Abstract
The two enteropathogens Yersinia pseudotuberculosis and Yersinia enterocolitica penetrate eukaryotic cells in vitro through invasin, a surface-exposed protein. In contrast, Yersinia pestis, the causative agent of plague, is unable to enter mammalian cell lines, although the inv gene is present on its chromosome. Although 99.3% identical to the inv gene of Y. pseudotuberculosis, the Y. pestis inv gene was disrupted in its central region by a 708-bp IS200-like element. Multiple copies of this insertion sequence element were found within the genome of the plague bacillus.
Full Text
The Full Text of this article is available as a PDF (323.1 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bisercić M., Ochman H. Natural populations of Escherichia coli and Salmonella typhimurium harbor the same classes of insertion sequences. Genetics. 1993 Mar;133(3):449–454. doi: 10.1093/genetics/133.3.449. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bisercić M., Ochman H. The ancestry of insertion sequences common to Escherichia coli and Salmonella typhimurium. J Bacteriol. 1993 Dec;175(24):7863–7868. doi: 10.1128/jb.175.24.7863-7868.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brubaker R. R. Factors promoting acute and chronic diseases caused by yersiniae. Clin Microbiol Rev. 1991 Jul;4(3):309–324. doi: 10.1128/cmr.4.3.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dower W. J., Miller J. F., Ragsdale C. W. High efficiency transformation of E. coli by high voltage electroporation. Nucleic Acids Res. 1988 Jul 11;16(13):6127–6145. doi: 10.1093/nar/16.13.6127. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Fetherston J. D., Perry R. D. The pigmentation locus of Yersinia pestis KIM6+ is flanked by an insertion sequence and includes the structural genes for pesticin sensitivity and HMWP2. Mol Microbiol. 1994 Aug;13(4):697–708. doi: 10.1111/j.1365-2958.1994.tb00463.x. [DOI] [PubMed] [Google Scholar]
- Fetherston J. D., Schuetze P., Perry R. D. Loss of the pigmentation phenotype in Yersinia pestis is due to the spontaneous deletion of 102 kb of chromosomal DNA which is flanked by a repetitive element. Mol Microbiol. 1992 Sep;6(18):2693–2704. doi: 10.1111/j.1365-2958.1992.tb01446.x. [DOI] [PubMed] [Google Scholar]
- Galán J. E., Ginocchio C., Costeas P. Molecular and functional characterization of the Salmonella invasion gene invA: homology of InvA to members of a new protein family. J Bacteriol. 1992 Jul;174(13):4338–4349. doi: 10.1128/jb.174.13.4338-4349.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gibert I., Barbé J., Casadesús J. Distribution of insertion sequence IS200 in Salmonella and Shigella. J Gen Microbiol. 1990 Dec;136(12):2555–2560. doi: 10.1099/00221287-136-12-2555. [DOI] [PubMed] [Google Scholar]
- Ginocchio C., Pace J., Galán J. E. Identification and molecular characterization of a Salmonella typhimurium gene involved in triggering the internalization of salmonellae into cultured epithelial cells. Proc Natl Acad Sci U S A. 1992 Jul 1;89(13):5976–5980. doi: 10.1073/pnas.89.13.5976. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Guiyoule A., Grimont F., Iteman I., Grimont P. A., Lefèvre M., Carniel E. Plague pandemics investigated by ribotyping of Yersinia pestis strains. J Clin Microbiol. 1994 Mar;32(3):634–641. doi: 10.1128/jcm.32.3.634-641.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Isberg R. R., Falkow S. A single genetic locus encoded by Yersinia pseudotuberculosis permits invasion of cultured animal cells by Escherichia coli K-12. Nature. 1985 Sep 19;317(6034):262–264. doi: 10.1038/317262a0. [DOI] [PubMed] [Google Scholar]
- Isberg R. R., Leong J. M. Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell. 1990 Mar 9;60(5):861–871. doi: 10.1016/0092-8674(90)90099-z. [DOI] [PubMed] [Google Scholar]
- Isberg R. R. Mammalian cell adhesion functions and cellular penetration of enteropathogenic Yersinia species. Mol Microbiol. 1989 Oct;3(10):1449–1453. doi: 10.1111/j.1365-2958.1989.tb00128.x. [DOI] [PubMed] [Google Scholar]
- Isberg R. R., Voorhis D. L., Falkow S. Identification of invasin: a protein that allows enteric bacteria to penetrate cultured mammalian cells. Cell. 1987 Aug 28;50(5):769–778. doi: 10.1016/0092-8674(87)90335-7. [DOI] [PubMed] [Google Scholar]
- Lam S., Roth J. R. IS200: a Salmonella-specific insertion sequence. Cell. 1983 Oct;34(3):951–960. doi: 10.1016/0092-8674(83)90552-4. [DOI] [PubMed] [Google Scholar]
- Lam S., Roth J. R. Structural and functional studies of insertion element IS200. J Mol Biol. 1986 Jan 20;187(2):157–167. doi: 10.1016/0022-2836(86)90225-1. [DOI] [PubMed] [Google Scholar]
- Leong J. M., Fournier R. S., Isberg R. R. Identification of the integrin binding domain of the Yersinia pseudotuberculosis invasin protein. EMBO J. 1990 Jun;9(6):1979–1989. doi: 10.1002/j.1460-2075.1990.tb08326.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Miller V. L., Falkow S. Evidence for two genetic loci in Yersinia enterocolitica that can promote invasion of epithelial cells. Infect Immun. 1988 May;56(5):1242–1248. doi: 10.1128/iai.56.5.1242-1248.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Miller V. L., Farmer J. J., 3rd, Hill W. E., Falkow S. The ail locus is found uniquely in Yersinia enterocolitica serotypes commonly associated with disease. Infect Immun. 1989 Jan;57(1):121–131. doi: 10.1128/iai.57.1.121-131.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Motin V. L., Pokrovskaya M. S., Telepnev M. V., Kutyrev V. V., Vidyaeva N. A., Filippov A. A., Smirnov G. B. The difference in the lcrV sequences between Y. pestis and Y. pseudotuberculosis and its application for characterization of Y. pseudotuberculosis strains. Microb Pathog. 1992 Mar;12(3):165–175. doi: 10.1016/0882-4010(92)90050-x. [DOI] [PubMed] [Google Scholar]
- O'Reilly C., Black G. W., Laffey R., McConnell D. J. Molecular analysis of an IS200 insertion in the gpt gene of Salmonella typhimurium LT2. J Bacteriol. 1990 Nov;172(11):6599–6601. doi: 10.1128/jb.172.11.6599-6601.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pepe J. C., Miller V. L. Yersinia enterocolitica invasin: a primary role in the initiation of infection. Proc Natl Acad Sci U S A. 1993 Jul 15;90(14):6473–6477. doi: 10.1073/pnas.90.14.6473. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Podladchikova O. N., Dikhanov G. G., Rakin A. V., Heesemann J. Nucleotide sequence and structural organization of Yersinia pestis insertion sequence IS100. FEMS Microbiol Lett. 1994 Sep 1;121(3):269–274. doi: 10.1111/j.1574-6968.1994.tb07111.x. [DOI] [PubMed] [Google Scholar]
- Protsenko O. A., Anisimov P. I., Mozharov O. T., Konnov N. P., Popov Iu A. Vyiavlenie i kharakteristika plazmid chumnogo mikroba, determiniruiushchikh sintez pestitsina I, antigena fraktsiia I i ékzotoksina "myshinogo" toksina. Genetika. 1983 Jul;19(7):1081–1090. [PubMed] [Google Scholar]
- Rosqvist R., Skurnik M., Wolf-Watz H. Increased virulence of Yersinia pseudotuberculosis by two independent mutations. Nature. 1988 Aug 11;334(6182):522–524. doi: 10.1038/334522a0. [DOI] [PubMed] [Google Scholar]
- Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sikkema D. J., Brubaker R. R. Resistance to pesticin, storage of iron, and invasion of HeLa cells by Yersiniae. Infect Immun. 1987 Mar;55(3):572–578. doi: 10.1128/iai.55.3.572-578.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Simonet M., Falkow S. Invasin expression in Yersinia pseudotuberculosis. Infect Immun. 1992 Oct;60(10):4414–4417. doi: 10.1128/iai.60.10.4414-4417.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Skurnik M., Wolf-Watz H. Analysis of the yopA gene encoding the Yop1 virulence determinants of Yersinia spp. Mol Microbiol. 1989 Apr;3(4):517–529. doi: 10.1111/j.1365-2958.1989.tb00198.x. [DOI] [PubMed] [Google Scholar]
- Sodeinde O. A., Subrahmanyam Y. V., Stark K., Quan T., Bao Y., Goguen J. D. A surface protease and the invasive character of plague. Science. 1992 Nov 6;258(5084):1004–1007. doi: 10.1126/science.1439793. [DOI] [PubMed] [Google Scholar]
- Straley S. C., Cibull M. L. Differential clearance and host-pathogen interactions of YopE- and YopK- YopL- Yersinia pestis in BALB/c mice. Infect Immun. 1989 Apr;57(4):1200–1210. doi: 10.1128/iai.57.4.1200-1210.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Straley S. C., Skrzypek E., Plano G. V., Bliska J. B. Yops of Yersinia spp. pathogenic for humans. Infect Immun. 1993 Aug;61(8):3105–3110. doi: 10.1128/iai.61.8.3105-3110.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Young V. B., Miller V. L., Falkow S., Schoolnik G. K. Sequence, localization and function of the invasin protein of Yersinia enterocolitica. Mol Microbiol. 1990 Jul;4(7):1119–1128. doi: 10.1111/j.1365-2958.1990.tb00686.x. [DOI] [PubMed] [Google Scholar]