The effects of anthrax lethal toxin on host barrier function

Toxins

Volumn 3, Issue 6, 2011, Pages 591-607

  Xie, Tao ^a   Auth, Roger D ^a   Frucht, David M ^a  

^a CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

Anthrax lethal toxin; Bacteria; Barrier function; Blood brain barrier; Endothelium; Epithelium; Infection; Intestine

Indexed keywords

ANTHRAX TOXIN; ANTIGEN; BACTERIAL TOXIN; EARLY GROWTH RESPONSE FACTOR 1; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; STRESS ACTIVATED PROTEIN KINASE; VASCULAR ENDOTHELIAL CADHERIN; X LINKED INHIBITOR OF APOPTOSIS;

ANTHRAX; BACILLUS ANTHRACIS; BLOOD BRAIN BARRIER; BRONCHOSCOPY; CELL FUNCTION; CELL MOTILITY; CELL POLARITY; CELL PROLIFERATION; CLINICAL FEATURE; COMPUTER ASSISTED TOMOGRAPHY; CYTOTOXICITY; DISEASE ASSOCIATION; DOWN REGULATION; ENDOTHELIUM CELL; EPITHELIUM CELL; HOMEOSTASIS; HOST PATHOGEN INTERACTION; HUMAN; IN VITRO STUDY; LUNG ALVEOLUS EPITHELIUM; MEMBRANE DAMAGE; MENINGOENCEPHALITIS; MOLECULAR BIOLOGY; NONHUMAN; PERMEABILITY BARRIER; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; REVIEW; THORAX RADIOGRAPHY; TOXIC INHALATION; TOXIN ANALYSIS; TOXIN SYNTHESIS;

ANIMALS; ANTHRAX; ANTIGENS, BACTERIAL; BACILLUS ANTHRACIS; BACTERIAL TOXINS; BLOOD-AQUEOUS BARRIER; ENDOTHELIUM, VASCULAR; EPITHELIUM; HOST-PATHOGEN INTERACTIONS; HUMANS; INTESTINES; LUNG;

ANIMALIA;

EID: 79959681046     PISSN: None     EISSN: 20726651     Source Type: Journal    
DOI: 10.3390/toxins3060591     Document Type: Review

References (86)

1. van der Goot, G.; Young, J.A. Receptors of anthrax toxin and cell entry. Mol. Aspects Med. 2009, 30, 406-412.
2. Xu, L.; Frucht, D.M. Bacillus anthracis: A multi-faceted role for anthrax lethal toxin in thwarting host immune defenses. Int. J. Biochem. Cell. Biol. 2007, 39, 20-24.
3. 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.
4. Cordoba-Rodriguez, R.; Fang, H.; Lankford, C.S.; Frucht, D.M. Anthrax lethal toxin rapidly activates caspase-1/ICE and induces extracellular release of interleukin (IL)-1beta and IL-18. J. Biol. Chem. 2004, 279, 20563-20566.
5. Boyden, E.D.; Dietrich, W.F. Nalp1b controls mouse macrophage susceptibility to anthrax lethal toxin. Nat. Genet. 2006, 38, 240-244.
6. Tournier, J.N.; Rossi Paccani, S.; Quesnel-Hellmann, A.; Baldari, C.T. Anthrax toxins: A weapon to systematically dismantle the host immune defenses. Mol. Aspects Med. 2009, 30, 456-466.
7. Stanley, J.L.; Smith, H. Purification of factor I and recognition of a third factor of the anthrax toxin. J. Gen. Microbiol. 1961, 26, 49-63.
8. Beall, F.A.; Taylor, M.J.; Thorne, C.B. Rapid lethal effect in rats of a third component found upon fractionating the toxin of Bacillus anthracis. J. Bacteriol. 1962, 83, 1274-1280.
9. Fish, D.C.; Klein, F.; Lincoln, R.E.; Walker, J.S.; Dobbs, J.P. Pathophysiological changes in the rat associated with anthrax toxin. J. Infect. Dis. 1968, 118, 114-124.
10. Fang, H.; Sun, C.; Xu, L.; Owen, R.J.; Auth, R.D.; Snoy, P.J.; Frucht, D.M. Neutrophil elastase mediates pathogenic effects of anthrax lethal toxin in the murine intestinal tract. J. Immunol.2010, 185, 5463-5467.
11. Gozes, Y.; Moayeri, M.; Wiggins, J.F.; Leppla, S.H. Anthrax lethal toxin induces ketotifen-sensitive intradermal vascular leakage in certain inbred mice. Infect. Immun. 2006, 74, 1266-1272.
12. Warfel, J.M.; Steele, A.D.; D'Agnillo, F. Anthrax lethal toxin induces endothelial barrier dysfunction. Am. J. Pathol. 2005, 166, 1871-1881.
13. Kirby, J.E. Anthrax lethal toxin induces human endothelial cell apoptosis. Infect. Immun. 2004, 72, 430-439.
14. Mullin, J.M.; Agostino, N.; Rendon-Huerta, E.; Thornton, J.J. Keynote review: Epithelial and endothelial barriers in human disease. Drug Discov. Today 2005, 10, 395-408.
15. Dejana, E. Endothelial cell-cell junctions: Happy together. Nat. Rev. Mol. Cell. Biol. 2004, 5, 261-270.
16. Groschwitz, K.R.; Hogan, S.P. Intestinal barrier function: molecular regulation and disease pathogenesis. J. Allergy Clin. Immunol. 2009, 124, 3-20; quiz 21-22.
17. Breitkreutz, D.; Mirancea, N.; Nischt, R. Basement membranes in skin: Unique matrix structures with diverse functions? Histochem. Cell. Biol. 2009, 132, 1-10.
18. Fromm, M.; Schulzke, J.D.; Hegel, U. Epithelial and subepithelial contributions to transmural electrical resistance of intact rat jejunum, in vitro. Pflugers Arch. 1985, 405, 400-402.
19. Gitter, A.H.; Bendfeldt, K.; Schulzke, J.D.; Fromm, M. Trans/paracellular, surface/crypt, and epithelial/subepithelial resistances of mammalian colonic epithelia. Pflugers Arch. 2000, 439, 477-482.
20. Turnbull, P.C. Introduction: Anthrax history, disease and ecology. Curr. Top. Microbiol. Immunol. 2002, 271, 1-19.
21. Martin, G.J.; Friedlander, A.M. Bacillus anthracis (anthrax). In Mandell, Douglas, and Bennett's Principles and Practice of Infectious Diseases, 7th ed.; Mandell, G.L., Bennett, J.E., Dolin, R., Eds.; Churchill Livingstone Elsevier: Philadelphia, PA, USA, 2010; Volume 2, pp. 2715-2725.
22. Jernigan, D.B.; Raghunathan, P.L.; Bell, B.P.; Brechner, R.; Bresnitz, E.A.; Butler, J.C.; Cetron, M.; Cohen, M.; Doyle, T.; Fischer, M. et al. Investigation of bioterrorism-related anthrax, United States, 2001: epidemiologic findings. Emerg. Infect. Dis. 2002, 8, 1019-1028.
23. Inglesby, T.V.; O'Toole, T.; Henderson, D.A.; Bartlett, J.G.; Ascher, M.S.; Eitzen, E.; Friedlander, A.M.; Gerberding, J.; Hauer, J.; Hughes, J.; McDade, J.; Osterholm, M.T.; Parker, G.; Perl, T.M.; Russell, P.K.; Tonat, K. Anthrax as a biological weapon, 2002: updated recommendations for management. JAMA 2002, 287, 2236-2252.
24. Booth, M.G.; Hood, J.; Brooks, T.J.; Hart, A. Anthrax infection in drug users. Lancet 2010, 375, 1345-1346.
25. 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.
26. Dutz, W.; Saidi, F.; Kohout, E. Gastric anthrax with massive ascites. Gut 1970, 11, 352-354.
27. Knudson, G.B. Treatment of anthrax in man: History and current concepts. Mil. Med. 1986, 151, 71-77.
28. Coleman, M.E.; Thran, B.; Morse, S.S.; Hugh-Jones, M.; Massulik, S. Inhalation anthrax: Dose response and risk analysis. Biosecur. Bioterror. 2008, 6, 147-160.
29. Peters, C.J.; Hartley, D.M. Anthrax inhalation and lethal human infection. Lancet 2002, 359, 710-711.
30. Reissman, D.B.; Whitney, E.A.; Taylor, T.H., Jr.; Hayslett, J.A.; Dull, P.M.; Arias, I.; Ashford, D.A.; Bresnitz, E.A.; Tan, C.; Rosenstein, N.; Perkins, B.A. One-year health assessment of adult survivors of Bacillus anthracis infection. JAMA 2004, 291, 1994-1998.
31. 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.
32. 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.
33. 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.
34. 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. Immunol. 2008, 76, 1036-1047.
35. Guidi-Rontani, C. The alveolar macrophage: The Trojan horse of Bacillus anthracis. Trends Microbiol. 2002, 10, 405-409.
36. Abramova, F.A.; Grinberg, L.M.; Yampolskaya, O.V.; Walker, D.H. Pathology of inhalational anthrax in 42 cases from the Sverdlovsk outbreak of 1979. Proc. Natl. Acad. Sci. USA 1993, 90, 2291-2294.
37. 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.
38. Fritz, D.L.; Jaax, N.K.; Lawrence, W.B.; Davis, K.J.; Pitt, M.L.; Ezzell, J.W.; Friedlander, A.M. Pathology of experimental inhalation anthrax in the rhesus monkey. Lab. Invest. 1995, 73, 691-702.
39. Rolando, M.; Munro, P.; Stefani, C.; Auberger, P.; Flatau, G.; Lemichez, E. Injection of Staphylococcus aureus EDIN by the Bacillus anthracis protective antigen machinery induces vascular permeability. Infect. Immunol. 2009, 77, 3596-3601.
40. Cui, X.; Moayeri, M.; Li, Y.; Li, X.; Haley, M.; Fitz, Y.; Correa-Araujo, R.; Banks, S.M.; Leppla, S.H.; Eichacker, P.Q. Lethality during continuous anthrax lethal toxin infusion is associated with circulatory shock but not inflammatory cytokine or nitric oxide release in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2004, 286, 699-709.
41. Rolando, M.; Stefani, C.; Flatau, G.; Auberger, P.; Mettouchi, A.; Mhlanga, M.; Rapp, U.; Galmiche, A.; Lemichez, E. Transcriptome dysregulation by anthrax lethal toxin plays a key role in induction of human endothelial cell cytotoxicity. Cell. Microbiol. 2010, 12, 891-905.
42. Moayeri, M.; Leppla, S.H. Cellular and systemic effects of anthrax lethal toxin and edema toxin. Mol. Aspects Med. 2009, 30, 439-455.
43. Guichard, A.; McGillivray, S.M.; Cruz-Moreno, B.; van Sorge, N.M.; Nizet, V.; Bier, E. Anthrax toxins cooperatively inhibit endocytic recycling by the Rab11/Sec15 exocyst. Nature 2010, 467, 854-858.
44. Warfel, J.M.; D'Agnillo, F. Anthrax lethal toxin enhances IkappaB kinase activation and differentially regulates pro-inflammatory genes in human endothelium. J. Biol. Chem. 2009, 284, 25761-25771.
45. Warfel, J.M.; D'Agnillo, F. Anthrax lethal toxin enhances TNF-induced endothelial VCAM-1 expression via an IFN regulatory factor-1-dependent mechanism. J. Immunol. 2008, 180, 7516-7524.
46. Steele, A.D.; Warfel, J.M.; D'Agnillo, F. Anthrax lethal toxin enhances cytokine-induced VCAM-1 expression on human endothelial cells. Biochem. Biophys. Res. Commun. 2005, 337, 1249-1256.
47. Steiner, O.; Coisne, C.; Cecchelli, R.; Boscacci, R.; Deutsch, U.; Engelhardt, B.; Lyck, R. Differential roles for endothelial ICAM-1, ICAM-2, and VCAM-1 in shear-resistant T cell arrest, polarization, and directed crawling on blood-brain barrier endothelium. J. Immunol. 2010, 185, 4846-4855.
48. Sundy, J.S.; Haynes, B.F. Cytokines and adhesion molecules in the pathogenesis of vasculitis. Curr. Rheumatol. Rep. 2000, 2, 402-410.
49. Jernigan, J.A.; Stephens, D.S.; Ashford, D.A.; Omenaca, C.; Topiel, M.S.; Galbraith, M.; Tapper, M.; Fisk, T.L.; Zaki, S.; Popovic, T.; Meyer, R.F.; Quinn, C.P.; Harper, S.A.; Fridkin, S.K.; Sejvar, J.J.; Shepard, C.W.; McConnell, M.; Guarner, J.; Shieh, W.J.; Malecki, J.M.; Gerberding, J.L.; Hughes, J.M.; Perkins, B.A. Bioterrorism-related inhalational anthrax: The first 10 cases reported in the United States. Emerg. Infect. Dis. 2001, 7, 933-944.
50. Kuo, S.R.; Willingham, M.C.; Bour, S.H.; Andreas, E.A.; Park, S.K.; Jackson, C.; Duesbery, N.S.; Leppla, S.H.; Tang, W.J.; Frankel, A.E. Anthrax toxin-induced shock in rats is associated with pulmonary edema and hemorrhage. Microb. Pathog. 2008, 44, 467-472.
51. Maniatis, N.A.; Kotanidou, A.; Catravas, J.D.; Orfanos, S.E. Endothelial pathomechanisms in acute lung injury. Vascul. Pharmacol. 2008, 49, 119-133.
52. Lehmann, M.; Noack, D.; Wood, M.; Perego, M.; Knaus, U.G. Lung epithelial injury by B. anthracis lethal toxin is caused by MKK-dependent loss of cytoskeletal integrity. PLoS One 2009, 4, e4755.
53. Popova, T.; Espina, V.; Bailey, C.; Liotta, L.; Petricoin, E.; Popov, S. Anthrax infection inhibits the AKT signaling involved in the E-cadherin-mediated adhesion of lung epithelial cells. FEMS Immunol. Med. Microbiol. 2009, 56, 129-142.
54. 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.
55. Potten, C.S. Epithelial cell growth and differentiation. II. Intestinal apoptosis. Am. J. Physiol. 1997, 273, 253-257.
56. Radtke, F.; Clevers, H. Self-renewal and cancer of the gut: Two sides of a coin. Science 2005, 307, 1904-1909.
57. Moore, R.; Carlson, S.; Madara, J.L. Rapid barrier restitution in an in vitro model of intestinal epithelial injury. Lab. Invest. 1989, 60, 237-244.
58. Nusrat, A.; Delp, C.; Madara, J.L. Intestinal epithelial restitution. Characterization of a cell culture model and mapping of cytoskeletal elements in migrating cells. J. Clin. Invest. 1992, 89, 1501-1511.
59. Chung, M.C.; Jorgensen, S.C.; Popova, T.G.; Bailey, C.L.; Popov, S.G. Neutrophil elastase and syndecan shedding contribute to antithrombin depletion in murine anthrax. FEMS Immunol. Med. Microbiol. 2008, 54, 309-318.
60. Hirahashi, J.; Mekala, D.; van Ziffle, J.; Xiao, L.; Saffaripour, S.; Wagner, D.D.; Shapiro, S.D.; Lowell, C.; Mayadas, T.N. Mac-1 signaling via Src-family and Syk kinases results in elastase-dependent thrombohemorrhagic vasculopathy. Immunity 2006, 25, 271-283.
61. Xu, L.; Fang, H.; Frucht, D.M. Anthrax lethal toxin increases superoxide production in murine neutrophils via differential effects on MAPK signaling pathways. J. Immunol. 2008, 180, 4139-4147.
62. Crawford, M.A.; Aylott, C.V.; Bourdeau, R.W.; Bokoch, G.M. Bacillus anthracis toxins inhibit human neutrophil NADPH oxidase activity. J. Immunol. 2006, 176, 7557-7565.
63. 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.
64. 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.
65. Gasbarrini, G.; Montalto, M. Structure and function of tight junctions. Role in intestinal barrier. Ital. J. Gastroenterol. Hepatol. 1999, 31, 481-488.
66. Fang, H.; Xu, L.; Chen, T.Y.; Cyr, J.M.; Frucht, D.M. Anthrax lethal toxin has direct and potent inhibitory effects on B cell proliferation and immunoglobulin production. J. Immunol. 2006, 176, 6155-6161.
67. Comer, J.E.; Chopra, A.K.; Peterson, J.W.; Konig, R. Direct inhibition of T-lymphocyte activation by anthrax toxins in vivo. Infect. Immunol.2005, 73, 8275-8281.
68. Fang, H.; Cordoba-Rodriguez, R.; Lankford, C.S.; Frucht, D.M. Anthrax lethal toxin blocks MAPK kinase-dependent IL-2 production in CD4+ T cells. J. Immunol. 2005, 174, 4966-4971.
69. 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.
70. Okugawa, S.; Moayeri, M.; Eckhaus, M.A.; Crown, D.; Miller-Randolph, S.; Liu, S.; Akira, S.; Leppla, S.H. MyD88-dependent signaling protects against anthrax lethal toxin-induced impairment of intestinal barrier function. Infect. Immunol. 2011, 79, 118-124.
71. Owens, W.E.; Berg, R.D. Bacterial translocation from the gastrointestinal tract of athymic (nu/nu) mice. Infect. Immunol. 1980, 27, 461-467.
72. Gautreaux, M.D.; Deitch, E.A.; Berg, R.D. Bacterial translocation from the gastrointestinal tract to various segments of the mesenteric lymph node complex. Infect. Immunol. 1994, 62, 2132-2134.
73. Lanska, D.J. Anthrax meningoencephalitis. Neurology 2002, 59, 327-334.
74. 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.
75. van Sorge, N.M.; Ebrahimi, C.M.; McGillivray, S.M.; Quach, D.; Sabet, M.; Guiney, D.G.; Doran, K.S. Anthrax toxins inhibit neutrophil signaling pathways in brain endothelium and contribute to the pathogenesis of meningitis. PLoS One 2008, 3, e2964.
76. Bonventre, P.F.; Sueoka, W.; True, C.W.; Klein, F.; Lincoln, R. Attempts to implicate the central nervous system as a primary site of action for Bacillus anthracis lethal toxin. Fed. Proc. 1967, 26, 1549-1553.
77. Argaw, A.T.; Zhang, Y.; Snyder, B.J.; Zhao, M.L.; Kopp, N.; Lee, S.C.; Raine, C.S.; Brosnan, C.F.; John, G.R. IL-1beta regulates blood-brain barrier permeability via reactivation of the hypoxia-angiogenesis program. J. Immunol. 2006, 177, 5574-5584.
78. Kern, J.W.; Schneewind, O. BslA, a pXO1-encoded adhesin of Bacillus anthracis. Mol. Microbiol. 2008, 68, 504-515.
79. Ebrahimi, C.M.; Kern, J.W.; Sheen, T.R.; Ebrahimi-Fardooee, M.A.; van Sorge, N.M.; Schneewind, O.; Doran, K.S. Penetration of the blood-brain barrier by Bacillus anthracis requires the pXO1-encoded BslA protein. J. Bacteriol. 2009, 191, 7165-7173.
80. Sweeney, D.A.; Cui, X.; Solomon, S.B.; Vitberg, D.A.; Migone, T.S.; Scher, D.; Danner, R.L.; Natanson, C.; Subramanian, G.M.; Eichacker, P.Q. Anthrax lethal and edema toxins produce different patterns of cardiovascular and renal dysfunction and synergistically decrease survival in canines. J. Infect. Dis. 2010, 202, 1885-1896.
81. Bouzianas, D.G. Medical countermeasures to protect humans from anthrax bioterrorism. Trends Microbiol. 2009, 17, 522-528.
82. Schneemann, A.; Manchester, M. Anti-toxin antibodies in prophylaxis and treatment of inhalation anthrax. Future Microbiol. 2009, 4, 35-43.
83. Arbibe, L.; Kim, D.W.; Batsche, E.; Pedron, T.; Mateescu, B.; Muchardt, C.; Parsot, C.; Sansonetti, P.J. An injected bacterial effector targets chromatin access for transcription factor NF-kappaB to alter transcription of host genes involved in immune responses. Nat. Immunol. 2007, 8, 47-56.
84. Mittal, R.; Peak-Chew, S.Y.; McMahon, H.T. Acetylation of MEK2 and I kappa B kinase (IKK) activation loop residues by YopJ inhibits signaling. Proc. Natl. Acad. Sci. USA 2006, 103, 18574-18579.
85. Lin, S.L.; Le, T.X.; Cowen, D.S. SptP, a Salmonella typhimurium type III-secreted protein, inhibits the mitogen-activated protein kinase pathway by inhibiting Raf activation. Cell Microbiol. 2003, 5, 267-275.
86. Shan, L.; He, P.; Sheen, J. Intercepting host MAPK signaling cascades by bacterial type III effectors. Cell Host Microbe 2007, 1, 167-174.