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References

  1. Al Dahouk S, Nockler K, Scholz HC, Tomaso H, Bogumil R, Neubauer H. 2006. Immunoproteomic characterization of Brucella abortus 1119-3 preparations used for the serodiagnosis of Brucella infection. J. Immunol. Methods 309: 34-47.
    CrossRef
  2. Baldi PC, Giambartolomei GH, Goldbaum FA, Abdon LF, Velikovsky CA, Kittelberger R, Fossati CA. 1996. Humoral immune response against lipopolysaccharide and cytoplasmic proteins of Brucella abortus in cattle vaccinated with B. abortus S19 or experimentally infected with Yersinia enterocolitica serotype O:9. Clin. Diagn. Lab. Immunol. 3: 472-476.
  3. Bricker BJ, Tabatabai LB, Judge BA, Deyoe BL, Mayfield JE. 1990. Cloning, expression, and occurrence of the Brucella Cu-Zn superoxide dismutase. Infect. Immun. 58: 2935-2939.
  4. Cha SB, Rayamajhi N, Kang ML, Lee WJ, Shin MK, Yoo HS. 2010. Comparative study of gamma interferon production in mice immunized with outer membrane proteins and whole bacteria of Brucella abortus. Jpn. J. Infect. Dis. 63: 49-51.
  5. Cloeckaert A, Jacques I, Bosseray N, Limet JN, Bowden R, Dubray G, Plommet M. 1991. Protection conferred on mice by monoclonal antibodies directed against outer-membraneprotein antigens of Brucella. J. Med. Microbiol. 34: 175-180.
    CrossRef
  6. Cloeckaert A, Verger JM, Grayon M, Vizcaino N. 1996. Molecular and immunological characterization of major outer membrane proteins of Brucella. FEMS Microbiob. Lett. 145: 1-8.
    CrossRef
  7. Cloeckaert A, Vizcaino N, Paquet JY, Bowden RA, Elzer PH. 2002. Major outer membrane proteins of Brucella spp.: past, present and future. Vet. Microbiol. 90: 229-247.
    CrossRef
  8. Connolly JP, Comerci D, Alefantis TG, Walz A, Quan M, Chafin R, et al. 2006. Proteomic analysis of Brucella abortus cell envelope and identification of immunogenic candidate proteins for vaccine development. Proteomics 6: 3767-3780.
    CrossRef
  9. Corbel MJ, Stuart FA, Brewer RA. 1984. Observations on serological cross-reaction between smooth Brucella species and organisms of other genera. Dev. Biol. Stand. 56: 341-348.
  10. Foster G, Osterman BS, Godfroid J, Jacques I, Cloeckaert A. 2007. Brucella ceti sp. nov. and Brucella pinnipedialis sp. nov. for Brucella strains with cetaceans and seals as their preferred host. Int. Syst. Evol. Microbiol. 57: 2688-2693.
    CrossRef
  11. Franco MP, Mulder M, Gilman RH, Smith HL. 2007. Human brucellosis. Lancet Infect. Dis. 7: 775-786.
    CrossRef
  12. Gee JM, Valderas MW, Kovach ME, Grippe VK, Robertson GT, Ng WL, et al. 2005. The Brucella abortus Cu, Zn superoxide dismutase is required for optimal resistance to oxidative killing by murine macrophages and wild-type virulence in experimentally infected mice. Infect. Immun. 73:2873-2880.
    CrossRef
  13. Golding B, Scott DE, Scharf OL, Huang LY, Zaitseva M, Lapham C, et al. 2001. Immunity and protection against Brucella abortus. Microbes Infect. 3: 43-48.
    CrossRef
  14. Guillermo HG, Zwerdling A, Cassataro J, Bruno L, Fossati CA, Philipp MT. 2004. Lipoprotein, not lipopolysaccharide, are the key mediators of proinflammatory response elicited by heat-killed Brucella abortus. J. Immunol. 173: 4635-4644.
    CrossRef
  15. Hadush A, Pal M. 2013. Brucellosis - an infectious reemerging bacterial zoonosis of global importance. Int. J. Livest. Res. 3: 28-33.
  16. Kittelberger R, Bundesen PG, Cloeckaert A, Greiser-Wilke I, Letesson JJ. 1998. Serological cross-reactivity between Brucella abortus and Yersinia enterocolitica 0:9. Vet. Microbiol. 60: 45-51.
    CrossRef
  17. Ko J, Splitter GA. 2003. Molecular host-pathogen interaction in brucellosis: current understanding and future approaches to vaccine development for mice and human. Clinic. Microbiol. Rev. 16: 65-78.
    CrossRef
  18. Ko KY, Kim JW, Her M, Kang SI, Jung SC, Cho DH, Kim JY. 2012. Immunogenic proteins of Brucella abortus to minimize cross reactions in brucellosis diagnosis. Vet. Microbiol. 156: 374-380.
    CrossRef
  19. Kumar S, Tuteja U, Batra HV. 2007. Generation and characterization of murine monoclonal antibodies to genusspecific 31-kilodalton recombinant cell surface protein of Brucella abortus. Hybridoma 26: 211-216.
    CrossRef
  20. Lettesson JJ, Tibor A, Van Eynde G, Wansard V, Weynants V, Denoel P, Saman E. 1999. Humoral immune responses of Brucella-infected cattle, sheep, and goats to eight purified recombinant Brucella proteins in an indirect enzyme-linked immunosorbent assay. Clinic. Diagnos. Lab. Immunol. 4: 556564.
  21. Lim JJ, Kim DH, Lee JJ, Kim DG, Min W, Lee WJ, et al. 2011. Evaluation of recombinant 28 kDa outer membrane protein of Brucella abortus for the clinical diagnosis of bovine brucellosis in Korea. J. Vet. Med. Sci. 74: 687-691.
    CrossRef
  22. Lim JJ, Kim DH, Lee JJ, Kim DG, Min W, Lee WJ, et al. 2012. Protective effects of recombinant Brucella abortus Omp28 against infection with a virulent strain of Brucella abortus 544 in mice. J. Vet. Sci. 13: 287-292.
    CrossRef
  23. Nielsen K, Smith P, Widdison J, Gall D, Kelly L, Kelly W, Nicoletti P. 2004. Serological relationship between cattle exposed to Brucella abortus, Yersinia enterocolitica O:9 and Escherichia coli O157:H7. Vet. Microbiol. 100: 25-30.
    CrossRef
  24. Onate AA, Vemulapalli R, Andrews E, Schurig GG, Boyle S, Folch H. 1999. Vaccination with live Escherichia coli expressing Brucella abortus Cu/Zn superoxide dismutase protects mice against virulent B. abortus. Infect. Immun. 67: 986-988.
  25. Paquet JY, Diaz MA, Genevrois S, Grayon M, Verger JM, de Bolle X, et al. 2001. Molecular, antigenic, and functional analyses of Omp2b porin size variants of Brucella spp. J. Bacteriol. 183: 4839-4847.
    CrossRef
  26. Riggs P. 2000. Expression and purification of recombinant proteins by fusion to maltose-binding proteins. Molec. Biotechnol. 15: 51-63.
    CrossRef
  27. Ruiz-Mesa JD, Sanchez-Gonzalez J, Reguera JM, Maritin L, Lopez-Palmero S, Colmenero JD. 2005. Rose Bengal test:diagnostic yield and use for the rapid diagnosis of human brucellosis in emergency departments in endemic area. Clinic. Microbiol. Infect. 11: 211-215.
    CrossRef
  28. Tabatabai LB, Pugh GW. 1994. Modulation of immune responses in BALB/c mice vaccinated with Brucella abortus Cu-Zn superoxide dismutase synthetic peptide vaccine. Vaccine 12: 919-924.
    CrossRef
  29. Vizcaino N, Cloeckaert A. 2012. Biology and genetics of the Brucella outer membrane, pp. 133-162. In Lopez-Goni I, O’Callaghan D (eds.). Brucella Molecular Microbiology and Genomics. Caister Academic Press, Norfork.
  30. Wang M, Qureshi N, Soeurt N, Splitter G. 2001. High levels of nitric oxide production decrease early but increase rate of survival of Brucella abortus in macrophage. Microb. Pathog. 31: 221-230.
    CrossRef
  31. Zhan Y, Kelso A, Cheers C. 1993. Cytokine production in the murine response to Brucella infection or immunization with antigenic extracts. Immunology 80: 458-464.
  32. Zhan Y, Cheers C. 1995. Different induction of macrophagederived cytokines by live or dead intracellular bacteria in vitro. Immunology 63: 720-723.

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Article

Research article

J. Microbiol. Biotechnol. 2014; 24(6): 854-861

Published online June 28, 2014 https://doi.org/10.4014/jmb.1312.12063

Copyright © The Korean Society for Microbiology and Biotechnology.

Induction of Immune Responses by Two Recombinant Proteins of Brucella abortus, Outer Membrane Proteins 2b Porin and Cu/Zn Superoxide Dismutase, in Mouse Model

Kyung Yong Sung 1, Myunghwan Jung 1, Min-Kyoung Shin 1, Hyun-Eui Park 1, Jin Ju Lee 2, Suk Kim 2 and Han Sang Yoo 1, 3*

1Department of Infectious Diseases, College of Veterinary Medicine, Seoul National University, Seoul 151-742, Republic of Korea, 2College of Veterinary Medicine, Gyeongsang National University, Jinju 660-701, Republic of Korea, 3Institute of Green Bio Sciences and Technology, Seoul National University, Pyeongchang 232-916, Republic of Korea

Received: December 24, 2013; Accepted: March 6, 2014

Abstract

The diagnosis of Brucella abortus is mainly based on serological methods using antibody
against LPS, which has diagnostic problems. Therefore, to solve this problem, we evaluated
two proteins of B. abortus, Cu/Zn superoxide dismutase (SodC) and outer membrane proteins
2b porin (Omp2b). The genes were cloned and expressed in a pMAL system, and the
recombinant proteins, rOmp2b and rSodC, were purified as fusion forms with maltosebinding
protein. The identity of the proteins was confirmed by SDS-PAGE and Western blot
analysis with sera of mice infected with B. abortus. Production of cytokines and nitric oxide
(NO) was investigated in RAW 264.7 cells and mouse splenocytes after stimulation with the
proteins. Moreover, cellular and humoral immune responses were investigated in BALB/c
mice after immunization with the proteins. TNF-α, IL-6, and NO were significantly inducible
in RAW 264.7 cells. Splenocytes of naive mice produced IFN-γ and IL-4 significantly by
stimulation. Moreover, number of IgG, IFN-γ, and IL-4 producing cells were increased in
immunized mice with the two proteins. Production of IgG and IgM with rOmp2b was higher
than those with rSodC in immunized mice. These results suggest that the two recombinant
proteins of B. abortus may be potential LPS-free proteins for diagnosis.

Keywords: Brucella abortus, cytokine, immunogenicity, Omp2b, SodC

References

  1. Al Dahouk S, Nockler K, Scholz HC, Tomaso H, Bogumil R, Neubauer H. 2006. Immunoproteomic characterization of Brucella abortus 1119-3 preparations used for the serodiagnosis of Brucella infection. J. Immunol. Methods 309: 34-47.
    CrossRef
  2. Baldi PC, Giambartolomei GH, Goldbaum FA, Abdon LF, Velikovsky CA, Kittelberger R, Fossati CA. 1996. Humoral immune response against lipopolysaccharide and cytoplasmic proteins of Brucella abortus in cattle vaccinated with B. abortus S19 or experimentally infected with Yersinia enterocolitica serotype O:9. Clin. Diagn. Lab. Immunol. 3: 472-476.
  3. Bricker BJ, Tabatabai LB, Judge BA, Deyoe BL, Mayfield JE. 1990. Cloning, expression, and occurrence of the Brucella Cu-Zn superoxide dismutase. Infect. Immun. 58: 2935-2939.
  4. Cha SB, Rayamajhi N, Kang ML, Lee WJ, Shin MK, Yoo HS. 2010. Comparative study of gamma interferon production in mice immunized with outer membrane proteins and whole bacteria of Brucella abortus. Jpn. J. Infect. Dis. 63: 49-51.
  5. Cloeckaert A, Jacques I, Bosseray N, Limet JN, Bowden R, Dubray G, Plommet M. 1991. Protection conferred on mice by monoclonal antibodies directed against outer-membraneprotein antigens of Brucella. J. Med. Microbiol. 34: 175-180.
    CrossRef
  6. Cloeckaert A, Verger JM, Grayon M, Vizcaino N. 1996. Molecular and immunological characterization of major outer membrane proteins of Brucella. FEMS Microbiob. Lett. 145: 1-8.
    CrossRef
  7. Cloeckaert A, Vizcaino N, Paquet JY, Bowden RA, Elzer PH. 2002. Major outer membrane proteins of Brucella spp.: past, present and future. Vet. Microbiol. 90: 229-247.
    CrossRef
  8. Connolly JP, Comerci D, Alefantis TG, Walz A, Quan M, Chafin R, et al. 2006. Proteomic analysis of Brucella abortus cell envelope and identification of immunogenic candidate proteins for vaccine development. Proteomics 6: 3767-3780.
    CrossRef
  9. Corbel MJ, Stuart FA, Brewer RA. 1984. Observations on serological cross-reaction between smooth Brucella species and organisms of other genera. Dev. Biol. Stand. 56: 341-348.
  10. Foster G, Osterman BS, Godfroid J, Jacques I, Cloeckaert A. 2007. Brucella ceti sp. nov. and Brucella pinnipedialis sp. nov. for Brucella strains with cetaceans and seals as their preferred host. Int. Syst. Evol. Microbiol. 57: 2688-2693.
    CrossRef
  11. Franco MP, Mulder M, Gilman RH, Smith HL. 2007. Human brucellosis. Lancet Infect. Dis. 7: 775-786.
    CrossRef
  12. Gee JM, Valderas MW, Kovach ME, Grippe VK, Robertson GT, Ng WL, et al. 2005. The Brucella abortus Cu, Zn superoxide dismutase is required for optimal resistance to oxidative killing by murine macrophages and wild-type virulence in experimentally infected mice. Infect. Immun. 73:2873-2880.
    CrossRef
  13. Golding B, Scott DE, Scharf OL, Huang LY, Zaitseva M, Lapham C, et al. 2001. Immunity and protection against Brucella abortus. Microbes Infect. 3: 43-48.
    CrossRef
  14. Guillermo HG, Zwerdling A, Cassataro J, Bruno L, Fossati CA, Philipp MT. 2004. Lipoprotein, not lipopolysaccharide, are the key mediators of proinflammatory response elicited by heat-killed Brucella abortus. J. Immunol. 173: 4635-4644.
    CrossRef
  15. Hadush A, Pal M. 2013. Brucellosis - an infectious reemerging bacterial zoonosis of global importance. Int. J. Livest. Res. 3: 28-33.
  16. Kittelberger R, Bundesen PG, Cloeckaert A, Greiser-Wilke I, Letesson JJ. 1998. Serological cross-reactivity between Brucella abortus and Yersinia enterocolitica 0:9. Vet. Microbiol. 60: 45-51.
    CrossRef
  17. Ko J, Splitter GA. 2003. Molecular host-pathogen interaction in brucellosis: current understanding and future approaches to vaccine development for mice and human. Clinic. Microbiol. Rev. 16: 65-78.
    CrossRef
  18. Ko KY, Kim JW, Her M, Kang SI, Jung SC, Cho DH, Kim JY. 2012. Immunogenic proteins of Brucella abortus to minimize cross reactions in brucellosis diagnosis. Vet. Microbiol. 156: 374-380.
    CrossRef
  19. Kumar S, Tuteja U, Batra HV. 2007. Generation and characterization of murine monoclonal antibodies to genusspecific 31-kilodalton recombinant cell surface protein of Brucella abortus. Hybridoma 26: 211-216.
    CrossRef
  20. Lettesson JJ, Tibor A, Van Eynde G, Wansard V, Weynants V, Denoel P, Saman E. 1999. Humoral immune responses of Brucella-infected cattle, sheep, and goats to eight purified recombinant Brucella proteins in an indirect enzyme-linked immunosorbent assay. Clinic. Diagnos. Lab. Immunol. 4: 556564.
  21. Lim JJ, Kim DH, Lee JJ, Kim DG, Min W, Lee WJ, et al. 2011. Evaluation of recombinant 28 kDa outer membrane protein of Brucella abortus for the clinical diagnosis of bovine brucellosis in Korea. J. Vet. Med. Sci. 74: 687-691.
    CrossRef
  22. Lim JJ, Kim DH, Lee JJ, Kim DG, Min W, Lee WJ, et al. 2012. Protective effects of recombinant Brucella abortus Omp28 against infection with a virulent strain of Brucella abortus 544 in mice. J. Vet. Sci. 13: 287-292.
    CrossRef
  23. Nielsen K, Smith P, Widdison J, Gall D, Kelly L, Kelly W, Nicoletti P. 2004. Serological relationship between cattle exposed to Brucella abortus, Yersinia enterocolitica O:9 and Escherichia coli O157:H7. Vet. Microbiol. 100: 25-30.
    CrossRef
  24. Onate AA, Vemulapalli R, Andrews E, Schurig GG, Boyle S, Folch H. 1999. Vaccination with live Escherichia coli expressing Brucella abortus Cu/Zn superoxide dismutase protects mice against virulent B. abortus. Infect. Immun. 67: 986-988.
  25. Paquet JY, Diaz MA, Genevrois S, Grayon M, Verger JM, de Bolle X, et al. 2001. Molecular, antigenic, and functional analyses of Omp2b porin size variants of Brucella spp. J. Bacteriol. 183: 4839-4847.
    CrossRef
  26. Riggs P. 2000. Expression and purification of recombinant proteins by fusion to maltose-binding proteins. Molec. Biotechnol. 15: 51-63.
    CrossRef
  27. Ruiz-Mesa JD, Sanchez-Gonzalez J, Reguera JM, Maritin L, Lopez-Palmero S, Colmenero JD. 2005. Rose Bengal test:diagnostic yield and use for the rapid diagnosis of human brucellosis in emergency departments in endemic area. Clinic. Microbiol. Infect. 11: 211-215.
    CrossRef
  28. Tabatabai LB, Pugh GW. 1994. Modulation of immune responses in BALB/c mice vaccinated with Brucella abortus Cu-Zn superoxide dismutase synthetic peptide vaccine. Vaccine 12: 919-924.
    CrossRef
  29. Vizcaino N, Cloeckaert A. 2012. Biology and genetics of the Brucella outer membrane, pp. 133-162. In Lopez-Goni I, O’Callaghan D (eds.). Brucella Molecular Microbiology and Genomics. Caister Academic Press, Norfork.
  30. Wang M, Qureshi N, Soeurt N, Splitter G. 2001. High levels of nitric oxide production decrease early but increase rate of survival of Brucella abortus in macrophage. Microb. Pathog. 31: 221-230.
    CrossRef
  31. Zhan Y, Kelso A, Cheers C. 1993. Cytokine production in the murine response to Brucella infection or immunization with antigenic extracts. Immunology 80: 458-464.
  32. Zhan Y, Cheers C. 1995. Different induction of macrophagederived cytokines by live or dead intracellular bacteria in vitro. Immunology 63: 720-723.