Immunoproteomic analysis of Brucella melitensis and identification of a new immunogenic candidate protein for the development of brucellosis subunit vaccine

Molecular Immunology

Volumn 49, Issue 1-2, 2011, Pages 175-184

  Yang, Yanling ^a,b   Wang, Lin ^d   Yin, Jigang ^c   Wang, Xinglong ^a,c   Cheng, Shipeng ^b   Lang, Xulong ^a   Wang, Xiuran ^a   Qu, Hailong ^a   Sun, Chunhui ^a   Wang, Jinglong ^a   Zhang, Rui ^a  

^a BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

^b INSTITUTE OF PLANT PROTECTION   (China)

^c JILIN UNIVERSITY   (China)

^d SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Brucellosis; Immunogenic proteins; Immunoproteomics; Subunit vaccine

Indexed keywords

BRUCELLA VACCINE; GAMMA INTERFERON; HYBRID PROTEIN; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 4; LORAINE SYNTHASE 2; POLYHISTIDINE TAG; RIBOFLAVIN; RIBOFLAVIN SYNTHASE; RIBOFLAVIN SYNTHASE ALPHA; SYNTHETASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRUCELLA MELITENSIS; BRUCELLOSIS; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG SYNTHESIS; ESCHERICHIA COLI; HUMORAL IMMUNITY; IMMUNOBLOTTING; IMMUNOGENICITY; IMMUNOPROTEOMICS; IN VITRO STUDY; LIQUID CHROMATOGRAPHY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEOMICS; SPLEEN CELL; TANDEM MASS SPECTROMETRY; TWO DIMENSIONAL ELECTROPHORESIS; VACCINATION;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; BRUCELLA MELITENSIS; BRUCELLA VACCINE; BRUCELLOSIS; CELL SEPARATION; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FEMALE; FLOW CYTOMETRY; GOATS; HUMANS; IMMUNOBLOTTING; IMMUNODOMINANT EPITOPES; MICE; MICE, INBRED BALB C; PROTEOMICS; RECOMBINANT PROTEINS; RIBOFLAVIN SYNTHASE; TANDEM MASS SPECTROMETRY; VACCINES, SUBUNIT;

BACTERIA (MICROORGANISMS); BRUCELLA; BRUCELLA MELITENSIS; CAPRA HIRCUS; ESCHERICHIA COLI; MUS;

EID: 82455181876     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2011.08.009     Document Type: Article

References (55)

1. Al-Mariri A. Protection of BALB/c mice against Brucella melitensis 16M infection induced by vaccination with live Escherchia coli expression Brucella P39 protein. Vaccine 2010, 28:1766-1770.
2. Al-Mariri A., Tibor A., Mertens P., De Bolle X., Michel P., Godfroid J., Walravens K., Letesson J.J. Induction of immune response in BALB/c mice with a DNA vaccine encoding bacterioferritin or P39 of Brucella spp. Infect. Immun. 2001, 69:6264-6270.
3. Altindis E., Tefon B.E., Yildirim V., Ozcengiz E., Becher D., Hecker M., Ozcengiz G. Immunoproteomic analysis of Bordetella pertussis and identification of new immunogenic proteins. Vaccine 2009, 27:542-548.
4. Andrews E., Salgado P., Folch H., Onate A. Vaccination with live Escherichia coli expressing Brucella abortus Cu/Zn superoxide-dismutase: II. Induction of specific CD8+ cytotoxic lymphocytes and sensitized CD4+ IFN-gamma-producing cell. Microbiol. Immunol. 2006, 50:389-393.
5. Araya L.N., Elzer P.H., Rowe G.E., Enright F.M., Winter A.J. Temporal development of protective cell-mediated and humoral immunity in BALB/c mice infected with Brucella abortus. J. Immunol. 1989, 143:3330-3337.
6. Araya L.N., Winter A.J. Comparative protection of mice against virulent and attenuated strains of Brucella abortus by passive transfer of immune T cells or serum. Infect. Immun. 1990, 58:254-256.
7. Ashford D.A., di Pietra J., Lingappa J., Woods C., Noll H., Neville B., Weyant R., Bragg S.L., Spiegel R.A., Tappero J., Perkins B.A. Adverse events in humans associated with accidental exposure to the livestock brucellosis vaccine RB51. Vaccine 2004, 22:3435-3439.
8. Berguer P.M., Mundinano J., Piazzon I., Goldbaum F.A. A polymeric bacterial protein activates dendritic cells via TLR4. J. Immunol. 2006, 176:2366-2372.
9. Bonomi H.R., Marchesini M.I., Klinke S., Ugalde J.E., Zylberman V., Ugalde R.A., Comerci D.J., Goldbaum F.A. An atypical riboflavin pathway is essential for Brucella abortus virulence. PLoS. One 2010, 5:e9435.
10. Bowden R.A., Estein S.M., Zygmunt M.S., Dubray G., Cloeckaert A. Identification of protective outer membrane antigens of Brucella ovis by passive immunization of mice with monoclonal antibodies. Microbes Infect. 2000, 2:481-488.
11. Bricker B.J., Halling S.M. Differentiation of Brucella abortus bv. 1, 2, and 4, Brucella melitensis, Brucella ovis, and Brucella suis bv. 1 by PCR. J. Clin. Microbiol. 1994, 32:2660-2666.
12. Cassataro J., Estein S.M., Pasquevich K.A., Velikovsky C.A., de la Barrera S., Bowden R., Fossati C.A., Giambartolomei G.H. Vaccination with the recombinant Brucella outer membrane protein 31 or a derived 27-amino-acid synthetic peptide elicits a CD4+ T helper 1 response that protects against Brucella melitensis infection. Infect. Immun. 2005, 73:8079-8088.
13. Cassataro J., Pasquevich K.A., Estein S.M., Laplagne D.A., Zwerdling A., de la Barrera S., Bowden R., Fossati C.A., Giambartolomei G.H., Goldbaum F.A. A DNA vaccine coding for the chimera BLSOmp31 induced a better degree of protection against B. ovis and a similar degree of protection against B. melitensis than Rev.1 vaccination. Vaccine 2007, 25:5958-5967.
14. Cespedes S., Andrews E., Folch H., Onate A. Identification and partial characterisation of a new protective antigen of Brucella abortus. J. Med. Microbiol. 2000, 49:165-170.
15. Cheers C. Pathogenesis and cellular immunity in experimental murine brucellosis. Dev. Biol. Stand. 1984, 56:237-246.
16. Connolly J.P., Comerci D., Alefantis T.G., Walz A., Quan M., Chafin R., Grewal P., Mujer C.V., Ugalde R.A., DelVecchio V.G. Proteomic analysis of Brucella abortus cell envelope and identification of immunogenic candidate proteins for vaccine development. Proteomics 2006, 6:3767-3780.
17. Delpino M.V., Estein S.M., Fossati C.A., Baldi P.C., Cassataro J. Vaccination with Brucella recombinant DnaK and SurA proteins induces protection against Brucella abortus infection in BALB/c mice. Vaccine 2007, 25:6721-6729.
18. Denoel P.A., Vo T.K., Weynants V.E., Tibor A., Gilson D., Zygmunt M.S., Limet J.N., Letesson J.J. Identification of the major T-cell antigens present in the Brucella melitensis B115 protein preparation, Brucellergene OCB. J. Med. Microbiol. 1997, 46:801-806.
19. Eko F.O., Lubitz W., McMillan L., Ramey K., Moore T.T., Ananaba G.A., Lyn D., Black C.M., Igietseme J.U. Recombinant Vibrio cholerae ghosts as a delivery vehicle for vaccinating against Chlamydia trachomatis. Vaccine 2003, 21:1694-1703.
20. Elzer P.H., Jacobson R.H., Jones S.M., Nielsen K.H., Douglas J.T., Winter A.J. Antibody-mediated protection against Brucella abortus in BALB/c mice at successive periods after infection: variation between virulent strain 2308 and attenuated vaccine strain 19. Immunology 1994, 82:651-658.
21. Eze M.O., Yuan L., Crawford R.M., Paranavitana C.M., Hadfield T.L., Bhattacharjee A.K., Warren R.L., Hoover D.L. Effects of opsonization and gamma interferon on growth of Brucella melitensis 16M in mouse peritoneal macrophages in vitro. Infect. Immun. 2000, 68:257-263.
22. Goldbaum F.A., Velikovsky C.A., Baldi P.C., Mortl S., Bacher A., Fossati C.A. The 18-kDa cytoplasmic protein of Brucella species - an antigen useful for diagnosis - is a lumazine synthase. J. Med. Microbiol. 1999, 48:833-839.
23. Gonzalez D., Grillo M.J., De Miguel M.J., Ali T., Arce-Gorvel V., Delrue R.M., Conde-Alvarez R., Munoz P., Lopez-Goni I., Iriarte M., Marin C.M., Weintraub A., Widmalm G., Zygmunt M., Letesson J.J., Gorvel J.P., Blasco J.M., Moriyon I. Brucellosis vaccines: assessment of Brucella melitensis lipopolysaccharide rough mutants defective in core and O-polysaccharide synthesis and export. PLoS One 2008, 3:e2760.
24. Görg A., Weiss W., Dunn M.J. Current two-dimensional electrophoresis technology for proteomics. Proteomics 2004, 4:3665-3685.
25. Henningsen R., Gale B.L., Straub K.M., DeNagel D.C. Application of zwitterionic detergents to the solubilization of integral membrane proteins for two-dimensional gel electrophoresis and mass spectrometry. Proteomics 2002, 2:1479-1488.
26. Jimenez de Bagues M.P., Elzer P.H., Jones S.M., Blasco J.M., Enright F.M., Schurig G.G., Winter A.J. Vaccination with Brucella abortus rough mutant RB51 protects BALB/c mice against virulent strains of Brucella abortus, Brucella melitensis, and Brucella ovis. Infect. Immun. 1994, 62:4990-4996.
27. Jungblut P.R., Grabher G., Stoffler G. Comprehensive detection of immunorelevant Borrelia garinii antigens by two-dimensional electrophoresis. Electrophoresis 1999, 20:3611-3622.
28. Kakoma I., Baek B.K., Boyle S.M., Srianganathan N., Olsen S., Young E. Comments on efforts to eradicate brucellosis. J. Am. Vet. Med. Assoc. 2007, 230:27.
29. Keller A., Nesvizhskii A.I., Kolker E., Aebersold R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 2002, 74:5383-5392.
30. Khan A.S., Mujer C.V., Alefantis T.G., Connolly J.P., Mayr U.B., Walcher P., Lubitz W., Delvecchio V.G. Proteomics and bioinformatics strategies to design countermeasures against infectious threat agents. J. Chem. Inf. Model 2006, 46:111-115.
31. Ko J., Splitter G.A. Molecular host-pathogen interaction in brucellosis: current understanding and future approaches to vaccine development for mice and humans. Clin. Microbiol. Rev. 2003, 16:65-78.
32. Laplagne D.A., Zylberman V., Ainciart N., Steward M.W., Sciutto E., Fossati C.A., Goldbaum F.A. Engineering of a polymeric bacterial protein as a scaffold for the multiple display of peptides. Proteins 2004, 57:820-828.
33. Link A.J., Eng J., Schieltz D.M., Carmack E., Mize G.J., Morris D.R., Garvik B.M., Yates J.R.J3rd Direct analysis of protein complexes using mass spectrometry. Nat. Biotechnol. 1999, 17:676-682.
34. Luo D., Ni B., Li P., Shi W., Zhang S., Han Y., Mao L., He Y., Wu Y., Wang X. Protective immunity elicited by a divalent DNA vaccine encoding both the L7/L12 and Omp16 genes of Brucella abortus in BALB/c mice. Infect. Immun. 2006, 74:2734-2741.
35. Luo D.Y., Li P., Xing L., Zhao G.Y., Shi W., Zhang S.L., Wang X.L. DNA vaccine encoding L7/L12-P39 of Brucella abortus induces protective immunity in BALB/c mice. Chin. Med. J. (Engl) 2006, 119:331-334.
36. Mallick A.I., Singha H., Chaudhuri P., Nadeem A., Khan S.A., Dar K.A., Owais M. Liposomised recombinant ribosomal L7/L12 protein protects BALB/c mice against Brucella abortus 544 infection. Vaccine 2007, 25:3692-3704.
37. Murphy E.A., Sathiyaseelan J., Parent M.A., Zou B., Baldwin C.L. Interferon-gamma is crucial for surviving a Brucella abortus infection in both resistant C57BL/6 and susceptible BALB/c mice. Immunology 2001, 103:511-518.
38. Nesvizhskii A.I., Keller A., Kolker E., Aebersold R. A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 2003, 75:4646-4658.
39. Nicoletti P. Brucellosis: past, present and future. Prilozi 2010, 31:21-32.
40. Oliveira S.C., Soeurt N., Splitter G. Molecular and cellular interactions between Brucella abortus antigens and host immune responses. Vet. Microbiol. 2002, 90:417-424.
41. Oliveira S.C., Splitter G.A. Immunization of mice with recombinant L7/L12 ribosomal protein confers protection against Brucella abortus infection. Vaccine 1996, 14:959-962.
42. Pakzad I., Rezaee A., Rasaee M.J., Tabbaraee B., Delpisheh A. Immunogencity of HSA-L7/L12 (Brucella abortus ribosomal protein) in an animal model. Iran J. Immunol. 2009, 6:12-21.
43. Pasquevich K.A., Estein S.M., Garcia Samartino C., Zwerdling A., Coria L.M., Barrionuevo P., Fossati C.A., Giambartolomei G.H., Cassataro J. Immunization with recombinant Brucella species outer membrane protein Omp16 or Omp19 in adjuvant induces specific CD4+ and CD8+ T cells as well as systemic and oral protection against Brucella abortus infection. Infect. Immun. 2009, 77:436-445.
44. Seleem M.N., Boyle S.M., Sriranganathan N. Brucellosis: a re-emerging zoonosis. Vet. Microbiol. 2010, 140:392-398.
45. Serruto D., Rappuoli R. Post-genomic vaccine development. FEBS Lett. 2006, 580:2985-2992.
46. Splitter G., Oliveira S., Carey M., Miller C., Ko J., Covert J. T lymphocyte mediated protection against facultative intracellular bacteria. Vet. Immunol. Immunopathol. 1996, 54:309-319.
47. Tabatabai L.B., Pugh G.W. Modulation of immune responses in Balb/c mice vaccinated with Brucella abortus Cu-Zn superoxide dismutase synthetic peptide vaccine. Vaccine 1994, 12:919-924.
48. Teixeira-Gomes A.P., Cloeckaert A., Bezard G., Bowden R.A., Dubray G., Zygmunt M.S. Identification and characterization of Brucella ovis immunogenic proteins using two-dimensional electrophoresis and immunoblotting. Electrophoresis 1997, 18:1491-1497.
49. Thakur S.D., Kumar R., Thapliyal D.C. Human brucellosis: review of an under-diagnosed animal transmitted disease. J. Commun. Dis. 2002, 34:287-301.
50. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. 1979. Biotechnology 1992, 24:145-149.
51. Velikovsky C.A., Cassataro J., Giambartolomei G.H., Goldbaum F.A., Estein S., Bowden R.A., Bruno L., Fossati C.A., Spitz M. A DNA vaccine encoding lumazine synthase from Brucella abortus induces protective immunity in BALB/c mice. Infect. Immun. 2002, 70:2507-2511.
52. Velikovsky C.A., Goldbaum F.A., Cassataro J., Estein S., Bowden R.A., Bruno L., Fossati C.A., Giambartolomei G.H. Brucella lumazine synthase elicits a mixed Th1-Th2 immune response and reduces infection in mice challenged with Brucella abortus 544 independently of the adjuvant formulation used. Infect. Immun. 2003, 71:5750-5755.
53. Vizcaino N., Cloeckaert A., Dubray G., Zygmunt M.S. Cloning, nucleotide sequence, and expression of the gene coding for a ribosome releasing factor-homologous protein of Brucella melitensis. Infect. Immun. 1996, 64:4834-4837.
54. Zhan Y., Yang J., Cheers C. Cytokine response of T-cell subsets from Brucella abortus-infected mice to soluble Brucella proteins. Infect. Immun. 1993, 61:2841-2847.
55. Zylberman V., Klinke S., Haase I., Bacher A., Fischer M., Goldbaum F.A. Evolution of vitamin B2 biosynthesis: 6,7-dimethyl-8-ribityllumazine synthases of Brucella. J. Bacteriol. 2006, 188:6135-6142.