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Genetically detoxified pertussis toxin (PT-9K/129G): implications for immunization and vaccines

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References

  • Tamura M, Nogimori K, Murai S, et al. Subunit structure of islet-activating protein, pertussis toxin, in conformity with the A-B model. Biochemistry 1982;21(22):5516-22
  • Nicosia A, Perugini M, Franzini C, et al. Cloning and sequencing of the pertussis toxin genes: operon structure and gene duplication. Proc Natl Acad Sci USA 1986;83(13):4631-5
  • Locht C, Keith JM. Pertussis toxin gene: nucleotide sequence and genetic organization. Science 1986;232(4755):1258-64
  • Locht C, Coutte L, Mielcarek N. The ins and outs of pertussis toxin. FEBS J 2011;278(23):4668-82
  • Arico B, Miller JF, Roy C, et al. Sequences required for expression of Bordetella pertussis virulence factors share homology with prokaryotic signal transduction proteins. Proc Natl Acad Sci USA 1989;86(17):6671-5
  • Weiss AA, Johnson FD, Burns DL. Molecular characterization of an operon required for pertussis toxin secretion. Proc Natl Acad Sci USA 1993;90(7):2970-4
  • Covacci A, Rappuoli R. Pertussis toxin export requires accessory genes located downstream from the pertussis toxin operon. Mol Microbiol 1993;8(3):429-34
  • Stein PE, Boodhoo A, Armstrong GD, et al. The crystal structure of pertussis toxin. Structure 1994;2(1):45-57
  • Katada T, Tamura M, Ui M. The A protomer of islet-activating protein, pertussis toxin, as an active peptide catalyzing ADP-ribosylation of a membrane protein. Arch Biochem Biophys 1983;224(1):290-8
  • Hewlett EL, Sauer KT, Myers GA, et al. Induction of a novel morphological response in Chinese hamster ovary cells by pertussis toxin. Infect Immun 1983;40(3):1198-203
  • el Baya A, Linnemann R, von Olleschik-Elbheim L, et al. Endocytosis and retrograde transport of pertussis toxin to the Golgi complex as a prerequisite for cellular intoxication. Eur J Cell Biol 1997;73(1):40-8
  • Xu Y, Barbieri JT. Pertussis toxin-mediated ADP-ribosylation of target proteins in Chinese hamster ovary cells involves a vesicle trafficking mechanism. Infect Immun 1995;63(3):825-32
  • Hazes B, Boodhoo A, Cockle SA, et al. Crystal structure of the pertussis toxin-ATP complex: a molecular sensor. J Mol Biol 1996;258(4):661-71
  • Barbieri JT, Rappuoli R, Collier RJ. Expression of the S-1 catalytic subunit of pertussis toxin in Escherichia coli. Infect Immun 1987;55(5):1321-3
  • Nicosia A, Bartoloni A, Perugini M, et al. Expression and immunological properties of the five subunits of pertussis toxin. Infect Immun 1987;55(4):963-7
  • Burnette WN, Mar VL, Cieplak W, et al. Direct expression of Bordetella pertussis toxin subunits to high levels in Escherichia coli. Nat Biotechnol 1988;6:699-706
  • Pizza M, Bartoloni A, Prugnola A, et al. Subunit S1 of pertussis toxin: mapping of the regions essential for ADP-ribosyltransferase activity. Proc Natl Acad Sci USA 1988;85(20):7521-5
  • Burnette WN, Cieplak W, Mar VL, et al. Pertussis toxin S1 mutant with reduced enzyme activity and a conserved protective epitope. Science 1988;242(4875):72-4
  • Barbieri JT, Cortina G. ADP-ribosyltransferase mutations in the catalytic S-1 subunit of pertussis toxin. Infect Immun 1988;56(8):1934-41
  • Bartoloni A, Pizza M, Bigio M, et al. Mapping of protective epitopes of pertussis toxin by in vitro refolding of recombinant fragments. Nat Biotechnol 1988;6:709-12
  • Domenighini M, Montecucco C, Ripka WC, et al. Computer modelling of the NAD binding site of ADP-ribosylating toxins: active-site structure and mechanism of NAD binding. Mol Microbiol 1991;5(1):23-31
  • Antoine R, Tallett A, van Heyningen S, et al. Evidence for a catalytic role of glutamic acid 129 in the NAD-glycohydrolase activity of the pertussis toxin S1 subunit. J Biol Chem 1993;268(32):24149-55
  • Pizza M, Covacci A, Bartoloni A, et al. Mutants of pertussis toxin suitable for vaccine development. Science 1989;246(4929):497-500
  • Metz B, Kersten GF, Hoogerhout P, et al. Identification of formaldehyde-induced modifications in proteins: reactions with model peptides. J Biol Chem 2004;279(8):6235-43
  • Oh H, Kim BG, Nam KT, et al. Characterization of the carbohydrate binding and ADP-ribosyltransferase activities of chemically detoxified pertussis toxins. Vaccine 2013;31(29):2988-93
  • Ibsen PH. The effect of formaldehyde, hydrogen peroxide and genetic detoxification of pertussis toxin on epitope recognition by murine monoclonal antibodies. Vaccine 1996;14(5):359-68
  • Sato H, Sato Y, Ohishi I. Comparison of pertussis toxin (PT)-neutralizing activities and mouse-protective activities of anti-PT mouse monoclonal antibodies. Infect Immun 1991;59(10):3832-5
  • Sutherland JN, Maynard JA. Characterization of a key neutralizing epitope on pertussis toxin recognized by monoclonal antibody 1B7. Biochemistry 2009;48(50):11982-93
  • Nencioni L, Volpini G, Peppoloni S, et al. Properties of pertussis toxin mutant PT-9K/129G after formaldehyde treatment. Infect Immun 1991;59(2):625-30
  • Fowler S, Xing DK, Bolgiano B, Yuen CT, Corbel MJ. Modifications of thecatalytic and binding subunits of pertussis toxin by formaldehyde: effects on toxicity and immunogenicity (2003). Vaccine. 21:2329-37
  • Li H, Wong WS. Mechanisms of pertussis toxin-induced myelomonocytic cell adhesion: role of CD14 and urokinase receptor. Immunology 2000;100(4):502-9
  • Schneider OD, Weiss AA, Miller WE. Pertussis toxin signals through the TCR to initiate cross-desensitization of the chemokine receptor CXCR4. J Immunol 2009;182(9):5730-9
  • Lobet Y, Feron C, Dequesne G, et al. Site-specific alterations in the B oligomer that affect receptor-binding activities and mitogenicity of pertussis toxin. J Exp Med 1993;177(1):79-87
  • Loosmore SM, Yacoob RK, Zealey GR, et al. Hybrid genes over-express pertactin from Bordetella pertussis. Vaccine 1995;13(6):571-80
  • Gray LS, Huber KS, Gray MC, et al. Pertussis toxin effects on T lymphocytes are mediated through CD3 and not by pertussis toxin catalyzed modification of a G protein. J Immunol 1989;142(5):1631-8
  • Tamura M, Nogimori K, Yajima M, et al. A role of the B-oligomer moiety of islet-activating protein, pertussis toxin, in development of the biological effects on intact cells. J Biol Chem 1983;258(11):6756-61
  • Nencioni L, Pizza MG, Volpini G, et al. Properties of the B oligomer of pertussis toxin. Infect Immun 1991;59(12):4732-4
  • Wong WS, Rosoff PM. Pharmacology of pertussis toxin B-oligomer. Can J Physiol Pharmacol 1996;74(5):559-64
  • Armstrong GD, Howard LA, Peppler MS. Use of glycosyltransferases to restore pertussis toxin receptor activity to asialoagalactofetuin. J Biol Chem 1988;263(18):8677-84
  • Hausman SZ, Burns DL. Binding of pertussis toxin to lipid vesicles containing glycolipids. Infect Immun 1993;61(1):335-7
  • Witvliet MH, Burns DL, Brennan MJ, et al. Binding of pertussis toxin to eucaryotic cells and glycoproteins. Infect Immun 1989;57(11):3324-30
  • Denkinger CM, Denkinger MD, Forsthuber TG. Pertussis toxin-induced cytokine differentiation and clonal expansion of T cells is mediated predominantly via costimulation. Cell Immunol 2007;246(1):46-54
  • Ryan M, McCarthy L, Rappuoli R, et al. 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 1998;10(5):651-62
  • Hofstetter HH, Shive CL, Forsthuber TG. Pertussis toxin modulates the immune response to neuroantigens injected in incomplete Freund’s adjuvant: induction of Th1 cells and experimental autoimmune encephalomyelitis in the presence of high frequencies of Th2 cells. J Immunol 2002;169(1):117-25
  • Mu HH, Sewell WA. Regulation of DTH and IgE responses by IL-4 and IFN-gamma in immunized mice given pertussis toxin. Immunology 1994;83(4):639-45
  • Chen X, Howard OM, Oppenheim JJ. Pertussis toxin by inducing IL-6 promotes the generation of IL-17-producing CD4 cells. J Immunol 2007;178(10):6123-9
  • Ryan MS, Griffin F, Mahon B, et al. The role of the S-1 and B-oligomer components of pertussis toxin in its adjuvant properties for Th1 and Th2 cells. Biochem Soc Trans 1997;25(1):126S
  • Nencioni L, Pizza M, Bugnoli M, et al. Characterization of genetically inactivated pertussis toxin mutants: candidates for a new vaccine against whooping cough. Infect Immun 1990;58(5):1308-15
  • Roberts M, Bacon A, Rappuoli R, et al. 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(6):2100-8
  • Ausiello CM, Fedele G, Urbani F, et al. 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 2002;186(3):351-60
  • Nasso M, Fedele G, Spensieri F, et al. Genetically detoxified pertussis toxin induces Th1/Th17 immune response through MAPKs and IL-10-dependent mechanisms. J Immunol 2009;183(3):1892-9
  • Cropley I, Douce G, Roberts M, et al. Mucosal and systemic immunogenicity of a recombinant, non-ADP-ribosylating pertussis toxin: effects of formaldehyde treatment. Vaccine 1995;13(17):1643-8
  • Wakatsuki A, Borrow P, Rigley K, et al. Cell-surface bound pertussis toxin induces polyclonal T cell responses with high levels of interferon-gamma in the absence of interleukin-12. Eur J Immunol 2003;33(7):1859-68
  • Wang ZY, Yang D, Chen Q, 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 2006;34(8):1115-24
  • Mills KH, Ryan M, Ryan E, et al. 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 1998;66(2):594-602
  • Ross PJ, Sutton CE, Higgins S, et al. Relative contribution of Th1 and Th17 cells in adaptive immunity to Bordetella pertussis: towards the rational design of an improved acellular pertussis vaccine. PLoS Pathog 2013;9(4):e1003264
  • Mahon BP, Ryan MS, Griffin F, et al. Interleukin-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 1996;64(12):5295-301
  • Higgs R, Higgins SC, Ross PJ, et al. Immunity to the respiratory pathogen Bordetella pertussis. Mucosal Immunol 2012;5(5):485-500
  • Mahon BP, Brady MT, Mills KH. Protection against Bordetella pertussis in mice in the absence of detectable circulating antibody: implications for long-term immunity in children. J Infect Dis 2000;181(6):2087-91
  • Higgins SC, Jarnicki AG, Lavelle EC, Mills KH. TLR4 mediates vaccine-induced protective cellular immunity to Bordetella pertussis: role of IL-17-producing T cells. J Immunol 2006;177(11):7980-9
  • Warfel JM, Zimmerman LI, Merkel TJ. Acellular pertussis vaccines protect against disease but fail to prevent infection and transmission in a nonhuman primate model. Proc Natl Acad Sci USA 2014;111(2):787-92
  • Warfel JM, Beren J, Kelly VK, et al. Nonhuman primate model of pertussis. Infect Immun 2012;80(4):1530-6
  • Warfel JM, Beren J, Merkel TJ. Airborne transmission of Bordetella pertussis. J Infect Dis 2012;206(6):902-6
  • Warfel JM, Merkel TJ. Bordetella pertussis infection induces a mucosal IL-17 response and long-lived Th17 and Th1 immune memory cells in nonhuman primates. Mucosal Immunol 2013;6(4):787-96
  • Jabbal-Gill I, Fisher AN, Rappuoli R, et al. Stimulation of mucosal and systemic antibody responses against Bordetella pertussis filamentous haemagglutinin and recombinant pertussis toxin after nasal administration with chitosan in mice. Vaccine 1998;16(20):2039-46
  • Ryan EJ, McNeela E, Murphy GA, et al. 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 1999;67(12):6270-80
  • Petre J, Pizza M, Nencioni L, et al. The reaction of bacterial toxins with formaldehyde and its use for antigen stabilization. Dev Biol Stand 1996;87:125-34
  • Podda A, Nencioni L, De Magistris MT, et al. Metabolic, humoral, and cellular responses in adult volunteers immunized with the genetically inactivated pertussis toxin mutant PT-9K/129G. J Exp Med 1990;172(3):861-8
  • Podda A, Nencioni L, Marsili I, et al. Phase I clinical trial of an acellular pertussis vaccine composed of genetically detoxified pertussis toxin combined with FHA and 69 kDa. Vaccine 1991;9(10):741-5
  • Di Tommaso A, Bartalini M, Peppoloni S, et al. Acellular pertussis vaccines containing genetically detoxified pertussis toxin induce long-lasting humoral and cellular responses in adults. Vaccine 1997;15(11):1218-24
  • Podda A, De Luca EC, Titone L, et al. Acellular pertussis vaccine composed of genetically inactivated pertussis toxin: safety and immunogenicity in 12- to 24- and 2- to 4-month-old children. J Pediatr 1992;120(5):680-5
  • Podda A, Carapella De Luca E, Titone L, et al. Immunogenicity of an acellular pertussis vaccine composed of genetically inactivated pertussis toxin combined with filamentous hemagglutinin and pertactin in infants and children. J Pediatr 1993;123(1):81-4
  • Podda A, De Luca EC, Contu B, et al. Comparative study of a whole-cell pertussis vaccine and a recombinant acellular pertussis vaccine. The Italian multicenter group for the study of recombinant acellular pertussis vaccine. J Pediatr 1994;124(6):921-6
  • Edwards KM, Meade BD, Decker MD, et al. Comparison of 13 acellular pertussis vaccines: overview and serologic response. Pediatrics 1995;96(3 Pt 2):548-57
  • Greco D, Salmaso S, Mastrantonio P, et al. A controlled trial of two acellular vaccines and one whole-cell vaccine against pertussis. Progetto Pertosse Working Group. N Engl J Med 1996;334(6):341-8
  • Salmaso S, Mastrantonio P, Wassilak SG, et al. Persistence of protection through 33 months of age provided by immunization in infancy with two three-component acellular pertussis vaccines. Stage II Working Group. Vaccine 1998;16(13):1270-5
  • Salmaso S, Mastrantonio P, Tozzi AE, et al. Sustained efficacy during the first 6 years of life of 3-component acellular pertussis vaccines administered in infancy: the Italian experience. Pediatrics 2001;108(5):E81
  • Cassone A, Ausiello CM, Urbani F, et al. Cell-mediated and antibody responses to Bordetella pertussis antigens in children vaccinated with acellular or whole-cell pertussis vaccines. The Progetto Pertosse-CMI Working Group. Arch Pediatr Adolesc Med 1997;151(3):283-9
  • Rosenblum E, McBane S, Wang W, Sawyer M. Protecting newborns by immunizing family members in a hospital-based vaccine clinic: a successful Tdap cocooning program during the 2010 California pertussis epidemic. Public Health Rep 2014;129(3):245-51
  • Munoz FM, Bond NH, Maccato M, et al. Safety and immunogenicity of tetanus diphtheria and acellular pertussis (Tdap) immunization during pregnancy in mothers and infants: a randomized clinical trial. JAMA 2014;311(17):1760-9
  • Robbins JB, Schneerson R, Trollfors B, et al. The diphtheria and pertussis components of diphtheria-tetanus toxoids-pertussis vaccine should be genetically inactivated mutant toxins. J Infect Dis 2005;191(1):81-8
  • Thorstensson R, Trollfors B, Al-Tawil N, et al. A phase I clinical study of a live attenuated Bordetella pertussis vaccine – BPZE1; a single centre, double-blind, placebo-controlled, dose-escalating study of BPZE1 given intranasally to healthy adult male volunteers. PLoS One 2014;9(1):e83449
  • Marsili I, Pizza M, Giovannoni F, et al. Cellular pertussis vaccine containing a Bordetella pertussis strain that produces a nontoxic pertussis toxin molecule. Infect Immun 1992;60(3):1150-5
  • Roberts R, Moreno G, Bottero D, et al. Outer membrane vesicles as acellular vaccine against pertussis. Vaccine 2008;26(36):4639-46
  • Fry SR, Chen AY, Daggard G, Mukkur TK. Parenteral immunization of mice with a genetically inactivated pertussis toxin DNA vaccine induces cell-mediated immunity and protection. J Med Microbiol 2008;57(Pt 1):28-35
  • Kamachi K, Arakawa Y. Development of safer pertussis DNA vaccine expressing non-toxic C180 polypeptide of pertussis toxin S1 subunit. Vaccine 2007;25(6):1000-6
  • Nascimento IP, Dias WO, Mazzantini RP, et al. Recombinant Mycobacterium bovis BCG expressing pertussis toxin subunit S1 induces protection against an intracerebral challenge with live Bordetella pertussis in mice. Infect Immun 2000;68(9):4877-83
  • Rappuoli R. The vaccine containing recombinant pertussis toxin induces early and long-lasting protection. Biologicals 1999;27(2):99-102
  • Rappuoli R. Rational design of vaccines. Nat Med 1997;3(4):374-6
  • Robbins JB, Schneerson R, Keith JM, et al. Pertussis vaccine: a critique. Pediatr Infect Dis J 2009;28(3):237-41

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