The adenylate cyclase toxin of Bordetella pertussis binds to target cells via the αMβ2 integrin (CD11b/CD18)

Journal of Experimental Medicine

Volumn 193, Issue 9, 2001, Pages 1035-1044

  Guermonprez, Pierre ^a   Khelef, Nadia ^a   Blouin, Eric ^a   Rieu, Philippe ^a   Ricciardi Castagnoli, Paola ^b   Guiso, Nicole ^a   Ladant, Daniel ^a   Leclerc, Claude ^a,c  

^a HÔPITAL NECKER ENFANTS MALADES   (France)

^b UNIVERSITY OF MILANO BICOCCA   (Italy)

^c INSTITUT PASTEUR   (France)

Author keywords

Adenylate cyclase; Bordetella; CD11b; Integrin; Toxin

Indexed keywords

ADENYLATE CYCLASE; ALPHA M BETA2 INTEGRIN; BACTERIAL TOXIN; CD11B ANTIGEN; CD18 ANTIGEN; CELL RECEPTOR; CYCLIC AMP; INTEGRIN; MONOCLONAL ANTIBODY; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ARTICLE; BORDETELLA PERTUSSIS; CELL DEATH; CELLULAR DISTRIBUTION; CHO CELL; DENDRITIC CELL; ENZYME BINDING; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MACROPHAGE; NATURAL KILLER CELL; NEUTROPHIL; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

ADENYLATE CYCLASE; ADENYLATE CYCLASE TOXIN; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD18; BACTERIAL PROTEINS; BORDETELLA PERTUSSIS; CALCIUM; CATIONS, DIVALENT; CELL LINE; CHO CELLS; CRICETINAE; CYCLIC AMP; HUMANS; MACROPHAGE-1 ANTIGEN; MAGNESIUM; MICE; PROTEIN PRECURSORS; RATS;

EID: 0035821250     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.193.9.1035     Document Type: Article

References (62)

1. 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. Inject. Dis. 150:219-222.
2. Weiss, A.A., and M.S. Goodwill. 1989. Lethal infection by Bordetella pertussis mutants in the infant mouse model. Infect. Immun. 57:3757-3764.
3. Gross, M.K., D.C. Au, A.L. Smith, and D.R. Storm. 1992. Targeted mutations that ablate either the adenylate cyclase or hemolysin function of the bifunctional cyaA toxin of Bordetella pertussis abolish virulence. Proc. Natl. Acad. Sci. USA. 89: 4898-4902.
4. 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.
5. Khelef, N., C.M. Kachelet, H.B. Vargaftig, and N. Guiso. 1994. Characterization of murine lung inflammation after infection with parental Bordetella pertussis and mutants deficient in adhesins or toxins. Infect. Immunn. 62:2893-2900.
6. 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.
7. Guiso, N., M. Rocancourt, M. Szatanik, and J.M. Alonso. 1989. Bordetella adenylate cyclase is a virulence associated factor and an immunoprotective antigen. Microb. Pathog. 7:373-380.
8. Guiso, N., M. Szatanik, and M. Rocancourt. 1991. Protective activity of Bordetella adenylate cyclase - hemolysin against bacterial colonization. Microb. Pathog. 11:423-431.
9. Betsou, F., P. Sebo, 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.
10. Betsou, F., P. Sebo, and N. Guiso. 1995. The C-terminal domain is essential for protective activity of the Bordetella pertussis adenylate cyclase-hemolysin. Inject. Immun. 63:3309-3315.
11. Hewlett, E., and J. Wolff. 1976. Soluble adenylate cyclase from the culture medium of Bordetella pertussis: purification and characterization. J. Bacteriol. 127:890-898.
12. Wolff J., G.H. Cook, A.R. Goldhammer, and S.A. Berkowitz. 1980. Calmodulin activates prokaryotic adenylate cyclase. Proc. Natl. Acad. Sci. U.S.A. 77:3841-3844.
13. Confer, D.L., and J.W. Eaton. 1982. Phagocyte impotence caused by an invasive bacterial adenylate cyclase. Science. 217: 948-950.
14. Lidant, D., and A. Ullmann. 1999. Bordetella pertussis adenylate cyclase: a toxin with multiple talents. Trends Microbiol. 7:172-176.
15. Sakamoto, H., J. Bellalou, P. Sebo, and D. Ladant. 1992. Bordetella pertussis adenylate cyclase toxin. Structural and functional independence of the catalytic and hemolytic activities. J. Biol. Chem. 267:13598-13602.
16. Benz, R., E. Maier, D. Ladant, A. Ullmann, and P. Sebo. 1994. Adenylate cyclase 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.
17. + efflux, intoxication, and hemolysis by Bordetella pertussis AC toxin. J. Biol. Chem. 273: 18260-18267.
18. 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.
19. Coote, J.G. 1992. Structural and functional relationships among the RTX toxin determinants of gram-negative bacteria. FEMS Microbiol. Rev: 8:137-161.
20. Barry, E.M., A.A. Weiss, I.E. Ehrmann, M.C. Gray, E.L. Hewlett, and M.S. Goodwill. 1991. Bordetella pertussis adenylate cyclase toxin and hemolytic activities require a second gene, cyaC, for activation. J. Bacteriol. 173:720-726.
21. Hackett, M., E. Guo, J. Shabanowitz, D.F. Hunt, and E.L. Hewlett. 1994. Internal lysine palmitoylation in adenylate cyclase toxin from Bordetella pertussis. Science. 266:433-135.
22. Rogel, A., and E. Hanski. 1992. Distinct steps in the penetration of adenylate cyclase toxin of Bordetella pertussis into sheep erythrocytes. J. Biol. Chem. 267:22599-22605.
23. + T cell epitopes into antigen-presenting cells. Proc. Natl. Acad. Sci. USA. 95: 12532-12537.
24. Otero, A.S., X.B. Yi, M.C. Gray, G. Szabo, and E.L. Hewlett. 1995. Membrane depolarization prevents cell invasion by Bordetella pertussis adenylate cyclase toxin. J. Biol. Chem. 270:9695-9697.
25. 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.
26. Friedman, R.L., R.L. Fiederlein, L. Glasser, and J.N. Galgiani. 1987. Borletella pertussis adenylate cyclase: effects of affinity-purified adenylate cyclase on human polymorphonuclear leukocyte functions. Infect. Immun. 55:135-140.
27. Njamkepo, E., F. Pinot, 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.
28. Bassinet, E., P. Gueirard, B. Maitre, B. Housset, P. Gounon, and N. Guiso. 2000. Role of adhesions and toxins in invasion of human tracheal epithelial cells by Bordetella pertussis. Infect. Immun. 68:1934-1941.
29. Khelef, N., A. Zychlinsky, and N. Guiso. 1993. Bordetella pertussis induces apoptosis in macrophages: role of adenylate cyclase-hemolysin. Infect, Immun. 61:4064-4071.
30. Khelef, N., and N. Guiso. 1995. Induction of macrophage apoptosis by Bordetella pertussis adenylate cyclase-hemolysin. FEMS Microbiol. Lett. 134:27-32.
31. Harvill, E.T., P.A. Cotter, M.H. Yuk, and J.F. Miller. 1999. Probing the function of Bordetella bronchiseptica adenylate cyclase toxin by manipulating host immunity. Infect. Immun. 67: 1493-1500.
32. Lally, E.T., I.R. Kieba, A. Sato, C. Green, J. Rosenbloom, J. Korostoff, J.F. Wang, B.J. Shenker, S. Ortlepp, M.K. Robinson, and P.C. Billings. 1997. RTX toxins recognize a β2 integrin on the surface of human target cells. J. Biol. Chem. 272:30463-30469.
33. Li, J., K.D. Clinkenbeard, and J.W. Ritchey. 1999. Bovine CD18 identified as a species specific receptor for Pasteurella haemolytica leukotoxin. Vet. Microbiol. 67:91-99.
34. Ambagala, T.C., A.P. Ambagala, and S. Srikumaran. 1999. The leukotoxin of Pasteurella haemolytica binds to β(2) integrins on bovine leukocytes. FEMS Microbiol. Lett. 179:161-167.
35. Arnaout, M.A. 1990. Structure and function of the leukocyte adhesion molecules CD11/CD18. Blood. 75:1037-1050.
36. Bell, D., J.W. Young, and J. Banchereau. 1999. Dendritic cells. Adv. Immunol. 72:255-324.
37. Girolomoni, G., M.B. Lutz, S. Pastore, C.U. Assmann, A. Cavani, and P. Ricciardi-Castagnoli. 1995. Establishment of a cell line with features of early dendritic cell precursors from fetal mouse skin. Eur. J. Immunol. 25:2163-2169.
38. Winzler, C., P. Rovere, M. Rescigno, F. Granucci, C. Penna, L. Adorini, V.S. Zimmermann, J. Davoust, and P. Ricciardi-Castagnoli. 1997. Maturation stages of mouse dendritic cells in growth factor-dependent long-term cultures. J. Exp. Med. 185:317-328.
39. 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.
40. Rieu, P., F. Porteu, G. Bessou, P. Lesavre, and L. Halbwachs-Mecarelli. 1992. Human neutrophils release their major membrane sialoprotein, leukosialin (CD43), during cell activation. Eur. J. Immunol. 22:3021-3026.
41. 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.
42. Gordon, V.M., S.H. Leppla, and E.L. Hewlett. 1988. Inhibitors of receptor-mediated endocytosis block the entry of Bacillus anthracis adenylate cyclase toxin but not that of Bordetella pertussis adenylate cyclase toxin. Infect. Immun. 56:1066-1069.
43. Plow, E.F., T.A. Haas, L. Zhang, J. Loftus, and J.W. Smith. 2000. Ligand binding to integrins. J. Biol. Chem. 275:21785-21788.
44. Gray, M.C., W. Ross, K. Kim, and E.L. Hewlett. 1999. Characterization of binding of adenylate cyclase toxin to target cells by flow cytometry. Infect. Immun. 67:4393-4399.
45. Dα2, binds preferentially to ICAM-3. Immunity. 3:683-690.
46. Diamond, M.S. J. Garcia-Aguilar, J.K. Bickford, A.L. Corbi, and T.A. Springer. 1993. The I domain is a major recognition site on the leukocyte integrin Mac-1 (CD11b/CD18) for four distinct adhesion ligands. J. Cell Biol. 120:1031-1043.
47. Michishita, M., V. Videm, and M.A. Arnaout. 1993. A novel divalent cation-binding site in the A domain of the integrin CR3 (CD11b/CD18) is essential for ligand binding. Cell. 72: 857-867.
48. Lee, J.O., P. Rieu, M.A. Arnaout, and R. Liddington. 1995. Crystal structure of the A domain from the subunit of integrin CR3 (CD11b/CD18). Cell. 80:631-638.
49. Yalamanchili, P., C. Lu, C. Oxvig, and T.A. Springer. 2000. Folding and function of I domain-deleted Mac-1 and lymphocyte function-associated antigen-1. J. Biol. Chem. 275: 21877-21882.
50. Vetvicka, V., B.P. Thornton, and G.D. Ross. 1996. Soluble β-glucan polysaccharide binding to the lectin site of neutrophil or natural killer cell complement receptor type 3 (CD11b/CD18) generates a primed state of the receptor capable of mediating cytotoxicity of iC3b-opsonized target cells. j. Clin. Invest. 98:50-61.
51. Zhou, M., R.F. Todd III, J.G. van de Winkel, and H.R. Petty. 1993. Cocapping of the leukoadhesin molecules complement receptor type 3 and lymphocyte function-associated antigen-1 with Fc γ receptor III on human neutrophils. Possible role of lectin-like interactions. J. Immunol. 150:3030-3041.
52. Montecucco, C., E. Papini, and G. Schiavo. 1994. Bacterial protein toxins penetrate cells via a four-step mechanism. FEBS Lett. 346:92-98.
53. Bretscher, M.S. 1992. Circulating integrins: α5β1, α6β4 and Mac-1, but not α3β1, α4β1 or LFA-1. EMBO (Eur. Mol. Biol. Organ.) J. 11:405-410.
54. Rabb, H., M. Michishita, C.P. Sharma, D. Brown, and M.A. Arnaout. 1993. Cytoplasmic tails of human complement receptor type 3 (CR3, CD11b/CD18) regulate ligand avidity and the internalization of occupied receptors. J. Immunol. 151:990-1002.
55. Welch, R.A. 1991. Pore-forming cytolysins of Grain-negative bacteria. Mol. Microbiol. 5:521-528.
56. Mβ2, CD11b/CD18) binds filamentous hemagglutinin of Bordetella pertussis. Cell. 61:1375-1382.
57. Saukkonen, K., C. Cabellos, M. Burroughs, S. Prasad, and E. Tuomanen. 1991. Integrin-mediated localization of Bordetella pertussis within macrophages: role in pulmonary colonization. J. Exp. Med. 173:1143-1149.
58. Ishibashi, Y., S. Claus, and D.A. Relman. 1994 Bordetella pertussis filamentous hemagglutinin interacts with a leukocyte signal transduction complex and stimulates bacterial adherence to monocyte CR3 (CD11b/CD18). J. Exp. Med. 180: 1225-1233.
59. Boschwitz, J.S., J.W. Batanghari, H. Kedem, and D.A. Relman. 1997. Bordetella pertussis infection of human monocytes inhibits antigen-dependent CD4 T cell proliferation. J. Infect. Dis. 176:678-686.
60. + T cell epitope from lymphocytic choriomeningitis virus. Proc. Natl. Acad. Sci. USA. 94:3314-3319.
61. Fayolle, C., D. Ladant, G. Karimova, A. Ullmann, and C. Leclerc. 1999. Therapy of murine tumors with recombinant Bordetella pertussis adenylate cyclase carrying a cytotoxic T cell epitope. J. Immunol. 162:4157-4162.
62. 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.