View More View Less
  • 1 Chonbuk National University College of Veterinary Medicine and Bio-Safety Research Institute 561-756 Jeonju South Korea
Restricted access

Purchase article

USD  $25.00

1 year subscription (Individual Only)

USD  $836.00

This study aimed to investigate the adjuvant effect of recombinant attenuated Salmonella expressing cholera toxin B subunit (CTB) and Escherichia coli heat-labile enterotoxin B subunit (LTB) for the P-fimbriae subunit-based vaccine of avian pathogenic E. coli (APEC) in a murine model. The PapA-specific sIgA and IgG responses were significantly enhanced after immunisation with the Salmonella-PapA vaccine in the presence of CTB or LTB. The group immunised with the Salmonella-LTB strain promoted Th1-type immunity, whereas that immunised with the Salmonella-CTB strain produced Th2-type immunity. We concluded that both Salmonella-CTB and -LTB strains can enhance the immune response to PapA, and that the LTB strain may be a more effective adjuvant for APEC vaccination, which requires higher Th1-type immunity for protection. Thus, our findings provide evidence that immunisation with an adjuvant, LTB, is one of the strategies of developing effective vaccines against P-fimbriated APEC.

  • Bastiani, M., Vidotto, M. C. and Horn, F. (2005): An avian pathogenic Escherichia coli isolate induces caspase 3/7 activation in J774 macrophages. FEMS. Microbiol. Lett. 253, 133–140.

    Horn F. , 'An avian pathogenic Escherichia coli isolate induces caspase 3/7 activation in J774 macrophages ' (2005 ) 253 FEMS. Microbiol. Lett. : 133 -140.

    • Search Google Scholar
  • Branger, C. G., Fetherston, J. D., Perry, R. D. and Curtiss, R. 3rd (2007): Oral vaccination with different antigens from Yersinia pestis KIM delivered by live attenuated Salmonella typhimurium elicits a protective immune response against plague. Adv. Exp. Med. Biol. 603, 387–399.

    Curtiss R. , 'Oral vaccination with different antigens from Yersinia pestis KIM delivered by live attenuated Salmonella typhimurium elicits a protective immune response against plague ' (2007 ) 603 Adv. Exp. Med. Biol. : 387 -399.

    • Search Google Scholar
  • Chappell, L., Kaiser, P., Barrow, P., Jones, M. A., Johnston, C. and Wigley, P. (2009): The immunobiology of avian systemic salmonellosis. Vet. Immunol. Immunopathol. 128, 53–59.

    Wigley P. , 'The immunobiology of avian systemic salmonellosis ' (2009 ) 128 Vet. Immunol. Immunopathol. : 53 -59.

    • Search Google Scholar
  • Dho-Moulin, M. and Fairbrother, J. M. (1999): Avian pathogenic Escherichia coli (APEC). Vet. Res. 30, 299–316.

    Fairbrother J. M. , 'Avian pathogenic Escherichia coli (APEC) ' (1999 ) 30 Vet. Res. : 299 -316.

    • Search Google Scholar
  • de Haan, L., Verweij, W. R., Feil, I. K., Holtrop, M., Brands, R., van Scharrenburg, G. J. M., Palache, A. M., Agsteribbe, E. and Wilschut, J. (2001): Nasal or intramuscular immunization of mice with influenza subunit antigen and the B subunit of Escherichia coli heat-labile toxin induces IgA-or IgG-mediated protective mucosal immunity. Vaccine 19, 2898–2907.

    Wilschut J. , 'Nasal or intramuscular immunization of mice with influenza subunit antigen and the B subunit of Escherichia coli heat-labile toxin induces IgA-or IgG-mediated protective mucosal immunity ' (2001 ) 19 Vaccine : 2898 -2907.

    • Search Google Scholar
  • Dziva, F. and Stevens, M. P. (2008): Colibacillosis in poultry: unraveling the molecular basis of virulence of avian pathogenic Escherichia coli in their natural hosts. Avian Pathol. 37, 355–366.

    Stevens M. P. , 'Colibacillosis in poultry: unraveling the molecular basis of virulence of avian pathogenic Escherichia coli in their natural hosts ' (2008 ) 37 Avian Pathol : 355 -366.

    • Search Google Scholar
  • Ewers, C., Antão, E. M., Diehl, I., Philipp, H. C. and Wieler, L. H. (2009): Intestine and environment of the chicken as reservoirs for extraintestinal pathogenic Escherichia coli strains with zoonotic potential. Appl. Environ. Microbiol. 75, 184–192.

    Wieler L. H. , 'Intestine and environment of the chicken as reservoirs for extraintestinal pathogenic Escherichia coli strains with zoonotic potential ' (2009 ) 75 Appl. Environ. Microbiol. : 184 -192.

    • Search Google Scholar
  • Ewers, C., Janben, T., Kiebling, S., Philipp, H. C. and Wieler, L. H. (2004): Molecular epidemiology of avian pathogenic Escherichia coli (APEC) isolated from colisepticemia in poultry. Vet. Microbiol. 104, 91–101.

    Wieler L. H. , 'Molecular epidemiology of avian pathogenic Escherichia coli (APEC) isolated from colisepticemia in poultry ' (2004 ) 104 Vet. Microbiol. : 91 -101.

    • Search Google Scholar
  • Fingerut, E., Gutter, B., Goldway, M., Eliahoo, D. and Pitcovski, J. (2006): B subunit of E.coli enterotoxin as adjuvant and carrier in oral and skin vaccination. Vet. Immunol. Immunopathol. 112, 253–263.

    Pitcovski J. , 'B subunit of E.coli enterotoxin as adjuvant and carrier in oral and skin vaccination ' (2006 ) 112 Vet. Immunol. Immunopathol. : 253 -263.

    • Search Google Scholar
  • Freytag, L. C. and Clements, J. D. (1999): Bacterial toxins as mucosal adjuvants. Curr. Top. Microbiol. Immunol. 236, 215–236.

    Clements J. D. , 'Bacterial toxins as mucosal adjuvants ' (1999 ) 236 Curr. Top. Microbiol. Immunol. : 215 -236.

    • Search Google Scholar
  • Freytag, L. C. and Clements, J. D. (2005): Mucosal adjuvants. Vaccine 23, 1804–1813.

    Clements J. D. , 'Mucosal adjuvants ' (2005 ) 23 Vaccine : 1804 -1813.

  • Goto, N., Maeyama, J. I., Yasuda, Y., Isaka, M., Matano, K., Kozuka, S., Taniguchi, T., Miura, Y., Okhuma, K. and Tochikubo, K. (2000): Safety evaluation of recombinant cholera toxin B subunit produced by Bacillus brevis as a mucosal adjuvant. Vaccine 18, 2164–2171.

    Tochikubo K. , 'Safety evaluation of recombinant cholera toxin B subunit produced by Bacillus brevis as a mucosal adjuvant ' (2000 ) 18 Vaccine : 2164 -2171.

    • Search Google Scholar
  • Gulig, P. A. and Curtiss, R. 3rd (1987): Plasmid-associated virulence of Salmonella Typhimurium. Infect. Immun. 55, 2891–2901.

    Curtiss R. , 'Plasmid-associated virulence of Salmonella Typhimurium ' (1987 ) 55 Infect. Immun. : 2891 -2901.

    • Search Google Scholar
  • Hayward, C. M. M., O’Gaora, P., Young, D. B., Griffin, G. E., Thole, J., Hirst, T. R., Castello-Branco, L. R. R. and Lewis, D. J. M. (1999): Construction and murine immunogenicity of recombinant Bacille Calmette Guerin vaccine expressing the B subunit of Escherichia coli heat labile enterotoxin. Vaccine 17, 1272–1281.

    Lewis D. J. M. , 'Construction and murine immunogenicity of recombinant Bacille Calmette Guerin vaccine expressing the B subunit of Escherichia coli heat labile enterotoxin ' (1999 ) 17 Vaccine : 1272 -1281.

    • Search Google Scholar
  • Holmgren, J. and Czerkinsky, C. (2005): Mucosal immunity and vaccines. Nat. Med. 11, S45–S53.

    Czerkinsky C. , 'Mucosal immunity and vaccines ' (2005 ) 11 Nat. Med. : S45 -S53.

  • Holmgren, J., Czerkinsky, C., Lycke, N. and Svennerholm, A-M. (1992): Mucosal immunity: implication for vaccine development. Immunobiology 184, 157–179.

    Svennerholm A.-M. , 'Mucosal immunity: implication for vaccine development ' (1992 ) 184 Immunobiology : 157 -179.

    • Search Google Scholar
  • Holmgren, J., Lycke, N. and Czerkinsky, C. (1993): Cholera toxin and cholera B subunit as oralmucosal adjuvant and antigen vector systems. Vaccine 11, 1179–1184.

    Czerkinsky C. , 'Cholera toxin and cholera B subunit as oralmucosal adjuvant and antigen vector systems ' (1993 ) 11 Vaccine : 1179 -1184.

    • Search Google Scholar
  • Isaka, M., Yasuda, Y., Kozuka, S., Tanguchi, T., Matano, K., Maeyama, J., Komiya, T., Ohkuma, K., Goto, N. and Tochikubo, K. (1999): Induction of systemic and mucosal antibody responses in mice immunized intranasally with aluminium-non-adsorbed diphtheria toxoid together with recombinant cholera toxin B subunit as an adjuvant. Vaccine 18, 743–751.

    Tochikubo K. , 'Induction of systemic and mucosal antibody responses in mice immunized intranasally with aluminium-non-adsorbed diphtheria toxoid together with recombinant cholera toxin B subunit as an adjuvant ' (1999 ) 18 Vaccine : 743 -751.

    • Search Google Scholar
  • Kang, H. Y., Srinivasan, J. and Curtiss, R. 3rd (2002): Immune responses to recombinant pneumococcal PspA antigen delivered by live attenuated Salmonella enterica serovar Typhimurium vaccine. Infect. Immun. 70, 1739–1749.

    Curtiss R. , 'Immune responses to recombinant pneumococcal PspA antigen delivered by live attenuated Salmonella enterica serovar Typhimurium vaccine ' (2002 ) 70 Infect. Immun. : 1739 -1749.

    • Search Google Scholar
  • McCluskie, M. J. and Davis, H. L. (1998): CpG DNA is a potent enhancer of systemic and mucosal immune responses against hepatitis B surface antigen with intranasal administration to mice. J. Immunol. 161, 4463–4466.

    Davis H. L. , 'CpG DNA is a potent enhancer of systemic and mucosal immune responses against hepatitis B surface antigen with intranasal administration to mice ' (1998 ) 161 J. Immunol. : 4463 -4466.

    • Search Google Scholar
  • McCluskie, M. J., Weeratna, R. D., Clements, J. D. and Davis, H. L. (2001): Mucosal immunization of mice using CpG DNA and/or mutants of the heat-labile enterotoxin of Escherichia coli as adjuvants. Vaccine 19, 3759–3768.

    Davis H. L. , 'Mucosal immunization of mice using CpG DNA and/or mutants of the heat-labile enterotoxin of Escherichia coli as adjuvants ' (2001 ) 19 Vaccine : 3759 -3768.

    • Search Google Scholar
  • Nakayama, K., Kelly, S. M. and Curtiss, R. 3rd (1998): Construction of an Asd+ expression-cloning vector: stable maintenance and high level expression of cloned genes in a Salmonella vaccine strain. Nature Biotechnol. 6, 693–697.

    Curtiss R. , 'Construction of an Asd+ expression-cloning vector: stable maintenance and high level expression of cloned genes in a Salmonella vaccine strain ' (1998 ) 6 Nature Biotechnol. : 693 -697.

    • Search Google Scholar
  • Ogra, P. L., Faden, H. and Welliver, R. C. (2001): Vaccination strategies for mucosal immune responses. Clin. Microbiol. Rev. 14, 430–445.

    Welliver R. C. , 'Vaccination strategies for mucosal immune responses ' (2001 ) 14 Clin. Microbiol. Rev. : 430 -445.

    • Search Google Scholar
  • Oh, I. G., Moon, B. M. and Lee, J. H. (2011): Induction of systemic and mucosal immune responses in mice orally administered with recombinant attenuated Salmonella expressing subunits of P fimbriae of avian pathogenic Escherichia coli. J. Vet. Clin. 28, 297–302.

    Lee J. H. , 'Induction of systemic and mucosal immune responses in mice orally administered with recombinant attenuated Salmonella expressing subunits of P fimbriae of avian pathogenic Escherichia coli ' (2011 ) 28 J. Vet. Clin. : 297 -302.

    • Search Google Scholar
  • Pourbakhsh, S. A., Boulianne, M., Martineau-Doize, B. and Fairbrother, J. M. (1997): Virulence mechanisms of avian fimbriated Escherichia coli in experimentally inoculated chickens. Vet. Microbiol. 58, 195–213.

    Fairbrother J. M. , 'Virulence mechanisms of avian fimbriated Escherichia coli in experimentally inoculated chickens ' (1997 ) 58 Vet. Microbiol. : 195 -213.

    • Search Google Scholar
  • Ruddock, L. W., Ruston, S. P., Kelly, S. M., Price, N. C., Freedman, R. B. and Hirst, T. R. (1995): Kinetics of acid-mediated disassembly of the B subunit pentamer of Escherichia coli heatlabile enterotoxin. Molecular basis of pH stability. J. Biol. Chem. 270, 29953–29958.

    Hirst T. R. , 'Kinetics of acid-mediated disassembly of the B subunit pentamer of Escherichia coli heatlabile enterotoxin. Molecular basis of pH stability ' (1995 ) 270 J. Biol. Chem. : 29953 -29958.

    • Search Google Scholar
  • Simmons, C. P., Ghaem-Magami, M., Petrovska, L., Lopes, L., Chain, B. M., Williams, N. A. and Dougan, G. (2001): Immunomodulation using bacterial enterotoxins. Scand. J. Immunol. 53, 218–226.

    Dougan G. , 'Immunomodulation using bacterial enterotoxins ' (2001 ) 53 Scand. J. Immunol. : 218 -226.

    • Search Google Scholar
  • Sirard, J. C., Niedergang, F. and Kraehenbuhl, J. P. (1999): Live attenuated salmonella: a paradigm of mucosal vaccine, Immunol. Rev. 171, 5–26.

    Kraehenbuhl J. P. , 'Live attenuated salmonella: a paradigm of mucosal vaccine ' (1999 ) 171 Immunol. Rev. : 5 -26.

    • Search Google Scholar
  • Slos, P., Dutot, P., Reymund, J., Kleinpeter, P., Prozzi, D., Kieny, M. P., Delcour, J., Mercenier, A. and Hols, P. (1998): Production of cholera toxin B subunit in Lactobacillus. FEMS Microbiol. Lett. 169, 29–36.

    Hols P. , 'Production of cholera toxin B subunit in Lactobacillus ' (1998 ) 169 FEMS Microbiol. Lett. : 29 -36.

    • Search Google Scholar
  • Strindelius, L., Filler, M. and Sjöholm, I. (2004): Mucosal immunization with purified flagellin from Salmonella induces systemic and mucosal immune responses in C3H/HeJ mice. Vaccine 22, 3797–3808.

    Sjöholm I. , 'Mucosal immunization with purified flagellin from Salmonella induces systemic and mucosal immune responses in C3H/HeJ mice ' (2004 ) 22 Vaccine : 3797 -3808.

    • Search Google Scholar
  • Tóth, I., Dobrindt, U., Koscsó, B., Kósa, A., Herpay, M. and Nagy, B. (2012): Genetic and phylogenetic analysis of avian extraintestinal and intestinal Escherichia coli. Acta Microbiol. Immunol. Hung. 59, 393–409.

    Nagy B. , 'Genetic and phylogenetic analysis of avian extraintestinal and intestinal Escherichia coli ' (2012 ) 59 Acta Microbiol. Immunol. Hung. : 393 -409.

    • Search Google Scholar
  • Vandemaele, F., Assadzadeh, A., Derijcke, J., Vereecken, M. and Goddeeris, B. M. (2002): Avian pathogenic Escherichia coli (APEC). Tijdschr. Diergeneeskd. 127, 582–588.

    Goddeeris B. M. , 'Avian pathogenic Escherichia coli (APEC) ' (2002 ) 127 Tijdschr. Diergeneeskd. : 582 -588.

    • Search Google Scholar
  • Verweij, W. R., de Haan, L., Holtrop, M., Agsteribbe, E., Brands, R., van Scharrenburg, G. J. M. and Wilschut, J. (1998): Mucosal immunoadjuvant activity of recombinant Escherichia coli heat-labile enterotoxin and its B subunit: Induction of systemic IgG and secretory IgA responses in mice by intranasal immunization with influenza virus surface antigen. Vaccine 16, 2069–2076.

    Wilschut J. , 'Mucosal immunoadjuvant activity of recombinant Escherichia coli heat-labile enterotoxin and its B subunit: Induction of systemic IgG and secretory IgA responses in mice by intranasal immunization with influenza virus surface antigen ' (1998 ) 16 Vaccine : 2069 -2076.

    • Search Google Scholar
  • Vindurampulle, C. J., Cuberos, L. F., Barry, E. M., Pasetti, M. F. and Levine, M. M. (2004): Recombinant Salmonella enterica serovar Typhi in a prime-boost strategy. Vaccine 22, 3744–3750.

    Levine M. M. , 'Recombinant Salmonella enterica serovar Typhi in a prime-boost strategy ' (2004 ) 22 Vaccine : 3744 -3750.

    • Search Google Scholar
  • Wigley, P., Hulme, S., Powers, C., Beal, R., Smith, A. and Barrow, P. (2005): Oral infection with the Salmonella enterica serovar Gallinarum 9R attenuated live vaccine as a model to characterise immunity to fowl typhoid in the chicken. BMC Vet. Res. 1, 2. 10.1186/1746-6148-1-2

    Barrow P. , 'Oral infection with the Salmonella enterica serovar Gallinarum 9R attenuated live vaccine as a model to characterise immunity to fowl typhoid in the chicken ' (2005 ) 1 BMC Vet. Res. : 2 -.

    • Search Google Scholar
  • Yamamoto, S., Kiyono, H., Yamamoto, M., Imaoka, K., Fujihashi, K., Van Ginkel, F. W., Noda, M., Takeda, Y. and McGhee, J. R. (1997): A nontoxic mutant of cholera toxin elicits Th2-type responses for enhanced mucosal immunity. Proc. Natl Acad. Sci. USA 13, 5267–5272.

    McGhee J. R. , 'A nontoxic mutant of cholera toxin elicits Th2-type responses for enhanced mucosal immunity ' (1997 ) 13 Proc. Natl Acad. Sci. USA : 5267 -5272.

    • Search Google Scholar
  • Zhang, L., Zhang, M., Li, J., Cao, T., Tian, X. and Zhou, F. (2008): Enhancement of mucosal immune responses by intranasal co-delivery of Newcastle disease vaccine plus CpG oligonucleotide in SPF chickens in vivo. Res. Vet. Sci. 85, 495–502.

    Zhou F. , 'Enhancement of mucosal immune responses by intranasal co-delivery of Newcastle disease vaccine plus CpG oligonucleotide in SPF chickens in vivo ' (2008 ) 85 Res. Vet. Sci. : 495 -502.

    • Search Google Scholar
  • Zhang, X., Zhang, X. and Yang, Q. (2007): Effect of compound mucosal immune adjuvant on mucosal and systemic immune responses in chicken orally vaccinated with attenuated Newcastle-disease vaccine. Vaccine 30, 3254–3262.

    Yang Q. , 'Effect of compound mucosal immune adjuvant on mucosal and systemic immune responses in chicken orally vaccinated with attenuated Newcastle-disease vaccine ' (2007 ) 30 Vaccine : 3254 -3262.

    • Search Google Scholar
  • Zhao, X., Zhang, M., Li, Z. and Frankel, F. R. (2006): Vaginal protection and immunity after oral immunization of mice with a novel vaccine strain of Listeria monocytogenes expressing human immunodeficiency virus type 1 gag. J. Virol. 80, 8880–8890.

    Frankel F. R. , 'Vaginal protection and immunity after oral immunization of mice with a novel vaccine strain of Listeria monocytogenes expressing human immunodeficiency virus type 1 gag ' (2006 ) 80 J. Virol. : 8880 -8890.

    • Search Google Scholar

Monthly Content Usage

Abstract Views Full Text Views PDF Downloads
Jun 2020 0 3 2
Jul 2020 1 0 0
Aug 2020 5 0 0
Sep 2020 2 0 0
Oct 2020 2 1 2
Nov 2020 3 2 0
Dec 2020 0 0 0