroblast behavior in tissue culture with an applied electric field. Proc. Natl. Acad. Sci. U. S. A. 81:3761- 3764.
22. Giaever, I., and C. R. Keese. 1993. A morphological biosensor for mammalian cells. Nature 366:591-592.
23. Guichard, A., et al. 2010. Anthrax toxins cooperatively inhibit endocytic recycling by the Rab11/Sec15 exocyst. Nature 467:854-858.
24. Gutierrez, M. G., et al. 2007. Protective role of autophagy against Vibrio cholerae cytolysin, a pore-forming toxin from V. cholerae. Proc. Natl. Acad. Sci. U. S. A. 104:1829-1834.
25. Hoover, D. L., et al. 1994. Anthrax edema toxin differentially regulates lipopolysaccharide-induced monocyte production of tumor necrosis factor alpha and interleukin-6 by increasing intracellular cyclic AMP. Infect. Immun. 62:4432-4439.
26. Iwai-Kanai, E., et al. 2008. A method to measure cardiac autophagic flux in vivo. Autophagy 4:322-329.
27. Janes, B. K., and S. Stibitz. 2006. Routine markerless gene replacement in Bacillus anthracis. Infect. Immun. 74:1949-1953.
28. Kabeya, Y., et al. 2004. LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J. Cell Sci. 117: 2805-2812.
29. Kim, K. S. 2008. Mechanisms of microbial traversal of the blood-brain barrier. Nat. Rev. Microbiol. 6:625-634.
30. Kim, K. S. 2002. Strategy of Escherichia coli for crossing the blood-brain barrier. J. Infect. Dis. 186(Suppl. 2):S220-S224.
31. Kim, S. O., et al. 2003. Sensitizing anthrax lethal toxin-resistant macrophages to lethal toxin-induced killing by tumor necrosis factor-alpha. J. Biol. Chem. 278:7413-7421.
32. Kugler, S., et al. 2007. Pertussis toxin transiently affects barrier integrity, organelle organization and transmigration of monocytes in a human brain microvascular endothelial cell barrier model. Cell. Microbiol. 9:619-632.
33. Lanska, D. J. 2002. Anthrax meningoencephalitis. Neurology 59:327-334.
34. Lehmann, M., D. Noack, M. Wood, M. Perego, and U. G. Knaus. 2009. Lung epithelial injury by B. anthracis lethal toxin is caused by MKK-dependent loss of cytoskeletal integrity. PLoS One 4:e4755.
35. Lembo, A., et al. 2010. Regulation of CovR expression in group B Streptococcus impacts blood-brain barrier penetration. Mol. Microbiol. 77:431-443.
36. Leppla, S. H. 1982. Anthrax toxin edema factor: a bacterial adenylate cyclase that increases cyclic AMP concentrations of eukaryotic cells. Proc. Natl. Acad. Sci. U. S. A. 79:3162-3166.
37. Leppla, S. H. 1984. Bacillus anthracis calmodulin-dependent adenylate cyclase: chemical and enzymatic properties and interactions with eucaryotic cells. Adv. Cyclic Nucleotide Protein Phosphorylation Res. 17:189-198.
38. Lo, C. M., C. R. Keese, and I. Giaever. 1995. Impedance analysis of MDCK cells measured by electric cell-substrate impedance sensing. Biophys. J. 69: 2800-2807.
39. Moayeri, M., D. Haines, H. A. Young, and S. H. Leppla. 2003. Bacillus anthracis lethal toxin induces TNF-alpha-independent hypoxia-mediated toxicity in mice. J. Clin. Invest. 112:670-682.
40. Moayeri, M., and S. H. Leppla. 2009. Cellular and systemic effects of anthrax lethal toxin and edema toxin. Mol. Aspects Med. 30:439-455.
41. Moayeri, M., and S. H. Leppla. 2004. The roles of anthrax toxin in pathogenesis. Curr. Opin. Microbiol. 7:19-24.
42. Mock, M., and A. Fouet. 2001. Anthrax. Annu. Rev. Microbiol. 55:647-671.
43. Mourez, M. 2004. Anthrax toxins. Rev. Physiol. Biochem. Pharmacol. 152: 135-164.
44. Nizet, V., et al. 1997. Invasion of brain microvascular endothelial cells by group B streptococci. Infect. Immun. 65:5074-5081.
45. 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.
46. Pentecost, M., G. Otto, J. A. Theriot, and M. R. Amieva. 2006. Listeria monocytogenes invades the epithelial junctions at sites of cell extrusion. PLoS Pathog. 2:29-40.
47. Pezard, C., P. Berche, and M. Mock. 1991. Contribution of individual toxin components to virulence of Bacillus anthracis. Infect. Immun. 59:3472-3477.
48. Py, B. F., M. M. Lipinski, and J. Yuan. 2007. Autophagy limits Listeria monocytogenes intracellular growth in the early phase of primary infection. Autophagy 3:117-125.
49. Rejman, J., S. Di Gioia, A. Bragonzi, and M. Conese. 2007. Pseudomonas aeruginosa infection destroys the barrier function of lung epithelium and enhances polyplex-mediated transfection. Hum. Gene Ther. 18:642-652.
50. Ring, A., J. N. Weiser, and E. I. Tuomanen. 1998. Pneumococcal trafficking across the blood-brain barrier. Molecular analysis of a novel bidirectional pathway. J. Clin. Invest. 102:347-360.
51. Sheen, T. R., et al. 2010. Penetration of the blood-brain barrier by Staphy-lococcus aureus: contribution of membrane-anchored lipoteichoic acid. J. Mol. Med. 88:633-639.
52. Soong, G., D. Parker, M. Magargee, and A. S. Prince. 2008. The type III toxins of Pseudomonas aeruginosa disrupt epithelial barrier function. J. Bacteriol. 190:2814-2821.
53. Stins, M. F., F. Gilles, and K. S. Kim. 1997. Selective expression of adhesion molecules on human brain microvascular endothelial cells. J. Neuroimmunol. 76:81-90.
54. Stins, M. F., N. V. Prasadarao, J. Zhou, M. Arditi, and K. S. Kim. 1997. Bovine brain microvascular endothelial cells transfected with SV40-large T antigen: development of an immortalized cell line to study pathophysiology of CNS disease. In Vitro Cell. Dev. Biol. Anim. 33:243-247.
55. Tan, Y. K., et al. 2009. Induction of autophagy by anthrax lethal toxin. Biochem. Biophys. Res. Commun. 379:293-297.
56. Tang, P., C. L. Sutherland, M. R. Gold, and B. B. Finlay. 1998. Listeria monocytogenes invasion of epithelial cells requires the MEK-1/ERK-2 mitogen-activated protein kinase pathway. Infect. Immun. 66:1106-1112.
57. Terebiznik, M. R., et al. 2009. Effect of Helicobacter pylori's vacuolating cytotoxin on the autophagy pathway in gastric epithelial cells. Autophagy 5:370-379.
58. van Sorge, N. M., et al. 2008. Anthrax toxins inhibit neutrophil signaling pathways in brain endothelium and contribute to the pathogenesis of meningitis. PLoS One 3:e2964.
59. 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(Pt 3):739-745.
60. Warfel, J. M., A. D. Steele, and F. D'Agnillo. 2005. Anthrax lethal toxin induces endothelial barrier dysfunction. Am. J. Pathol. 166:1871-1881.
61. Webster, J. I., et al. 2003. Anthrax lethal factor represses glucocorticoid and progesterone receptor activity. Proc. Natl. Acad. Sci. U. S. A. 100:5706-5711.