Resistance of human alveolar macrophages to Bacillus anthracis lethal toxin

Journal of Immunology

Volumn 183, Issue 9, 2009, Pages 5799-5806

  Wu, Wenxin ^a   Mehta, Harshini ^b   Chakrabarty, Kaushik ^a   Booth, J Leland ^a   Duggan, Elizabeth S ^a   Patel, Krupa B ^a   Ballard, Jimmy D ^a   Coggeshall, K Mark ^b   Metcalf, Jordan P ^a  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^b OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRAX TOXIN RECEPTOR 1; ANTHRAX TOXIN RECEPTOR 2; BACTERIAL TOXIN; CYTOKINE; LETHAL TOXIN; RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; AUTOPSY; BACILLUS ANTHRACIS; BONE MARROW CELL; CELL DIFFERENTIATION; CELL MATURATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; INNATE IMMUNITY; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ANTHRAX; ANTIGENS, BACTERIAL; BACILLUS ANTHRACIS; BACTERIAL TOXINS; CELL LINE; CYTOKINES; HUMANS; IMMUNITY, INNATE; IMMUNOSUPPRESSIVE AGENTS; MACROPHAGES, ALVEOLAR; MICE; MICE, INBRED C57BL; VIRULENCE;

EID: 77954167608     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0803406     Document Type: Article

References (45)

1. Dixon, T. C., M. Meselson, J. Guillemin, and P. C. Hanna. 1999. Anthrax. N. Engl. J. Med. 341: 815-826.
2. Meselson, M., J. Guillemin, M. Hugh-Jones, A. Langmuir, I. Popova, A. Shelokov, and O. Yampolskaya. 1994. The Sverdlovsk anthrax outbreak of 1979. Science 266: 1202-1208.
3. Druett, H. A., D. W. Henderson, L. Packman, and S. Peacock. 1953. Studies on respiratory infection. I. The influence of particle size on respiratory infection with anthrax spores. J. Hyg. 51: 359-371.
4. Albrink, W. S., and R. J. Goodlow. 1959. Experimental inhalation anthrax in the chimpanzee. Am. J. Pathol. 35: 1055-1065.
5. Cleret, A., A. Quesnel-Hellmann, A. Vallon-Eberhard, B. Verrier, S. Jung, D. Vidal, J. Mathieu, and J. N. Tournier. 2007. Lung dendritic cells rapidly mediate anthrax spore entry through the pulmonary route. J. Immunol. 178: 7994-8001.
6. Grinberg, L. M., F. A. Abramova, O. V. Yampolskaya, D. H. Walker, and J. H. Smith. 2001. Quantitative pathology of inhalational anthrax I: quantitative microscopic findings. Mod. Pathol. 14: 482-495.
7. Cote, C. K., N. Van Rooijen, and S. L. Welkos. 2006. Roles of macrophages and neutrophils in the early host response to Bacillus anthracis spores in a mouse model of infection. Infect. Immun. 74: 469-480.
8. Guidi-Rontani, C. 2002. The alveolar macrophage: the Trojan horse of Bacillus anthracis. Trends Microbiol. 10: 405-409.
9. Ross, J. M. 1957. The pathogenesis of anthrax following the administration of spores by the respiratory route. J. Pathol. Bacteriol. 73: 485-494.
10. Welkos, S. L., T. J. Keener, and P. H. Gibbs. 1986. Differences in susceptibility of inbred mice to Bacillus anthracis. Infect. Immun. 51: 795-800.
11. Prince, A. S. 2003. The host response to anthrax lethal toxin: unexpected observations. J. Clin. Invest. 112: 656-658.
12. Hanna, P. C., D. Acosta, and R. J. Collier. 1993. On the role of macrophages in anthrax. Proc. Natl. Acad. Sci. USA 90: 10198-10201.
13. Heninger, S., M. Drysdale, J. Lovchik, J. Hutt, M. F. Lipscomb, T. M. Koehler, and C. R. Lyons. 2006. Toxin-deficient mutants of Bacillus anthracis are lethal in a murine model for pulmonary anthrax. Infect. Immun. 74: 6067-6074.
14. Auerbach, S., and G. G. Wright. 1955. Studies on immunity in anthrax. VI. Immunizing activity of protective antigen against various strains of Bacillus anthracis. J. Immunol. 75: 129-133.
15. Peterson, J. W., J. E. Comer, W. B. Baze, D. M. Noffsinger, A. Wenglikowski, K. G. Walberg, J. Hardcastle, J. Pawlik, K. Bush, J. Taormina, et al. 2007. Human monoclonal antibody AVP-21D9 to protective antigen reduces dissemination of the Bacillus anthracis Ames strain from the lungs in a rabbit model. Infect. Immun. 75: 3414-3424.
16. Weiss, S., D. Kobiler, H. Levy, H. Marcus, A. Pass, N. Rothschild, and Z. Altboum. 2006. Immunological correlates for protection against intranasal challenge of Bacillus anthracis spores conferred by a protective antigen-based vaccine in rabbits. Infect. Immun. 74: 394-398.
17. 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.
18. Banks, D. J., M. Barnajian, F. J. Maldonado-Arocho, A. M. Sanchez, and K. A. Bradley. 2005. Anthrax toxin receptor 2 mediates Bacillus anthracis killing of macrophages following spore challenge. Cell Microbiol. 7: 1173-1185.
19. Chakrabarty, K., W. Wu, J. L. Booth, E. S. Duggan, K. M. Coggeshall, and J. P. Metcalf. 2006. Bacillus anthracis spores stimulate cytokine and chemokine innate immune responses in human alveolar macrophages through multiple mitogen- activated protein kinase pathways. Infect. Immun. 74: 4430-4438.
20. Premanandan, C., M. D. Lairmore, S. Fernandez, and A. J. Phipps. 2006. Quantitative measurement of anthrax toxin receptor messenger RNA in primary mononuclear phagocytes. Microb. Pathog. 41: 193-198.
21. Erwin, J. L., L. M. DaSilva, S. Bavari, S. F. Little, A. M. Friedlander, and T. C. Chanh. 2001. Macrophage-derived cell lines do not express proinflammatory cytokines after exposure to Bacillus anthracis lethal toxin. Infect. Immun. 69: 1175-1177.
22. Seger, R., N. G. Ahn, T. G. Boulton, G. D. Yancopoulos, N. Panayotatos, E. Radziejewska, L. Ericsson, R. L. Bratlien, M. H. Cobb, and E. G. Krebs. 1991. Microtubule-associated protein 2 kinases, ERK1 and ERK2, undergo autophosphorylation on both tyrosine and threonine residues: implications for their mechanism of activation. Proc. Natl. Acad. Sci. USA 88: 6142-6146.
23. Wu, J., A. J. Rossomando, J. H. Her, R. Del Vecchio, M. J. Weber, and T. W. Sturgill. 1991. Autophosphorylation in vitro of recombinant 42-kilodalton mitogen-activated protein kinase on tyrosine. Proc. Natl. Acad. Sci. USA 88: 9508-9512.
24. Duesbery, N. S., and G. F. Vande Woude. 1999. Anthrax lethal factor causes proteolytic inactivation of mitogen-activated protein kinase kinase. J. Appl. Microbiol. 87: 289-293.
25. 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.
26. Popov, S. G., R. Villasmil, J. Bernardi, E. Grene, J. Cardwell, A. Wu, D. Alibek, C. Bailey, and K. Alibek. 2002. Lethal toxin of Bacillus anthracis causes apoptosis of macrophages. Biochem. Biophys. Res. Commun. 293: 349-355.
27. Lin, C. G., Y. T. Kao, W. T. Liu, H. H. Huang, K. C. Chen, T. M. Wang, and H. C. Lin. 1996. Cytotoxic effects of anthrax lethal toxin on macrophage-like cell line J774A.1. Curr. Microbiol. 33: 224-227.
28. Ribot, W. J., R. G. Panchal, K. C. Brittingham, G. Ruthel, T. A. Kenny, D. Lane, B. Curry, T. A. Hoover, A. M. Friedlander, and S. Bavari. 2006. Anthrax lethal toxin impairs innate immune functions of alveolar macrophages and facilitates Bacillus anthracis survival. Infect. Immun. 74: 5029-5034.
29. Hu, H., Q. Sa, T. M. Koehler, A. I. Aronson, and D. Zhou. 2006. Inactivation of Bacillus anthracis spores in murine primary macrophages. Cell Microbiol. 8: 1634-1642.
30. Liu, S., and S. H. Leppla. 2003. Cell surface tumor endothelium marker 8 cytoplasmic tail-independent anthrax toxin binding, proteolytic processing, oligomer formation, and internalization. J. Biol. Chem. 278: 5227-5234.
31. Scobie, H. M., G. J. Rainey, K. A. Bradley, and J. A. Young. 2003. Human capillary morphogenesis protein 2 functions as an anthrax toxin receptor. Proc. Natl. Acad. Sci. USA 100: 5170-5174.
32. Popov, S. G., R. Villasmil, J. Bernardi, E. Grene, J. Cardwell, T. Popova, A. Wu, D. Alibek, C. Bailey, and K. Alibek. 2002. Effect of Bacillus anthracis lethal toxin on human peripheral blood mononuclear cells. FEBS Lett. 527: 211-215.
33. Gold, J. A., Y. Hoshino, S. Hoshino, M. B. Jones, A. Nolan, and M. D. Weiden. 2004. Exogenous γ and α/β interferon rescues human macrophages from cell death induced by Bacillus anthracis. Infect. Immun. 72: 1291-1297.
34. Komuro, I., T. Yasuda, A. Iwamoto, and K. S. Akagawa. 2005. Catalase plays a critical role in the CSF-independent survival of human macrophages via regulation of the expression of BCL-2 family. J. Biol. Chem. 280: 41137-41145.
35. Liao, H. S., A. Matsumoto, H. Itakura, T. Pittman, T. Kodama, and Y. J. Geng. 1999. De novo expression of the class-A macrophage scavenger receptor conferring resistance to apoptosis in differentiated human THP-1 monocytic cells. Cell Death Differ. 6: 245-255.
36. Blanc-Brude, O. P., E. Teissier, Y. Castier, G. Leseche, A. P. Bijnens, M. Daemen, B. Staels, Z. Mallat, and A. Tedgui. 2007. IAP survivin regulates atherosclerotic macrophage survival. Arterioscler. Thromb. Vasc. Biol. 27: 901-907.
37. Piris-Gimenez, A., M. Paya, G. Lambeau, M. Chignard, M. Mock, L. Touqui, and P. L. Goossens. 2005. In vivo protective role of human group IIa phospholipase A2 against experimental anthrax. J. Immunol. 175: 6786-6791.
38. 2 expression by alveolar macrophages. PLoS Pathog. 3: e187.
39. Williamson, E. D., I. Hodgson, N. J. Walker, A. W. Topping, M. G. Duchars, J. M. Mott, J. Estep, C. Lebutt, H. C. Flick-Smith, H. E. Jones, H. Li, and C. P. Quinn. 2005. Immunogenicity of recombinant protective antigen and efficacy against aerosol challenge with anthrax. Infect. Immun. 73: 5978-5987.
40. Brittingham, K. C., G. Ruthel, R. G. Panchal, C. L. Fuller, W. J. Ribot, T. A. Hoover, H. A. Young, A. O. Anderson, and S. Bavari. 2005. Dendritic cells endocytose Bacillus anthracis spores: implications for anthrax pathogenesis. J. Immunol. 174: 5545-5552.
41. 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.
42. + lung cells are impaired by anthrax toxins after spore infection. J. Infect. Dis. 194: 86-94.
43. Dahlgren, C. M., L. M. Buchanan, H. M. Decker, S. W. Freed, C. R. Phillips, and P. S. Brachman. 1960. Bacillus anthracis aerosols in goat hair processing mills. Am. J. Hyg. 72: 24-31.
44. Brachman, P. S. 1980. Inhalation anthrax. Ann. NY Acad. Sci. 353: 83-93.
45. Inglesby, T. V., T. O'Toole, D. A. Henderson, J. G. Bartlett, M. S. Ascher, E. Eitzen, A. M. Friedlander, J. Gerberding, J. Hauer, J. Hughes, et al. 2002. Anthrax as a biological weapon, 2002: updated recommendations for management. J. Am. Med. Assoc. 287: 2236-2252.