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. 1986 Apr;52(1):85–89. doi: 10.1128/iai.52.1.85-89.1986

Serotype-related HEp-2 cell interaction of Yersinia enterocolitica.

J Lassen, G Kapperud
PMCID: PMC262201  PMID: 2870030

Abstract

The ability of human clinical isolates of Yersinia enterocolitica to interact with HEp-2 cells was found to vary considerably between the serotypes O:3, O:8, and O:9. Although all three serotypes adhered initially to the cell surface, regardless of incubation temperature of the bacterial inoculum or presence of the 40- to 48-megadalton virulence plasmid, the ability to localize intracellularly was not uniformly expressed. By using a combined light optical method based on differential interference contrast and UV incident light microscopy, we found that in serotype O:3, resistance to internalization was dependent upon prior growth at 37 degrees C and carriage of the virulence plasmid; in serotype O:9, this property was plasmid dependent but not temperature dependent; in serotype O:8, it was constitutive. The ability of serotype O:3 to resist internalization was correlated with the expression of plasmid-associated fibrillae on the bacterial surface. No relationship between fibrillation and HEp-2 cell interaction was apparent for serotype O:8 or O:9. Serotypes O:8 and O:9, unlike the O:3 strains studied, associated with HEp-2 cells in greater number after cultivation at 22 degrees C than after cultivation at 37 degrees C. We failed to establish a correlation between the expression of surface fibrillae and the ability to evoke guinea pig conjunctivitis.

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Selected References

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  1. Allen R. D., David G. B., Nomarski G. The zeiss-Nomarski differential interference equipment for transmitted-light microscopy. Z Wiss Mikrosk. 1969 Nov;69(4):193–221. [PubMed] [Google Scholar]
  2. Aulisio C. C., Hill W. E., Stanfield J. T., Sellers R. L., Jr Evaluation of virulence factor testing and characteristics of pathogenicity in Yersinia enterocolitica. Infect Immun. 1983 Apr;40(1):330–335. doi: 10.1128/iai.40.1.330-335.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Birnboim H. C., Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. doi: 10.1093/nar/7.6.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bradford W. D., Noce P. S., Gutman L. T. Pathologic features of enteric infection with Yersinia enterocolitica. Arch Pathol. 1974 Jul;98(1):17–22. [PubMed] [Google Scholar]
  5. Bukholm G., Johansen B. V., Namork E., Lassen J. Bacterial adhesiveness and invasiveness in cell culture monolayer. Acta Pathol Microbiol Immunol Scand B. 1982 Dec;90(6):403–408. doi: 10.1111/j.1699-0463.1982.tb00138.x. [DOI] [PubMed] [Google Scholar]
  6. Bölin I., Norlander L., Wolf-Watz H. Temperature-inducible outer membrane protein of Yersinia pseudotuberculosis and Yersinia enterocolitica is associated with the virulence plasmid. Infect Immun. 1982 Aug;37(2):506–512. doi: 10.1128/iai.37.2.506-512.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bölin I., Portnoy D. A., Wolf-Watz H. Expression of the temperature-inducible outer membrane proteins of yersiniae. Infect Immun. 1985 Apr;48(1):234–240. doi: 10.1128/iai.48.1.234-240.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Carter P. B., Collins F. M. Experimental Yersinia enterocolitica infection in mice: kinetics of growth. Infect Immun. 1974 May;9(5):851–857. doi: 10.1128/iai.9.5.851-857.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Carter P. B. Pathogenecity of Yersinia enterocolitica for mice. Infect Immun. 1975 Jan;11(1):164–170. doi: 10.1128/iai.11.1.164-170.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Carter P. B., Zahorchak R. J., Brubaker R. R. Plague virulence antigens from Yersinia enterocolitica. Infect Immun. 1980 May;28(2):638–640. doi: 10.1128/iai.28.2.638-640.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gemski P., Lazere J. R., Casey T. Plasmid associated with pathogenicity and calcium dependency of Yersinia enterocolitica. Infect Immun. 1980 Feb;27(2):682–685. doi: 10.1128/iai.27.2.682-685.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Heesemann J., Algermissen B., Laufs R. Genetically manipulated virulence of Yersinia enterocolitica. Infect Immun. 1984 Oct;46(1):105–110. doi: 10.1128/iai.46.1.105-110.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Heesemann J., Keller C., Morawa R., Schmidt N., Siemens H. J., Laufs R. Plasmids of human strains of Yersinia enterocolitica: molecular relatedness and possible importance for pathogenesis. J Infect Dis. 1983 Jan;147(1):107–115. doi: 10.1093/infdis/147.1.107. [DOI] [PubMed] [Google Scholar]
  14. Kapperud G., Lassen J. Relationship of virulence-associated autoagglutination to hemagglutinin production in Yersinia enterocolitica and Yersinia enterocolitica-like bacteria. Infect Immun. 1983 Oct;42(1):163–169. doi: 10.1128/iai.42.1.163-169.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kapperud G., Namork E., Skarpeid H. J. Temperature-inducible surface fibrillae associated with the virulence plasmid of Yersinia enterocolitica and Yersinia pseudotuberculosis. Infect Immun. 1985 Feb;47(2):561–566. doi: 10.1128/iai.47.2.561-566.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kapperud G., Skarpeid H. J., Solberg R., Bergan T. Outer membrane proteins and plasmids in different Yersinia enterocolitica serogroups isolated from man and animals. Acta Pathol Microbiol Immunol Scand B. 1985 Feb;93(1):27–35. doi: 10.1111/j.1699-0463.1985.tb02847.x. [DOI] [PubMed] [Google Scholar]
  17. Kapperud G. Studies on the pathogenicity of Yersinia enterocolitica and Y. enterocolitica-like bacteria. 2. Interaction with HeLa cells among environmental and human isolates from Scandinavia. Acta Pathol Microbiol Scand B. 1980 Oct;88(5):293–297. [PubMed] [Google Scholar]
  18. Kapperud G. Yersinia enterocolitica and Yersinia like microbes isolated from mammals and water in Norway and Denmark. Acta Pathol Microbiol Scand B. 1977 Apr;85(2):129–135. doi: 10.1111/j.1699-0463.1977.tb01686.x. [DOI] [PubMed] [Google Scholar]
  19. Kronvall G., Myhre E. Differential staining of bacteria in clinical specimens using acridine orange buffered at low pH. Acta Pathol Microbiol Scand B. 1977 Aug;85(4):249–254. doi: 10.1111/j.1699-0463.1977.tb01970.x. [DOI] [PubMed] [Google Scholar]
  20. Lachica R. V., Zink D. L., Ferris W. R. Association of fibril structure formation with cell surface properties of Yersinia enterocolitica. Infect Immun. 1984 Oct;46(1):272–275. doi: 10.1128/iai.46.1.272-275.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Laird W. J., Cavanaugh D. C. Correlation of autoagglutination and virulence of yersiniae. J Clin Microbiol. 1980 Apr;11(4):430–432. doi: 10.1128/jcm.11.4.430-432.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lee W. H., McGrath P. P., Carter P. H., Eide E. L. The ability of some Yersinia enterocolitica strains to invade HeLa cells. Can J Microbiol. 1977 Dec;23(12):1714–1722. doi: 10.1139/m77-247. [DOI] [PubMed] [Google Scholar]
  23. Maclagan R. M., Old D. C. Haemagglutinins and fimbriae in different serotypes and biotypes of Yersinia enterocolitica. J Appl Bacteriol. 1980 Oct;49(2):353–360. doi: 10.1111/j.1365-2672.1980.tb05135.x. [DOI] [PubMed] [Google Scholar]
  24. Martinez R. J. Plasmid-mediated and temperature-regulated surface properties of Yersinia enterocolitica. Infect Immun. 1983 Sep;41(3):921–930. doi: 10.1128/iai.41.3.921-930.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Mors V., Pai C. H. Pathogenic properties of Yersinia enterocolitica. Infect Immun. 1980 Apr;28(1):292–294. doi: 10.1128/iai.28.1.292-294.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Mäki M., Vesikari T., Rantala I., Sundqvist C., Grönroos P. Pathogenicity of 42-44 Mdal plasmid positive and negative Yersinia pseudotuberculosis I and Yersinia enterocolitica 0:8 and 0:9 studied in the guinea pig eye model (Serény test). Acta Pathol Microbiol Immunol Scand B. 1983 Aug;91(4):241–244. doi: 10.1111/j.1699-0463.1983.tb00040.x. [DOI] [PubMed] [Google Scholar]
  27. Okamoto K., Inoue T., Ichikawa H., Kawamoto Y., Hara S., Miyama A. Adherence of Yersinia enterocolitica to mammalian epithelial cell lines. Microbiol Immunol. 1980;24(11):1013–1022. doi: 10.1111/j.1348-0421.1980.tb02907.x. [DOI] [PubMed] [Google Scholar]
  28. Old D. C., Adegbola R. A. Relationships among broad-spectrum and narrow-spectrum mannose-resistant fimbrial hemagglutinins in different Yersinia species. Microbiol Immunol. 1984;28(12):1303–1311. doi: 10.1111/j.1348-0421.1984.tb00788.x. [DOI] [PubMed] [Google Scholar]
  29. Old D. C., Robertson J. Adherence of fimbriate and non-fimbriate strains of Yersinia enterocolitica to human epithelial cells. Microbiol Immunol. 1981;25(10):993–998. doi: 10.1111/j.1348-0421.1981.tb00105.x. [DOI] [PubMed] [Google Scholar]
  30. Pai C. H., Mors V., Seemayer T. A. Experimental Yersinia enterocolitica enteritis in rabbits. Infect Immun. 1980 Apr;28(1):238–244. doi: 10.1128/iai.28.1.238-244.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Perry R. D., Brubaker R. R. Vwa+ phenotype of Yersinia enterocolitica. Infect Immun. 1983 Apr;40(1):166–171. doi: 10.1128/iai.40.1.166-171.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Portnoy D. A., Moseley S. L., Falkow S. Characterization of plasmids and plasmid-associated determinants of Yersinia enterocolitica pathogenesis. Infect Immun. 1981 Feb;31(2):775–782. doi: 10.1128/iai.31.2.775-782.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Portnoy D. A., Wolf-Watz H., Bolin I., Beeder A. B., Falkow S. Characterization of common virulence plasmids in Yersinia species and their role in the expression of outer membrane proteins. Infect Immun. 1984 Jan;43(1):108–114. doi: 10.1128/iai.43.1.108-114.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. SERENY B. Experimental keratoconjunctivitis shigellosa. Acta Microbiol Acad Sci Hung. 1957;4(4):367–376. [PubMed] [Google Scholar]
  35. Schiemann D. A., Devenish J. A. Relationship of HeLa cell infectivity to biochemical, serological, and virulence characteristics of Yersinia enterocolitica. Infect Immun. 1982 Feb;35(2):497–506. doi: 10.1128/iai.35.2.497-506.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Schiemann D. A., Devenish J. A. Virulence of Yersinia enterocolitica determined by lethality in Mongolian gerbils and by the Serény test. Infect Immun. 1980 Aug;29(2):500–506. doi: 10.1128/iai.29.2.500-506.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Skurnik M., Bölin I., Heikkinen H., Piha S., Wolf-Watz H. Virulence plasmid-associated autoagglutination in Yersinia spp. J Bacteriol. 1984 Jun;158(3):1033–1036. doi: 10.1128/jb.158.3.1033-1036.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Une T. Studies on the pathogenicity of Yersinia enterocolitica. I. Experimental infection in rabbits. Microbiol Immunol. 1977;21(7):341–363. [PubMed] [Google Scholar]
  39. Vesikari T., Nurmi T., Mäki M., Skurnik M., Sundqvist C., Granfors K., Grönroos P. Plasmids in Yersinia enterocolitica serotypes O:3 and O:9: correlation with epithelial cell adherence in vitro. Infect Immun. 1981 Sep;33(3):870–876. doi: 10.1128/iai.33.3.870-876.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Vesikari T., Sundqvist C., Mäki M. Adherence and toxicity of Yersinia enterocolitica 0:3 and 0:9 containing virulence-associated plasmids for various cultured cells. Acta Pathol Microbiol Immunol Scand B. 1983 Apr;91(2):121–127. doi: 10.1111/j.1699-0463.1983.tb00020.x. [DOI] [PubMed] [Google Scholar]
  41. Zink D. L., Feeley J. C., Wells J. G., Vanderzant C., Vickery J. C., Roof W. D., O'Donovan G. A. Plasmid-mediated tissue invasiveness in Yersinia enterocolitica. Nature. 1980 Jan 10;283(5743):224–226. doi: 10.1038/283224a0. [DOI] [PubMed] [Google Scholar]

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