Adjuvanticity of native and detoxified adenylate cyclase toxin of Bordetella pertussis towards co-administered antigens

Vaccine

Volumn 22, Issue 31-32, 2004, Pages 4270-4281

  MacDonald Fyall, Julia ^a,b   Xing, Dorothy ^b   Corbel, Michael ^b   Baillie, Susan ^a   Parton, Roger ^a   Coote, John ^a  

^a Joseph Black Bldg Univ G   (United Kingdom)

^b NATIONAL INSTITUTE FOR BIOLOGICAL STANDARDS AND CONTROL   (United Kingdom)

Author keywords

Adenylate cyclase toxin; Adjuvant; Bordetella pertussis

Indexed keywords

ADENYLATE CYCLASE TOXIN; GAMMA INTERFERON; HEMAGGLUTININ; IMMUNOGLOBULIN G ANTIBODY; IMMUNOLOGICAL ADJUVANT; NITRIC OXIDE; PERTACTIN; PERTUSSIS TOXIN; PERTUSSIS VACCINE;

ANIMAL EXPERIMENT; ANTIBODY TITER; ARTICLE; BORDETELLA PERTUSSIS; CELL CULTURE; CONTROLLED STUDY; ENZYME ACTIVITY; EXPERIMENTAL INFECTION; FEMALE; IMMUNE RESPONSE; IMMUNIZATION; INFECTION PREVENTION; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PERTUSSIS; PRIORITY JOURNAL; PROVOCATION TEST; SPLEEN CELL;

ADENYLATE CYCLASE; ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIBODIES, BACTERIAL; ANTIGENS, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; BLOTTING, WESTERN; BORDETELLA PERTUSSIS; CELLS, CULTURED; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENZYME-LINKED IMMUNOSORBENT ASSAY; ESCHERICHIA COLI; FEMALE; HEMAGGLUTININS; MACROPHAGES; MICE; NITRIC OXIDE; PERTUSSIS TOXIN; SPLEEN; VACCINES, ACELLULAR; VIRULENCE FACTORS, BORDETELLA; WHOOPING COUGH;

EID: 4944237705     PISSN: 0264410X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vaccine.2004.04.033     Document Type: Article

References (64)

1. M.D. Decker, and K.M. Edwards Acellular pertussis vaccines Pediatr. Clin. N. Am. 47 2000 309 335
2. S.A. Halperin Developing better pediatric vaccines BioDrugs 12 1999 175 191
3. S.A. Plotkin, and M. Cadoz The acellular pertussis vaccine trials: an interpretation Pediatr. Infect. Dis. J. 16 1997 508 517
4. R.M. Brownlie, J.G. Coote, R. Parton, J.E. Schultz, A. Rogel, and E. Hanski Cloning of the adenylate cyclase genetic determinant of Bordetella pertussis and its expression in Escherichia coli and Bordetella pertussis Microb. Pathog. 4 1988 335 344
5. M.S. Goodwin, and A.A. Weiss Adenylate cyclase toxin is critical for lethal infection by Bordetella pertussis in infant mice Infect. Immun. 58 1990 3445 3447
6. N. Khelef, H. Sakamoto, and N. Guiso Both adenylate cyclase and hemolytic activities are required for Bordetella pertussis to initiate infection Microb. Pathog. 12 1992 227 235
7. A.A. Weiss, E.L. Hewlett, G.A. Myers, and S. Falkow Pertussis toxin and extracytoplasmic adenylate cyclase as virulence factors of Bordetella pertussis J. Infect. Dis. 150 1984 219 222
8. P. Gueirard, A. Druilhe, M. Pretolani, and N. Guiso Role of adenylate cyclase-hemolysin in alveolar macrophage apoptosis during Bordetella pertussis infection in vivo Infect. Immun. 66 1998 1718 1725
9. E. Hanski Invasive adenylate cyclase toxin of B. pertussis Trends Biochem. Sci. 14 1989 459 463
10. D. Ladant, and A. Ullmann Bordetella pertussis adenylate cyclase: a toxin with multiple talents Trends Microbiol. 4 1999 172 176
11. J.L. Arciniega, E.L. Hewlett, F.D. Johnson, A. Deforest, A. Wassilak, and I.M. Onorato Human serological responses to envelope associated proteins and adenylate cyclase toxin of Bordetella pertussis J. Infect. Dis. 163 1991 135 142
12. F. Betsou, P. Sebo, and N. Guiso CyaC mediated activation is important not only for toxic but also for protective activities of Bordetella pertussis adenylate cyclase-hemolysin Infect. Immun. 61 1993 3583 3589
13. Z. Farfel, S. Konen, E. Wiertz, R. Klapmuts, P.A.K. Addy, and E. Hanski Antibodies to Bordetella pertussis adenylate cyclase are produced in man during pertussis infection and after vaccination J. Med. Microbiol. 32 1990 173 177
14. N. Guiso, M. Rocancourt, M. Szatanik, and J.M. Alonso Bordetella adenylate cyclase is a virulence associated factor and an immunoprotective antigen Microb. Pathog. 7 1989 373 380
15. N. Guiso, M. Szatanik, and M. Rocancourt Protective activity of Bordetella adenylate cyclase-hemolysin against bacterial colonisation Microb. Pathog. 11 1991 423 431
16. K. Hormozi, R. Parton, and J.G. Coote Adjuvant and protective properties of native and recombinant Bordetella pertussis adenylate cyclase toxin preparations in mice FEMS Immunol. Med. Microbiol. 23 1999 273 282
17. F. Betsou, P. Sebo, and N. Guiso The C-terminal domain is essential for protective activity of the Bordetella pertussis adenylate cyclase-hemolysin Infect. Immun. 63 1995 3309 3315
18. G.D. Westrop, E.K. Hormozi, N.A. da Costa, R. Parton, and J.G. Coote Bordetella pertussis adenylate cyclase toxin: proCyaA and CyaC proteins synthesised separately in Escherichia coli produce active toxin in vitro Gene 180 1996 91 99
19. G.D. Westrop, E.K. Hormozi, N.A. da Costa, R. Parton, and J.G. Coote Structure-function studies of the adenylate cyclase toxin of Bordetella pertussis and the leukotoxin of Pasteurella haemolytica by heterologous C protein activation and construction of hybrid toxins J. Bacteriol. 179 1997 871 879
20. D. Ladant, P. Glaser, and A. Ullmann Insertional mutagenesis of Bordetella pertussis adenylate cyclase J. Biol. Chem. 267 1992 2244 2250
21. H. Sakamoto, J. Bellalou, P. Sebo, and D. Ladant Bordetella pertussis adenylate cyclase toxin: structural and functional independence of the catalytic and hemolytic activities J. Biol. Chem. 267 1992 13598 13602
22. D. Ladant, S. Michelson, R. Sarfati, A.M. Gilles, R. Predeleanu, and O. Bârzu Characterisation of the calmodulin-binding and of the catalytic domains of Bordetella pertussis adenylate cyclase J. Biol. Chem. 264 1989 4015 4020
23. A.J. Lawrence, J.G. Coote, F.Y. Kazi, P.D. Lawrence, J. MacDonald-Fyall, and B.M. Orr A direct pyrophosphate-coupled assay provides new insights into the activation of the secreted adenylate cyclase from Bordetella pertussis by calmodulin J. Biol. Chem. 277 2002 22289 22296
24. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein using the principle of protein-dye binding Anal. Biochem. 72 1976 248 257
25. D. Xing, R. Gaines Das, L. Williams, C. Canthaboo, J. Tremmil, and M.J. Corbel An aerosol challenge model of Bordetella pertussis infcetion as a potential bioassay for acellular pertussis vaccines Vaccine 17 1999 565 576
26. R. Gaines Das, D. Xing, P. Rigsby, P. Newland, and M.J. Corbel International collaborative study: evaluation of proposed International Reference Reagent of pertussis antiserum (mouse) 97/642 Biologicals 29 2001 137 148
27. K.P. Beckerman, H.W. Rogers, J.A. Corbett, R.D. Schreiber, M.L. McDaniel, and E.R. Unanue Release of nitric oxide during the T-cell independent pathway of macrophage activation J. Immunol. 150 1993 888 895
28. D. Xing, C. Canthaboo, and M.J. Corbel Nitric oxide induction in murine macrophages and spleen cells by whole-cell Bordetella pertussis vaccine Vaccine 16 1998 16 23
29. D. Torre, G. Ferrario, G. Bonetta, L. Perversi, and F. Speranza In vitro and in vivo induction of nitric oxide by murine macrophages stimulated with Bordetella pertussis FEMS Immunol. Med. Microbiol. 13 1996 95 99
30. N. Khelef, and N. Guiso Induction of macrophage apoptosis by Bordetella pertussis adenylate cyclase-hemolysin FEMS Microbiol. Letts. 134 1995 27 32
31. E. Duprez, B.J. Gjertsen, O. Bernard, M. Lanotte, and S.O. Doskeland Antiapoptotic effect of heterozygously expressed mutant R1 (Ala366-Asp) subunit of cAMP kinase 1 in a rat leukaemia cell line J. Biol. Chem. 268 1993 8332 8340
32. D.H. Lenz, C.L. Weingart, and A.A. Weiss Phagocytosed Bordetella pertussis fails to survive in human neutrophils Infect. Immun. 68 2000 956 959
33. P. McGuirk, and KH.G. Mills A regulatory role for interleukin 4 in differential inflammatory responses in the lung following infection of mice primed with Th1- or Th2-inducing pertussis vaccines Infect. Immun. 68 2000 1383 1390
34. C.L. Weingart, P.S. Mobberley-Schuman, E.K. Hewlett, M.C. Gray, and A.A. Weiss Neutralising antibodies to adenylate cyclase toxin promote phagocytosis of Bordetella pertussis by human neutrophils Infect. Immun. 68 2000 7152 7155
35. + T cells while decreasing IL-2 release and NF-AT induction J. Int. Immun. 6 1994 1333 1341
36. J.J. Munoz Action of pertussigen (pertussis toxin) on the host immune system A.C. Wardlaw R. Parton Pathogenesis and Immunity in Pertussis 1988 Wiley Chichester and New York 173 192
37. M. Roberts, A. Bacon, R. Rappuoli, M. Pizza, I. Cropley, and G. Douce A mutant pertussis toxin molecule that lacks ADP-ribosyltransferase activity, PT-9K/129G, is an effective mucosal adjuvant for intranasally delivered proteins Infect. Immun. 63 1995 2100 2108
38. + T cells for key functions other than specific antibody production J. Exp. Med. 191 2000 1841 1852
39. K.H.G. Mills, A. Barnard, J. Watkins, and K. Redhead Cell-mediated immunity to Bordetella pertussis: role of Th1 cells in bacterial clearance in a murine respiratory infection model Infect. Immun. 61 1993 399 410
40. M. Ryan, G. Murphy, L. Gothefors, L. Nilsson, J. Storsaeter, and KH.G. Mills Bordetella pertussis respiratory infection in children is associated with preferential activation of type 1 T helper cells J. Infect. Dis. 175 1997 1246 1250
41. D. Xing, C. Canthaboo, and M.J. Corbel Effect of pertussis toxin on the induction of nitric oxide synthesis in murine macrophages and on protection in vivo Vaccine 18 2000 2110 2119
42. A.H. Ding, C.F. Nathan, and D.J. Stuehr Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production J. Immunol. 141 1988 2407 2412
43. X. Zhang, and D.C. Morrison Pertussis toxin-sensitive factor differentially regulates lipopolysaccharide-induced tumor necrosis factor-α and nitric oxide production in mouse peritoneal macrphages J. Immunol. 150 1993 1011 1018
44. S. Sakurai, K. Kamachi, T. Konda, N. Miyajima, M. Kohase, and S. Yamamoto Nitric oxide induction by pertussis toxin in mouse spleen cells via gamma interferon Infect. Immun. 64 1996 1309 1313
45. R. Rappuoli, M. Pizza, G. Douce, and G. Dougan Structure and mucosal adjuvanticity of cholera and Escherichia coli heat-labile enterotoxins Immunol. Today 20 1999 493 500
46. E.J. Ryan, L. McCarthy, R. Rappuoli, B.P. Mahon, and K.H.G. Mills Pertussis toxin potentiates Th1 and Th2 responses to co-injected antigen: adjuvant action is associated with enhanced regulatory cytokine production and expression of the co-stimulatory molecules B7-1, B7-2 and CD28 Int. Immunol. 10 1998 651 662
47. E.J. Ryan, E. McNeela, G.A. Murphy, H. Stewart, D. O'Hagan, and M. Pizza Mutants of Escherichia coli heat-labile toxin act as effective mucosal adjuvants for nasal delivery of an acellular pertussis vaccine: differential effects of the nontoxic AB complex and enzyme activity on Th1 and Th2 cells Infect. Immun. 67 1999 6270 6280
48. E.J. Ryan, E. McNeela, M. Pizza, R. Rappuoli, L. O'Neill, and K.H.G. Mills Modulation of innate and acquired immune responses by Escherichia coli heat-labile toxin: distinct pro- and anti-inflammatory effects of the nontoxic AB complex and the enzyme activity J. Immunol. 165 2000 5750 5759
49. K.C. Bagley, S.F. Abdelwahab, R.G. Tuskan, T.R. Fouts, and G.K. Lewis Pertussis toxin and adenylate cyclase toxin from Bordetella pertussis activate human monocyte-derived dendritic cells and dominantly inhibit cytokine production through a cAMP-dependent pathway J. Leuk. Biol. 72 2002 962 969
50. C.M. Ausiello, G. Fedele, F. Urbani, R. Lande, B. Di Carlo, and A. Cassone Native and genetically inactivated pertussis toxins induce human dendritic cell maturation and synergize with lipopolysaccharide in promoting T helper type 1 responses J. Infect. Dis. 186 2002 351 360
51. J. He, S. Gurunathan, A. Iwasaki, B. Ash-Shaheed, and B.L. Kelsall Primary role for Gi protein signalling in the regulation of interleukin 12 production and the induction of T helper cell type 1 responses J. Exp. Med. 191 2000 1605 1610
52. W. Hou, Y. Wu, S. Sun, M. Shi, Y. Sun, and C. Yang Pertussis toxin enhances Th 1 responses by stimulation of dendritic cells J. Immunol. 170 2003 1728 1736
53. P. Guermonprez, N. Khelef, E. Blouin, P. Rieu, P. Ricciardi-Castagnoli, and N. Guiso The adenylate cyclase toxin of Bordetella pertussis binds to target cells via the alpha(M)beta(2) integrin (CD11b/CD18) J. Exp. Med. 193 2001 1035 1044
54. C. Reis e Sousa, and R.N. Germain Analysis of adjuvant function by direct visualisation of antigen presentation in vivo: endotoxin promotes accumulation of antigen-bearing dendritic cells in the T cell areas of lymphoid tissue J. Immunol. 162 1999 6552 6561
55. KH.G. Mills Immunity to Bordetella pertussis Microb. Infect. 3 2001 655 677
56. C. Canthaboo, L. Williams, D. Xing, and M.J. Corbel Investigation of cellular and humoral immune responses to whole cell and acellular pertussis vaccines Vaccine 19 2001 637 643
57. A. Barnard, B.P. Mahon, J. Watkins, K. Redhead, and K.H.G. Mills Th1/Th2 dichotomy in acquired immunity to B. pertussis: variables in the in vivo priming and in vitro cytokine detection techniques affect the classification of T cell subsets as Th1, Th2 or Th0 Immunology 87 1996 372 380
58. B.P. Mahon, M.S. Ryan, F. Griffin, and KH.G. Mills IL-12 is produced by macrophages in response to live or killed Bordetella pertussis and enhances the efficacy of an acellular pertussis vaccine by promoting induction of Th1 cells Infect. Immun. 64 1996 5295 5301
59. K.H.G. Mills, M. Ryan, E. Ryan, and B.P. Mahon A murine model in which protection correlates with pertussis vaccine efficacy in children reveals complementary roles for humoral and cell-mediated immunity in protection against Bordetella pertussis Infect. Immun. 66 1998 594 602
60. J.W. Petersen, P.H. Ibsen, K. Haslov, and I. Heron Proliferative responses and gamma interferon and tumor necrosis factor production by lymphocytes isolated from tracheobronchial lymph nodes and spleens of mice aerosol infected with Bordetella pertussis Infect. Immun. 60 1992 4563 4570
61. K. Redhead, J. Watkins, A. Barnard, and K.H.G. Mills Effective immunization against Bordetella pertussis respiratory infection in mice is dependent on induction of cell-mediated immunity Infect. Immun. 61 1993 3190 3198
62. + T cell clones against Bordetella pertussis Infect. Immun. 59 1991 3768 3773
63. C. Ausiello, F. Urbani, A. La Sala, R. Lande, and A. Cassone Vaccine- and antigen-dependent type 1 and type 2 cytokine induction after primary vaccination of infants with whole cell or acellular pertussis vaccines Infect. Immun. 65 1997 2168 2174
64. M. Ryan, G. Murphy, E. Ryan, L. Nilsson, F. Shackley, and L. Gothefors Distinct T-cell subtypes induced with whole cell and acellular pertussis vaccines in children Immunology 93 1998 1 10