Abstract
Yersinia enterocolitica is the causative agent of a variety of gastrointestinal syndromes ranging from acute enteritis to mesenteric lymphadenitis. In addition, systemic infections resulting in high mortality rates can occur in elderly and immunocompromised patients. More than 50 serotypes of Y. enterocolitica have been identified, but only a few of them commonly cause disease in otherwise healthy hosts. Those serotypes that cause disease have been divided into two groups, American and non-American, based on their geographical distributions, biotypes, and pathogenicity. We have been studying two genes, inv and ail, from Y. enterocolitica that confer in tissue culture assays an invasive phenotype that strongly correlates with virulence. Some differences between the American and non-American serotypes at the ail locus were noted previously and have been investigated further in this report. The ail locus was cloned from seven Y. enterocolitica strains (seven different serotypes). Although the different clones produced similar amounts of Ail, the product of the ail gene from non-American serotypes (AilNA) was less able to promote invasion by Escherichia coli than was the product of the ail gene from American serotypes (AilA). This difference is probably due to one or more of the eight amino acid changes found in the derived amino acid sequence for the mature form of AilNA compared with that of AilA. Seven of these changes are predicted to be in cell surface domains of the protein (a model for the proposed folding of Ail within the outer membrane is presented). These results are discussed in relation to the growing family of outer membrane proteins, which includes Lom from bacteriophage lambda, PagC from salmonella typhimurium, and OmpX from Enterobacter cloacae.
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- Bachmann B. J. Pedigrees of some mutant strains of Escherichia coli K-12. Bacteriol Rev. 1972 Dec;36(4):525–557. doi: 10.1128/br.36.4.525-557.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baker P. M., Farmer J. J., 3rd New bacteriophage typing system for Yersinia enterocolitica, Yersinia kristensenii, Yersinia frederiksenii, and Yersinia intermedia: correlation with serotyping, biotyping, and antibiotic susceptibility. J Clin Microbiol. 1982 Mar;15(3):491–502. doi: 10.1128/jcm.15.3.491-502.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Barondess J. J., Beckwith J. A bacterial virulence determinant encoded by lysogenic coliphage lambda. Nature. 1990 Aug 30;346(6287):871–874. doi: 10.1038/346871a0. [DOI] [PubMed] [Google Scholar]
- Bissett M. L., Powers C., Abbott S. L., Janda J. M. Epidemiologic investigations of Yersinia enterocolitica and related species: sources, frequency, and serogroup distribution. J Clin Microbiol. 1990 May;28(5):910–912. doi: 10.1128/jcm.28.5.910-912.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Blake M. S., Johnston K. H., Russell-Jones G. J., Gotschlich E. C. A rapid, sensitive method for detection of alkaline phosphatase-conjugated anti-antibody on Western blots. Anal Biochem. 1984 Jan;136(1):175–179. doi: 10.1016/0003-2697(84)90320-8. [DOI] [PubMed] [Google Scholar]
- Bottone E. J. Current trends of Yersinia enterocolitica isolates in the New York City area. J Clin Microbiol. 1983 Jan;17(1):63–67. doi: 10.1128/jcm.17.1.63-67.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bottone E. J. Yersinia enterocolitica: a panoramic view of a charismatic microorganism. CRC Crit Rev Microbiol. 1977;5(2):211–241. doi: 10.3109/10408417709102312. [DOI] [PubMed] [Google Scholar]
- Bufill J. A., Ritch P. S. Yersinia enterocolitica serotype 0:3 sepsis after blood transfusion. N Engl J Med. 1989 Mar 23;320(12):810–810. doi: 10.1056/NEJM198903233201220. [DOI] [PubMed] [Google Scholar]
- Burnette W. N. "Western blotting": electrophoretic transfer of proteins from sodium dodecyl sulfate--polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal Biochem. 1981 Apr;112(2):195–203. doi: 10.1016/0003-2697(81)90281-5. [DOI] [PubMed] [Google Scholar]
- Carniel E., Mazigh D., Mollaret H. H. Expression of iron-regulated proteins in Yersinia species and their relation to virulence. Infect Immun. 1987 Jan;55(1):277–280. doi: 10.1128/iai.55.1.277-280.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Carniel E., Mercereau-Puijalon O., Bonnefoy S. The gene coding for the 190,000-dalton iron-regulated protein of Yersinia species is present only in the highly pathogenic strains. Infect Immun. 1989 Apr;57(4):1211–1217. doi: 10.1128/iai.57.4.1211-1217.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cornelis G., Laroche Y., Balligand G., Sory M. P., Wauters G. Yersinia enterocolitica, a primary model for bacterial invasiveness. Rev Infect Dis. 1987 Jan-Feb;9(1):64–87. doi: 10.1093/clinids/9.1.64. [DOI] [PubMed] [Google Scholar]
- Cover T. L., Aber R. C. Yersinia enterocolitica. N Engl J Med. 1989 Jul 6;321(1):16–24. doi: 10.1056/NEJM198907063210104. [DOI] [PubMed] [Google Scholar]
- Delor I., Kaeckenbeeck A., Wauters G., Cornelis G. R. Nucleotide sequence of yst, the Yersinia enterocolitica gene encoding the heat-stable enterotoxin, and prevalence of the gene among pathogenic and nonpathogenic yersiniae. Infect Immun. 1990 Sep;58(9):2983–2988. doi: 10.1128/iai.58.9.2983-2988.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Eisenberg D., Schwarz E., Komaromy M., Wall R. Analysis of membrane and surface protein sequences with the hydrophobic moment plot. J Mol Biol. 1984 Oct 15;179(1):125–142. doi: 10.1016/0022-2836(84)90309-7. [DOI] [PubMed] [Google Scholar]
- Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
- 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]
- Gergen J. P., Stern R. H., Wensink P. C. Filter replicas and permanent collections of recombinant DNA plasmids. Nucleic Acids Res. 1979 Dec 20;7(8):2115–2136. doi: 10.1093/nar/7.8.2115. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ichinohe H., Yoshioka M., Fukushima H., Kaneko S., Maruyama T. First isolation of Yersinia enterocolitica serotype O:8 in Japan. J Clin Microbiol. 1991 Apr;29(4):846–847. doi: 10.1128/jcm.29.4.846-847.1991. [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., 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]
- Janot C., Briquel M. E., Streiff F., Burdin J. C. Infectious complications due to transfusion acquired Yersinia enterocolitica. Transfusion. 1989 May;29(4):372–373. doi: 10.1046/j.1537-2995.1989.29489242811.x. [DOI] [PubMed] [Google Scholar]
- 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]
- Lee L. A., Gerber A. R., Lonsway D. R., Smith J. D., Carter G. P., Puhr N. D., Parrish C. M., Sikes R. K., Finton R. J., Tauxe R. V. Yersinia enterocolitica O:3 infections in infants and children, associated with the household preparation of chitterlings. N Engl J Med. 1990 Apr 5;322(14):984–987. doi: 10.1056/NEJM199004053221407. [DOI] [PubMed] [Google Scholar]
- 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]
- Mekalanos J. J. Duplication and amplification of toxin genes in Vibrio cholerae. Cell. 1983 Nov;35(1):253–263. doi: 10.1016/0092-8674(83)90228-3. [DOI] [PubMed] [Google Scholar]
- Miller S. I., Kukral A. M., Mekalanos J. J. A two-component regulatory system (phoP phoQ) controls Salmonella typhimurium virulence. Proc Natl Acad Sci U S A. 1989 Jul;86(13):5054–5058. doi: 10.1073/pnas.86.13.5054. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Miller V. L., Bliska J. B., Falkow S. Nucleotide sequence of the Yersinia enterocolitica ail gene and characterization of the Ail protein product. J Bacteriol. 1990 Feb;172(2):1062–1069. doi: 10.1128/jb.172.2.1062-1069.1990. [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]
- Miller V. L., Mekalanos J. J. Synthesis of cholera toxin is positively regulated at the transcriptional level by toxR. Proc Natl Acad Sci U S A. 1984 Jun;81(11):3471–3475. doi: 10.1073/pnas.81.11.3471. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pepe J. C., Miller V. L. The Yersinia enterocolitica inv gene product is an outer membrane protein that shares epitopes with Yersinia pseudotuberculosis invasin. J Bacteriol. 1990 Jul;172(7):3780–3789. doi: 10.1128/jb.172.7.3780-3789.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pierson D. E., Falkow S. Nonpathogenic isolates of Yersinia enterocolitica do not contain functional inv-homologous sequences. Infect Immun. 1990 Apr;58(4):1059–1064. doi: 10.1128/iai.58.4.1059-1064.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Pulkkinen W. S., Miller S. I. A Salmonella typhimurium virulence protein is similar to a Yersinia enterocolitica invasion protein and a bacteriophage lambda outer membrane protein. J Bacteriol. 1991 Jan;173(1):86–93. doi: 10.1128/jb.173.1.86-93.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Robins-Browne R. M., Prpic J. K. Effects of iron and desferrioxamine on infections with Yersinia enterocolitica. Infect Immun. 1985 Mar;47(3):774–779. doi: 10.1128/iai.47.3.774-779.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Robins-Browne R. M., Tzipori S., Gonis G., Hayes J., Withers M., Prpic J. K. The pathogenesis of Yersinia enterocolitica infection in gnotobiotic piglets. J Med Microbiol. 1985 Jun;19(3):297–308. doi: 10.1099/00222615-19-3-297. [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]
- 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]
- Schnaitman C. A. Solubilization of the cytoplasmic membrane of Escherichia coli by Triton X-100. J Bacteriol. 1971 Oct;108(1):545–552. doi: 10.1128/jb.108.1.545-552.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schwartz E., Kröger M., Rak B. IS150: distribution, nucleotide sequence and phylogenetic relationships of a new E. coli insertion element. Nucleic Acids Res. 1988 Jul 25;16(14B):6789–6802. doi: 10.1093/nar/16.14.6789. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schägger H., von Jagow G. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem. 1987 Nov 1;166(2):368–379. doi: 10.1016/0003-2697(87)90587-2. [DOI] [PubMed] [Google Scholar]
- Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
- Stoorvogel J., van Bussel M. J., Tommassen J., van de Klundert J. A. Molecular characterization of an Enterobacter cloacae outer membrane protein (OmpX). J Bacteriol. 1991 Jan;173(1):156–160. doi: 10.1128/jb.173.1.156-160.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Struyvé M., Moons M., Tommassen J. Carboxy-terminal phenylalanine is essential for the correct assembly of a bacterial outer membrane protein. J Mol Biol. 1991 Mar 5;218(1):141–148. doi: 10.1016/0022-2836(91)90880-f. [DOI] [PubMed] [Google Scholar]
- Tacket C. O., Narain J. P., Sattin R., Lofgren J. P., Konigsberg C., Jr, Rendtorff R. C., Rausa A., Davis B. R., Cohen M. L. A multistate outbreak of infections caused by Yersinia enterocolitica transmitted by pasteurized milk. JAMA. 1984 Jan 27;251(4):483–486. [PubMed] [Google Scholar]
- Une T. Studies on the pathogenicity of Yersinia enterocolitica. II. Interaction with cultured cells in vitro. Microbiol Immunol. 1977;21(7):365–377. doi: 10.1111/j.1348-0421.1977.tb00301.x. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]


