Bordetella pertussis commits human dendritic cells to promote a Th1/Th17 response through the activity of adenylate cyclase toxin and MAPK-pathways

PLoS ONE

Volumn 5, Issue 1, 2010, Pages

  Fedele, Giorgio ^a   Spensieri, Fabiana ^a   Palazzo, Raffaella ^a   Nasso, Maria ^a   Cheung, Gordon Yiu Chong ^b,c   Coote, John Graham ^b   Ausiello, Clara Maria ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE TOXIN; INTERLEUKIN 12P70; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; TOLL LIKE RECEPTOR 11; TOLL LIKE RECEPTOR 4; CYTOKINE; PHOSPHATIDYLINOSITOL 3 KINASE;

ARTICLE; BORDETELLA PERTUSSIS; CELL MATURATION; CELL POLARITY; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; ENZYME ACTIVITY; EX VIVO STUDY; HOST; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNE RESPONSE; IMMUNOMODULATION; MONOCYTE; NONHUMAN; PHENOTYPE; POLARIZATION; SIGNAL TRANSDUCTION; TH1 CELL; TH17 CELL; WILD TYPE; BIOSYNTHESIS; HELPER CELL; IMMUNOLOGY; METABOLISM; PHYSIOLOGY;

BACTERIA (MICROORGANISMS); BORDETELLA PERTUSSIS;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ADENYLATE CYCLASE TOXIN; BORDETELLA PERTUSSIS; CYTOKINES; DENDRITIC CELLS; HUMANS; MAP KINASE SIGNALING SYSTEM; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 77649278937     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0008734     Document Type: Article

References (48)

1. von König CH, Halperin S, Riffelmann M, Guiso N (2002) Pertussis of adults and infants. Lancet Infect Dis 2: 744-750.
2. Mattoo S, Cherry JD (2005) Molecular pathogenesis, epidemiology, and clinical manifestations of respiratory infections due to Bordetella pertussis and other Bordetella subspecies. Clin Microbiol Rev 18: 326-382.
3. Hewlett EL, Edwards KM (2005) Clinical practice. Pertussis - not just for kids. N Engl J Med 352: 1215-1222.
4. He Q, Mertsola J (2008) Factors contributing to pertussis resurgence. Future Microbiol 3: 329-339.
5. Locht C, Antoine R, Jacob-Dubuisson F (2001) Bordetella pertussis, molecular pathogenesis under multiple aspects. Curr Opin Microbiol 4: 82-89.
6. Mills KH (2001) Immunity to Bordetella pertussis. Microbes Infect 3: 655-677.
7. Guermonprez P, Khelef N, Blouin E, Rieu P, Ricciardi-Castagnoli P, et al. (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.
8. Bouhss A, Krin E, Munier H, Gilles AM, Danchin A, et al. (1993) Cooperative phenomena in binding and activation of Bordetella pertussis adenylate cyclase by calmodulin. J Biol Chem 268: 1690-1694.
9. Hewlett EL, Gray L, Allietta M, Ehrmann I, Gordon VM, et al. (1991) Adenylate cyclase toxin from Bordetella pertussis. Conformational change associated with toxin activity. J Biol Chem 266: 17503-17508.
10. Vojtova J, Kamanova J, Sebo P (2006) Bordetella adenylate cyclase toxin: a swift saboteur of host defense. Curr Opin Microbiol 9: 69-75.
11. Bassinet L, Gueirard P, Maitre B, Housset B, Gounon P, et al. (2000) Role of adhesins and toxins in invasion of human tracheal epithelial cells by Bordetella pertussis. Infect Immun 68: 1934-1941.
12. Bagley KC, Abdelwahab SF, Tuskan RG, Fouts TR, Lewis GK (2002) Pertussis toxin and the adenylate cyclase toxin from Bordetella pertussis activate human monocyte-derived dendritic cells and dominantly inhibit cytokine production through a cAMP-dependent pathway. J Leukoc Biol 72: 962-969.
13. Ross PJ, Lavelle EC, Mills KH, Boyd AP (2004) Adenylate cyclase toxin from Bordetella pertussis synergizes with lipopolysaccharide to promote innate interleukin-10 production and enhances the induction of Th2 and regulatory T cells. Infect Immun 72: 1568-1579.
14. Boyd AP, Ross PJ, Conroy H, Mahon N, Lavelle EC, Mills KH (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: 730-738.
15. Spensieri F, Fedele G, Fazio C, Nasso M, Stefanelli P, et al. (2006) Bordetella pertussis inhibition of interleukin-12 (IL-12) p70 in human monocyte-derived dendritic cells blocks IL-12 p35 through adenylate cyclase toxin-dependent cyclic AMP induction. Infect Immun 74: 2831-2838.
16. Hickey FB, Brereton CF, Mills KH (2008) Adenylate cyclase toxin of Bordetella pertussis inhibits TLR-induced IRF-1 and IRF-8 activation and IL-12 production and enhances IL-10 through MAPK activation in dendritic cells. J Leukoc Biol 84: 234-243.
17. Goodwin MS, Weiss AA (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. Khelef N, Sakamoto H, Guiso N (1992) Both adenylate cyclase and hemolytic activities are required by Bordetella pertussis to initiate infection. Microb Pathog 12: 227-235.
19. Khelef N, Zychlinsky A, Guiso N (1993) Bordetella pertussis induces apoptosis in macrophages: role of adenylate cyclase-hemolysin. Infect Immun 61: 4064-4071.
20. Khelef N, Guiso N (1995) Induction of macrophage apoptosis by Bordetella pertussis adenylate cyclase-hemolysin. FEMS Microbiol Lett 134: 27-32.
21. Rescigno M (2002) Dendritic cells and the complexity of bacterial infection. Trends Microbiol 10: 425-461.
22. Steinman RM, Hemmi H (2006) Dendritic cells: translating innate to adaptive immunity. Curr Top Microbiol Immunol 311: 17-58.
23. Fedele G, Stefanelli P, Spensieri F, Fazio C, Mastrantonio P, et al. (2005) Bordetella pertussis-infected human monocyte-derived dendritic cells undergo maturation and induce Th1 polarization and interleukin-23 expression. Infect Immun 73: 1590-1597.
24. Westrop GD, Hormozi EK, Da Costa NA, Parton R, Coote JG (1997) Bordetella pertussis adenylate cyclase toxin: proCyaA and CyaC proteins synthesised separately in Escherichia coli produce active toxin in vitro. Gene 180: 91-99.
25. Cheung GY, Xing D, Prior S, Corbel MJ, Parton R, et al. (2006) Effect of different forms of adenylate cyclase toxin of Bordetella pertussis on protection afforded by an acellular pertussis vaccine in a murine model. Infect Immun 74: 6797-6805.
26. Frasca L, Fedele G, Deaglio S, Capuano C, Palazzo R, et al. (2006) CD38 orchestrates migration, survival, and Th1 immune response of human mature dendritic cells. Blood 107: 2392-2399.
27. Fedele G, Frasca L, Palazzo R, Ferrero E, Malavasi F, et al. (2004) CD38 is expressed on human mature monocyte-derived dendritic cells and is functionally involved in CD83 expression and IL-12 induction. Eur J Immunol 34: 1342-1350.
28. Weaver CT, Hatton RD, Mangan PR, Harrington LE (2007) IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu Rev Immunol 25: 821-852.
29. Acosta-Rodriguez EV, Napolitani G, Lanzavecchia A, Sallusto F (2007) Interleukins 1beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells. Nat Immunol 8: 942-949.
30. Wilson NJ, Boniface K, Chan JR, McKenzie BS, Blumenschein WM, et al. (2007) Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat Immunol 8: 950-957.
31. Fedele G, Celestino I, Spensieri F, Frasca L, Nasso M, et al. (2007) Lipooligosaccharide from Bordetella pertussis induces mature human monocyte-derived dendritic cells and drives a Th2 biased response. Microbes Infect 9: 855-863.
32. Sabroe I, Parker LC, Dower SK, Whyte MK (2008) The role of TLR activation in inflammation. J Pathol 214: 126-135.
33. Arbibe L, Mira PJ, Teusch N, Kline L, Guha M, et al. (2000) Toll-like receptor 2-mediated NF-κB activation requires a Rac1-dependent pathway. Nat Immunol 1: 533-540.
34. Ausiello CM, Lande R, Urbani F, Di Carlo B, Stefanelli P, et al. (2000) Cell-mediated immunity and antibody responses to Bordetella pertussis antigens in children with a history of pertussis infection and in recipients of an acellular pertussis vaccine. J Infect Dis 181: 1989-1995.
35. Mascart F, Verscheure V, Malfroot A, Hainaut M, Piérard D, et al. (2003) Bordetella pertussis infection in 2-month-old infants promotes type 1 T cell responses. J Immunol 170: 1504-1509.
36. Malavasi F, Deaglio S, Funaro A, Ferrero E, Horenstein AL, et al. (2008) Evolution and Function of the ADP Ribosyl Cyclase/CD38 Gene Family in Physiology and Pathology. Physiol Rev 88: 841-886.
37. Carbonetti NH (2007) Immunomodulation in the pathogenesis of Bordetella pertussis infection and disease. Curr Opin Pharmacol 7: 272-278.
38. Siciliano NA, Skinner JA, Yuk MH (2006) Bordetella bronchiseptica modulates macrophage phenotype leading to the inhibition of CD4+ T cell proliferation and the initiation of a Th17 immune response. J Immunol 177: 7131-7138.
39. Higgins SC, Jarnicki AG, Lavelle EC, Mills KH (2006) TLR4 mediates vaccine-induced protective cellular immunity to Bordetella pertussis: role of IL-17-producing T cells. J Immunol 177: 7980-7989.
40. Fedele G, Nasso M, Spensieri F, Palazzo R, Frasca L, et al. (2008) Lipopolysaccharides from Bordetella pertussis and Bordetella parapertussis differently modulate human dendritic cell functions resulting in divergent prevalence of Th17-polarized responses. J Immunol 181: 208-216.
41. Nasso M, Fedele G, Spensieri F, Palazzo R, Costantino P, et al. (2009) Genetically detoxified pertussis toxin induces Th1/Th17 immune response through mitogen-activated protein kinases and IL-10-dependent mechanisms. J Immunol 183: 1892-1899.
42. Hoeve MA, Savage ND, de Boer T, Langenberg DM, de Waal Malefyt R, et al. (2006) Divergent effects of IL-12 and IL-23 on the production of IL-17 by human T cells. Eur J Immunol 36: 661-670.
43. Higgins SC, Lavelle EC, McCann C, Keogh B, McNeela E, et al. (2003) Toll-like receptor 4-mediated innate IL-10 activates antigen-specific regulatory T cells and confers resistance to Bordetella pertussis by inhibiting inflammatory pathology. J Imuunol 171: 3119-3127.
44. Akira S, Takeda K (2004) Toll-like receptor signalling. Nat Rev Immunol 4: 499-511.
45. Gautier G, Humbert M, Deauvieau F, Scuiller M, Hiscott J, et al. (2005) A type I interferon autocrine-paracrine loop is involved in Toll-like receptor-induced interleukin-12p70 secretion by dendritic cells. J Exp Med 201: 1435-1446.
46. Khelef N, Bachelet CM, Vargaftig BB, Guiso N (1994) Characterization of murine lung inflammation after infection with parental Bordetella pertussis and mutants deficient in adhesins or toxins. Infect Immun 62: 2893-2900.
47. Harvill ET, Cotter PA, Yuk MH, Miller JF (1999) Probing the function of Bordetella bronchiseptica adenylate cyclase toxin by manipulating host immunity. Infect Immun 67: 1493-1500.
48. Nembrini C, Marsland BJ, Kopf M (2009) IL-17-producing T cells in lung immunity and inflammation. J Allergy Clin Immunol 123: 986-994.