Noninvasive imaging technologies reveal edema toxin as a key virulence factor in anthrax

American Journal of Pathology

Volumn 178, Issue 6, 2011, Pages 2523-2535

  Dumetz, Fabien ^a,e,h   Jouvion, Grégory ^b   Khun, Huot ^c   Glomski, Ian Justin ^f   Corre, Jean Philippe ^a,e   Rougeaux, Clémence ^a,e   Tang, Wei Jen ^g   Mock, Michèle ^d,e   Huerre, Michel ^c   Goossens, Pierre Louis ^a,d,e  

^a Pathogenesis of Bacterial Toxi Infections Laboratory   (France)

^b Human Histopathology and Animal Models Unit   (France)

^c Department of Infectious Disease and Epidemiology   (France)

^d INSTITUT PASTEUR   (France)

^e CNRS   (France)

^f UNIVERSITY OF VIRGINIA   (United States)

^g UNIVERSITY OF CHICAGO   (United States)

^h UMR1319 MICALIS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADEFOVIR DIPIVOXIL; ANTIGEN; EDEMA TOXIN; LETHAL TOXIN; TOXIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTHRAX; APOPTOSIS; ARTICLE; BACILLUS ANTHRACIS; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BIOLUMINESCENCE; CONTROLLED STUDY; DISEASE COURSE; EXPERIMENTAL GUINEA PIG; FEMALE; HISTOPATHOLOGY; LD 50; LYMPHOID CELL; NON INVASIVE PROCEDURE; NONHUMAN; PRIORITY JOURNAL; SPLEEN; WILD TYPE;

EID: 79959416404     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.02.027     Document Type: Article

References (45)

1. Germain RN, Miller MJ, Dustin ML, Nussenzweig MC: Dynamic imaging of the immune system: progress, pitfalls and promise. Nat Rev Immunol 2006, 6:497-507 (Pubitemid 43980522)
2. Mock M, Fouet A: Anthrax. Annu Rev Microbiol 2001, 55:647-671
3. Candela T, Fouet A: Bacillus anthracis CapD, belonging to the gamma- glutamyltranspeptidase family, is required for the covalent anchoring of capsule to peptidoglycan. Mol Microbiol 2005, 57:717-726 (Pubitemid 41025954)
4. Moayeri M, Leppla S: Cellular and systemic effects of anthrax lethal toxin and edema toxin. Mol Aspects Med 2009, 30:439-455
5. Tournier JN, Rossi Paccani S, Quesnel-Hellmann A, Baldari CT: Anthrax toxins: a weapon to systematically dismantle the host immune defenses. Mol Aspects Med 2009, 30:456-466
6. Glomski IJ, Corre JP, Mock M, Goossens PL: Noncapsulated toxinogenic Bacillus anthracis presents a specific growth and dissemination pattern in naive and protective antigen-immune mice. Infect Immun 2007, 75:4754-4761 (Pubitemid 47502144)
7. Glomski IJ, Dumetz F, Jouvion G, Huerre MR, Mock M, Goossens PL: Inhaled non-capsulated Bacillus anthracis in A/J mice: nasopharynx and alveolar space as dual portals of entry, delayed dissemination, and specific organ targeting. Microbes Infect 2008, 10:1398-1404
8. Glomski IJ, Piris-Gimenez A, Huerre M, Mock M, Goossens PL: Primary involvement of pharynx and Peyer's patch in inhalational and intestinal anthrax. PLoS Pathog 2007, 3:e76
9. Duong S, Chiaraviglio L, Kirby JE: Histopathology in a murine model of anthrax. Int J Exp Pathol 2006, 87:131-137
10. Fritz DL, Jaax NK, Lawrence WB, Davis KJ, Pitt ML, Ezzell JW, Friedlander AM: Pathology of experimental inhalation anthrax in the rhesus monkey. Lab Invest 1995, 73:691-702
11. Grinberg LM, Abramova FA, Yampolskaya OV, Walker DH, Smith JH: Quantitative pathology of inhalational anthrax I: quantitative microscopic findings. Mod Pathol 2001, 14:482-495 (Pubitemid 32448748)
12. Guarner J, Jernigan JA, Shieh WJ, Tatti K, Flannagan LM, Stephens DS, Popovic T, Ashford DA, Perkins BA, Zaki SR; Inhalational Anthrax Pathology Working Group: Pathology and pathogenesis of bioterrorism- related inhalational anthrax. Am J Pathol 2003, 163:701-709 (Pubitemid 36909431)
13. Lever MS, Stagg AJ, Nelson M, Pearce P, Stevens DJ, Scott EA, Simpson AJ, Fulop MJ: Experimental respiratory anthrax infection in the common marmoset (Callithrix jacchus). Int J Exp Pathol 2008, 89:171-179 (Pubitemid 351661564)
14. Shieh WJ, Guarner J, Paddock C, Greer P, Tatti K, Fischer M, Layton M, Philips M, Bresnitz E, Quinn CP, Popovic T, Perkins BA, Zaki SR; Anthrax Bioterrorism Investigation Team: The critical role of pathology in the investigation of bioterrorism-related cutaneous anthrax. Am J Pathol 2003, 163:1901-1910 (Pubitemid 37310020)
15. Vasconcelos D, Barnewall R, Babin M, Hunt R, Estep J, Nielsen C, Carnes R, Carney J: Pathology of inhalation anthrax in cynomolgus monkeys (Macaca fascicularis). Lab Invest 2003, 83:1201-1209 (Pubitemid 37013055)
16. Firoved AM, Miller GF, Moayeri M, Kakkar R, Shen Y, Wiggins JF, McNally EM, Tang WJ, Leppla SH: Bacillus anthracis edema toxin causes extensive tissue lesions and rapid lethality in mice. Am J Pathol 2005, 167:1309-1320 (Pubitemid 41541417)
17. Moayeri M, Haines D, Young HA, Leppla SH: Bacillus anthracis lethal toxin induces TNF-alpha-independent hypoxia-mediated toxicity in mice. J Clin Invest 2003, 112:670-682 (Pubitemid 38057708)
18. Loving CL, Khurana T, Osorio M, Lee GM, Kelly VK, Stibitz S, Merkel TJ: Role of anthrax toxins in dissemination, disease progression, and induction of protective adaptive immunity in the mouse aerosol challenge model. Infect Immun 2009, 77:255-265
19. Pezard C, Berche P, Mock M: Contribution of individual toxin components to virulence of Bacillus anthracis. Infect Immun 1991, 59: 3472-3477
20. Drysdale M, Olson G, Koehler TM, Lipscomb MF, Lyons CR: Murine innate immune response to virulent toxigenic and nontoxigenic Bacillus anthracis strains. Infect Immun 2007, 75:1757-1764 (Pubitemid 46559442)
21. Heninger S, Drysdale M, Lochia J, Hutt J, Lipscomb MF, Koehler TM, Lyons CR: Toxin-deficient mutants of Bacillus anthracis are lethal in a murine model for pulmonary anthrax. Infect Immun 2006, 74:6067-6074 (Pubitemid 44657384)
22. Chan HS, Drysdale M, Lochia J, Koehler TM, Lipscomb MF, Lyons CR: Discriminating virulence mechanisms among Bacillus anthracis strains by using a murine subcutaneous infection model. Infect Immun 2009, 77:429-435
23. Brassier F, Levy M, Mock M: Anthrax spores make an essential contribution to vaccine efficacy. Infect Immun 2002, 70:661-664 (Pubitemid 34083825)
24. Brassier F, Weber-Levy M, Mock M, Sicard JC: Protective antigenmediated antibody response against a heterologous protein produced in vivo by Bacillus anthracis. Infect Immun 2000, 68:5731-5734
25. Remise V, Part G, Garrigue H, Guerdon JL, Mock M: Identification and characterization of Bacillus anthracis by multiplex PCR analysis of sequences on plasmids pXO1 and pXO2 and chromosomal DNA. FEMS Microbiol Lett 1996, 145:9-16 (Pubitemid 26366682)
26. Gauthier YP, Tournier JN, PaCOD JC, Corre JP, Mock M, Goossens PL, Vidal DR: Efficacy of a vaccine based on protective antigen and killed spores against experimental inhalational anthrax. Infect Immun 2009, 77:1197-1207
27. Reed LJ, Muench H: A simple method of estimating fifty percent endpoints. Am J Hyg 1938, 27:493-497
28. Keppie J, Smith H, Harris-Smith PW: The chemical basis of the virulence of Bacillus anthracis. III. The role of the terminal bacteraemia in death of guinea-pigs from anthrax. Br J Exp Pathol 1955, 36:315-322
29. Shen Y, Zhukovskaya NL, Zimmer MI, Soelaiman S, Bergson P, Wang CR, Gibbs CS, Tang WJ: Selective inhibition of anthrax edema factor by adefovir, a drug for chronic hepatitis B virus infection. Proc Natl Acad Sci USA 2004, 101:3242-3247 (Pubitemid 38327765)
30. Khokhar A, Afdhal NH: Therapeutic strategies for chronic hepatitis B virus infection in 2008. Am J Med 2008, 121(12 Suppl):S33-S44
31. Goossens P: Animal models of human anthrax: The quest for the holy grail. Mol Aspects Med 2009, 30:467-480
32. Maldonado-Arocho FJ, Fulcher JA, Lee B, Bradley KA: Anthrax oedema toxin induces anthrax toxin receptor expression in monocytederived cells. Mol Microbiol 2006, 61:324-337 (Pubitemid 44356566)
33. Kim C, Wilcox-Adelman S, Sano Y, Tang WJ, Collier RJ, Park JM: Antiinflammatory cAMP signaling and cell migration genes co-opted by the anthrax bacillus. Proc Natl Acad Sci USA 2008, 105:6150-6155 (Pubitemid 351758414)
34. Szarowicz SE, During RL, Li W, Quinn CP, Tang WJ, Southwick FS: Bacillus anthracis edema toxin impairs neutrophil actin-based motility. Infect Immun 2009, 77:2455-2464
35. Terra JK, Cote CK, France B, Jenkins AL, Bozue JA, Welkos SL, LeVine SM, Bradley KA: Cutting edge: resistance to Bacillus anthracis infection mediated by a lethal toxin sensitive allele of Nalp1b/Nlrp1b. J Immunol 2010, 184:17-20
36. Welkos SL, Vietri NJ, Gibbs PH: Non-toxigenic derivatives of the Ames strain of Bacillus anthracis are fully virulent for mice: role of plasmid pX02 and chromosome in strain-dependent virulence. Microb Pathog 1993, 14:381-388
37. Salles II, Tucker AE, Voth DE, Ballard JD: Toxin-induced resistance in Bacillus anthracis lethal toxin-treated macrophages. Proc Natl Acad Sci USA 2003, 100:12426-12431 (Pubitemid 37271576)
38. Firoved AM, Moayeri M, Wiggins JF, Shen Y, Tang WJ, Leppla SH: Anthrax edema toxin sensitizes DBA/2J mice to lethal toxin. Infect Immun 2007, 75:2120-2125 (Pubitemid 46744297)
39. Piris-Gimenez A, Corre JP, Jouvion G, Candela T, Khun H, Goossens PL: Encapsulated Bacillus anthracis interacts closely with liver endothelium. J Infect Dis 2009, 200:1381-1389
40. Tonello F, Seveso M, Marin O, Mock M, Montecucco C: Screening inhibitors of anthrax lethal factor. Nature 2002, 418:386 (Pubitemid 34826833)
41. Nguyen ML, Crowe SR, Kurella S, Teryzan S, Cao B, Ballard JD, James JA, Farris AD: Sequential B-cell epitopes of Bacillus anthracis lethal factor bind lethal toxin-neutralizing antibodies. Infect Immun 2009, 77:162-169
42. Chen Z, Moayeri M, Zhao H, Crown D, Leppla SH, Purcell RH: Potent neutralization of anthrax edema toxin by a humanized monoclonal antibody that competes with calmodulin for edema factor binding. Proc Natl Acad Sci USA 2009, 106:13487-13492
43. Winterroth L, Rivera J, Nakouzi AS, Dadachova E, Casadevall A: Neutralizing monoclonal antibody to edema toxin and its effect on murine anthrax. Infect Immun 2010, 78:2890-2898
44. Padilla-Carlin DJ, McMurray DN, Hickey AJ: The guinea pig as a model of infectious diseases. Comp Med 2008, 58:324-340
45. Tree JA, Elmore MJ, Javed S, Williams A, Marsh PD: Development of a guinea pig immune response-related microarray and its use to define the host response following Mycobacterium bovis BCG vaccination. Infect Immun 2006, 74:1436-1441 (Pubitemid 43185590)