MyD88-dependent signaling protects against anthrax lethal toxin-induced impairment of intestinal barrier function

Infection and Immunity

Volumn 79, Issue 1, 2011, Pages 118-124

  Okugawa, Shu ^a   Moayeri, Mahtab ^a   Eckhaus, Michael A ^b   Crown, Devorah ^a   Miller Randolph, Sharmina ^a   Liu, Shihui ^a   Akira, Shizuo ^c   Leppla, Stephen H ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRAX TOXIN; MYELOID DIFFERENTIATION FACTOR 88;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTHRAX; ARTICLE; BACILLUS ANTHRACIS; BACTEREMIA; HISTOPATHOLOGY; INFECTION SENSITIVITY; INTESTINE EPITHELIUM; INTESTINE INJURY; INTESTINE ULCER; MOUSE; NONHUMAN; PERITONITIS; PERMEABILITY BARRIER; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; ANTHRAX; ANTIGENS, BACTERIAL; BACTEREMIA; BACTERIAL TOXINS; GENETIC PREDISPOSITION TO DISEASE; INTESTINES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID DIFFERENTIATION FACTOR 88; SIGNAL TRANSDUCTION; SPORES, BACTERIAL;

EID: 78650877511     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00963-10     Document Type: Article

References (42)

1. Adachi, O., T. Kawai, K. Takeda, M. Matsumoto, H. Tsutsui, M. Sakagami, K. Nakanishi, and S. Akira. 1998. Targeted disruption of the MyD88 gene results in loss of IL-1-and IL-18-mediated function. Immunity 9:143-150.
2. 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. (Pubitemid 36899376)
3. Akira, S., S. Uematsu, and O. Takeuchi. 2006. Pathogen recognition and innate immunity. Cell 124:783-801.
4. Berg, R. D. 1999. Bacterial translocation from the gastrointestinal tract. Adv. Exp. Med. Biol. 473:11-30.
5. Bonuccelli, G., F. Sotgia, P. G. Frank, T. M. Williams, C. J. de Almeida, H. B. Tanowitz, P. E. Scherer, K. A. Hotchkiss, B. I. Terman, B. Rollman, A. Alileche, J. Brojatsch, and M. P. Lisanti. 2005. Anthrax toxin receptor (ATR/TEM8) is highly expressed in epithelial cells lining the toxin's three sites of entry (lung, skin, and intestine). Am. J. Physiol. Cell Physiol. 288: C1402-C1410.
6. Bradley, K. A., J. Mogridge, M. Mourez, R. J. Collier, and J. A. Young. 2001. Identification of the cellular receptor for anthrax toxin. Nature 414:225-229.
7. Brook, I., T. B. Elliott, R. A. Harding, S. S. Bouhaouala, S. J. Peacock, G. D. Ledney, and G. B. Knudson. 2001. Susceptibility of irradiated mice to Bacillus anthracis Sterne by the intratracheal route of infection. J. Med. Mi-crobiol. 50:702-711.
8. 60Co-gamma-photon-irradiated and sham-irradiated mice. J. Antimicrob. Chemother. 56:1074-1080.
9. Cai, S., S. Batra, L. Shen, N. Wakamatsu, and S. Jeyaseelan. 2009. Both TRIF-and MyD88-dependent signaling contribute to host defense against pulmonary Klebsiella infection. J. Immunol. 183:6629-6638.
10. 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.
11. Friedlander, A. M., R. Bhatnagar, S. H. Leppla, L. Johnson, and Y. Singh. 1993. Characterization of macrophage sensitivity and resistance to anthrax lethal toxin. Infect. Immun. 61:245-252.
12. Gautreaux, M. D., E. A. Deitch, and R. D. Berg. 1994. T lymphocytes in host defense against bacterial translocation from the gastrointestinal tract. Infect. Immun. 62:2874-2884.
13. Gupta, P. K., M. Moayeri, D. Crown, R. J. Fattah, and S. H. Leppla. 2008. Role of N-terminal amino acids in the potency of anthrax lethal factor. PLoS One 3:e3130.
14. Hanks, S., S. Adams, J. Douglas, L. Arbour, D. J. Atherton, S. Balci, H. Bode, M. E. Campbell, M. Feingold, G. Keser, W. Kleijer, G. Mancini, J. A. McGrath, F. Muntoni, A. Nanda, M. D. Teare, M. Warman, F. M. Pope, A. Superti-Furga, P. A. Futreal, and N. Rahman. 2003. Mutations in the gene encoding capillary morphogenesis protein 2 cause juvenile hyaline fibroma-tosis and infantile systemic hyalinosis. Am. J. Hum. Genet. 73:791-800.
15. 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.
16. Hughes, M. A., C. S. Green, L. Lowchyj, G. M. Lee, V. K. Grippe, M. F. Smith, Jr., L. Y. Huang, E. T. Harvill, and T. J. Merkel. 2005. MyD88-dependent signaling contributes to protection following Bacillus anthracis spore challenge of mice: implications for Toll-Like receptor signaling. Infect. Immun. 73:7535-7540.
17. Kawai, T., O. Adachi, T. Ogawa, K. Takeda, and S. Akira. 1999. Unrespon-siveness of MyD88-deficient mice to endotoxin. Immunity 11:115-122.
18. Kawai, T., and S. Akira. 2007. TLR signaling. Semin. Immunol. 19:24-32.
19. Koh, A. Y., J. R. Kohler, K. T. Coggshall, R. N. Van, and G. B. Pier. 2008. Mucosal damage and neutropenia are required for Candida albicans dissemination. PLoS Pathog. 4:e35.
20. Koh, A. Y., G. P. Priebe, and G. B. Pier. 2005. Virulence of Pseudomonas aeruginosa in a murine model of gastrointestinal colonization and dissemination in neutropenia. Infect. Immun. 73:2262-2272.
21. 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.
22. 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.
23. Liu, S., D. Crown, S. Miller-Randolph, M. Moayeri, H. Wang, H. Hu, T. Morley, and S. H. Leppla. 2009. Capillary morphogenesis protein-2 is the major receptor mediating lethality of anthrax toxin in vivo. Proc. Natl. Acad. Sci. U.S.A. 106:12424-12429.
24. Malago, J. J., J. F. Koninkx, and J. E. van Dijk. 2002. The heat shock response and cytoprotection of the intestinal epithelium. Cell Stress Chap-erones 7:191-199.
25. Moayeri, M., D. Haines, H. A. Young, and S. H. Leppla. 2003. Bacillus anthracis lethal toxin induces TNF-a-independent hypoxia-mediated toxicity in mice. J. Clin. Invest. 112:670-682.
26. Moayeri, M., and S. H. Leppla. 2009. Cellular and systemic effects of anthrax lethal toxin and edema toxin. Mol. Aspects Med. 30:439-455.
27. Moayeri, M., N. W. Martinez, J. Wiggins, H. A. Young, and S. H. Leppla. 2004. Mouse susceptibility to anthrax lethal toxin is influenced by genetic factors in addition to those controlling macrophage sensitivity. Infect. Im-mun. 72:4439-4447.
28. Newman, Z. L., S. H. Leppla, and M. Moayeri. 2009. CA-074Me protection against anthrax lethal toxin. Infect. Immun. 77:4327-4336.
29. O'Brien, J., A. Friedlander, T. Dreier, J. Ezzell, and S. H. Leppla. 1985. Effects of anthrax toxin components on human neutrophils. Infect. Immun. 47:306-310.
30. Owens, W. E., and R. D. Berg. 1980. Bacterial translocation from the gastrointestinal tract of athymic (nu/nu) mice. Infect. Immun. 27:461-467.
31. Pezard, C, P. Berche, and M. Mock. 1991. Contribution of individual toxin components to virulence of Bacillus anthracis. Infect. Immun. 59:3472-3477.
32. Pomerantsev, A. P., R. Sitaraman, C. R. Galloway, V. Kivovich, and S. H. Leppla. 2006. Genome engineering in Bacillus anthracis using Cre recombi-nase. Infect. Immun. 74:682-693.
33. Rakoff-Nahoum, S., J. Paglino, F. Eslami-Varzaneh, S. Edberg, and R. Medzhitov. 2004. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118:229-241.
34. 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. U.S.A. 100:5170-5174.
35. Soelaiman, S., B. Q. Wei, P. Bergson, Y. S. Lee, Y. Shen, M. Mrksich, B. K. Shoichet, and W. J. Tang. 2003. Structure-based inhibitor discovery against adenylyl cyclase toxins from pathogenic bacteria that cause anthrax and whooping cough. J. Biol. Chem. 278:25990-25997.
36. Takeuchi, O., K. Hoshino, and S. Akira. 2000. Cutting edge: TLR2-deficient and MyD88-deficient mice are highly susceptible to Staphylococcus aureus infection. J. Immunol. 165:5392-5396.
37. Twenhafel, N. A., E. Leffel, and M. L. Pitt. 2007. Pathology of inhalational anthrax infection in the African green monkey. Vet. Pathol. 44:716-721.
38. Vaishnava, S., C. L. Behrendt, A. S. Ismail, L. Eckmann, and L. V. Hooper. 2008. Paneth cells directly sense gut commensals and maintain homeostasis at the intestinal host-microbial interface. Proc. Natl. Acad. Sci. U.S.A. 105:20858-20863.
39. Varughese, M., A. Chi, A. V. Teixeira, P. J. Nicholls, J. M. Keith, and S. H. Leppla. 1998. Internalization of a Bacillus anthracis protective antigen-c-Myc fusion protein mediated by cell surface anti-c-Myc antibodies. Mol. Med. 4:87-95.
40. Warfel, J. M., A. D. Steele, and F. D'Agnillo. 2005. Anthrax lethal toxin induces endothelial barrier dysfunction. Am. J. Pathol. 166:1871-1881.
41. Wu, C. C, M. Sabet, T. Hayashi, R. Tawatao, J. Fierer, D. A. Carson, D. G. Guiney, and M. Corr. 2008. In vivo efficacy of a phosphodiester TLR-9 aptamer and its beneficial effect in a pulmonary anthrax infection model. Cell. Immunol. 251:78-85.
42. Young, J. A., and R. J. Collier. 2007. Anthrax toxin: receptor-binding, internalization, pore formation, and translocation. Annu. Rev. Biochem. 76:243-265.