Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1993 Jan;175(1):12–18. doi: 10.1128/jb.175.1.12-18.1993

Thin, aggregative fimbriae mediate binding of Salmonella enteritidis to fibronectin.

S K Collinson 1, P C Doig 1, J L Doran 1, S Clouthier 1, T J Trust 1, W W Kay 1
PMCID: PMC196092  PMID: 8093237

Abstract

The binding of human fibronectin and Congo red by an autoaggregative Salmonella enteritidis strain was found to be dependent on its ability to produce thin, aggregative fimbriae, named SEF 17 (for Salmonella enteritidis fimbriae with an apparent fimbrin molecular mass of 17 kDa). Two other fimbrial types produced by S. enteritidis, SEF 14 and SEF 21, were not responsible for the aggregative phenotype or for fibronectin binding. SEF 17-negative TnphoA mutants which retained the ability to produce SEF 14 and SEF 21 were unable to bind human fibronectin or Congo red and lost the ability to autoaggregate. Only purified SEF 17 but not purified SEF 14 or SEF 21 bound fibronectin in a solid-phase binding assay. Furthermore, only SEF 17 was able to inhibit fibronectin binding to S. enteritidis whole cells in a direct competition enzyme-linked immunosorbent assay. These results indicate that SEF 17 are the fimbriae responsible for binding fibronectin by this enteropathogen.

Full text

PDF
12

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aleksić S., Aleksić V. Reindarstellung und physikalisch-chemische Analyse des Fimbrien-Antigens bei zwei verschiedenen Enterobacteriaceae: Salmonella enteritidis und Yersinia enterocolitica. Zentralbl Bakteriol Orig A. 1979 Apr;243(2-3):177–196. [PubMed] [Google Scholar]
  2. Bhaduri S., Turner-Jones C., Lachica R. V. Convenient agarose medium for simultaneous determination of the low-calcium response and Congo red binding by virulent strains of Yersinia enterocolitica. J Clin Microbiol. 1991 Oct;29(10):2341–2344. doi: 10.1128/jcm.29.10.2341-2344.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Blake M. S., MacDonald C. M., Klugman K. P. Colony morphology of piliated Neisseria meningitidis. J Exp Med. 1989 Nov 1;170(5):1727–1736. doi: 10.1084/jem.170.5.1727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chan R. K., Botstein D., Watanabe T., Ogata Y. Specialized transduction of tetracycline resistance by phage P22 in Salmonella typhimurium. II. Properties of a high-frequency-transducing lysate. Virology. 1972 Dec;50(3):883–898. doi: 10.1016/0042-6822(72)90442-4. [DOI] [PubMed] [Google Scholar]
  5. Collinson S. K., Emödy L., Müller K. H., Trust T. J., Kay W. W. Purification and characterization of thin, aggregative fimbriae from Salmonella enteritidis. J Bacteriol. 1991 Aug;173(15):4773–4781. doi: 10.1128/jb.173.15.4773-4781.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Collinson S. K., Emödy L., Trust T. J., Kay W. W. Thin aggregative fimbriae from diarrheagenic Escherichia coli. J Bacteriol. 1992 Jul;174(13):4490–4495. doi: 10.1128/jb.174.13.4490-4495.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Courtney H. S., Simpson W. A., Beachey E. H. Binding of streptococcal lipoteichoic acid to fatty acid-binding sites on human plasma fibronectin. J Bacteriol. 1983 Feb;153(2):763–770. doi: 10.1128/jb.153.2.763-770.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Crichton P. B., Yakubu D. E., Old D. C., Clegg S. Immunological and genetical relatedness of type-1 and type-2 fimbriae in salmonellas of serotypes Gallinarum, Pullorum and Typhimurium. J Appl Bacteriol. 1989 Sep;67(3):283–291. doi: 10.1111/j.1365-2672.1989.tb02497.x. [DOI] [PubMed] [Google Scholar]
  9. Doig P., Emödy L., Trust T. J. Binding of laminin and fibronectin by the trypsin-resistant major structural domain of the crystalline virulence surface array protein of Aeromonas salmonicida. J Biol Chem. 1992 Jan 5;267(1):43–49. [PubMed] [Google Scholar]
  10. Duguid J. P., Anderson E. S., Campbell I. Fimbriae and adhesive properties in Salmonellae. J Pathol Bacteriol. 1966 Jul;92(1):107–138. doi: 10.1002/path.1700920113. [DOI] [PubMed] [Google Scholar]
  11. Emödy L., Heesemann J., Wolf-Watz H., Skurnik M., Kapperud G., O'Toole P., Wadström T. Binding to collagen by Yersinia enterocolitica and Yersinia pseudotuberculosis: evidence for yopA-mediated and chromosomally encoded mechanisms. J Bacteriol. 1989 Dec;171(12):6674–6679. doi: 10.1128/jb.171.12.6674-6679.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ernst R. K., Dombroski D. M., Merrick J. M. Anaerobiosis, type 1 fimbriae, and growth phase are factors that affect invasion of HEp-2 cells by Salmonella typhimurium. Infect Immun. 1990 Jun;58(6):2014–2016. doi: 10.1128/iai.58.6.2014-2016.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Evans D. G., Evans D. J., Jr, Tjoa W. Hemagglutination of human group A erythrocytes by enterotoxigenic Escherichia coli isolated from adults with diarrhea: correlation with colonization factor. Infect Immun. 1977 Nov;18(2):330–337. doi: 10.1128/iai.18.2.330-337.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Feutrier J., Kay W. W., Trust T. J. Purification and characterization of fimbriae from Salmonella enteritidis. J Bacteriol. 1986 Oct;168(1):221–227. doi: 10.1128/jb.168.1.221-227.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Fröman G., Switalski L. M., Faris A., Wadström T., Hök M. Binding of Escherichia coli to fibronectin. A mechanism of tissue adherence. J Biol Chem. 1984 Dec 10;259(23):14899–14905. [PubMed] [Google Scholar]
  16. Isberg R. R. Discrimination between intracellular uptake and surface adhesion of bacterial pathogens. Science. 1991 May 17;252(5008):934–938. doi: 10.1126/science.1674624. [DOI] [PubMed] [Google Scholar]
  17. Kay W. W., Phipps B. M., Ishiguro E. E., Trust T. J. Porphyrin binding by the surface array virulence protein of Aeromonas salmonicida. J Bacteriol. 1985 Dec;164(3):1332–1336. doi: 10.1128/jb.164.3.1332-1336.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kelly N. M., Kluftinger J. L., Pasloske B. L., Paranchych W., Hancock R. E. Pseudomonas aeruginosa pili as ligands for nonopsonic phagocytosis by fibronectin-stimulated macrophages. Infect Immun. 1989 Dec;57(12):3841–3845. doi: 10.1128/iai.57.12.3841-3845.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  20. Lindquist B. L., Lebenthal E., Lee P. C., Stinson M. W., Merrick J. M. Adherence of Salmonella typhimurium to small-intestinal enterocytes of the rat. Infect Immun. 1987 Dec;55(12):3044–3050. doi: 10.1128/iai.55.12.3044-3050.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Manoil C., Beckwith J. TnphoA: a transposon probe for protein export signals. Proc Natl Acad Sci U S A. 1985 Dec;82(23):8129–8133. doi: 10.1073/pnas.82.23.8129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Müller K. H., Collinson S. K., Trust T. J., Kay W. W. Type 1 fimbriae of Salmonella enteritidis. J Bacteriol. 1991 Aug;173(15):4765–4772. doi: 10.1128/jb.173.15.4765-4772.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Old D. C., Corneil I., Gibson L. F., Thomson A. D., Duguid J. P. Fimbriation, pellicle formation and the amount of growth of salmonellas in broth. J Gen Microbiol. 1968 Apr;51(1):1–16. doi: 10.1099/00221287-51-1-1. [DOI] [PubMed] [Google Scholar]
  24. Olsén A., Jonsson A., Normark S. Fibronectin binding mediated by a novel class of surface organelles on Escherichia coli. Nature. 1989 Apr 20;338(6217):652–655. doi: 10.1038/338652a0. [DOI] [PubMed] [Google Scholar]
  25. Omoike I., Lindquist B., Abud R., Merrick J., Lebenthal E. The effect of protein-energy malnutrition and refeeding on the adherence of Salmonella typhimurium to small intestinal mucosa and isolated enterocytes in rats. J Nutr. 1990 Apr;120(4):404–411. doi: 10.1093/jn/120.4.404. [DOI] [PubMed] [Google Scholar]
  26. Payne S. M., Finkelstein R. A. Detection and differentiation of iron-responsive avirulent mutants on Congo red agar. Infect Immun. 1977 Oct;18(1):94–98. doi: 10.1128/iai.18.1.94-98.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Rosner J. L. Formation, induction, and curing of bacteriophage P1 lysogens. Virology. 1972 Jun;48(3):679–689. doi: 10.1016/0042-6822(72)90152-3. [DOI] [PubMed] [Google Scholar]
  28. Stugard C. E., Daskaleros P. A., Payne S. M. A 101-kilodalton heme-binding protein associated with congo red binding and virulence of Shigella flexneri and enteroinvasive Escherichia coli strains. Infect Immun. 1989 Nov;57(11):3534–3539. doi: 10.1128/iai.57.11.3534-3539.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Swaney L. M., Liu Y. P., To C. M., To C. C., Ippen-Ihler K., Brinton C. C., Jr Isolation and characterization of Escherichia coli phase variants and mutants deficient in type 1 pilus production. J Bacteriol. 1977 Apr;130(1):495–505. doi: 10.1128/jb.130.1.495-505.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Tarkkanen A. M., Allen B. L., Westerlund B., Holthöfer H., Kuusela P., Risteli L., Clegg S., Korhonen T. K. Type V collagen as the target for type-3 fimbriae, enterobacterial adherence organelles. Mol Microbiol. 1990 Aug;4(8):1353–1361. doi: 10.1111/j.1365-2958.1990.tb00714.x. [DOI] [PubMed] [Google Scholar]
  31. Thorns C. J., Sojka M. G., Chasey D. Detection of a novel fimbrial structure on the surface of Salmonella enteritidis by using a monoclonal antibody. J Clin Microbiol. 1990 Nov;28(11):2409–2414. doi: 10.1128/jcm.28.11.2409-2414.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Valkonen K. H., Veijola J., Dagberg B., Uhlin B. E. Binding of basement-membrane laminin by Escherichia coli. Mol Microbiol. 1991 Sep;5(9):2133–2141. doi: 10.1111/j.1365-2958.1991.tb02143.x. [DOI] [PubMed] [Google Scholar]
  33. Westerlund B., Kuusela P., Risteli J., Risteli L., Vartio T., Rauvala H., Virkola R., Korhonen T. K. The O75X adhesin of uropathogenic Escherichia coli is a type IV collagen-binding protein. Mol Microbiol. 1989 Mar;3(3):329–337. doi: 10.1111/j.1365-2958.1989.tb00178.x. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES