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Review

Pertussis Toxin and Adenylate Cyclase Toxin: Key Virulence Factors of Bordetella Pertussis and Cell Biology Tools

Nicholas H CarbonettiDepartment of Microbiology & Immunology, University of Maryland School of Medicine, Baltimore, MD 21201, USA.Tel.: +1 410 706 7677 Fax: +1 410 706 [email protected]View further author information
Pages 455-469 | Published online: 08 Mar 2010

Bibliography

  • Mattoo S , CherryJD: Molecular pathogenesis, epidemiology, and clinical manifestations of respiratory infections due to Bordetella pertussis and other Bordetella subspecies.Clin. Microbiol. Rev.18 , 326–382 (2005).
  • Wood N , McIntyreP: Pertussis: review of epidemiology, diagnosis, management and prevention.Paediatr. Respir. Rev.9 , 201–211 (2008).
  • Carbonetti NH : Immunomodulation in the pathogenesis of Bordetella pertussis infection and disease.Curr. Opin. Pharmacol.7 , 272–278 (2007).
  • Paddock CD , SandenGN, CherryJD et al.: Pathology and pathogenesis of fatal Bordetella pertussis infection in infants.Clin. Infect. Dis.47 , 328–338 (2008).
  • He Q , MertsolaJ: Factors contributing to pertussis resurgence.Future Microbiol.3 , 329–339 (2008).
  • Mills KH : Immunity to Bordetella pertussis.Microbes Infect.3 , 655–677 (2001).
  • Verma A , BurnsDL: Requirements for assembly of PtlH with the pertussis toxin transporter apparatus of Bordetella pertussis.Infect. Immun.75 , 2297–2306 (2007).
  • Verma A , CheungAM, BurnsDL: Stabilization of the pertussis toxin secretion apparatus by the C terminus of PtlD.J. Bacteriol.190 , 7285–7290 (2008).
  • Witvliet MH , BurnsDL, BrennanMJ, PoolmanJT, ManclarkCR: Binding of pertussis toxin to eucaryotic cells and glycoproteins.Infect. Immun.57 , 3324–3330 (1989).
  • Wong WS , RosoffPM: Pharmacology of pertussis toxin B-oligomer.Can. J. Physiol. Pharmacol.74 , 559–564 (1996).
  • Saukkonen K , BurnetteWN, MarVL, MasureHR, TuomanenEI: Pertussis toxin has eukaryotic-like carbohydrate recognition domains.Proc. Natl Acad. Sci. USA89 , 118–122 (1992).
  • Stein PE , BoodhooA, ArmstrongGD et al.: Structure of a pertussis toxin–sugar complex as a model for receptor binding.Nat. Struct. Biol.1 , 591–596 (1994).
  • Katada T , TamuraM, UiM: The A protomer of islet-activating protein, pertussis toxin, as an active peptide catalyzing ADP-ribosylation of a membrane protein.Arch. Biochem. Biophys.224 , 290–298 (1983).
  • Moss J , StanleySJ, BurnsDL et al.: Activation by thiol of the latent NAD glycohydrolase and ADP-ribosyltransferase activities of Bordetella pertussis toxin (islet-activating protein).J. Biol. Chem.258 , 11879–11882 (1983).
  • Burns DL , ManclarkCR: Adenine nucleotides promote dissociation of pertussis toxin subunits.J. Biol. Chem.261 , 4324–4327 (1986).
  • Hazes B , BoodhooA, CockleSA, ReadRJ: Crystal structure of the pertussis toxin-ATP complex: a molecular sensor.J. Mol. Biol.258 , 661–671 (1996).
  • Stein PE , BoodhooA, ArmstrongGD, CockleSA, KleinMH, ReadRJ: The crystal structure of pertussis toxin.Structure2 , 45–57 (1994).
  • Pierce C , KleinN, PetersM: Is leukocytosis a predictor of mortality in severe pertussis infection?Intensive Care Med.26 , 1512–1514 (2000).
  • Mikelova LK , HalperinSA, ScheifeleD et al.: Predictors of death in infants hospitalized with pertussis: a case–control study of 16 pertussis deaths in Canada.J. Pediatr.143 , 576–581 (2003).
  • Trollfors B , TarangerJ, LagergardT et al.: A placebo-controlled trial of a pertussis-toxoid vaccine.N. Engl. J. Med.333 , 1045–1050 (1995).
  • Plaut RD , CarbonettiNH: Retrograde transport of pertussis toxin in the mammalian cell.Cell. Microbiol.10 , 1130–1139 (2008).
  • Vembar SS , BrodskyJL: One step at a time: endoplasmic reticulum-associated degradation.Nat. Rev. Mol. Cell. Biol.9 , 944–957 (2008).
  • Worthington ZE , CarbonettiNH: Evading the proteasome: absence of lysine residues contributes to pertussis toxin activity by evasion of proteasome degradation.Infect. Immun.75 , 2946–2953 (2007).
  • Pande AH , MoeD, JamnadasM, TatulianSA, TeterK: The pertussis toxin S1 subunit is a thermally unstable protein susceptible to degradation by the 20S proteasome.Biochemistry45 , 13734–13740 (2006).
  • Munoz JJ , AraiH, BergmanRK, SadowskiPL: Biological activities of crystalline pertussigen from Bordetella pertussis.Infect. Immun.33 , 820–826 (1981).
  • Goodwin MS , WeissAA: 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 (1990).
  • Carbonetti NH , ArtamonovaGV, AndreasenC, BusharN: Pertussis toxin and adenylate cyclase toxin provide a one-two punch for establishment of Bordetella pertussis infection of the respiratory tract.Infect. Immun.73 , 2698–2703 (2005).
  • Carbonetti NH , ArtamonovaGV, MaysRM, WorthingtonZE: Pertussis toxin plays an early role in respiratory tract colonization by Bordetella pertussis.Infect. Immun.71 , 6358–6366 (2003).
  • Carbonetti NH , ArtamonovaGV, Van Rooijen N, Ayala VI: Pertussis toxin targets airway macrophages to promote Bordetella pertussis infection of the respiratory tract. Infect. Immun.75 , 1713–1720 (2007).
  • Lattin J , ZidarDA, SchroderK, KellieS, HumeDA, SweetMJ: G-protein-coupled receptor expression, function, and signaling in macrophages.J. Leukoc. Biol.82 , 16–32 (2007).
  • Andreasen C , CarbonettiNH: Pertussis toxin inhibits early chemokine production to delay neutrophil recruitment in response to Bordetella pertussis respiratory tract infection in mice.Infect. Immun.76 , 5139–5148 (2008).
  • Kirimanjeswara GS , AgostoLM, KennettMJ, BjornstadON, HarvillET: Pertussis toxin inhibits neutrophil recruitment to delay antibody-mediated clearance of Bordetella pertussis.J. Clin. Invest.115 , 3594–3601 (2005).
  • Reutershan J , BasitA, GalkinaEV, LeyK: Sequential recruitment of neutrophils into lung and bronchoalveolar lavage fluid in LPS-induced acute lung injury.Am. J. Physiol. Lung Cell. Mol. Physiol.289 , L807–L815 (2005).
  • Pero RS , BorchersMT, SpicherK et al.: Gai2-mediated signaling events in the endothelium are involved in controlling leukocyte extravasation.Proc. Natl Acad. Sci. USA104 , 4371–4376 (2007).
  • Higgins SC , JarnickiAG, LavelleEC, MillsKH: TLR4 mediates vaccine-induced protective cellular immunity to Bordetella pertussis: role of IL-17-producing T cells.J. Immunol.177 , 7980–7989 (2006).
  • Ross PJ , LavelleEC, MillsKH, BoydAP: 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 (2004).
  • Mann PB , WolfeD, LatzE, GolenbockD, PrestonA, HarvillET: Comparative toll-like receptor 4-mediated innate host defense to Bordetella infection.Infect. Immun.73 , 8144–8152 (2005).
  • Banus S , StengerRM, GremmerER et al.: The role of Toll-like receptor-4 in pertussis vaccine-induced immunity.BMC Immunol.9 , 21 (2008).
  • Fedele G , NassoM, SpensieriF et al.: 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 (2008).
  • Lentschat A , KarahashiH, MichelsenKS et al.: Mastoparan, a G protein agonist peptide, differentially modulates TLR4- and TLR2-mediated signaling in human endothelial cells and murine macrophages.J. Immunol.174 , 4252–4261 (2005).
  • Fan H , PeckOM, TempelGE, HalushkaPV, CookJA: Toll-like receptor 4 coupled GI protein signaling pathways regulate extracellular signal-regulated kinase phosphorylation and AP-1 activation independent of NFκB activation.Shock22 , 57–62 (2004).
  • Andreasen C , CarbonettiNH: Role of neutrophils in response to Bordetella pertussis infection in mice.Infect. Immun.77 , 1182–1188 (2009).
  • Andreasen C , PowellD, CarbonettiNH: Pertussis toxin stimulates IL-17 production in response to Bordetella pertussis infection in mice.PLoS ONE4 , E7079 (2009).
  • Wolfe DN , MannPB, BuboltzAM, HarvillET: Delayed role of tumor necrosis factor- a in overcoming the effects of pertussis toxin.J. Infect. Dis.196 , 1228–1236 (2007).
  • Carbonetti NH , ArtamonovaGV, AndreasenC, DudleyE, MaysRM, WorthingtonZE: Suppression of serum antibody responses by pertussis toxin after respiratory tract colonization by Bordetella pertussis and identification of an immunodominant lipoprotein.Infect. Immun.72 , 3350–3358 (2004).
  • Shumilla JA , LacailleV, HornellTM et al.: Bordetella pertussis infection of primary human monocytes alters HLA-DR expression.Infect. Immun.72 , 1450–1462 (2004).
  • Martino A , VolpeE, AuricchioG, ColizziV, BaldiniPM: Influence of pertussis toxin on CD1a isoform expression in human dendritic cells.J. Clin. Immunol.26 , 153–159 (2006).
  • Bouchez V , BrunD, CantinelliT, DoreG, NjamkepoE, GuisoN: First report and detailed characterization of B. pertussis isolates not expressing pertussis toxin or pertactin.Vaccine27(43) , 6034–6041 (2009).
  • Mooi FR , van Loo IHM, van Gent M et al.: Bordetella pertussis strains with increased toxin production associated with pertussis resurgence. Emerg. Infect. Dis.15 , 1206–1213 (2009).
  • Robbins JB , SchneersonR, KeithJM, MillerMA, Kubler-KielbJ, TrollforsB: Pertussis vaccine: a critique.Pediatr. Infect. Dis. J.28 , 237–241 (2009).
  • Pizza M , CovacciA, BartoloniA et al.: Mutants of pertussis toxin suitable for vaccine development.Science246 , 497–500 (1989).
  • Alfano M , SchmidtmayerovaH, AmellaCA, PushkarskyT, BukrinskyM: The B-oligomer of pertussis toxin deactivates CC chemokine receptor 5 and blocks entry of M-tropic HIV-1 strains.J. Exp. Med.190 , 597–605 (1999).
  • Rizzi C , AlfanoM, BugattiA, CamozziM, PoliG, RusnatiM: Inhibition of intra- and extra-cellular Tat function and HIV expression by pertussis toxin B-oligomer.Eur. J. Immunol.34 , 530–536 (2004).
  • Zocchi MR , ContiniP, AlfanoM, PoggiA: Pertussis toxin (PTX) B subunit and the nontoxic PTX mutant PT9K/129G inhibit Tat-induced TGF-β production by NK cells and TGF-β-mediated NK cell apoptosis.J. Immunol.174 , 6054–6061 (2005).
  • Poggi A , ZocchiMR: HIV-1 Tat triggers TGF-β production and NK cell apoptosis that is prevented by pertussis toxin B.Clin. Dev. Immunol.13 , 369–372 (2006).
  • Jajoo S , MukherjeaD, BrewerGJ, RamkumarV: Pertussis toxin B-oligomer suppresses human immunodeficiency virus-1 Tat-induced neuronal apoptosis through feedback inhibition of phospholipase C-β by protein kinase C.Neuroscience151 , 525–532 (2008).
  • Rizzi C , CrippaMP, JeeningaRE et al.: Pertussis toxin B-oligomer suppresses IL-6 induced HIV-1 and chemokine expression in chronically infected U1 cells via inhibition of activator protein 1.J. Immunol.176 , 999–1006 (2006).
  • Hu Q , YounsonJ, GriffinGE, KellyC, ShattockRJ: Pertussis toxin and its binding unit inhibit HIV-1 infection of human cervical tissue and macrophages involving a CD14 pathway.J. Infect. Dis.194 , 1547–1556 (2006).
  • Lapenta C , SpadaM, SantiniSM et al.: Pertussis toxin B-oligomer inhibits HIV infection and replication in hu-PBL-SCID mice.Int. Immunol.17 , 469–475 (2005).
  • Alfano M , GrivelJC, GhezziS et al.: Pertussis toxin B-oligomer dissociates T cell activation and HIV replication in CD4 T cells released from infected lymphoid tissue.AIDS19 , 1007–1014 (2005).
  • Ryan M , McCarthyL, RappuoliR, MahonBP, MillsKH: 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 , 651–662 (1998).
  • Wang ZY , YangD, ChenQ et al.: Induction of dendritic cell maturation by pertussis toxin and its B subunit differentially initiate Toll-like receptor 4-dependent signal transduction pathways.Exp. Hematol.34 , 1115–1124 (2006).
  • Nasso M , FedeleG, SpensieriF et al.: Genetically detoxified pertussis toxin induces Th1/Th17 immune response through MAPKs and IL-10-dependent mechanisms.J. Immunol.183 , 1892–1899 (2009).
  • Schneider OD , WeissAA, MillerWE: Pertussis toxin utilizes proximal components of the T-cell receptor complex to initiate signal transduction events in T cells.Infect. Immun.75 , 4040–4049 (2007).
  • Schneider OD , WeissAA, MillerWE: Pertussis toxin signals through the TCR to initiate cross-desensitization of the chemokine receptor CXCR4.J. Immunol.182 , 5730–5739 (2009).
  • Munoz JJ , BernardCC, MackayIR: Elicitation of experimental allergic encephalomyelitis (EAE) in mice with the aid of pertussigen.Cell. Immunol.83 , 92–100 (1984).
  • Kugler S , BockerK, HeusippG, GreuneL, KimKS, SchmidtMA: Pertussis toxin transiently affects barrier integrity, organelle organization and transmigration of monocytes in a human brain microvascular endothelial cell barrier model.Cell. Microbiol.9 , 619–632 (2007).
  • Kerfoot SM , LongEM, HickeyMJ et al.: TLR4 contributes to disease-inducing mechanisms resulting in central nervous system autoimmune disease.J. Immunol.173 , 7070–7077 (2004).
  • Chen X , Winkler-PickettRT, CarbonettiNH et al.: Pertussis toxin as an adjuvant suppresses the number and function of CD4+CD25+ T regulatory cells.Eur. J. Immunol.36 , 671–680 (2006).
  • Cassan C , PiaggioE, ZappullaJP et al.: Pertussis toxin reduces the number of splenic Foxp3+ regulatory T cells.J. Immunol.177 , 1552–1560 (2006).
  • Amend B , DosterH, LangeC et al.: Induction of autoimmunity by expansion of autoreactive CD4+CD62Low cells in vivo.J. Immunol.177 , 4384–4390 (2006).
  • Chen X , HowardOM, OppenheimJJ: Pertussis toxin by inducing IL-6 promotes the generation of IL-17-producing CD4 cells.J. Immunol.178 , 6123–6129 (2007).
  • Komiyama Y , NakaeS, MatsukiT et al.: IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis.J. Immunol.177 , 566–573 (2006).
  • Millward JM , CarusoM, CampbellIL, GauldieJ, OwensT: IFN-γ-induced chemokines synergize with pertussis toxin to promote T cell entry to the central nervous system.J. Immunol.178 , 8175–8182 (2007).
  • Fujimoto C , ShiG, GeryI: Microbial products trigger autoimmune ocular inflammation.Ophthalmic Res.40 , 193–199 (2008).
  • Fujimoto C , YuCR, ShiG et al.: Pertussis toxin is superior to TLR ligands in enhancing pathogenic autoimmunity, targeted at a neo-self antigen, by triggering robust expansion of Th1 cells and their cytokine production.J. Immunol.177 , 6896–6903 (2006).
  • Vojtova J , KamanovaJ, SeboP: Bordetella adenylate cyclase toxin: a swift saboteur of host defense.Curr. Opin. Microbiol.9 , 69–75 (2006).
  • Gray MC , DonatoGM, JonesFR, KimT, HewlettEL: Newly secreted adenylate cyclase toxin is responsible for intoxication of target cells by Bordetella pertussis.Mol. Microbiol.53 , 1709–1719 (2004).
  • Guermonprez P , KhelefN, BlouinE et al.: The adenylate cyclase toxin of Bordetella pertussis binds to target cells via the a(M)b(2) integrin (CD11b/CD18).J. Exp. Med.193 , 1035–1044 (2001).
  • Morova J , OsickaR, MasinJ, SeboP: RTX cytotoxins recognize b2 integrin receptors through N -linked oligosaccharides.Proc. Natl Acad. Sci. USA105 , 5355–5360 (2008).
  • Guo Q , ShenY, LeeYS, GibbsCS, MrksichM, TangWJ: Structural basis for the interaction of Bordetella pertussis adenylyl cyclase toxin with calmodulin.EMBO J.24 , 3190–3201 (2005).
  • Guo Q , JurellerJE, WarrenJT, SolomahaE, FlorianJ, TangWJ: Protein–protein docking and analysis reveal that two homologous bacterial adenylyl cyclase toxins interact with calmodulin differently.J. Biol. Chem.283 , 23836–23845 (2008).
  • El-Azami-El-Idrissi M , BaucheC, LouckaJ et al.: Interaction of Bordetella pertussis adenylate cyclase with CD11b/CD18: role of toxin acylation and identification of the main integrin interaction domain.J. Biol. Chem.278 , 38514–38521 (2003).
  • Masin J , BaslerM, KnappO et al.: Acylation of lysine 860 allows tight binding and cytotoxicity of Bordetella adenylate cyclase on CD11b-expressing cells.Biochemistry44 , 12759–12766 (2005).
  • Lee SJ , GrayMC, ZuK, HewlettEL: Oligomeric behavior of Bordetella pertussis adenylate cyclase toxin in solution.Arch. Biochem. Biophys.438 , 80–87 (2005).
  • Vojtova-Vodolanova J , BaslerM, OsickaR et al.: Oligomerization is involved in pore formation by Bordetella adenylate cyclase toxin.Faseb. J.23 , 2831–2843 (2009).
  • Basler M , KnappO, MasinJ et al.: Segments crucial for membrane translocation and pore-forming activity of Bordetella adenylate cyclase toxin.J. Biol. Chem.282 , 12419–12429 (2007).
  • Powthongchin B , AngsuthanasombatC: Effects on haemolytic activity of single proline substitutions in the Bordetella pertussis CyaA pore-forming fragment.Arch. Microbiol.191 , 1–9 (2009).
  • Knapp O , MaierE, MasinJ, SeboP, BenzR: Pore formation by the Bordetella adenylate cyclase toxin in lipid bilayer membranes: role of voltage and pH.Biochim. Biophys. Acta1778 , 260–269 (2008).
  • Lilie H , HaehnelW, RudolphR, BaumannU: Folding of a synthetic parallel β-roll protein.FEBS Lett.470 , 173–177 (2000).
  • Bauche C , ChenalA, KnappO et al.: Structural and functional characterization of an essential RTX subdomain of Bordetella pertussis adenylate cyclase toxin.J. Biol. Chem.281 , 16914–16926 (2006).
  • Chenal A , GuijarroJI, RaynalB, DelepierreM, LadantD: RTX calcium binding motifs are intrinsically disordered in the absence of calcium: implication for protein secretion.J. Biol. Chem.284 , 1781–1789 (2009).
  • Hewlett EL , DonatoGM, GrayMC: Macrophage cytotoxicity produced by adenylate cyclase toxin from Bordetella pertussis: more than just making cyclic AMP!Mol. Microbiol.59 , 447–459 (2006).
  • Basler M , MasinJ, OsickaR, SeboP: Pore-forming and enzymatic activities of Bordetella pertussis adenylate cyclase toxin synergize in promoting lysis of monocytes.Infect. Immun.74 , 2207–2214 (2006).
  • Fiser R , MasinJ, BaslerM et al.: 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 (2007).
  • Vojtova J , KofronovaO, SeboP, BenadaO: Bordetella adenylate cyclase toxin induces a cascade of morphological changes of sheep erythrocytes and localizes into clusters in erythrocyte membranes.Microsc. Res. Tech.69 , 119–129 (2006).
  • Ohnishi H , MiyakeM, KamitaniS, HoriguchiY: The morphological changes in cultured cells caused by Bordetella pertussis adenylate cyclase toxin.FEMS Microbiol. Lett.279 , 174–179 (2008).
  • Kamanova J , KofronovaO, MasinJ et al.: Adenylate cyclase toxin subverts phagocyte function by RhoA inhibition and unproductive ruffling.J. Immunol.181 , 5587–5597 (2008).
  • Johansson D , BergstromP, HenrikssonR et al.: Adenylate cyclase toxin from Bordetella pertussis enhances cisplatin-induced apoptosis to lung cancer cells in vitro.Oncol. Res.15 , 423–430 (2006).
  • Cheung GY , KellySM, JessTJ et al.: Functional and structural studies on different forms of the adenylate cyclase toxin of Bordetella pertussis.Microb. Pathog.46 , 36–42 (2009).
  • Confer D , EatonJ: Phagocyte impotence caused by an invasive bacterial adenylate cyclase.Science217 , 948–950 (1982).
  • Gross MK , AuDC, SmithAL, StormDR: 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. USA89 , 4898–4902 (1992).
  • Khelef N , SakamotoH, GuisoN: Both adenylate cyclase and hemolytic activities are required by Bordetella pertussis to initiate infection.Microb. Pathog.12 , 227–235 (1992).
  • Gueirard P , DruilheA, PretolaniM, GuisoN: Role of adenylate cyclase-hemolysin in alveolar macrophage apoptosis during Bordetella pertussis infection in vivo.Infect. Immun.66 , 1718–1725 (1998).
  • Khelef N , GuisoN: Induction of macrophage apoptosis by Bordetella pertussis adenylate cyclase-hemolysin.FEMS Microbiol. Lett.134 , 27–32 (1995).
  • Khelef N , ZychlinskyA, GuisoN: Bordetella pertussis induces apoptosis in macrophages: role of adenylate cyclase-hemolysin.Infect. Immun.61 , 4064–4071 (1993).
  • Mobberley-Schuman PS , WeissAA: Influence of CR3 (CD11b/CD18) expression on phagocytosis of Bordetella pertussis by human neutrophils.Infect. Immun.73 , 7317–7323 (2005).
  • Veal-Carr WL , StibitzS: Demonstration of differential virulence gene promoter activation in vivo in Bordetella pertussis using RIVET.Mol. Microbiol.55 , 788–798 (2005).
  • Boyd AP , RossPJ, ConroyH, MahonN, LavelleEC, MillsKH: 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 (2005).
  • Skinner JA , ReissingerA, ShenH, YukMH: Bordetella type III secretion and adenylate cyclase toxin synergize to drive dendritic cells into a semimature state.J. Immunol.173 , 1934–1940 (2004).
  • Spensieri F , FedeleG, FazioC et al.: 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 (2006).
  • Hickey FB , BreretonCF, MillsKH: 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 (2008).
  • Paccani SR , Dal Molin F, Benagiano M et al.: Suppression of T-lymphocyte activation and chemotaxis by the adenylate cyclase toxin of Bordetella pertussis.Infect. Immun.76 , 2822–2832 (2008).
  • Rossi Paccani S , BenagianoM, CapitaniN et al.: 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 (2009).
  • Perkins DJ , GrayMC, HewlettEL, VogelSN: Bordetella pertussis adenylate cyclase toxin (ACT) induces cyclooxygenase-2 (COX-2) in murine macrophages and is facilitated by ACT interaction with CD11b/CD18 (Mac-1).Mol. Microbiol.66 , 1003–1015 (2007).
  • Cheung GY , DickinsonP, SingG et al.: Transcriptional responses of murine macrophages to the adenylate cyclase toxin of Bordetella pertussis.Microb. Pathog.44 , 61–70 (2008).
  • Schlecht G , LouckaJ, NajarH, SeboP, LeclercC: Antigen targeting to CD11b allows efficient presentation of CD4+ and CD8+ T cell epitopes and in vivo Th1-polarized T cell priming.J. Immunol.173 , 6089–6097 (2004).
  • Simsova M , SeboP, LeclercC: The adenylate cyclase toxin from Bordetella pertussis – a novel promising vehicle for antigen delivery to dendritic cells.Int. J. Med. Microbiol.293 , 571–576 (2004).
  • Fayolle C , BaucheC, LadantD, LeclercC: Bordetella pertussis adenylate cyclase delivers chemically coupled CD8+ T-cell epitopes to dendritic cells and elicits CTL in vivo.Vaccine23 , 604–614 (2004).
  • Mascarell L , BaucheC, FayolleC et al.: Delivery of the HIV-1 Tat protein to dendritic cells by the CyaA vector induces specific Th1 responses and high affinity neutralizing antibodies in non human primates.Vaccine24 , 3490–3499 (2006).
  • Mascarell L , FayolleC, BaucheC, LadantD, LeclercC: Induction of neutralizing antibodies and Th1-polarized and CD4-independent CD8+ T-cell responses following delivery of human immunodeficiency virus type 1 Tat protein by recombinant adenylate cyclase of Bordetella pertussis.J. Virol.79 , 9872–9884 (2005).
  • Tartz S , RussmannH, KamanovaJ et al.: Complete protection against P. berghei malaria upon heterologous prime/boost immunization against circumsporozoite protein employing Salmonella type III secretion system and Bordetella adenylate cyclase toxoid.Vaccine26 , 5935–5943 (2008).
  • Connell TG , SheyMS, SeldonR et al.: Enhanced ex vivo stimulation of Mycobacterium tuberculosis -specific T cells in human immunodeficiency virus-infected persons via antigen delivery by the Bordetella pertussis adenylate cyclase vector.Clin. Vaccine Immunol.14 , 847–854 (2007).
  • Wilkinson KA , SimsovaM, ScholvinckE et al.: Efficient ex vivo stimulation of Mycobacterium tuberculosis -specific T cells by genetically detoxified Bordetella pertussis adenylate cyclase antigen toxoids.Infect. Immun.73 , 2991–2998 (2005).
  • Dautin N , KarimovaG, LadantD: Bordetella pertussis adenylate cyclase toxin: a versatile screening tool.Toxicon40 , 1383–1387 (2002).
  • Geddes K , WorleyM, NiemannG, HeffronF: Identification of new secreted effectors in Salmonella enterica serovar Typhimurium.Infect. Immun.73 , 6260–6271 (2005).
  • Gendlina I , HeldKG, BartraSS et al.: Identification and type III-dependent secretion of the Yersinia pestis insecticidal-like proteins.Mol. Microbiol.64 , 1214–1227 (2007).
  • Furutani A , TakaokaM, SanadaH et al.: Identification of novel type III secretion effectors in Xanthomonas oryzae pv. oryzae.Mol. Plant Microbe Interact.22 , 96–106 (2009).
  • Miyake M , SakaneS, KobayashiC et al.: A colorimetric assay for studying effector secretion through the bacterial type III secretion system.FEMS Microbiol. Lett.278 , 36–42 (2008).
  • Karimova G , RobichonC, LadantD: Characterization of YmgF, a 72-residue inner membrane protein that associates with the Escherichia coli cell division machinery.J. Bacteriol.191 , 333–346 (2009).
  • Real SM , MarzeseDM, GomezLC, MayorgaLS, RoqueM: Development of a premature stop codon-detection method based on a bacterial two-hybrid system.BMC Biotechnol.6 , 38 (2006).
  • Guiso N , SzatanikM, RocancourtM: Protective activity of Bordetella adenylate cyclase-hemolysin against bacterial colonization.Microb. Pathog.11 , 423–431 (1991).
  • Weingart CL , Mobberley-SchumanPS, HewlettEL, GrayMC, WeissAA: Neutralizing antibodies to adenylate cyclase toxin promote phagocytosis of Bordetella pertussis by human neutrophils.Infect. Immun.68 , 7152–7155 (2000).
  • Cheung GY , XingD, PriorS, CorbelMJ, PartonR, CooteJG: 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 (2006).
  • Prior S , FleckRA, GillettML et al.: Evaluation of adenyl cyclase toxin constructs from Bordetella pertussis as candidate vaccine components in an in vitro model of complement-dependent intraphagocytic killing.Vaccine24 , 4794–4803 (2006).

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