Pore-forming and enzymatic activities of Bordetella pertussis adenylate cyclase toxin synergize in promoting lysis of monocytes

Infection and Immunity

Volumn 74, Issue 4, 2006, Pages 2207-2214

  Basler, Marek ^a   Masin, Jiri ^a   Osicka, Radim ^a   Sebo, Peter ^a  

^a INSTITUTE OF MICROBIOLOGY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; BETA2 INTEGRIN; CD11B ANTIGEN; CD18 ANTIGEN; CYCLIC AMP; HEMOLYSIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BORDETELLA PERTUSSIS; CELL INVASION; CHANNEL GATING; CONTROLLED STUDY; CYTOLYSIS; CYTOTOXICITY; ENZYME ACTIVITY; GENE MUTATION; MONOCYTE; MOUSE; NONHUMAN; PHAGOCYTE; PRIORITY JOURNAL;

ADENOSINE TRIPHOSPHATE; ADENYLATE CYCLASE TOXIN; ANIMALS; ANTIGENS, CD11B; ANTIGENS, CD18; BORDETELLA PERTUSSIS; CELL DEATH; CELL LINE; CELL MEMBRANE PERMEABILITY; CHO CELLS; CRICETINAE; CRICETULUS; CYCLIC AMP; CYTOTOXICITY, IMMUNOLOGIC; ERYTHROCYTES; MICE; MONOCYTES; SHEEP;

EID: 33645508143     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.74.4.2207-2214.2006     Document Type: Article

References (57)

1. Bachelet, M., M. J. Richard, D. Francois, and B. S. Polla. 2002. Mitochondrial alterations precede Bordetella pertussis-induced apoptosis. FEMS Immunol. Med. Microbiol. 32:125-131.
2. Barry, E. M., A. A. Weiss, I. E. Ehrmann, M. C. Gray, E. L. Hewlett, and M. S. Goodwin. 1991. Bordetella pertussis adenylate cyclase toxin and hemolytic activities require a second gene, cyaC, for activation. J. Bacteriol. 173:720-726.
3. Basar, T., V. Havlicek, S. Bezouskova, M. Hackett, and P. Sebo. 2001. Acylation of lysine 983 is sufficient for toxin activity of Bordetella pertussis adenylate cyclase. Substitutions of alanine 140 modulate acylation site selectivity of the toxin acyltransferase CyaC. J. Biol. Chem. 276:348-354.
4. Basar, T., V. Havlicek, S. Bezouskova, P. Halada, M. Hackett, and P. Sebo. 1999. The conserved lysine 860 in the additional fatty-acylation site of Bordetella pertussis adenylate cyclase toxin is crucial for toxin function independently of its acylation status. J. Biol. Chem. 274:10777-10783.
5. Baumann, U., S. Wu, K. M. Flaherty, and D. B. McKay. 1993. Three-dimensional structure of the alkaline protease of Pseudomonas aeruginosa: a two-domain protein with a calcium binding parallel beta roll motif. EMBO J. 12:3357-3364.
6. Bellalou, J., H. Sakamoto, D. Ladant, C. Geoffroy, and A. Ullmann. 1990. Deletions affecting hemolytic and toxin activities of Bordetella pertussis adenylate cyclase. Infect. Immun. 58:3242-3247.
7. Benz, R., E. Maier, D. Ladant, A. Ullmann, and P. Sebo. 1994. Adenylate cyclasc toxin (CyaA) of Bordetella pertussis. Evidence for the formation of small ion-permeable channels and comparison with HlyA of Escherichia coli. J. Biol. Chem. 269:27231-27239.
8. Betsou, F., P. Sěbo, and N. Guiso. 1993. CyaC-mediated activation is important not only for toxic but also for protective activities of Bordetella pertussis adenylate cyclase-hemolysin. Infect. Immun. 61:3583-3589.
9. Boyd, A. P., P. J. Ross, H. Conroy, N. Mahon, E. C. Lavelle, and K. H. Mills. 2005. Bordetella pertussis adenylate cyclase toxin modulates innate and adaptive immune responses: distinct roles for acylation and enzymatic activity in immunomodulation and cell death. J. Immunol. 175:730-873.
10. Confer, D. L., and J. W. Eaton. 1982. Phagocyte impotence caused by an invasive bacterial adenylate cyclase. Science 217:948-950.
11. Ehrmann, I. E., M. C. Gray, V. M. Gordon, L. S. Gray, and E. L. Hewlett. 1991. Hemolytic activity of adenylate cyclase toxin from Bardetella pertussis. FEBS Lett. 278:79-83.
12. El-Azami-El-Idrissi, M., C. Bauche, J. Loucka, R. Osicka, P. Sebo, D. Ladant, and C. Leclerc. 2003. Interaction of Bordetella pertussis adenylate cyclase with CD11b/CD18: role of toxin acylation and identification of the main integrin interaction domain. J. Biol. Chem. 278:38514-38521.
13. Friedman, R. L., R. L. Fiederlein, L. Glasser, and J. N. Galgiani. 1987. Bordetella pertussis adenylate cyclase: effects of affinity-purified adenylate cyclase on human polymorphonuclear leukocyte functions. Infect. Immun. 55:135-140.
14. Gentile, F., A. Raptis, L. G. Knipling, and J. Wolff. 1988. Bordetella pertussis adenylate cyclase: penetration into host cells. Eur. J. Biochem. 175:447-453.
15. Glaser, P., D. Ladant, O. Sezer, F. Pichot, A. Ullmann, and A. Danchin. 1988. The calmodulin-sensitive adenylale cyclase of Bordetella pertussis: cloning and expression in Escherichia coli. Mol. Microbiol. 2:19-30.
16. Glaser, P., H. Sakamoto, J. Bellalou, A. Ullmann, and A. Danchin. 1988. Secretion of cyclolysin. the calmodulin-sensitive adenylate cyclase-haemolysin bifunctional protein of Bordetella pertussis. EMBO J. 7:3997-4004.
17. Goodwin, M. S. M., and A. A. Weiss. 1990. Adenylate cyclase toxin is critical for colonization and pertussis toxin is critical for lethal infection by Bordetella pertussis in infant mice. Infect. Immun. 58:3445-3447.
18. Gray, M. C., G. M. Donato, F. R. Jones, T. Kim, and E. L. Hewlett. 2004. Newly secreted adenylate cyclase toxin is responsible for intoxication of target cells by Bordetella pertussis. Mol. Microbiol. 53:1709-1719.
19. Gross, M. K., D. C. Au, A. L. Smith, and D. R. Storm. 1992. Targeted mutations that ablate cither the adenylate cyclase or hemolysin function of the bifunctional cyaA toxin of Bordetella pertussis abolish virulence. Proc. Natl. Acad. Sci. USA 89:4898-4902.
20. Gueirard, P., A. Druilhe, M. Pretolani, and N. Guiso. 1998. Role of adenylate cyclase-hemolysin in alveolar macrophage apoptosis during Bordetella pertussis infection in vivo. Infect. Immun. 66:1718-1725.
21. Guermonprez, P., N. Khelef, E. Blouin, P. Rieu, P. Ricciardi-Castagnoli, N. Guiso, D. Ladant, and C. Leclerc. 2001. The adenylate cyclase toxin of Bordetella pertussis binds to target cells via the alpha(M)beta(2) integrin (CD11b/CD18). J. Exp. Med. 193:1035-1044.
22. Guermonprez, P., D. Ladant, G. Karimova, A. Ullmann, and C. Leclerc. 1999. Direct delivery of the Bordetella pertussis adenylate cyclase toxin to the MHC class I antigen presentation pathway. J. Immunol. 162:1910-1916.
23. Hackett, M., L. Guo, J. Shabanowitz, D. F. Hunt, and E. L. Hewlett. 1994. Internal lysine palmitoylation in adenylate cyclase toxin from Bordetella pertussis. Science 266:433-435.
24. Hackett, M., C. B. Walker, L. Guo, M. C. Gray, C. S. Van, A. Ullmann, J. Shabanowitz, D. F. Hunt, E. L. Hewlett, and P. Sebo. 1995. Hemolytic, but not cell-invasive activity, of adenylate cyclase toxin is selectively affected by differential fatty-acylation in Escherichia coli. J. Biol. Chem. 270:20250-20253.
25. Hanski, E. 1989. Invasive adenylate cyclase toxin of Bordetella pertussis. Trends Biochem. Sci. 14:459-463.
26. Hanski, E., and Z. Farfel. 1985. Bordetella pertussis invasive adenylate cyclase: partial resolution and properties of its cellular penetration. J. Biol. Chem. 260:5526-5532.
27. Havlicek, V., L. Higgins, W. Chen, P. Halada, P. Sebo, H. Sakamoto, and M. Hackett. 2001. Mass spectrometric analysis of recombinant adenylate cyclase toxin from Bordetella pertussis strain 18323/pHSP9. J. Mass Spectrom. 36:384-391.
28. Hewlett, E., and J. Wolff. 1976. Soluble adenylate cyclase from the culture medium of Bordetella pertussis: purification and characterization. J. Bacteriol. 127:890-898.
29. Hewlett, E. L., G. M. Donato, and M. C. Gray. 2006. Macrophage cytotoxicity produced by adenylate cyclase toxin from Bordetella pertussis: more than just making cyclic AMP! Mol. Microbiol. 59:447-459.
30. Hewlett, E. L., L. Gray, M. Allietta, I. E. Ehrmann, V. M. Gordon, and M. C. Gray. 1991. Adenylate cyclase toxin from Bordetella pertussis. Conformational change associated with toxin activity. J. Biol. Chem. 266:17503-17508.
31. Hewlett, E. L., D. L. Smith, G. A. Myers, R. D. Pearson, and H. D. Kay. 1983. In vitro inhibition of human natural killer (NK) cell cytotoxicity by Bordetella cyclase and pertussis toxin. Clin. Res. 31:365A.
32. Hewlett, E. L., M. A. Urban, C. R. Manclark, and J. Wolff. 1976. Extra-cytoplasmic adenylate cyclase of Bordetella pertussis. Proc. Natl. Acad. Sci. USA 73:1926-1930.
33. Ingalls, R. R., M. A. Arnaout, R. L. Delude, S. Flaherty, R. Savedra, Jr., and D. T. Golenbock. 1998. The CD11/CD18 integrins: characterization of three novel LPS signaling receptors. Prog. Clin. Biol. Res. 397:107-117.
34. Karimova, G., C. Fayolle, S. Gmira, A. Ullmann, C. Leclerc, and D. Ladant. 1998. Charge-dependent translocation of Bordetella pertussis adenylate cyclase toxin into eukaryotic cells: implication for the in vivo delivery of CD8(+) T cell epitopes into antigen-presenting cells. Proc. Natl. Acad. Sci. USA 95:12532-12537.
35. Karimova, G., J. Pidoux, A. Ullmann, and D. Ladant. 1998. A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc. Natl. Acad. Sci. USA 95:5752-5756.
36. Khelef, N., and N. Guiso. 1995. Induction of macrophage apoptosis by Bordetella pertussis adenylate cyclase-hemolysin. FEMS Microbiol. Lett. 134:27-32.
37. Khelef, N., H. Sakamoto, and N. Guiso. 1992. Both adenylate cyclase and hemolytic activities are required by Bordetella pertussis to initiate infection. Microb. Pathog. 12:227-235.
38. Khelef, N., A. Zychlinsky, and N. Guiso. 1993. Bordetella pertussis induces apoptosis in macrophages: role of adenylate cyclase-hemolysin. Infect. Immun. 61:4064-4071.
39. Knapp, O., E. Maier, G. Polleichtner, J. Masin, P. Sebo, and R. Benz. 2003. Channel formation in model membranes by the adenylate cyclase toxin of Bordetella pertussis: effect of calcium. Biochemistry 42:8077-8084.
40. Koronakis, V., C. Andersen, and C. Hughes. 2001. Channel-tunnels. Curr. Opin. Struct. Biol. 11:403-407.
41. Ladant, D., P. Glaser, and A. Ullmann. 1992. Insertional mutagenesis of Bordetella pertussis adenylate cyclase. J. Biol. Chem. 267:2244-2250.
42. Ladant, D., and A. Ullmann. 1999. Bordetella pertussis adenylate cyclase: a toxin with multiple talents. Trends Microbiol. 7:172-176.
43. Masin, J., M. Basler, O. Knapp, M. El-Azami-El-Idrissi, E. Maier, I. Konopasek, R. Benz, C. Leclerc, and P. Sebo. 2005. Acylation of lysine 860 allows tight binding and cytotoxicity of Bordetella adenylate cyclase on CD11b-expressing cells. Biochemistry 44:12759-12766.
44. Njamkepo, E., F. Pinol, D. Francois, N. Guiso, B. S. Polla, and M. Bachelet. 2000. Adaptive responses of human monocytes infected by Bordetella pertussis: the role of adenylate cyclase hemolysin. J. Cell Physiol. 183:91-99.
45. + T-cell epitopes into major histocompatibility complex class I antigen presentation pathway by Bordetella pertussis adenylate cyclase: delineation of cell invasive structures and permissive insertion sites. Infect. Immun. 68:247-256.
46. Osickova, A., R. Osicka, E. Maier, R. Benz, and P. Sebo. 1999. An amphipathic alpha-helix including glutamates 509 and 516 is crucial for membrane translocation of adenylate cyclase toxin and modulates formation and cation selectivity of its membrane channels. J. Biol. Chem. 274:37644-37650.
47. Pearson, R. D., P. Symes, M. Conboy, A. A. Weiss, and E. L. Hewlett. 1987. Inhibition of monocyte oxidative responses by Bordetella pertussis adenylate cyclase toxin. J. Immunol. 139:2749-2754.
48. Rogel, A., R. Meller, and E. Hanski. 1991. Adenylate cyclase toxin from Bordetella pertussis. The relationship between induction of cAMP and hemolysis. J. Biol. Chem. 266:3154-3161.
49. Rogel, A., J. E. Schultz, R. M. Brownlie, J. G. Coote, R. Parton, and E. Hanski. 1989. Bordetella pertussis adenylate cyclase: purification and characterization of the toxic form of the enzyme. EMBO J. 8:2755-2760.
50. Rose, T., P. Sebo, J. Bellalou, and D. Ladant. 1995. Interaction of calcium with Bordetella pertussis adenylate cyclase toxin. Characterization of multiple calcium-binding sites and calcium-induced conformational changes. J. Biol. Chem. 270:26370-26376.
51. Schlecht, G., J. Loucka, H. Najar, P. Sebo, and C. Leclerc. 2004. Antigen targeting to CD11b allows efficient presentation of CD4+ and CD8+ T cell epitopes and in vivo Th1-polarized T cell priming. J. Immunol. 173:6089-6097.
52. Sebo, P., P. Glaser, H. Sakamoto, and A. Ullmann. 1991. High-level synthesis of active adenylate cyclase toxin of Bordetella pertussis in a reconstructed Escherichia coli system. Gene 104:19-24.
53. Szabo, G., M. C. Gray, and E. L. Hewlett. 1994. Adenylate cyclase toxin from Bordetella pertussis produces ion conductance across artificial lipid bilayers in a calcium and polarity-dependent manner. J. Biol. Chem. 269:22496-22499.
54. Vojtova, J., J. Kamanova, and P. Sebo. 4 January 2006. Bordetella adenylate cyclase toxin: a swift saboteur of host defense. Curr. Opin. Microbiol. [Epub ahead of print.]
55. Weingart, C. L., and A. A. Weiss. 2000. Bordetella pertussis virulence factors affect phagocytosis by human neutrophils. Infect. Immun. 68:1735-1739.
56. Weiss, A. A., E. L. Hewlett, G. A. Myers, and S. Falkow. 1984. Pertussis toxin and extracytoplasmic adenylate cyclase as virulence factors of Bordetella pertussis. J. Infect. Dis. 150:219-222.
57. Wolff, J., G. H. Cook, A. R. Goldhammer, and S. A. Berkowitz. 1980. Calmodulin activates prokaryotic adenylate cyclase. Proc. Natl. Acad. Sci. USA 77:3841-3844.