Bordetella adenylate cyclase toxin differentially modulates toll-like receptor-stimulated activation, migration and T cell stimulatory capacity of dendritic cells

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Adkins, Irena ^a   Kamanova, Jana ^a   Kocourkova, Aneta ^b   Svedova, Martina ^a   Tomala, Jakub ^a   Janova, Hana ^a   Masin, Jiri ^a   Chladkova, Barbora ^a   Bumba, Ladislav ^a   Kovar, Marek ^a   Ross, Padraig J ^c   Tuckova, Ludmila ^a   Spisek, Radek ^b   Mills, Kingston H G ^c   Sebo, Peter ^a  

^a INSTITUTE OF MICROBIOLOGY   (Czech Republic)

^b CHARLES UNIVERSITY   (Czech Republic)

^c TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE TOXIN; BORDETELLA VIRULENCE FACTOR; CD4 ANTIGEN; CD40 ANTIGEN; CYCLIC AMP; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 17; INTERLEUKIN 2 RECEPTOR ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; SECONDARY LYMPHOID TISSUE CHEMOKINE; TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR FOXP3; LEUKOCYTE ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN PRESENTATION; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL ADHESION; CELL DETACHMENT; CELL EXPANSION; CELL MATURATION; CELL MIGRATION; CELL SURVIVAL; CELL VIABILITY; CELLULAR IMMUNITY; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; HUMAN; HUMAN CELL; IMMUNOMODULATION; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; LYMPHATIC DRAINAGE; LYMPHOCYTE ACTIVATION; LYMPHOCYTE PROLIFERATION; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; ANIMAL; BORDETELLA PERTUSSIS; C57BL MOUSE; CELL DEATH; CELL MOTION; CELL PROLIFERATION; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; IMMUNOLOGY; METABOLISM; SOLUBILITY;

ADENYLATE CYCLASE TOXIN; ANIMALS; ANTIGENS, CD; BORDETELLA PERTUSSIS; CD8-POSITIVE T-LYMPHOCYTES; CELL ADHESION; CELL DEATH; CELL MOVEMENT; CELL PROLIFERATION; DENDRITIC CELLS; HUMANS; LYMPHOCYTE ACTIVATION; MICE, INBRED C57BL; SOLUBILITY; T-LYMPHOCYTES, REGULATORY; TOLL-LIKE RECEPTORS;

EID: 84905454774     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0104064     Document Type: Article

References (57)

1. de Gouw D, Diavatopoulos DA, Bootsma HJ, Hermans PW, Mooi FR (2011) Pertussis: a matter of immune modulation. FEMS Microbiol Rev 35: 441-474.
2. Plotkin SA (2014) The pertussis problem. Clin Infect Dis 58: 830-833.
3. Higgs R, Higgins SC, Ross PJ, Mills KH (2012) Immunity to the respiratory pathogen Bordetella pertussis. Mucosal Immunol 5: 485-500.
4. Vojtova J, Kamanova J, Sebo P (2006) Bordetella adenylate cyclase toxin: a swift saboteur of host defense. Curr Opin Microbiol 9: 69-75. (Pubitemid 43184339)
5. 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. (Pubitemid 20293461)
6. Fiser R, Masin J, Basler M, Krusek J, Spulakova V, et al. (2007) Third activity of Bordetella adenylate cyclase (AC) toxin-hemolysin. Membrane translocation of AC domain polypeptide promotes calcium influx into CD11b+ monocytes independently of the catalytic and hemolytic activities. J Biol Chem 282: 2808-2820. (Pubitemid 47084337)
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. (Pubitemid 32436197)
8. Ladant D, Ullmann A (1999) Bordatella pertussis adenylate cyclase: a toxin with multiple talents. Trends Microbiol 7: 172-176. (Pubitemid 29229904)
9. Dunne A, Ross PJ, Pospisilova E, Masin J, Meaney A, et al. (2010) Inflammasome activation by adenylate cyclase toxin directs Th17 responses and protection against Bordetella pertussis. J Immunol 185: 1711-1719.
10. Confer DL, Eaton JW (1982) Phagocyte impotence caused by an invasive bacterial adenylate cyclase. Science 217: 948-950. (Pubitemid 12047357)
11. Pearson RD, Symes P, Conboy M, Weiss AA, Hewlett EL (1987) Inhibition of monocyte oxidative responses by Bordetella pertussis adenylate cyclase toxin. J Immunol 139: 2749-2754. (Pubitemid 17153955)
12. Khelef N, Zychlinsky A, Guiso N (1993) Bordetella pertussis induces apoptosis in macrophages: role of adenylate cyclase-hemolysin. Infect Immun 61: 4064-4071. (Pubitemid 23298555)
13. Basler M, Masin J, Osicka R, Sebo P (2006) Pore-forming and enzymatic activities of Bordetella pertussis adenylate cyclase toxin synergize in promoting lysis of monocytes. Infect Immun 74: 2207-2214.
14. Kamanova J, Kofronova O, Masin J, Genth H, Vojtova J, et al. (2008) Adenylate cyclase toxin subverts phagocyte function by RhoA inhibition and unproductive ruffling. J Immunol 181: 5587-5597.
15. 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. (Pubitemid 35365170)
16. Boyd AP, Ross PJ, Conroy H, Mahon N, Lavelle EC, et al. (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. (Pubitemid 41094953)
17. Hickey FB, Brereton CF, Mills KH (2008) Adenylate cycalse 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. (Pubitemid 351960299)
18. 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. (Pubitemid 38263779)
19. 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. (Pubitemid 43672993)
20. Fedele G, Spensieri F, Palazzo R, Nasso M, Cheung GY, et al. (2010) Bordetella pertussis commits human dendritic cells to promote a Th1/Th17 response through the activity of adenylate cyclase toxin and MAPK-pathways. PLoS One 5: e8734.
21. 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. (Pubitemid 44846315)
22. Leef M, Elkins KL, Barbic J, Shahin RD (2000) Protective immunity to Bordetella pertussis requires both B cells and CD4(+) T cells for key functions other than specific antibody production. J Exp Med 191: 1841-1852. (Pubitemid 30390348)
23. Mills KH, Barnard A, Watkins J, Redhead K (1993) Cell-mediated immunity to Bordetella pertussis: role of Th1 cells in bacterial clearance in a murine respiratory infection model. Infect Immun 61: 399-410. (Pubitemid 23030823)
24. Dirix V, Verscheure V, Vermeulen F, De Schutter I, Goetghebuer T, et al. (2012) Both CD4(+) and CD8(+) lymphocytes participate in the IFN-gamma response to filamentous hemagglutinin from Bordetella pertussis in infants, children, and adults. Clin Dev Immunol 2012: 795958.
25. Rieber N, Graf A, Hartl D, Urschel S, Belohradsky BH, et al. (2011) Acellular pertussis booster in adolescents induces Th1 and memory CD8+ T cell immune response. PLoS One 6: e17271.
26. Eby JC, Gray MC, Warfel JM, Paddock CD, Jones TF, et al. (2013) Quantification of the adenylate cyclase toxin of Bordetella pertussis in vitro and during respiratory infection. Infect Immun 81: 1390-1398.
27. Lutz MB, Rovere P, Kleijmeer MJ, Rescigno M, Assmann CU, et al. (1997) Intracellular routes and selective retention of antigens in mildly acidic cathepsin D/lysosome-associated membrane protein-1/MHC class II-positive vesicles in immature dendritic cells. J Immunol 159: 3707-3716. (Pubitemid 127469624)
28. Spisek R, Brazova J, Rozkova D, Zapletalova K, Sediva A, et al. (2004) Maturation of dendritic cells by bacterial immunomodulators. Vaccine 22: 2761-2768. (Pubitemid 38900652)
29. Tartz S, Kamanova J, Simsova M, Sebo P, Bolte S, et al. (2006) Immunization with a circumsporozoite epitope fused to Bordetella pertussis adenylate cyclase in conjunction with cytotoxic T-lymphocyte-associated antigen 4 blockade confers protection against Plasmodium berghei liver-stage malaria. Infect Immun 74: 2277-2285.
30. Masin J, Basler M, Knapp O, El-Azami-El-Idrissi M, Maier E, et al. (2005) Acylation of lysine 860 allows tight binding and cytotoxicity of Bordetella adenylate cyclase on CD11b-expressing cells. Biochemistry 44: 12759-12766. (Pubitemid 41377315)
31. Atienza JM, Zhu J, Wang X, Xu X, Abassi Y (2005) Dynamic monitoring of cell adhesion and spreading on microelectronic sensor arrays. J Biomol Screen 10: 795-805. (Pubitemid 41818155)
32. Adkins I, Koberle M, Grobner S, Autenrieth SE, Bohn E, et al. (2008) Y. enterocolitica inhibits antigen degradation in dendritic cells. Microbes Infect 10: 798-806.
33. Burgdorf S, Kautz A, Bohnert V, Knolle PA, Kurts C (2007) Distinct pathways of antigen uptake and intracellular routing in CD4 and CD8 T cell activation. Science 316: 612-616. (Pubitemid 46683149)
34. Tanaka Y, Nakano H, Ishikawa F, Yoshida M, Gyotoku Y, et al. (1999) Cholera toxin increases intracellular pH in B lymphoma cells and decreases their antigen-presenting ability. Eur J Immunol 29: 1561-1570. (Pubitemid 29224461)
35. Hori S, Nomura T, Sakaguchi S (2003) Control of regulatory T cell development by the transcription factor Foxp3. Science 299: 1057-1061. (Pubitemid 36222930)
36. Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, et al. (2000) Immunobiology of dendritic cells. Annu Rev Immunol 18: 767-811. (Pubitemid 30365397)
37. Dunne PJ, Moran B, Cummins RC, Mills KH (2009) CD11c+CD8alpha+ dendritic cells promote protective immunity to respiratory infection with Bordetella pertussis. J Immunol 183: 400-410.
38. Ricart BG, John B, Lee D, Hunter CA, Hammer DA (2011) Dendritic cells distinguish individual chemokine signals through CCR7 and CXCR4. J Immunol 186: 53-61.
39. Palecek SP, Loftus JC, Ginsberg MH, Lauffenburger DA, Horwitz AF (1997) Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature 385: 537-540. (Pubitemid 27074672)
40. Fedele G, Bianco M, Debrie AS, Locht C, Ausiello CM (2011) Attenuated Bordetella pertussis vaccine candidate BPZE1 promotes human dendritic cell CCL21-induced migration and drives a Th1/Th17 response. J Immunol 186: 5388-5396.
41. Boschwitz JS, Batanghari JW, Kedem H, Relman DA (1997) Bordetella pertussis infection of human monocytes inhibits antigen-dependent CD4 T cell proliferation. J Infect Dis 176: 678-686. (Pubitemid 27360533)
42. McGuirk P, Mahon BP, Griffin F, Mills KH (1998) Compartmentalization of T cell responses following respiratory infection with Bordetella pertussis: hyporesponsiveness of lung T cells is associated with modulated expression of the co-stimulatory molecule CD28. Eur J Immunol 28: 153-163. (Pubitemid 28048286)
43. Challier J, Bruniquel D, Sewell AK, Laugel B (2013) Adenosine and cAMP signalling skew human dendritic cell differentiation towards a tolerogenic phenotype with defective CD8(+) T-cell priming capacity. Immunology 138: 402-410.
44. Rossi Paccani S, Benagiano M, Capitani N, Zornetta I, Ladant D, et al. (2009) The adenylate cyclase toxins of Bacillus anthracis and Bordetella pertussis promote Th2 cell development by shaping T cell antigen receptor signaling. PLoS Pathog 5: e1000325.
45. Matousek MP, Nedrud JG, Harding CV (1996) Distinct effects of recombinant cholera toxin B subunit and holotoxin on different stages of class II MHC antigen processing and presentation by macrophages. J Immunol 156: 4137-4145. (Pubitemid 26165808)
46. Matousek MP, Nedrud JG, Cieplak W Jr, Harding CV (1998) Inhibition of class II major histocompatibility complex antigen processing by Escherichia coli heat-labile enterotoxin requires an enzymatically active A subunit. Infect Immun 66: 3480-3484. (Pubitemid 28303160)
47. Curtsinger JM, Schmidt CS, Mondino A, Lins DC, Kedl RM, et al. (1999) Inflammatory cytokines provide a third signal for activation of naive CD4+ and CD8+ T cells. J Immunol 162: 3256-3262. (Pubitemid 29313572)
48. Schmidt CS, Mescher MF (2002) Peptide antigen priming of naive, but not memory, CD8 T cells requires a third signal that can be provided by IL-12. J Immunol 168: 5521-5529. (Pubitemid 34556131)
49. Day PM, Yewdell JW, Porgador A, Germain RN, Bennink JR (1997) Direct delivery of exogenous MHC class I molecule-binding oligopeptides to the endoplasmic reticulum of viable cells. Proc Natl Acad Sci U S A 94: 8064-8069. (Pubitemid 27343777)
50. Granados DP, Tanguay PL, Hardy MP, Caron E, de Verteuil D, et al. (2009) ER stress affects processing of MHC class I-associated peptides. BMC Immunol 10: 10.
51. Bartoszewski R, Brewer JW, Rab A, Crossman DK, Bartoszewska S, et al. (2011) The unfolded protein response (UPR)-activated transcription factor X-box-binding protein 1 (XBP1) induces microRNA-346 expression that targets the human antigen peptide transporter 1 (TAP1) mRNA and governs immune regulatory genes. J Biol Chem 286: 41862-41870.
52. McGuirk P, McCann C, Mills KH (2002) 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 Bordetella pertussis. J Exp Med 195: 221-231. (Pubitemid 34461266)
53. McGuirk P, Mills KH (2000) 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 30: 415-422. (Pubitemid 30098833)
54. Coleman MM, Finlay CM, Moran B, Keane J, Dunne PJ, et al. (2012) The immunoregulatory role of CD4(+) FoxP3(+) CD25(-) regulatory T cells in lungs of mice infected with Bordetella pertussis. FEMS Immunol Med Microbiol 64: 413-424.
55. Anderson P, Gonzalez-Rey E (2010) Vasoactive intestinal peptide induces cell cycle arrest and regulatory functions in human T cells at multiple levels. Mol Cell Biol 30: 2537-2551.
56. Hamada H, Garcia-Hernandez Mde L, Reome JB, Misra SK, Strutt TM, et al. (2009) Tc17, a unique subset of CD8 T cells that can protect against lethal influenza challenge. J Immunol 182: 3469-3481.
57. Lamberti YA, Hayes JA, Perez Vidakovics ML, Harvill ET, Rodriguez ME (2010) Intracellular trafficking of Bordetella pertussis in human macrophages. Infect Immun 78: 907-913.