Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1991 Jan;173(1):86–93. doi: 10.1128/jb.173.1.86-93.1991

A Salmonella typhimurium virulence protein is similar to a Yersinia enterocolitica invasion protein and a bacteriophage lambda outer membrane protein.

W S Pulkkinen 1, S I Miller 1
PMCID: PMC207160  PMID: 1846140

Abstract

The phoP-phoQ-regulated pagC locus is essential for full virulence and survival within macrophages of Salmonella typhimurium. The protein product, DNA sequence, and transcript of pagC were determined. The pagC locus encodes a single 188-amino-acid membrane protein that is similar to the ail-encoded eucaryotic cell invasion protein of Yersinia enterocolitica and the lom-encoded protein of bacteriophage lambda. The similarity of PagC and Ail to Lom leads us to hypothesize that Lom is a virulence protein and that bacteriophage gene transfer and lysogeny could have led to the development of proteins essential to survival within macrophages and eucaryotic cell invasion.

Full text

PDF
86

Images in this article

87Image
on p.87
89Image
on p.89
90Image
on p.90
90Image
on p.90

Selected References

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

  1. 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]
  2. Betley M. J., Miller V. L., Mekalanos J. J. Genetics of bacterial enterotoxins. Annu Rev Microbiol. 1986;40:577–605. doi: 10.1146/annurev.mi.40.100186.003045. [DOI] [PubMed] [Google Scholar]
  3. Binns M. M., Davies D. L., Hardy K. G. Cloned fragments of the plasmid ColV,I-K94 specifying virulence and serum resistance. Nature. 1979 Jun 28;279(5716):778–781. doi: 10.1038/279778a0. [DOI] [PubMed] [Google Scholar]
  4. Brickman E., Beckwith J. Analysis of the regulation of Escherichia coli alkaline phosphatase synthesis using deletions and phi80 transducing phages. J Mol Biol. 1975 Aug 5;96(2):307–316. doi: 10.1016/0022-2836(75)90350-2. [DOI] [PubMed] [Google Scholar]
  5. Buchmeier N. A., Heffron F. Intracellular survival of wild-type Salmonella typhimurium and macrophage-sensitive mutants in diverse populations of macrophages. Infect Immun. 1989 Jan;57(1):1–7. doi: 10.1128/iai.57.1.1-7.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Case C. C., Roels S. M., González J. E., Simons E. L., Simons R. W. Analysis of the promoters and transcripts involved in IS10 anti-sense RNA control. Gene. 1988 Dec 10;72(1-2):219–236. doi: 10.1016/0378-1119(88)90147-3. [DOI] [PubMed] [Google Scholar]
  7. Chuba P. J., Leon M. A., Banerjee A., Palchaudhuri S. Cloning and DNA sequence of plasmid determinant iss, coding for increased serum survival and surface exclusion, which has homology with lambda DNA. Mol Gen Genet. 1989 Apr;216(2-3):287–292. doi: 10.1007/BF00334367. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Feinberg A. P., Vogelstein B. "A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity". Addendum. Anal Biochem. 1984 Feb;137(1):266–267. doi: 10.1016/0003-2697(84)90381-6. [DOI] [PubMed] [Google Scholar]
  10. Fields P. I., Groisman E. A., Heffron F. A Salmonella locus that controls resistance to microbicidal proteins from phagocytic cells. Science. 1989 Feb 24;243(4894 Pt 1):1059–1062. doi: 10.1126/science.2646710. [DOI] [PubMed] [Google Scholar]
  11. Finlay B. B., Gumbiner B., Falkow S. Penetration of Salmonella through a polarized Madin-Darby canine kidney epithelial cell monolayer. J Cell Biol. 1988 Jul;107(1):221–230. doi: 10.1083/jcb.107.1.221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Friedman A. M., Long S. R., Brown S. E., Buikema W. J., Ausubel F. M. Construction of a broad host range cosmid cloning vector and its use in the genetic analysis of Rhizobium mutants. Gene. 1982 Jun;18(3):289–296. doi: 10.1016/0378-1119(82)90167-6. [DOI] [PubMed] [Google Scholar]
  13. Galán J. E., Curtiss R., 3rd Virulence and vaccine potential of phoP mutants of Salmonella typhimurium. Microb Pathog. 1989 Jun;6(6):433–443. doi: 10.1016/0882-4010(89)90085-5. [DOI] [PubMed] [Google Scholar]
  14. George D. G., Barker W. C., Hunt L. T. The protein identification resource (PIR). Nucleic Acids Res. 1986 Jan 10;14(1):11–15. doi: 10.1093/nar/14.1.11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Groisman E. A., Chiao E., Lipps C. J., Heffron F. Salmonella typhimurium phoP virulence gene is a transcriptional regulator. Proc Natl Acad Sci U S A. 1989 Sep;86(18):7077–7081. doi: 10.1073/pnas.86.18.7077. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. 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]
  19. Merril C. R., Goldman D., Van Keuren M. L. Gel protein stains: silver stain. Methods Enzymol. 1984;104:441–447. doi: 10.1016/s0076-6879(84)04111-2. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Miller S. I., Landfear S. M., Wirth D. F. Cloning and characterization of a Leishmania gene encoding a RNA spliced leader sequence. Nucleic Acids Res. 1986 Sep 25;14(18):7341–7360. doi: 10.1093/nar/14.18.7341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Miller S. I., Mekalanos J. J. Constitutive expression of the phoP regulon attenuates Salmonella virulence and survival within macrophages. J Bacteriol. 1990 May;172(5):2485–2490. doi: 10.1128/jb.172.5.2485-2490.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Miller S. I., Pulkkinen W. S., Selsted M. E., Mekalanos J. J. Characterization of defensin resistance phenotypes associated with mutations in the phoP virulence regulon of Salmonella typhimurium. Infect Immun. 1990 Nov;58(11):3706–3710. doi: 10.1128/iai.58.11.3706-3710.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. 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]
  26. 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]
  27. Newland J. W., Strockbine N. A., Miller S. F., O'Brien A. D., Holmes R. K. Cloning of Shiga-like toxin structural genes from a toxin converting phage of Escherichia coli. Science. 1985 Oct 11;230(4722):179–181. doi: 10.1126/science.2994228. [DOI] [PubMed] [Google Scholar]
  28. O'Farrell P. H. High resolution two-dimensional electrophoresis of proteins. J Biol Chem. 1975 May 25;250(10):4007–4021. [PMC free article] [PubMed] [Google Scholar]
  29. Peterson K. M., Mekalanos J. J. Characterization of the Vibrio cholerae ToxR regulon: identification of novel genes involved in intestinal colonization. Infect Immun. 1988 Nov;56(11):2822–2829. doi: 10.1128/iai.56.11.2822-2829.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Ronson C. W., Nixon B. T., Ausubel F. M. Conserved domains in bacterial regulatory proteins that respond to environmental stimuli. Cell. 1987 Jun 5;49(5):579–581. doi: 10.1016/0092-8674(87)90530-7. [DOI] [PubMed] [Google Scholar]
  31. Sanger F., Coulson A. R., Hong G. F., Hill D. F., Petersen G. B. Nucleotide sequence of bacteriophage lambda DNA. J Mol Biol. 1982 Dec 25;162(4):729–773. doi: 10.1016/0022-2836(82)90546-0. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Shine J., Dalgarno L. The 3'-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci U S A. 1974 Apr;71(4):1342–1346. doi: 10.1073/pnas.71.4.1342. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Smith H. W., Green P., Parsell Z. Vero cell toxins in Escherichia coli and related bacteria: transfer by phage and conjugation and toxic action in laboratory animals, chickens and pigs. J Gen Microbiol. 1983 Oct;129(10):3121–3137. doi: 10.1099/00221287-129-10-3121. [DOI] [PubMed] [Google Scholar]
  35. Smith R. F., Smith T. F. Automatic generation of primary sequence patterns from sets of related protein sequences. Proc Natl Acad Sci U S A. 1990 Jan;87(1):118–122. doi: 10.1073/pnas.87.1.118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. 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]
  37. Stock J. B., Ninfa A. J., Stock A. M. Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol Rev. 1989 Dec;53(4):450–490. doi: 10.1128/mr.53.4.450-490.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Thomas P. S. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201–5205. doi: 10.1073/pnas.77.9.5201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. von Heijne G. How signal sequences maintain cleavage specificity. J Mol Biol. 1984 Feb 25;173(2):243–251. doi: 10.1016/0022-2836(84)90192-x. [DOI] [PubMed] [Google Scholar]
  40. von Heijne G. Signal sequences. The limits of variation. J Mol Biol. 1985 Jul 5;184(1):99–105. doi: 10.1016/0022-2836(85)90046-4. [DOI] [PubMed] [Google Scholar]

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

RESOURCES