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PMID: 10655518 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

A role for Salmonella fimbriae in intraperitoneal infections.

Edwards RA, Schifferli DM, Maloy SR

Abstract

Enteric bacteria possess multiple fimbriae, many of which play critical roles in attachment to epithelial cell surfaces. SEF14 fimbriae are only found in Salmonella enterica serovar Enteritidis (S. enteritidis) and closely related serovars, suggesting that SEF14 fimbriae may affect serovar-specific virulence traits. Despite evidence that SEF14 fimbriae are expressed by S. enteritidis in vivo, previous studies showed that SEF14 fimbriae do not mediate adhesion to the intestinal epithelium. Therefore, we tested whether SEF14 fimbriae are required for virulence at a stage in infection after the bacteria have passed the intestinal barrier. Polar mutations that disrupt the entire sef operon decreased virulence in mice more than 1,000-fold. Nonpolar mutations that disrupted sefA (encoding the major structural subunit) did not affect virulence, but mutations that disrupted sefD (encoding the putative adhesion subunit) resulted in a severe virulence defect. The results indicate that the putative SEF14 adhesion subunit is specifically required for a stage of the infection subsequent to transit across the intestinal barrier. Therefore, we tested whether SefD is required for uptake or survival in macrophages. The majority of wild-type bacteria were detected inside macrophages soon after i.p. infection, but the sefD mutants were not readily internalized by peritoneal macrophages. These results indicate that the potential SEF14 adhesion subunit is essential for efficient uptake or survival of S. enteritidis in macrophages. This report describes a role of fimbriae in intracellular infection, and indicates that fimbriae may be required for systemic infections at stages beyond the initial colonization of host epithelial surfaces.

MeSH Terms
Animals Bacterial Adhesion/physiology Bacterial Proteins/genetics,physiology Cell Adhesion Molecules/genetics,physiology Female Fimbriae Proteins Fimbriae, Bacterial/physiology Liver/microbiology Mice Mice, Inbred BALB C Models, Biological Molecular Chaperones/genetics,physiology Operon Peritonitis/microbiology Phagocytosis Salmonella Infections, Animal/microbiology Salmonella enteritidis/physiology Spleen/microbiology Virulence
Chemicals
Bacterial Proteins Cell Adhesion Molecules Molecular Chaperones SefD protein, Salmonella sefA protein, Salmonella enteritidis sefB protein, Salmonella sefC protein, Salmonella enteritidis Fimbriae Proteins
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Edwards R A
Department of Microbiology, University of Illinois at Urbana-Champaign, B103 Chemical and Life Sciences Building, 601 S. Goodwin Avenue, Urbana, IL 61801, USA. [email protected]
Schifferli D M
Maloy S R
References (31)
31 references, click to expand
  1. Inhibition of macrophage phagosome-lysosome fusion by Salmonella typhimurium.
    Infect Immun. 1991 Jul;59(7):2232-8 PMID: 2050395
  2. X-ray structure of the FimC-FimH chaperone-adhesin complex from uropathogenic Escherichia coli.
    Science. 1999 Aug 13;285(5430):1061-6 PMID: 10446051
  3. A 'safe-site' for Salmonella typhimurium is within splenic cells during the early phase of infection in mice.
    Microb Pathog. 1991 Apr;10(4):297-310 PMID: 1895929
  4. Salmonella choleraesuis and Salmonella typhimurium associated with liver cells after intravenous inoculation of rats are localized mainly in Kupffer cells and multiply intracellularly.
    Infect Immun. 1992 Jul;60(7):2758-68 PMID: 1612743
  5. Characterization of three fimbrial genes, sefABC, of Salmonella enteritidis.
    J Bacteriol. 1993 May;175(9):2523-33 PMID: 8097515
  6. Yersinia pestis pH 6 antigen forms fimbriae and is induced by intracellular association with macrophages.
    Mol Microbiol. 1993 Apr;8(2):311-24 PMID: 8100346
  7. Monoclonal antibody-based detection system for Salmonella enteritidis.
    Avian Dis. 1993 Apr-Jun;37(2):501-7 PMID: 8363514
  8. Passive immunisation against experimental salmonellosis in mice by orally administered hen egg-yolk antibodies specific for 14-kDa fimbriae of Salmonella enteritidis.
    J Med Microbiol. 1994 Jul;41(1):29-35 PMID: 7911840
  9. A Salmonella enteritidis 11RX pilin induces strong T-lymphocyte responses.
    Infect Immun. 1994 Dec;62(12):5376-83 PMID: 7960117
  10. FimH adhesin of type 1 pili is assembled into a fibrillar tip structure in the Enterobacteriaceae.
    Proc Natl Acad Sci U S A. 1995 Mar 14;92(6):2081-5 PMID: 7892228
  11. Genomic structure, promoter sequence, and induction of expression of the mouse Nramp1 gene in macrophages.
    Genomics. 1995 May 1;27(1):9-19 PMID: 7665187
  12. Host restriction phenotypes of Salmonella typhi and Salmonella gallinarum.
    Infect Immun. 1995 Nov;63(11):4329-35 PMID: 7591067
  13. The pef fimbrial operon of Salmonella typhimurium mediates adhesion to murine small intestine and is necessary for fluid accumulation in the infant mouse.
    Infect Immun. 1996 Jan;64(1):61-8 PMID: 8557375
  14. The lpf fimbrial operon mediates adhesion of Salmonella typhimurium to murine Peyer's patches.
    Proc Natl Acad Sci U S A. 1996 Jan 9;93(1):279-83 PMID: 8552622
  15. Neutrophils prevent extracellular colonization of the liver microvasculature by Salmonella typhimurium.
    Infect Immun. 1996 Mar;64(3):1043-7 PMID: 8641757
  16. The psa locus is responsible for thermoinducible binding of Yersinia pseudotuberculosis to cultured cells.
    Infect Immun. 1996 Jul;64(7):2483-9 PMID: 8698470
  17. Studies into the role of the SEF14 fimbrial antigen in the pathogenesis of Salmonella enteritidis.
    Microb Pathog. 1996 Apr;20(4):235-46 PMID: 8737493
  18. A possible mechanism for host-specific pathogenesis of Salmonella serovars.
    Microb Pathog. 1996 Dec;21(6):435-46 PMID: 8971684
  19. Critical roles of neutrophils in host defense against experimental systemic infections of mice by Listeria monocytogenes, Salmonella typhimurium, and Yersinia enterocolitica.
    Infect Immun. 1997 Feb;65(2):630-5 PMID: 9009323
  20. Role of SefA subunit protein of SEF14 fimbriae in the pathogenesis of Salmonella enterica serovar Enteritidis.
    Infect Immun. 1997 Feb;65(2):708-17 PMID: 9009334
  21. Transduction of low-copy number plasmids by bacteriophage P22.
    Genetics. 1997 Jun;146(2):447-56 PMID: 9177996
  22. Fimbrial adhesins of Salmonella typhimurium. Role in bacterial interactions with epithelial cells.
    Adv Exp Med Biol. 1997;412:149-58 PMID: 9192007
  23. Murine salmonellosis studied by confocal microscopy: Salmonella typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effect on phagocytes in vivo.
    J Exp Med. 1997 Aug 18;186(4):569-80 PMID: 9254655
  24. Survival of FimH-expressing enterobacteria in macrophages relies on glycolipid traffic.
    Nature. 1997 Oct 9;389(6651):636-9 PMID: 9335508
  25. Improved allelic exchange vectors and their use to analyze 987P fimbria gene expression.
    Gene. 1998 Jan 30;207(2):149-57 PMID: 9511756
  26. The crucial role of polymorphonuclear leukocytes in resistance to Salmonella dublin infections in genetically susceptible and resistant mice.
    Proc Natl Acad Sci U S A. 1998 Jun 23;95(13):7676-81 PMID: 9636209
  27. Fimbrial expression in enteric bacteria: a critical step in intestinal pathogenesis.
    Trends Microbiol. 1998 Jul;6(7):282-7 PMID: 9717217
  28. Differential effects of integrin alpha chain mutations on invasin and natural ligand interaction.
    J Biol Chem. 1998 Nov 27;273(48):31837-43 PMID: 9822651
  29. Fimbriae- and flagella-mediated association with and invasion of cultured epithelial cells by Salmonella enteritidis.
    Microbiology. 1999 May;145 ( Pt 5):1023-31 PMID: 10376817
  30. Structural basis of chaperone function and pilus biogenesis.
    Science. 1999 Aug 13;285(5430):1058-61 PMID: 10446050
  31. Type 1 fimbriae of Salmonella enteritidis.
    J Bacteriol. 1991 Aug;173(15):4765-72 PMID: 1677356
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2000-02-01
Pages
1258-62
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC15588
Subset
IM
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