1887

Abstract

In BALB/c mouse models of serovar Typhimurium infection, a single oral immunization with a mutant strain with an insertion of the chloramphenicol resistance gene into the ATP-dependent protease or gene decreased the number of salmonellae in each tissue sample 5 days after oral challenge with virulent . Typhimurium at weeks 26 and 54 post-immunization. These data suggested that an oral immunization with the ClpP- or Lon-disrupted . Typhimurium strain could provide long-term protection against oral challenge with virulent . Typhimurium. Accordingly, recombinant oral non-typhoidal (NTS) vaccines were constructed by incorporating mutants of both Typhimurium and serovar Enteritidis harbouring stable in-frame markerless deletions of the (suppressor of ), or (acyltransferase) genes. Amongst these orally administered vaccine candidates, those with the gene deletion mutants of Typhimurium and Enteritidis protected BALB/c and C57BL/6J mice against oral challenge with both virulent . Typhimurium and virulent Enteritidis. Therefore, the in-frame markerless gene deletion mutant of . Typhimurium or Enteritidis could be a promising cross-protective NTS live vaccine candidate for practical use in humans.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.000014
2015-03-01
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/jmm/64/3/295.html?itemId=/content/journal/jmm/10.1099/jmm.0.000014&mimeType=html&fmt=ahah

References

  1. Alaniz R. C., Deatherage B. L., Lara J. C., Cookson B. T. 2007; Membrane vesicles are immunogenic facsimiles of Salmonella typhimurium that potently activate dendritic cells, prime B and T cell responses, and stimulate protective immunity in vivo. J Immunol 179:7692–7701 [View Article][PubMed]
    [Google Scholar]
  2. Bumann D. 2014; Identification of protective antigens for vaccination against systemic salmonellosis. Front Immunol 5:381 [View Article][PubMed]
    [Google Scholar]
  3. Cerutti A., Cols M., Gentile M., Cassis L., Barra C. M., He B., Puga I., Chen K. 2011; Regulation of mucosal IgA responses: lessons from primary immunodeficiencies. Ann N Y Acad Sci 1238:132–144 [View Article][PubMed]
    [Google Scholar]
  4. Cherepanov P. P., Wackernagel W. 1995; Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158:9–14 [View Article][PubMed]
    [Google Scholar]
  5. Clementz T., Zhou Z., Raetz C. R. 1997; Function of the Escherichia coli msbB gene, a multicopy suppressor of htrB knockouts, in the acylation of lipid A. Acylation by MsbB follows laurate incorporation by HtrB. J Biol Chem 272:10353–10360 [View Article][PubMed]
    [Google Scholar]
  6. Datsenko K. A., Wanner B. L. 2000; One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97:6640–6645 [View Article][PubMed]
    [Google Scholar]
  7. Eguchi M., Sekiya Y., Kikuchi Y., Takaya A., Yamamoto T., Matsui H. 2007a; Expressed Salmonella antigens within macrophages enhance the proliferation of CD4+ and CD8+ T lymphocytes by means of bystander dendritic cells. FEMS Immunol Med Microbiol 50:411–420 [View Article][PubMed]
    [Google Scholar]
  8. Eguchi M., Sekiya Y., Suzuki M., Yamamoto T., Matsui H. 2007b; An oral Salmonella vaccine promotes the down-regulation of cell surface Toll-like receptor 4 (TLR4) and TLR2 expression in mice. FEMS Immunol Med Microbiol 50:300–308 [View Article][PubMed]
    [Google Scholar]
  9. Eom J. S., Seok Kim J., Im Jang J., Kim B. H., Young Yoo S., Hyeon Choi J., Bang I. S., Lee I. S., Keun Park Y. 2013; Enhancement of host immune responses by oral vaccination to Salmonella enterica serovar Typhimurium harboring both FliC and FljB flagella. PLoS One 8:e74850 [View Article][PubMed]
    [Google Scholar]
  10. Fass E., Groisman E. A. 2009; Control of Salmonella pathogenicity island-2 gene expression. Curr Opin Microbiol 12:199–204 [View Article][PubMed]
    [Google Scholar]
  11. Germanier R., Füer E. 1975; Isolation and characterization of Gal E mutant Ty 21a of Salmonella typhi: a candidate strain for a live, oral typhoid vaccine. J Infect Dis 131:553–558 [View Article][PubMed]
    [Google Scholar]
  12. Gulig P. A., Curtiss R. III 1987; Plasmid-associated virulence of Salmonella typhimurium. Infect Immun 55:2891–2901[PubMed]
    [Google Scholar]
  13. Hassan J. O., Curtiss R. III 1990; Control of colonization by virulent Salmonella typhimurium by oral immunization of chickens with avirulent ΔcyaΔcrp S. typhimurium. Res Microbiol 141:839–850 [View Article][PubMed]
    [Google Scholar]
  14. Humphrey S., Macvicar T., Stevenson A., Roberts M., Humphrey T. J., Jepson M. A. 2011; SulA-induced filamentation in Salmonella enterica serovar Typhimurium: effects on SPI-1 expression and epithelial infection. J Appl Microbiol 111:185–196 [View Article][PubMed]
    [Google Scholar]
  15. Kodama C., Matsui H. 2004; Salmonella flagellin is not a dominant protective antigen in oral immunization with attenuated live vaccine strains. Infect Immun 72:2449–2451 [View Article][PubMed]
    [Google Scholar]
  16. Kodama C., Eguchi M., Sekiya Y., Yamamoto T., Kikuchi Y., Matsui H. 2005; Evaluation of the Lon-deficient Salmonella strain as an oral vaccine candidate. Microbiol Immunol 49:1035–1045 [View Article][PubMed]
    [Google Scholar]
  17. Lutkenhaus J., Addinall S. G. 1997; Bacterial cell division and the Z ring. Annu Rev Biochem 66:93–116 [View Article][PubMed]
    [Google Scholar]
  18. MacLennan C. A., Levine M. M. 2013; Invasive nontyphoidal Salmonella disease in Africa: current status. Expert Rev Anti Infect Ther 11:443–446 [View Article][PubMed]
    [Google Scholar]
  19. Mastroeni P., Ménager N. 2003; Development of acquired immunity to Salmonella. J Med Microbiol 52:453–459 [View Article][PubMed]
    [Google Scholar]
  20. Matsui H., Suzuki M., Isshiki Y., Kodama C., Eguchi M., Kikuchi Y., Motokawa K., Takaya A., Tomoyasu T., Yamamoto T. 2003; Oral immunization with ATP-dependent protease-deficient mutants protects mice against subsequent oral challenge with virulent Salmonella enterica serovar Typhimurium. Infect Immun 71:30–39 [View Article][PubMed]
    [Google Scholar]
  21. Matulova M., Havlickova H., Sisak F., Rychlik I. 2013; Vaccination of chickens with SPI1-lon and SPI1-lon-fliC mutant of Salmonella enterica serovar Enteritidis. PLoS One 8:e66172 [View Article][PubMed]
    [Google Scholar]
  22. McGhie E. J., Brawn L. C., Hume P. J., Humphreys D., Koronakis V. 2009; Salmonella takes control: effector-driven manipulation of the host. Curr Opin Microbiol 12:117–124 [View Article][PubMed]
    [Google Scholar]
  23. Mizel S. B., Bates J. T. 2010; Flagellin as an adjuvant: cellular mechanisms and potential. J Immunol 185:5677–5682 [View Article][PubMed]
    [Google Scholar]
  24. Nakamura M., Nagamine N., Norimatsu M., Suzuki S., Ohishi K., Kijima M., Tamura Y., Sato S. 1993; The ability of Salmonella enteritidis isolated from chicks imported from England to cause transovarian infection. J Vet Med Sci 55:135–136 [View Article][PubMed]
    [Google Scholar]
  25. Rabsch W., Tschäpe H., Bäumler A. J. 2001; Non-typhoidal salmonellosis: emerging problems. Microbes Infect 3:237–247 [View Article][PubMed]
    [Google Scholar]
  26. Ramos-Morales F. 2012; Impact of Salmonella enterica Type III secretion system effectors on the eukaryotic host cell. ISRN Cell Biol 2012:1–36 [View Article]
    [Google Scholar]
  27. Schmieger H. 1972; Phage P22-mutants with increased or decreased transduction abilities. Mol Gen Genet 119:75–88 [View Article][PubMed]
    [Google Scholar]
  28. Silva C. A., Blondel C. J., Quezada C. P., Porwollik S., Andrews-Polymenis H. L., Toro C. S., Zaldívar M., Contreras I., McClelland M., Santiviago C. A. 2012; Infection of mice by Salmonella enterica serovar Enteritidis involves additional genes that are absent in the genome of serovar Typhimurium. Infect Immun 80:839–849 [View Article][PubMed]
    [Google Scholar]
  29. Simon R., Tennant S. M., Galen J. E., Levine M. M. 2011a; Mouse models to assess the efficacy of non-typhoidal Salmonella vaccines: revisiting the role of host innate susceptibility and routes of challenge. Vaccine 29:5094–5106 [View Article][PubMed]
    [Google Scholar]
  30. Simon R., Tennant S. M., Wang J. Y., Schmidlein P. J., Lees A., Ernst R. K., Pasetti M. F., Galen J. E., Levine M. M. 2011b; Salmonella enterica serovar enteritidis core O polysaccharide conjugated to H : g,m flagellin as a candidate vaccine for protection against invasive infection with S. Enteritidis. Infect Immun 79:4240–4249 [View Article][PubMed]
    [Google Scholar]
  31. Simon R., Wang J. Y., Boyd M. A., Tulapurkar M. E., Ramachandran G., Tennant S. M., Pasetti M., Galen J. E., Levine M. M. 2013; Sustained protection in mice immunized with fractional doses of Salmonella Enteritidis core and O polysaccharide-flagellin glycoconjugates. PLoS One 8:e64680 [View Article][PubMed]
    [Google Scholar]
  32. Stocker B. A., Hoiseth S. K., Smith B. P. 1983; Aromatic-dependent “Salmonella sp.” as live vaccine in mice and calves. Dev Biol Stand 53:47–54[PubMed]
    [Google Scholar]
  33. Takaya A., Tomoyasu T., Tokumitsu A., Morioka M., Yamamoto T. 2002; The ATP-dependent Lon protease of Salmonella enterica serovar Typhimurium regulates invasion and expression of genes carried on Salmonella pathogenicity island 1. J Bacteriol 184:224–232 [View Article][PubMed]
    [Google Scholar]
  34. Tsolis R. M., Xavier M. N., Santos R. L., Bäumler A. J. 2011; How to become a top model: impact of animal experimentation on human Salmonella disease research. Infect Immun 79:1806–1814 [View Article][PubMed]
    [Google Scholar]
  35. Valdez Y., Grassl G. A., Guttman J. A., Coburn B., Gros P., Vallance B. A., Finlay B. B. 2009; Nramp1 drives an accelerated inflammatory response during Salmonella-induced colitis in mice. Cell Microbiol 11:351–362 [View Article][PubMed]
    [Google Scholar]
  36. Yamamoto T., Sashinami H., Takaya A., Tomoyasu T., Matsui H., Kikuchi Y., Hanawa T., Kamiya S., Nakane A. 2001; Disruption of the genes for ClpXP protease in Salmonella enterica serovar Typhimurium results in persistent infection in mice, and development of persistence requires endogenous gamma interferon and tumor necrosis factor alpha. Infect Immun 69:3164–3174 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.000014
Loading
/content/journal/jmm/10.1099/jmm.0.000014
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error