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. 1984 Oct;46(1):105–110. doi: 10.1128/iai.46.1.105-110.1984

Genetically manipulated virulence of Yersinia enterocolitica.

J Heesemann, B Algermissen, R Laufs
PMCID: PMC261428  PMID: 6480101

Abstract

Mobilizable virulence plasmids of Yersinia enterocolitica of serotypes O:3 and O:9 were constructed by cointegration of a mobilizable vector into the virulence plasmids. The obtained cointegrates were mobilized into plasmidless Y. enterocolitica strains of serotypes O:3, O:5, O:8, and O:9. The transfer experiments revealed the existence of two different subgroups of plasmid-associated traits. (i) Animal virulence functions (mouse lethality and conjuctivitis provocation) were only transferable to plasmid-cured derivatives of virulent parent strains (serotypes O:3, O:8, and O:9), but they were not transferable to Y. enterocolitica antigen reference strains (serotypes O:3 and O:8) or to a plasmidless clinical isolate of serotype O:5. A further striking result was that a serotype O:8 strain regained the mouse lethality trait after receipt of a plasmid from a strain not lethal to mice. These results demonstrate that plasmid-mediated animal virulence functions are not uniformly expressed within Y. enterocolitica. (ii) The second subgroup of plasmid-mediated traits (calcium dependency, surface agglutinogens, HEp-2 cell adherence, and protein release) were transferable to all Y. enterocolitica recipient strains tested (serotypes O:3, O:5, O:8, and O:9 of different origin). For the first time HEp-2 cell adherence and temperature-induced release of five major protein species are described as transferable traits.

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Selected References

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  1. 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]
  2. BURROWS T. W. VIRULENCE OF PASTEURELLA PESTIS AND IMMUNITY TO PLAGUE. Ergeb Mikrobiol Immunitatsforsch Exp Ther. 1963;37:59–113. doi: 10.1007/978-3-662-36742-1_2. [DOI] [PubMed] [Google Scholar]
  3. Ben-Gurion R., Shafferman A. Essential virulence determinants of different Yersinia species are carried on a common plasmid. Plasmid. 1981 Mar;5(2):183–187. doi: 10.1016/0147-619x(81)90019-6. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Brubaker R. R. The genus Yersinia: biochemistry and genetics of virulence. Curr Top Microbiol Immunol. 1972;57:111–158. doi: 10.1007/978-3-642-65297-4_4. [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., Wolf-Watz H. Molecular cloning of the temperature-inducible outer membrane protein 1 of Yersinia pseudotuberculosis. Infect Immun. 1984 Jan;43(1):72–78. doi: 10.1128/iai.43.1.72-78.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Dagert M., Ehrlich S. D. Prolonged incubation in calcium chloride improves the competence of Escherichia coli cells. Gene. 1979 May;6(1):23–28. doi: 10.1016/0378-1119(79)90082-9. [DOI] [PubMed] [Google Scholar]
  10. Ditta G., Stanfield S., Corbin D., Helinski D. R. Broad host range DNA cloning system for gram-negative bacteria: construction of a gene bank of Rhizobium meliloti. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7347–7351. doi: 10.1073/pnas.77.12.7347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Doyle M. P., Hugdahl M. B., Chang M. T., Beery J. T. Serological relatedness of mouse-virulent Yersinia enterocolitica. Infect Immun. 1982 Sep;37(3):1234–1240. doi: 10.1128/iai.37.3.1234-1240.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ferber D. M., Brubaker R. R. Plasmids in Yersinia pestis. Infect Immun. 1981 Feb;31(2):839–841. doi: 10.1128/iai.31.2.839-841.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gankema H., Wensink J., Guinée P. A., Jansen W. H., Witholt B. Some characteristics of the outer membrane material released by growing enterotoxigenic Escherichia coli. Infect Immun. 1980 Aug;29(2):704–713. doi: 10.1128/iai.29.2.704-713.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Gemski P., Lazere J. R., Casey T., Wohlhieter J. A. Presence of a virulence-associated plasmid in Yersinia pseudotuberculosis. Infect Immun. 1980 Jun;28(3):1044–1047. doi: 10.1128/iai.28.3.1044-1047.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. HIGUCHI K., SMITH J. L. Studies on the nutrition and physiology of Pasteurella pestis. VI. A differential plating medium for the estimation of the mutation rate to avirulence. J Bacteriol. 1961 Apr;81:605–608. doi: 10.1128/jb.81.4.605-608.1961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Heesemann J., Laufs R. Construction of a mobilizable Yersinia enterocolitica virulence plasmid. J Bacteriol. 1983 Aug;155(2):761–767. doi: 10.1128/jb.155.2.761-767.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. LAWTON W. D., ERDMAN R. L., SURGALLA M. J. BIOSYNTHESIS AND PURIFICATION OF V AND W ANTIGEN IN PASTEURELLA PESTIS. J Immunol. 1963 Aug;91:179–184. doi: 10.21236/ad0299868. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Lee W. H., Smith R. E., Damaré J. M., Harris M. E., Johnston R. W. Evaluation of virulence test procedures for Yersinia enterocolitica recovered from foods. J Appl Bacteriol. 1981 Jun;50(3):529–539. doi: 10.1111/j.1365-2672.1981.tb04255.x. [DOI] [PubMed] [Google Scholar]
  22. Meyers J. A., Sanchez D., Elwell L. P., Falkow S. Simple agarose gel electrophoretic method for the identification and characterization of plasmid deoxyribonucleic acid. J Bacteriol. 1976 Sep;127(3):1529–1537. doi: 10.1128/jb.127.3.1529-1537.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. Pai C. H., DeStephano L. Serum resistance associated with virulence in Yersinia enterocolitica. Infect Immun. 1982 Feb;35(2):605–611. doi: 10.1128/iai.35.2.605-611.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. Peterson G. L. A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal Biochem. 1977 Dec;83(2):346–356. doi: 10.1016/0003-2697(77)90043-4. [DOI] [PubMed] [Google Scholar]
  27. Portnoy D. A., Blank H. F., Kingsbury D. T., Falkow S. Genetic analysis of essential plasmid determinants of pathogenicity in Yersinia pestis. J Infect Dis. 1983 Aug;148(2):297–304. doi: 10.1093/infdis/148.2.297. [DOI] [PubMed] [Google Scholar]
  28. Portnoy D. A., Falkow S. Virulence-associated plasmids from Yersinia enterocolitica and Yersinia pestis. J Bacteriol. 1981 Dec;148(3):877–883. doi: 10.1128/jb.148.3.877-883.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. 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]
  31. Quinnan G. V., Schooley R., Dolin R., Ennis F. A., Gross P., Gwaltney J. M. Serologic responses and systemic reactions in adults after vaccination with monovalent A/USSR/77 and trivalent A/USSR/77, A/Texas/77, B/Hong Kong/72 influenza vaccines. Rev Infect Dis. 1983 Jul-Aug;5(4):748–757. doi: 10.1093/clinids/5.4.748. [DOI] [PubMed] [Google Scholar]
  32. SERENY B. Experimental shigella keratoconjunctivitis; a preliminary report. Acta Microbiol Acad Sci Hung. 1955;2(3):293–296. [PubMed] [Google Scholar]
  33. Sansonetti P. J., Hale T. L., Dammin G. J., Kapfer C., Collins H. H., Jr, Formal S. B. Alterations in the pathogenicity of Escherichia coli K-12 after transfer of plasmid and chromosomal genes from Shigella flexneri. Infect Immun. 1983 Mar;39(3):1392–1402. doi: 10.1128/iai.39.3.1392-1402.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Straley S. C., Brubaker R. R. Cytoplasmic and membrane proteins of yersiniae cultivated under conditions simulating mammalian intracellular environment. Proc Natl Acad Sci U S A. 1981 Feb;78(2):1224–1228. doi: 10.1073/pnas.78.2.1224. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. 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]
  36. 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]
  37. 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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