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. 1989 Jan;171(1):254–262. doi: 10.1128/jb.171.1.254-262.1989

Homology between virF, the transcriptional activator of the Yersinia virulence regulon, and AraC, the Escherichia coli arabinose operon regulator.

G Cornelis 1, C Sluiters 1, C L de Rouvroit 1, T Michiels 1
PMCID: PMC209580  PMID: 2644192

Abstract

Virulent yersiniae (Yersinia pestis, Y. pseudotuberculosis, and Y. enterocolitica) restrict their growth at 37 degrees C in rich medium deprived of calcium. This property, called calcium dependency, correlates with the secretion of Yersinia outer membrane proteins (Yops) and with pathogenicity. It is mediated by a 70-kilobase plasmid called pYV. The structural genes of the Yops (yop genes), as well as genes involved in the control of their expression (vir genes), have been localized on pYV. In this communication we show that virF encodes a transcriptional activator controlling the yop regulon. This activator is a 30,879-dalton protein related to AraC, the regulator of the Escherichia coli and Salmonella typhimurium arabinose operons. We also show in this paper that transcription of virF is thermodependent and presumably autoregulated. virF is thus responsible for the effect of temperature on the production of the Yops. Finally, we show that virF activates transcription of the yop genes independently of the presence of calcium ions. The role of calcium therefore remains unaccounted for.

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Selected References

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

  1. Balligand G., Laroche Y., Cornelis G. Genetic analysis of virulence plasmid from a serogroup 9 Yersinia enterocolitica strain: role of outer membrane protein P1 in resistance to human serum and autoagglutination. Infect Immun. 1985 Jun;48(3):782–786. doi: 10.1128/iai.48.3.782-786.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. Biot T., Cornelis G. R. The replication, partition and yop regulation of the pYV plasmids are highly conserved in Yersinia enterocolitica and Y. pseudotuberculosis. J Gen Microbiol. 1988 Jun;134(6):1525–1534. doi: 10.1099/00221287-134-6-1525. [DOI] [PubMed] [Google Scholar]
  4. Bölin I., Forsberg A., Norlander L., Skurnik M., Wolf-Watz H. Identification and mapping of the temperature-inducible, plasmid-encoded proteins of Yersinia spp. Infect Immun. 1988 Feb;56(2):343–348. doi: 10.1128/iai.56.2.343-348.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bölin I., Wolf-Watz H. The plasmid-encoded Yop2b protein of Yersinia pseudotuberculosis is a virulence determinant regulated by calcium and temperature at the level of transcription. Mol Microbiol. 1988 Mar;2(2):237–245. doi: 10.1111/j.1365-2958.1988.tb00025.x. [DOI] [PubMed] [Google Scholar]
  6. Casadaban M. J. Regulation of the regulatory gene for the arabinose pathway, araC. J Mol Biol. 1976 Jul 5;104(3):557–566. doi: 10.1016/0022-2836(76)90120-0. [DOI] [PubMed] [Google Scholar]
  7. Clarke P., Lin H. C., Wilcox G. The nucleotide sequence of the araC regulatory gene in Salmonella typhimurium LT2. Gene. 1982 May;18(2):157–163. doi: 10.1016/0378-1119(82)90113-5. [DOI] [PubMed] [Google Scholar]
  8. Claverie J. M. A common philosophy and FORTRAN 77 software package for implementing and searching sequence databases. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):397–407. doi: 10.1093/nar/12.1part1.397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Click E. M., McDonald G. A., Schnaitman C. A. Translational control of exported proteins that results from OmpC porin overexpression. J Bacteriol. 1988 May;170(5):2005–2011. doi: 10.1128/jb.170.5.2005-2011.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Close T. J., Rodriguez R. L. Construction and characterization of the chloramphenicol-resistance gene cartridge: a new approach to the transcriptional mapping of extrachromosomal elements. Gene. 1982 Dec;20(2):305–316. doi: 10.1016/0378-1119(82)90048-8. [DOI] [PubMed] [Google Scholar]
  11. Cornelis G., Abraham E. P. Beta-lactamases from Yersinia enterocolitica. J Gen Microbiol. 1975 Apr;87(2):273–284. doi: 10.1099/00221287-87-2-273. [DOI] [PubMed] [Google Scholar]
  12. Cornelis G., Colson C. Restriction of DNA in Yersinia enterocolitica detected by recipient ability for a derepressed R factor from Escherichia coli. J Gen Microbiol. 1975 Apr;87(2):285–291. doi: 10.1099/00221287-87-2-285. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Cornelis G., Sory M. P., Laroche Y., Derclaye I. Genetic analysis of the plasmid region controlling virulence in Yersinia enterocolitica 0:9 by Mini-Mu insertions and lac gene fusions. Microb Pathog. 1986 Aug;1(4):349–359. doi: 10.1016/0882-4010(86)90067-7. [DOI] [PubMed] [Google Scholar]
  15. Cornelis G., Vanootegem J. C., Sluiters C. Transcription of the yop regulon from Y. enterocolitica requires trans acting pYV and chromosomal genes. Microb Pathog. 1987 May;2(5):367–379. doi: 10.1016/0882-4010(87)90078-7. [DOI] [PubMed] [Google Scholar]
  16. Dale R. M., McClure B. A., Houchins J. P. A rapid single-stranded cloning strategy for producing a sequential series of overlapping clones for use in DNA sequencing: application to sequencing the corn mitochondrial 18 S rDNA. Plasmid. 1985 Jan;13(1):31–40. doi: 10.1016/0147-619x(85)90053-8. [DOI] [PubMed] [Google Scholar]
  17. Derbyshire K. M., Hatfull G., Willetts N. Mobilization of the non-conjugative plasmid RSF1010: a genetic and DNA sequence analysis of the mobilization region. Mol Gen Genet. 1987 Jan;206(1):161–168. doi: 10.1007/BF00326552. [DOI] [PubMed] [Google Scholar]
  18. Dodd I. B., Egan J. B. Systematic method for the detection of potential lambda Cro-like DNA-binding regions in proteins. J Mol Biol. 1987 Apr 5;194(3):557–564. doi: 10.1016/0022-2836(87)90681-4. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Forsberg A., Bölin I., Norlander L., Wolf-Watz H. Molecular cloning and expression of calcium-regulated, plasmid-coded proteins of Y. pseudotuberculosis. Microb Pathog. 1987 Feb;2(2):123–137. doi: 10.1016/0882-4010(87)90104-5. [DOI] [PubMed] [Google Scholar]
  21. Forsberg A., Wolf-Watz H. The virulence protein Yop5 of Yersinia pseudotuberculosis is regulated at transcriptional level by plasmid-plB1-encoded trans-acting elements controlled by temperature and calcium. Mol Microbiol. 1988 Jan;2(1):121–133. [PubMed] [Google Scholar]
  22. 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]
  23. 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]
  24. Goguen J. D., Yother J., Straley S. C. Genetic analysis of the low calcium response in Yersinia pestis mu d1(Ap lac) insertion mutants. J Bacteriol. 1984 Dec;160(3):842–848. doi: 10.1128/jb.160.3.842-848.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Gren E. J. Recognition of messenger RNA during translational initiation in Escherichia coli. Biochimie. 1984 Jan;66(1):1–29. doi: 10.1016/0300-9084(84)90188-3. [DOI] [PubMed] [Google Scholar]
  26. Harley C. B., Reynolds R. P. Analysis of E. coli promoter sequences. Nucleic Acids Res. 1987 Mar 11;15(5):2343–2361. doi: 10.1093/nar/15.5.2343. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. Kapperud G., Namork E., Skurnik M., Nesbakken T. Plasmid-mediated surface fibrillae of Yersinia pseudotuberculosis and Yersinia enterocolitica: relationship to the outer membrane protein YOP1 and possible importance for pathogenesis. Infect Immun. 1987 Sep;55(9):2247–2254. doi: 10.1128/iai.55.9.2247-2254.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Laroche Y., van Bouchaute M., Cornelis G. A restriction map of virulence plasmid pVYE439-80 from a serogroup 9 Yersinia enterocolitica strain. Plasmid. 1984 Jul;12(1):67–70. doi: 10.1016/0147-619x(84)90069-6. [DOI] [PubMed] [Google Scholar]
  30. Michiels T., Cornelis G. Tn951 derivatives designed for high-frequency plasmid-specific transposition and deletion mutagenesis. Gene. 1986;43(3):175–181. doi: 10.1016/0378-1119(86)90205-2. [DOI] [PubMed] [Google Scholar]
  31. Miller V. L., Taylor R. K., Mekalanos J. J. Cholera toxin transcriptional activator toxR is a transmembrane DNA binding protein. Cell. 1987 Jan 30;48(2):271–279. doi: 10.1016/0092-8674(87)90430-2. [DOI] [PubMed] [Google Scholar]
  32. Nicosia A., Rappuoli R. Promoter of the pertussis toxin operon and production of pertussis toxin. J Bacteriol. 1987 Jun;169(6):2843–2846. doi: 10.1128/jb.169.6.2843-2846.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Ogden S., Haggerty D., Stoner C. M., Kolodrubetz D., Schleif R. The Escherichia coli L-arabinose operon: binding sites of the regulatory proteins and a mechanism of positive and negative regulation. Proc Natl Acad Sci U S A. 1980 Jun;77(6):3346–3350. doi: 10.1073/pnas.77.6.3346. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. 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]
  35. Raibaud O., Schwartz M. Positive control of transcription initiation in bacteria. Annu Rev Genet. 1984;18:173–206. doi: 10.1146/annurev.ge.18.120184.001133. [DOI] [PubMed] [Google Scholar]
  36. Recsei P., Kreiswirth B., O'Reilly M., Schlievert P., Gruss A., Novick R. P. Regulation of exoprotein gene expression in Staphylococcus aureus by agar. Mol Gen Genet. 1986 Jan;202(1):58–61. doi: 10.1007/BF00330517. [DOI] [PubMed] [Google Scholar]
  37. 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]
  38. Schmidhauser T. J., Helinski D. R. Regions of broad-host-range plasmid RK2 involved in replication and stable maintenance in nine species of gram-negative bacteria. J Bacteriol. 1985 Oct;164(1):446–455. doi: 10.1128/jb.164.1.446-455.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Shaw W. V. Chloramphenicol acetyltransferase from chloramphenicol-resistant bacteria. Methods Enzymol. 1975;43:737–755. doi: 10.1016/0076-6879(75)43141-x. [DOI] [PubMed] [Google Scholar]
  40. Simatake H., Rosenberg M. Purified lambda regulatory protein cII positively activates promoters for lysogenic development. Nature. 1981 Jul 9;292(5819):128–132. doi: 10.1038/292128a0. [DOI] [PubMed] [Google Scholar]
  41. Straley S. C., Bowmer W. S. Virulence genes regulated at the transcriptional level by Ca2+ in Yersinia pestis include structural genes for outer membrane proteins. Infect Immun. 1986 Feb;51(2):445–454. doi: 10.1128/iai.51.2.445-454.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Tabor S., Richardson C. C. A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc Natl Acad Sci U S A. 1985 Feb;82(4):1074–1078. doi: 10.1073/pnas.82.4.1074. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Tabor S., Richardson C. C. DNA sequence analysis with a modified bacteriophage T7 DNA polymerase. Proc Natl Acad Sci U S A. 1987 Jul;84(14):4767–4771. doi: 10.1073/pnas.84.14.4767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Wallace R. G., Lee N., Fowler A. V. The araC gene of Escherichia coli: transcriptional and translational start-points and complete nucleotide sequence. Gene. 1980 Dec;12(3-4):179–190. doi: 10.1016/0378-1119(80)90100-6. [DOI] [PubMed] [Google Scholar]
  45. Wolf-Watz H., Portnoy D. A., Bölin I., Falkow S. Transfer of the virulence plasmid of Yersinia pestis to Yersinia pseudotuberculosis. Infect Immun. 1985 Apr;48(1):241–243. doi: 10.1128/iai.48.1.241-243.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Wozniak D. J., Cram D. C., Daniels C. J., Galloway D. R. Nucleotide sequence and characterization of toxR: a gene involved in exotoxin A regulation in Pseudomonas aeruginosa. Nucleic Acids Res. 1987 Mar 11;15(5):2123–2135. doi: 10.1093/nar/15.5.2123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Yanisch-Perron C., Vieira J., Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. doi: 10.1016/0378-1119(85)90120-9. [DOI] [PubMed] [Google Scholar]
  48. Yother J., Chamness T. W., Goguen J. D. Temperature-controlled plasmid regulon associated with low calcium response in Yersinia pestis. J Bacteriol. 1986 Feb;165(2):443–447. doi: 10.1128/jb.165.2.443-447.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Yother J., Goguen J. D. Isolation and characterization of Ca2+-blind mutants of Yersinia pestis. J Bacteriol. 1985 Nov;164(2):704–711. doi: 10.1128/jb.164.2.704-711.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Zaleska M., Lounatmaa K., Nurminen M., Wahlström E., Mäkelä P. H. A novel virulence-associated cell surface structure composed of 47-kd protein subunits in Yersinia enterocolitica. EMBO J. 1985 Apr;4(4):1013–1018. doi: 10.1002/j.1460-2075.1985.tb03732.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. 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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