Bordetella pertussis toxin induces the release of inflammatory cytokines and dendritic cell activation in whole blood: Impaired responses in human newborns

European Journal of Immunology

Volumn 32, Issue 11, 2002, Pages 3118-3125

  Tonon, Sandrine ^a   Goriely, Stanislas ^a   Aksoy, Ezra ^a   Pradier, Olivier ^a   Del Giudice, Guiseppe ^b   Trannoy, Emmanuelle ^c   Willems, Fabienne ^a   Goldman, Michel ^a   De Wit, Dominique ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b CHIRON VACCINES   (Italy)

^c SANOFI PASTEUR   (France)

Author keywords

Dendritic cell; IL 12; Newborn; Pertussis toxin

Indexed keywords

ACELLULAR VACCINE; ADJUVANT; FORMALDEHYDE; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; INTERLEUKIN 2; INTERLEUKIN 4; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MUTANT PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PERTUSSIS TOXIN; PERTUSSIS VACCINE; POLYMYXIN B; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; BORDETELLA PERTUSSIS; CELL ACTIVATION; CELL MATURATION; CONTROLLED STUDY; CULTURE MEDIUM; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; DRUG INACTIVATION; ENZYME ACTIVITY; EXPERIMENTAL DESIGN; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; IMMUNOCOMPETENT CELL; IMMUNOSTIMULATION; IN VITRO STUDY; INFECTION SENSITIVITY; LEUKOCYTE CULTURE; MONOCYTE; MOUSE; NEWBORN; NONHUMAN; PERTUSSIS; PRIORITY JOURNAL; REVIEW; TH2 CELL; TOXIN STRUCTURE; UMBILICAL CORD BLOOD; UPREGULATION;

ADULT; CYTOKINES; DENDRITIC CELLS; DOSE-RESPONSE RELATIONSHIP, DRUG; FETAL BLOOD; HUMANS; INFANT, NEWBORN; INTERLEUKIN-12; NF-KAPPA B; PERTUSSIS TOXIN;

EID: 0036857834     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/1521-4141(200211)32:11<3118::AID-IMMU3118>3.0.CO;2-B     Document Type: Review

References (38)

1. Falnes, P. O. and Sandvig, K., Penetration of protein toxins into cells. Curr. Opin. Cell Biol. 2000. 12: 407-413.
2. Grenier-Brossette, N., Bourget, I., Breittmayer, J. P., Ferrua, B., Fehlmann, M. and Cousin, J. L., Pertussis toxin-induced mitogenesis in human T lymphocytes. Immunopharmacology 1991. 21: 109-119.
3. Macintyre, E. A., Tatham, P. E., Abdul-Gaffar, R. and Linch, D. C., The effects of pertussis toxin on human T lymphocytes. Immunology 1988. 64: 427-432.
4. Samore, M. H. and Siber, G. R., Pertussis toxin enhanced IgG1 and IgE responses to primary tetanus immunization are mediated by interleukin-4 and persist during secondary responses to tetanus alone. Vaccine 1996. 14: 290-297.
5. Mu, H. H. and Sewell, W. A., Regulation of DTH and IgE responses by IL-4 and IFN-gamma in immunized mice given pertussis toxin. Immunology 1994. 83: 639-645.
6. Jee, Y. and Matsumoto, Y., Two-step activation of T cells, clonal expansion and subsequent Th1 cytokine production, is essential for the development of clinical autoimmune encephalomyelitis. Eur. J. Immunol. 2001. 31: 1800-1812.
7. Hu, Y. J., Zang, L., L., Wu, Y. D. and Sun, B., High IFN-alpha expression is associated with the induction of experimental autoimmune uveitis (EAU) in Fischer 344 rat. Cell Res. 2001. 11: 293-300.
8. Roberts, M., Bacon, A., Rappuoli, R., Pizza, M., Cropley, I., Douce, G., Dougan, G., Marinaro, M., McGhee, J. and Chatfield, S., A mutant pertussis toxin molecule that lacks ADP-ribosyltransferase activity, PT-9K/129G, is an effective mucosal adjuvant for intranasally delivered proteins. Infect. Immun. 1995. 63: 2100-2108.
9. Shive, C. L., Hofstetter, H., Arredondo, L., Shaw, C. and Forsthuber, T. G., The enhanced antigen-specific production of cytokines induced by pertussis toxin is due to clonal expansion of T cells and not to altered effector functions of long-term memory cells. Eur. J. Immunol. 2000. 30: 2422-2431.
10. Ryan, M., McCarthy, L., Rappuoli, R., Mahon, B. P. and Mills, K. H., Pertussis toxin potentiates Th1 and Th2 responses to coinjected antigen: adjuvant action is associated with enhanced regulatory cytokine production and expression of the costimulatory molecules B7-1, B7-2 and CD28. Int. Immunol. 1998. 10: 651-662.
11. Pizza, M., Covacci, A., Bartoloni, A., Perugini, M., Nencioni, L., De Magistris, M. T., Villa, L., Nucci, D., Manetti, R. and Bugnoli, M., Mutants of pertussis toxin suitable for vaccine development. Science 1989. 246: 497-500.
12. Rappuoli, R., Rational design of vaccines. Nature Med. 1997. 3: 374-376.
13. Pizza, M., Greco, D., Salmaso, S., Mastrantonio, P., Giuliano, M., Tozzi, A. E., Anemona, A., Ciofi degli Atti, M. L., Giammanco, A., Panei, P., Blackwelder, W. C., Klein, D. L. and Wassilak, S. G., Mutants A controlled trial of two accellular vaccines and one whole-cell against pertussis. Progetto Pertosse Working Group. N. Engl. J. Med. 1996. 334: 341-348.
14. He, J., Gurunathan, S., Iwasaki, A., Ash-Shaheed, B. and Kelsall, B. L., Primary role for Gi protein signaling in the regulation of interleukin 12 production and the induction of T helper cell type 1 responses. J. Exp. Med. 2000. 191: 1605-1610.
15. O'Doherty, U., Peng, M., Gezelter, S., Swiggard, W. J., Betjes, M., Bhardwaj, N. and Steinman, R. M., Human blood contains two subsets of dendritic cells, one immunologically mature and the other immature. Immunology 1994. 82: 487-493.
16. Hartmann, G., Weiner, G. and Krieg, A. M., CpG DNA: A potent signal for growth, activation and maturation of human dendritic cells. Proc. Natl. Acad. Sci. USA 1999. 96: 9305-9310.
17. Pichyangkul, S., Yongvanitchit, K., Kum-arb, U., Krieg, A. M., Heppner, D. G. and Walsh, D. S., Wole blood cultures to assess the immunostimulatory activities of CpG oligonucleotides. J. Immunol. Methods 2001. 247: 83-94.
18. de Jong, E. C., Vieira, P. L., Kalinski, P., Schuitemaker, J. H., Tanaka, Y., Wierenga, E. A., Yazdanbakhsh, M. and Kapsenberg, M. L., Microbial compounds selectively induce Th1 cell-promoting or Th2 cell-promoting dendritic cells in vitro with diverse th cell-polarizing signals. J. Immunol. 2002. 168: 1704-1709.
19. Rescigno, M., Martino, M., Sutherland, C. L., Gold, M. R. and Ricciardi-Castagnoli, P., Dendritic cell survival and maturation are regulated by different signaling pathways. J. Exp. Med. 1998. 188: 2175-2180.
20. Akira, S., Toll-like receptors and innate immunity. Adv. Immunol. 2001. 78: 1-56.
21. Saukkonen, K., Burnette, W. N., Mar, V. L., Masure, H. R. and Tuomanen, E. I., Pertussis toxin has eukaryotic-like carbohydrate recognition domains. Proc. Natl. Acad. Sci. USA 1992. 89: 118-122.
22. Prescott, S. L., Macaubas, C., Holt, B. J., Smallacombe, T. B., Loh, R., Sly, P. D. and Holt, P. G., Transplacental priming of the human immune system to environmental allergens: universal skewing of initial T cell responses toward the Th2 cytokine profile. J. Immunol. 1998. 160: 4730-4737.
23. Goriely, S., Vincart, B., Stordeur, P., Vekemans, J., Willems, F., Goldman, M. and De Wit, D., Deficient II-12(p35) gene expression by dendritic cells derived from neonatal monocytes. J. Immunol. 2001. 166: 2141-2146.
24. Mills, K. H., Ryan, M., Ryan, E. and Mahon, B. P., 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 Bordetalla pertussis. Infect. Immun. 1998. 66: 594-602.
25. Leef, M., Elkins, K. L., Barbic, J. and Shahin, R. D., Protective immunity to Bordetella pertussis requires both B cells and CD4(+)T cells for key functions other than specific antibody production. J. Exp. Med. 2000. 191: 1841-1852.
26. Ryan, M., Murphy, G., Gothefors, L., Nilsson, L., Storsaeter, J. and Mills, K. H., Bordetalla pertussis respiratory infection in children is associated with preferential activation of type 1 T helper cells. J. Infect. Dis. 1997. 175: 1246-1250.
27. Rowe, C., Macaubas, C., Monger, T. M., Holt, B. J., Harvey, J., Poolman, J. T., Sly, P. D. and Holt, P. G., Antigen-specific responses to diphtheria-tetanus-acellular pertussis vaccine in human infants are initially Th2 polarized. Infect. Immun. 2000. 68: 3873-3877.
28. Ryan, M., Gothefors, L., Storsaeter, J. and Mills, K. H., Bordetalla pertussis-specific Th1/Th2 cells generated following respiratory infection or immunization with an acellular vaccine: comparison of the T cell cytokine profiles in infants and mice. Dev. Biol. Stand. 1997. 89: 297-305.
29. Ryan, M., Murphy, G., Ryan, E., Nilsson, L., Shackley, F., Gothefors, L., Oymar, K., Miller, E., Storsaeter, J. and Mills, K. H., Distinct T-cell subtypes induced with whole cell and acellular pertussis vaccines in children. Immunology 1998. 93: 1-10.
30. Mcguirk, P., McCann, C. and Mills, K. H., Pathogen-specific T Regulatory 1 Cells Induced in the Respiratory Tract by a Bacterial Molecule that Stimulates Interleukin 10 Production by Dendritic Cells: A Novel Strategy for Evasion of Protective T Helper Type 1 Responses by Bordetalla pertussis. J. Exp. Med. 2002. 195: 221-231.
31. Mcguirk, P. and Mills, K. H., Direct anti-inflammatory effect of a bacterial virulence factor: IL-10 dependent suppression of IL-12 production by filamentous hemagglutinin from Bordetella pertussis. Eur. J. Immunol. 2000. 30: 415-422.
32. Siegrist, C. A., Neonatal and early life vaccinology. Vaccine 2001. 19: 3331-3346.
33. Marchand, A., Goetghebuer, T., Ota, M. O., Wolfe, I., Ceesay, S. J., De Groote, D., Corrah, T., Bennett, S., Wheeler, J., Huygen, K., Aaby, P., McAdam, K. P. and Newport, M. J., Newborns develop a Th1-type immune response to Mycobacterium bovis bacillus Calmette-Guerin vaccination. J. Immunol. 1999. 163: 2249-2255.
34. Ota, M. O., Vekemans, J., Schlegel-Haueter, S. E., Fielding, K., Sanneh, M., Kidd, M., Newport, M. J., Aaby, P., Whittle, H., Lambert, P. H., McAdam, K. P., Siegrist, C. A. and Marchant, A., Influence of Mycobacterium bovis bacillus Calmette-Guerin on antibody and cytokine responses to human neonatal vaccination. J. Immunol. 2002: 168: 919-925.
35. Roduit, C., Bozzoti, P., Mielcarek, N., Lambert, P- H., del Giudice, G., Locht, C. and Siegrist, C. A., Immunogenecity and protective efficacy of neonatal vaccination against Bordetella pertussis in a murine model: evidence for early control of pertussis. Infect. Immun. 2002. 70: 3521-3528.
36. Romani, N., Gruner, S., Brang, D., Kampgen, E., Lenz, A., Trockenbacher, B., Konwalinka, G., Fritsch, P. O., Steinman, R. M. and Schuler, G., Proliferating dendritic cell progenitors in human blood. J. Exp. Med. 1994. 180: 83-93.
37. Dignam, J. D., Lebovitz, R. M. and Roeder, R. G., Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983: 11: 1475-1489.
38. Van Lint, C., Ghysdael, J., Paras, P., Jr., Burny, A. and Verdin, E., A transcriptional regulatory element is associated with a nuclease-hypersensitive site in the pol gene of human immunodeficiency virus type 1. J. Virol. 1994. 68: 2632-2648.