Key aspects of the molecular and cellular basis of inhalational anthrax

Microbes and Infection

Volumn 13, Issue 14-15, 2011, Pages 1146-1155

  Cote, Christopher K ^a   Welkos, Susan L ^a   Bozue, Joel ^a  

^a UNITED STATES ARMY MEDICAL RESEARCH INSTITUTE OF INFECTIOUS DISEASES   (United States)

Author keywords

Bacillus anthracis; Germination; Inhalational anthrax; Phagocytes; Spores

Indexed keywords

ANTHRAX TOXIN; BACILLUS COLLAGEN LIKE PROTEIN A; BACTERIAL PROTEIN; CD11B ANTIGEN; PROTEIN A; UNCLASSIFIED DRUG;

ANTHRAX; B LYMPHOCYTE; BACILLUS ANTHRACIS; BACTERIAL MEMBRANE; BACTERIAL SPORE; BACTERIAL VIRULENCE; DEATH; DENDRITIC CELL; DISEASE COURSE; DISEASE MODEL; HOST; HUMAN; IN VITRO STUDY; INHALATIONAL ANTHRAX; LUNG INJURY; MACROPHAGE; NEUTROPHIL; NONHUMAN; PATHOGENESIS; PHAGOCYTE; PRIORITY JOURNAL; SEPTICEMIA; SHORT SURVEY; SPORE GERMINATION; TOXEMIA; TOXIC INHALATION;

ANIMALS; ANTHRAX; ANTHRAX VACCINES; BACILLUS ANTHRACIS; BACTERIAL CAPSULES; BACTERIAL TOXINS; BRONCHIOLES; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; INHALATION EXPOSURE; MICE; PATHOLOGY, MOLECULAR; PHAGOCYTES; SPORES, BACTERIAL; VACCINATION; VIRULENCE FACTORS;

BACILLUS ANTHRACIS;

EID: 81155131004     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2011.07.005     Document Type: Short Survey

References (90)

1. Anthrax in humans and animals 2008, WHO Press, Geneva. P. Turnbull (Ed.).
2. Mock M., Fouet A. Anthrax. Annu. Rev. Microbiol. 2001, 55:647-671.
3. Ringertz S.H., Hoiby E.A., Jensenius M., Maehlen J., Caugant D.A., Myklebust A., Fossum K. Injectional anthrax in a heroin skin-popper. Lancet 2000, 356:1574-1575.
4. Mason J.M., Setlow P. Essential role of small, acid-soluble spore proteins in resistance of Bacillus subtilis spores to UV light. J. Bacteriol. 1986, 167:174-178.
5. Popham D.L. Specialized peptidoglycan of the bacterial endospore: the inner wall of the lockbox. Cell Mol. Life Sci. 2002, 59:426-433.
6. Giorno R., Bozue J., Cote C., Wenzel T., Moody K.S., Mallozzi M., Ryan M., Wang R., Zielke R., Maddock J.R., Friedlander A., Welkos S., Driks A. Morphogenesis of the Bacillus anthracis spore. J. Bacteriol. 2007, 189:691-705.
7. Steichen C.T., Kearney J.F., Turnbough C.L. Characterization of the exosporium basal layer protein BxpB of Bacillus anthracis. J. Bacteriol. 2005, 187:5868-5876.
8. Sylvestre P., Couture-Tosi E., Mock M. Contribution of ExsFA and ExsFB proteins to the localization of BclA on the spore surface and to the stability of the Bacillus anthracis exosporium. J. Bacteriol. 2005, 187:5122-5128.
9. Gerhardt P., Ribi E. Ultrastructure of the exosporium enveloping spores of Bacillus cereus. J. Bacteriol. 1964, 88:1774-1789.
10. Sylvestre P., Couture-Tosi E., Mock M. A collagen-like surface glycoprotein is a structural component of the Bacillus anthracis exosporium. Mol. Microbiol. 2002, 45:169-178.
11. Brahmbhatt T.N., Janes B.K., Stibitz E.S., Darnell S.C., Sanz P., Rasmussen S.B., O'Brien A.D. Bacillus anthracis exosporium protein BclA affects spore germination, interaction with extracellular matrix proteins, and hydrophobicity. Infect. Immun. 2007, 75:5233-5239.
12. Daubenspeck J.M., Zeng H., Chen P., Dong S., Steichen C.T., Krishna N.R., Pritchard D.G., Turnbough C.L. Novel oligosaccharide side chains of the collagen-like region of BclA, the major glycoprotein of the Bacillus anthracis exosporium. J. Biol. Chem. 2004, 279:30945-30953.
13. Bozue J., Cote C.K., Moody K.L., Welkos S.L. Fully virulent Bacillus anthracis does not require the immunodominant protein, BclA, for pathogenesis. Infect. Immun. 2007, 75:508-511.
14. Bozue J., Moody K.L., Cote C.K., Stiles B.G., Friedlander A.M., Welkos S.L., Hale M.L. Bacillus anthracis spores of the bclA mutant exhibit increased adherence to epithelial cells, fibroblasts, and endothelial cells but not to macrophages. Infect. Immun. 2007, 75:4498-4505.
15. Oliva C.R., Swiecki M.K., Griguer C.E., Lisanby M.W., Bullard D.C., Turnbough C.L., Kearney J.F. The integrin Mac-1 (CR3) mediates internalization and directs Bacillus anthracis spores into professional phagocytes. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:1261-1266.
16. Kang T.J., Fenton M.J., Weiner M.A., Hibbs S., Basu S., Baillie L., Cross A.S. Murine macrophages kill the vegetative form of Bacillus anthracis. Infect. Immun. 2005, 73:7495-7501.
17. Cybulski R.J., Sanz P., Alem F., Stibitz S., Bull R.L., O'Brien A.D. Four superoxide dismutases contribute to Bacillus anthracis virulence and provide spores with redundant protection from oxidative stress. Infect. Immun. 2008, 77:274-285.
18. Redmond C., Baillie L.W., Hibbs S., Moir A.J., Moir A. Identification of proteins in the exosporium of Bacillus anthracis. Microbiology 2004, 150:355-363.
19. McKevitt M.T., Bryant K.M., Shakir S.M., Larabee J.L., Blanke S.R., Lovchik J., Lyons C.R., Ballard J.D. Effects of endogenous D-alanine synthesis and autoinhibition of Bacillus anthracis germination on in vitro and in vivo infections. Infect. Immun. 2007, 75:5726-5734.
20. Fisher N., Shetron-Rama L., Herring-Palmer A., Heffernan B., Bergman N., Hanna P. The dltABCD operon of Bacillus anthracis sterne is required for virulence and resistance to peptide, enzymatic, and cellular mediators of innate immunity. J. Bacteriol. 2006, 188:1301-1309.
21. Guidi-Rontani C., Pereira Y., Ruffie S., Sirard J.C., Weber-Levy M., Mock M. Identification and characterization of a germination operon on the virulence plasmid pXO1 of Bacillus anthracis. Mol. Microbiol. 1999, 33:407-414.
22. Moir A., Smith D. The genetics of bacterial spore germination. Annu. Rev. Microbiol. 1990, 44:5331-5553.
23. Carr K.A., Lybarger S.R., Anderson E.C., Janes B.K., Hanna P.C. The role of Bacillus anthracis germinant receptors in germination and virulence. Mol. Microbiol. 2010, 75:365-375.
24. Read T.D., Peterson S.N., Tourasse N., Baillie L.W., Paulsen I.T., Nelson K.E., Tettelin H., Fouts D.E., Eisen J.A., Gill S.R., Holtzapple E.K., Okstad O.A., Helgason E., Rilstone J., Wu M., Kolonay J.F., Beanan M.J., Dodson R.J., Brinkac L.M., Gwinn M., DeBoy R.T., Madpu R., Daugherty S.C., Durkin A.S., Haft D.H., Nelson W.C., Peterson J.D., Pop M., Khouri H.M., Radune D., Benton J.L., Mahamoud Y., Jiang L., Hance I.R., Weidman J.F., Berry K.J., Plaut R.D., Wolf A.M., Watkins K.L., Nierman W.C., Hazen A., Cline R., Redmond C., Thwaite J.E., White O., Salzberg S.L., Thomason B., Friedlander A.M., Koehler T.M., Hanna P.C., Kolsto A.B., Fraser C.M. The genome sequence of Bacillus anthracis Ames and comparison to closely related bacteria. Nature 2003, 423:81-86.
25. Guidi-Rontani C., Weber-Levy M., Labruyere E., Mock M. Germination of Bacillus anthracis spores within alveolar macrophages. Mol. Microbiol. 1999, 31:9-17.
26. Weiner M.A., Hanna P.C. Macrophage-mediated germination of Bacillus anthracis endospores requires the gerH operon. Infect. Immun. 2003, 71:3954-3959.
27. Ireland J., Hanna P.C. Macrophage-enhanced germination of Bacillus anthracis endospores requires gerS. Infect. Immun. 2002, 70:5870-5872.
28. Barua S., McKevitt M., DeGiusti K., Hamm E.E., Larabee J., Shakir S., Bryant K., Koehler T.M., Blanke S.R., Dyer D., Gillaspy A., Ballard J.D. The mechanism of Bacillus anthracis intracellular germination requires multiple and highly diverse genetic loci. Infect. Immun 2009, 77:23-31.
29. Setlow P. Spore germination. Curr. Opin. Microbiol. 2003, 6:550-556.
30. Steichen C.T., Kearney J.F., Turnbough C.L. Non-uniform assembly of the Bacillus anthracis exosporium and a bottle cap model for spore germination and outgrowth. Mol. Microbiol. 2007, 64:359-367.
31. Ross J.M. The pathogenesis of anthrax following the administration of spores by the respiratory route. J. Pathol. Bacteriol. 1957, 73:485-494.
32. Glomski I.J., Dumetz F., Jouvion G., Huerre M.R., Mock M., Goossens P.L. 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.
33. Glomski I.J., Piris-Gimenez A., Huerre M., Mock M., Goossens P.L. Primary involvement of pharynx and Peyer's patch in inhalational and intestinal anthrax. PLoS Pathog. 2007, 3:e76.
34. Russell B.H., Liu Q., Jenkins S.A., Tuvim M.J., Xu Y. In vivo demonstration and quantification of intracellular Bacillus anthracis in lung epithelial cells. Infect. Immun. 2008, 76:3975-3983.
35. Pickering A.K., Osorio M., Lee G.M., Grippe V.K., Bray M., Merkel T.J. Cytokine response to infection with Bacillus anthracis spores. Infect. Immun. 2004, 72:6382-6389.
36. Sanz P., Teel L.D., Alem F., Carvalho H.M., Darnell S.C., O'Brien A.D. Detection of Bacillus anthracis spore germination in vivo by bioluminescence imaging. Infect. Immun. 2008, 76:1036-1047.
37. Heninger S., Drysdale M., Lovchik J., Hutt J., Lipscomb M.F., Koehler T.M., Lyons C.R. Toxin-deficient mutants of Bacillus anthracis are lethal in a murine model for pulmonary anthrax. Infect. Immun. 2006, 74:6067-6074.
38. Cote C.K., Bozue J., Twenhafel N., Welkos S.L. Effects of altering the germination potential of Bacillus anthracis spores by exogenous means in a mouse model. J. Med. Microbiol. 2009, 58:816-825.
39. Cleret A., Quesnel-Hellmann A., Vallon-Eberhard A., Verrier B., Jung S., Vidal D., Mathieu J., Tournier J.N. Lung dendritic cells rapidly mediate anthrax spore entry through the pulmonary route. J. Immunol. 2007, 178:7994-8001.
40. Twenhafel N.A. Pathology of inhalational anthrax animal models. Vet. Pathol. 2010, 47:819-830.
41. Grinberg L.M., Abramova F.A., Yampolskaya O.V., Walker D.H., Smith J.H. Quantitative pathology of inhalational anthrax I: quantitative microscopic findings. Mod. Pathol. 2001, 14:482-495.
42. Welkos S.L., Trotter R.W., Becker D.M., Nelson G.O. Resistance to the Sterne strain of B. anthracis: phagocytic cell responses of resistant and susceptible mice. Microb. Pathog. 1989, 7:15-35.
43. Bozue J.A., Parthasarathy N., Phillips L.R., Cote C.K., Fellows P.F., Mendelson I., Shafferman A., Friedlander A.M. Construction of a rhamnose mutation in Bacillus anthracis affects adherence to macrophages but not virulence in guinea pigs. Microb. Pathog. 2005, 38:1-12.
44. Banks D.J., Barnajian M., Maldonado-Arocho F.J., Sanchez A.M., Bradley K.A. Anthrax toxin receptor 2 mediates Bacillus anthracis killing of macrophages following spore challenge. Cell. Microbiol. 2005, 7:1173-1185.
45. Welkos S., Friedlander A., Weeks S., Little S., Mendelson I. In-vitro characterisation of the phagocytosis and fate of anthrax spores in macrophages and the effects of anti-PA antibody. J. Med. Microbiol. 2002, 51:821-831.
46. Cote C.K., Dimezzo T.L., Banks D.J., France B., Bradley K.A., Welkos S.L. Early interactions between fully virulent Bacillus anthracis and macrophages that influence the balance between spore clearance and development of a lethal infection. Microbes Infect. 2008, 10:613-619.
47. Hu H., Sa Q., Koehler T.M., Aronson A.I., Zhou D. Inactivation of Bacillus anthracis spores in murine primary macrophages. Cell. Microbiol. 2006, 8:1634-1642.
48. Ribot W.J., Panchal R.G., Brittingham K.C., Ruthel G., Kenny T.A., Lane D., Curry B., Hoover T.A., Friedlander A.M., Bavari S. Anthrax lethal toxin impairs innate immune functions of alveolar macrophages and facilitates Bacillus anthracis survival. Infect. Immun. 2006, 74:5029-5034.
49. Chakrabarty K., Wu W., Booth J.L., Duggan E.S., Coggeshall K.M., Metcalf J.P. Bacillus anthracis spores stimulate cytokine and chemokine innate immune responses in human alveolar macrophages through multiple mitogen-activated protein kinase pathways. Infect. Immun. 2006, 74:4430-4438.
50. Guidi-Rontani C. The alveolar macrophage: the Trojan horse of Bacillus anthracis. Trends Microbiol. 2002, 10:405-409.
51. Cote C.K., van Rooijen N., Welkos S.L. The roles of macrophages and neutrophils in the early host response to Bacillus anthracis spores using a mouse model of infection. Infect. Immun. 2006, 74:469-480.
52. Mayer-Scholl A., Hurwitz R., Brinkmann V., Schmid M., Jungblut P., Weinrauch Y., Zychlinsky A. Human neutrophils kill Bacillus anthracis. PLoS Pathog. 2005, 1:e23.
53. Brittingham K.C., Ruthel G., Panchal R.G., Fuller C.L., Ribot W.J., Hoover T.A., Young H.A., Anderson A.O., Bavari S. Dendritic cells endocytose Bacillus anthracis spores: implications for anthrax pathogenesis. J. Immunol. 2005, 174:5545-5552.
54. Barnes J.M. The development of anthrax following the administration of spores by Inhalation. Br. J. Exp. Pathol. 1947, 28:385-393.
55. Welkos S., Little S., Friedlander A., Fritz D., Fellows P. The role of antibodies to Bacillus anthracis and anthrax toxin components in inhibiting the early stages of infection by anthrax spores. Microbiology 2001, 147:1677-1685.
56. Cote C.K., Rossi C.A., Kang A.S., Morrow P.R., Lee J.S., Welkos S.L. The detection of protective antigen (PA) associated with spores of Bacillus anthracis and the effects of anti-PA antibodies on spore germination and macrophage interactions. Microb. Pathog. 2005, 38:209-225.
57. Baldari C.T., Tonello F., Paccani S.R., Montecucco C. Anthrax toxins: a paradigm of bacterial immune suppression. Trends Immunol. 2006, 27:434-440.
58. Cleret A., Quesnel-Hellmann A., Mathieu J., Vidal D., Tournier J.N. Resident CD11c+ lung cells are impaired by anthrax toxins after spore infection. J. Infect. Dis. 2006, 194:86-94.
59. Duesbery N.S., Vande Woude G.F. Anthrax toxins. Cell Mol. Life Sci. 1999, 55:1599-1609.
60. During R.L., Li W., Hao B., Koenig J.M., Stephens D.S., Quinn C.P., Southwick F.S. Anthrax lethal toxin paralyzes neutrophil actin-based motility. J. Infect. Dis. 2005, 192:837-845.
61. Friedlander A.M., Bhatnagar R., Leppla S.H., Johnson L., Singh Y. Characterization of macrophage sensitivity and resistance to anthrax lethal toxin. Infect. Immun. 1993, 61:245-252.
62. Hanna P.C., Acosta D., Collier R.J. On the role of macrophages in anthrax. Proc. Natl. Acad. Sci. U.S.A 1993, 90:10198-10201.
63. Tournier J.N., Quesnel-Hellmann A., Mathieu J., Montecucco C., Tang W.J., Mock M., Vidal D.R., Goossens P.L. Anthrax edema toxin cooperates with lethal toxin to impair cytokine secretion during infection of dendritic cells. J. Immunol. 2005, 174:4934-4941.
64. Young J.A., Collier R.J. Anthrax toxin: receptor binding, internalization, pore formation, and translocation. Annu. Rev. Biochem. 2007, 76:243-265.
65. Banks D.J., Ward S.C., Bradley K.A. New insights into the functions of anthrax toxin. Expert Rev. Mol. Med. 2006, 8:1-18.
66. Firoved A.M., Miller G.F., Moayeri M., Kakkar R., Shen Y., Wiggins J.F., McNally E.M., Tang W.J., Leppla S.H. Bacillus anthracis edema toxin causes extensive tissue lesions and rapid lethality in mice. Am. J. Pathol. 2005, 167:1309-1320.
67. Moayeri M., Haines D., Young H.A., Leppla S.H. Bacillus anthracis lethal toxin induces TNF-alpha-independent hypoxia-mediated toxicity in mice. J. Clin. Invest. 2003, 112:670-682.
68. Bradley K.A., Mogridge J., Mourez M., Collier R.J., Young J.A. Identification of the cellular receptor for anthrax toxin. Nature 2001, 414:225-229.
69. Scobie H.M., Rainey G.J., Bradley K.A., Young J.A. Human capillary morphogenesis protein 2 functions as an anthrax toxin receptor. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:5170-5174.
70. Friedlander A.M. Macrophages are sensitive to anthrax lethal toxin through an acid-dependent process. J. Biol. Chem. 1986, 261:7123-7126.
71. O'Brien J., Friedlander A., Dreier T., Ezzell J., Leppla S. Effects of anthrax toxin components on human neutrophils. Infect. Immun. 1985, 47:306-310.
72. Paccani S.R., Tonello F., Ghittoni R., Natale M., Muraro L., D'Elios M.M., Tang W.J., Montecucco C., Baldari C.T. Anthrax toxins suppress T lymphocyte activation by disrupting antigen receptor signaling. J. Exp. Med. 2005, 201:325-331.
73. Hu H., Leppla S.H. Anthrax toxin uptake by primary immune cells as determined with a lethal factor-beta-lactamase fusion protein. PLoS One 2009, 4:e7946.
74. Agrawal A., Lingappa J., Leppla S.H., Agrawal S., Jabbar A., Quinn C., Pulendran B. Impairment of dendritic cells and adaptive immunity by anthrax lethal toxin. Nature 2003, 424:329-334.
75. Jones W.I., Klein F., Walker J.S., Mahlandt B.G., Dobbs J.P., Lincoln R.E. In vivo growth and distribution of anthrax bacilli in resistant, susceptible, and immunized hosts. J. Bacteriol. 1967, 94:600-608.
76. Welkos S.L., Friedlander A.M. Pathogenesis and genetic control of resistance to the Sterne strain of Bacillus anthracis. Microb. Pathog. 1988, 4:53-69.
77. Welkos S.L., Keener T.J., Gibbs P.H. Differences in susceptibility of inbred mice to Bacillus anthracis. Infect. Immun. 1986, 51:795-800.
78. Lincoln R.E., Walker J.S., Klein F., Rosenwald A.J., Jones W.I. Value of field data for extrapolation in anthrax. Fed. Proc. 1967, 26:1558-1562.
79. Beall F.A., Dalldorf F.G. The pathogenesis of the lethal effect of anthrax toxin in the rat. J. Infect. Dis. 1966, 116:377-389.
80. Liu S., Miller-Randolph S., Crown D., Moayeri M., Sastalla I., Okugawa S., Leppla S.H. Anthrax toxin targeting of myeloid cells through the CMG2 receptor is essential for establishment of Bacillus anthracis infections in mice. Cell Host Microbe 2010, 8:455-462.
81. Terra J.K., Cote C.K., France B., Jenkins A.L., Bozue J.A., Welkos S.L., LeVine S.M., Bradley K.A. Cutting edge: resistance to Bacillus anthracis infection mediated by a lethal toxin sensitive allele of Nalp1b/Nlrp1b. J. Immunol. 2010, 184:17-20.
82. Bruckner V., Kovacs J., Denes G. Structure of poly-D-glutamic acid isolated from capsulated strains of B. anthracis. Nature 1953, 172:508.
83. 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.
84. Chabot D.J., Scorpio A., Tobery S.A., Little S.F., Norris S.L., Friedlander A.M. Anthrax capsule vaccine protects against experimental infection. Vaccine 2004, 23:43-47.
85. Kozel T.R., Thorkildson P., Brandt S., Welch W.H., Lovchik J.A., AuCoin D.P., Vilai J., Lyons C.R. Protective and immunochemical activities of monoclonal antibodies reactive with the Bacillus anthracis polypeptide capsule. Infect. Immun. 2007, 75:152-163.
86. Makino S., Uchida I., Terakado N., Sasakawa C., Yoshikawa M. Molecular characterization and protein analysis of the cap region, which is essential for encapsulation in Bacillus anthracis. J. Bacteriol. 1989, 171:722-730.
87. Scorpio A., Tobery S.A., Ribot W.J., Friedlander A.M. Treatment of experimental anthrax with recombinant capsule depolymerase. Antimicrob. Agents Chemother. 2008, 52:1014-1020.
88. Bradley K.A., LeVine S.M. Anthrax toxin delivers a one-two punch. Cell Host Microbe 2010, 8:394-395.
89. Klein F., Haines B.W., Mahlandt B.G., Dearmon I.A., Lincoln R.E. Dual nature of resistance mechanisms as revealed by studies of anthrax septicemia. J. Bacteriol. 1963, 85:1032-1038.
90. Friedlander A.M., Welkos S.L., Pitt M.L., Ezzell J.W., Worsham P.L., Rose K.J., Ivins B.E., Lowe J.R., Howe G.B., Mikesell P. Postexposure prophylaxis against experimental inhalation anthrax. J. Infect. Dis. 1993, 167:1239-1243.