Bacillus anthracis edema toxin impairs neutrophil actin-based motility

Infection and Immunity

Volumn 77, Issue 6, 2009, Pages 2455-2464

  Szarowicz, Sarah E ^a   During, Russell L ^a   Li, Wei ^a   Quinn, Conrad P ^b   Tang, Wei Jen ^c   Southwick, Frederick S ^a  

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

^b CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BACILLUS ANTHRACIS EDEMA TOXIN; BACTERIAL TOXIN; FORMYLMETHIONYLLEUCYLPHENYLALANINE; UNCLASSIFIED DRUG; ANTHRAX TOXIN; BACTERIAL ANTIGEN; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE;

ARTICLE; BACILLUS ANTHRACIS; CELL MOTILITY; CHEMOKINESIS; CHEMOTAXIS; CONTROLLED STUDY; FEMALE; HELA CELL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; LISTERIA MONOCYTOGENES; NEUTROPHIL; POLARIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; ADULT; CELL CULTURE; CHEMISTRY; CYTOPLASM; DRUG ANTAGONISM; DRUG EFFECT; IMMUNOLOGY; LOCOMOTION; MALE; METABOLISM; MICROBIOLOGY; MIDDLE AGED; PATHOGENICITY; PHOSPHORYLATION;

ACTINS; ADULT; ANTIGENS, BACTERIAL; BACILLUS ANTHRACIS; BACTERIAL TOXINS; CELLS, CULTURED; CHEMOTAXIS; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYTOPLASM; FEMALE; HUMANS; LOCOMOTION; MALE; MIDDLE AGED; NEUTROPHILS; PHOSPHORYLATION; YOUNG ADULT;

EID: 66549085594     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00839-08     Document Type: Article

References (41)

1. Abramova, F. A., L. M. Grinberg, O. V. Yampolskaya, and D. H. Walker. 1993. Pathology of inhalational anthrax in 42 cases from the Sverdlovsk outbreak of 1979. Proc. Natl. Acad. Sci. USA 90:2291-2294.
2. Bernardini, M. L., J. Mounier, H. d'Hauteville, M. Coquis-Rondon, and P. J. Sansonetti. 1989. Identification of icsA, a plasmid locus of Shigella flexneri that governs bacterial intra- and intercellular spread through interaction with F-actin. Proc. Natl. Acad. Sci. USA 86:3867-3871.
3. Cartier, C., B. Hemonnot, B. Gay, M. Bardy, C. Sanchiz, C. Devaux, and L. Briant. 2003. Active cAMP-dependent protein kinase incorporated within highly purified HIV-1 particles is required for viral infectivity and interacts with viral capsid protein. J. Biol. Chem. 278:35211-35219.
4. Collier, R. J., and J. A. Young. 2003. Anthrax toxin. Annu. Rev. Cell Dev. Biol. 19:45-70.
5. Cossart, P., and P. J. Sansonetti. 2004. Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 304:242-248. (Pubitemid 38452169)
6. Crawford, M. A., C. V. Aylott, R. W. Bourdeau, and G. M. Bokoch. 2006. Bacillus anthracis toxins inhibit human neutrophil NADPH oxidase activity. J. Immunol. 176:7557-7565. (Pubitemid 43849059)
7. Dabiri, G. A., J. M. Sanger, D. A. Portnoy, and F. S. Southwick. 1990. Listeria monocytogenes moves rapidly through the host-cell cytoplasm by inducing directional actin assembly. Proc. Natl. Acad. Sci. USA 87:6068-6072.
8. Dal Molin, F., F. Tonello, D. Ladant, I. Zornetta, I. Zamparo, G. Di Benedetto, M. Zaccolo, and C. Montecucco. 2006. Cell entry and cAMP imaging of anthrax edema toxin. EMBO J. 25:5405-5413. (Pubitemid 44764149)
9. Dal Molin, F., I. Zornetta, A. Puhar, F. Tonello, M. Zaccolo, and C. Montecucco. 2008. cAMP imaging of cells treated with pertussis toxin, cholera toxin, and anthrax edema toxin. Biochem. Biophys. Res. Commun. 376:429-433.
10. DeMali, K. A., K. Wennerberg, and K. Burridge. 2003. Integrin signaling to the actin cytoskeleton. Curr. Opin. Cell Biol. 15:572-582.
11. Downey, G. P., E. L. Elson, B. Schwab III, S. C. Erzurum, S. K. Young, and G. S. Worthen. 1991. Biophysical properties and microfilament assembly in neutrophils: modulation by cyclic AMP. J. Cell Biol. 114:1179-1190. (Pubitemid 21909878)
12. 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. (Pubitemid 28243347)
13. During, R. L., B. G. Gibson, W. Li, E. A. Bishai, G. S. Sidhu, J. Landry, and F. S. Southwick. 2007. Anthrax lethal toxin paralyzes actin-based motility by blocking Hsp27 phosphorylation. EMBO J. 26:2240-2250. (Pubitemid 46685867)
14. During, R. L., W. Li, B. Hao, J. M. Koenig, D. S. Stephens, C. P. Quinn, and F. S. Southwick. 2005. Anthrax lethal toxin paralyzes neutrophil actin-based motility. J. Infect. Dis. 192:837-845.
15. Fincham, V. J., M. James, M. C. Frame, and S. J. Winder. 2000. Active ERK/MAP kinase is targeted to newly forming cell-matrix adhesions by integrin engagement and v-Src. EMBO J. 19:2911-2923. (Pubitemid 30386763)
16. Guarner, J., J. A. Jernigan, W. J. Shieh, K. Tatti, L. M. Flannagan, D. S. Stephens, T. Popovic, D. A. Ashford, B. A. Perkins, and S. R. Zaki. 2003. Pathology and pathogenesis of bioterrorism-related inhalational anthrax. Am. J. Pathol. 163:701-709.
17. Guo, Q., Y. Shen, N. L. Zhukovskaya, J. Florian, and W. J. Tang. 2004. Structural and kinetic analyses of the interaction of anthrax adenylyl cyclase toxin with reaction products cAMP and pyrophosphate. J. Biol. Chem. 279:29427-29435.
18. Harvath, L., J. D. Robbins, A. A. Russell, and K. B. Seamon. 1991. cAMP and human neutrophil chemotaxis. Elevation of cAMP differentially affects chemotactic responsiveness. J. Immunol. 146:224-232.
19. Holty, J. E., D. M. Bravata, H. Liu, R. A. Olshen, K. M. McDonald, and D. K. Owens. 2006. Systematic review: a century of inhalational anthrax cases from 1900 to 2005. Ann. Intern. Med. 144:270-280.
20. Hong, J., J. Beeler, N. L. Zhukovskaya, W. He, W. J. Tang, and M. R. Rosner. 2005. Anthrax edema factor potency depends on mode of cell entry. Biochem. Biophys. Res. Commun. 335:850-857.
21. Jernigan, D. B., P. L. Raghunathan, B. P. Bell, R. Brechner, E. A. Bresnitz, J. C. Butler, M. Cetron, M. Cohen, T. Doyle, M. Fischer, C. Greene, K. S. Griffith, J. Guarner, J. L. Hadler, J. A. Hayslett, R. Meyer, L. R. Petersen, M. Phillips, R. Pinner, T. Popovic, C. P. Quinn, J. Reefhuis, D. Reissman, N. Rosenstein, A. Schuchat, W. J. Shieh, L. Siegal, D. L. Swerdlow, F. C. Tenover, M. Traeger, J. W. Ward, I. Weisfuse, S. Wiersma, K. Yeskey, S. Zaki, D. A. Ashford, B. A. Perkins, S. Ostroff, J. Hughes, D. Fleming, J. P. Koplan, and J. L. Gerberding. 2002. Investigation of bioterrorism-related anthrax, United States, 2001: epidemiologic findings. Emerg. Infect. Dis. 8:1019-1028.
22. Jernigan, J. A., D. S. Stephens, D. A. Ashford, C. Omenaca, M. S. Topiel, M. Galbraith, M. Tapper, T. L. Fisk, S. Zaki, T. Popovic, R. F. Meyer, C. P. Quinn, S. A. Harper, S. K. Fridkin, J. J. Sejvar, C. W. Shepard, M. McConnell, J. Guarner, W. J. Shieh, J. M. Malecki, J. L. Gerberding, J. M. Hughes, and B. A. Perkins. 2001. Bioterrorism-related inhalational anthrax: the first 10 cases reported in the United States. Emerg. Infect. Dis. 7:933-944.
23. Kim, C., S. Wilcox-Adelman, Y. Sano, W. J. Tang, R. J. Collier, and J. M. Park. 2008. Antiinflammatory cAMP signaling and cell migration genes co-opted by the anthrax bacillus. Proc. Natl. Acad. Sci. USA 105:6150-6155.
24. Kumar, P., N. Ahuja, and R. Bhatnagar. 2001. Purification of anthrax edema factor from Escherichia coli and identification of residues required for binding to anthrax protective antigen. Infect. Immun. 69:6532-6536.
25. Lawrence, D. W., and K. B. Pryzwansky. 2001. The vasodilator-stimulated phosphoprotein is regulated by cyclic GMP-dependent protein kinase during neutrophil spreading. J. Immunol. 166:5550-5556. (Pubitemid 32374177)
26. Leppla, S. H. 1982. Anthrax toxin edema factor: a bacterial adenylate cyclase that increases cyclic AMP concentrations of eukaryotic cells. Proc. Natl. Acad. Sci. USA 79:3162-3166.
27. Puhar, A., F. Dal Molin, S. Horvath, D. Ladants, and C. Montecucco. 2008. Anthrax edema toxin modulates PKA- and CREB-dependent signaling in two phases. PLoS ONE 3:e3564.
28. Quinn, C. P., C. C. Shone, P. C. Turnbull, and J. Melling. 1988. Purification of anthrax-toxin components by high-performance anion-exchange, gel-filtration and hydrophobic-interaction chromatography. Biochem. J. 252:753-758. (Pubitemid 18153515)
29. Rivkin, I., J. Rosenblatt, and E. L. Becker. 1975. The role of cyclic AMP in the chemotactic responsiveness and spontaneous motility of rabbit peritoneal neutrophils. The inhibition of neutrophil movement and the elevation of cyclic AMP levels by catecholamines, prostaglandins, theophylline and cholera toxin. J. Immunol. 115:1126-1134.
30. Sanger, J. M., J. W. Sanger, and F. S. Southwick. 1992. Host cell actin assembly is necessary and likely to provide the propulsive force for intracellular movement of Listeria monocytogenes. Infect. Immun. 60:3609-3619.
31. Selliah, N., M. M. Bartik, S. L. Carlson, W. H. Brooks, and T. L. Roszman. 1995. cAMP accumulation in T-cells inhibits anti-CD3 monoclonal antibody-induced actin polymerization. J. Neuroimmunol. 56:107-112.
32. Sidhu, G. S., W. Li, N. Laryngakis, E. Bishai, T. Balla, and F. S. Southwick. 2005. Phosphoinositide-3-kinase is required for intracellular Listeria monocytogenes actin-based motility and filopod formation. J. Biol. Chem. 280:11379-11386.
33. 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.
34. Southwick, F. S., G. A. Dabiri, M. Paschetto, and S. H. Zigmond. 1989. Polymorphonuclear leukocyte adherence induces actin polymerization by a transduction pathway which differs from that used by chemoattractants. J. Cell Biol. 109:1561-1569. (Pubitemid 19251209)
35. Theriot, J. A., T. J. Mitchison, L. G. Tilney, and D. A. Portnoy. 1992. The rate of actin-based motility of intracellular Listeria monocytogenes equals the rate of actin polymerization. Nature 357:257-260.
36. Tilney, L. G., and D. A. Portnoy. 1989. Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J. Cell Biol. 109:1597-1608.
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. Wade, B. H., G. G. Wright, E. L. Hewlett, S. H. Leppla, and G. L. Mandell. 1985. Anthrax toxin components stimulate chemotaxis of human polymorphonuclear neutrophils. Proc. Soc. Exp. Biol. Med. 179:159-162.
39. Ydrenius, L., M. Majeed, B. J. Rasmusson, O. Stendahl, and E. Sarndahl. 2000. Activation of cAMP-dependent protein kinase is necessary for actin rearrangements in human neutrophils during phagocytosis. J. Leukoc. Biol. 67:520-528.
40. Ydrenius, L., L. Molony, J. Ng-Sikorski, and T. Andersson. 1997. Dual action of cAMP-dependent protein kinase on granulocyte movement. Biochem. Biophys. Res. Commun. 235:445-450.
41. Zeile, W. L., D. L. Purich, and F. S. Southwick. 1996. Recognition of two classes of oligoproline sequences in profilin-mediated acceleration of actin-based Shigella motility. J. Cell Biol. 133:49-59. (Pubitemid 126618597)