Advertisement

Polynucleotide Phosphorylase and the T3SS

  • Jason A. Rosenzweig
  • Kurt Schesser
Part of the Advances In Experimental Medicine And Biology book series (AEMB, volume 603)

Low temperatures as well as encounters with host phagocytes are two stresses that have been relatively well studied in many species of bacteria. The exoribonuclease polynucleotide phosphorylase (PNPase) has previously been shown to be required by several species of bacteria, including Yersinia, for low-temperature growth. We have shown that PNPase also enhances the ability of Yersinia to withstand the killing activities of murine macrophages. We have gone on to show that PNPase is required for the optimal functioning of Yersinia’s type three secretion system (T3SS), an organelle that injects effector proteins directly into host cells. Surprisingly, the PNPase-mediated effect on T3SS activity is independent of PNPase’s ribonuclease activity and instead requires only its S1 RNA-binding domain. In stark contrast, the catalytic activity of PNPase is strictly required for enhanced growth at low temperature. Preliminary experiments suggest that the RNA-binding interface of the S1 domain is critical for its T3SS-enhancing activity. Our findings indicate that PNPase plays versatile roles in promoting Yersinia’s survival in response to stressful conditions.

Keywords

Yersinia Enterocolitica Yersinia Pestis Virulence Plasmid Yersinia Species Yersinia Pseudotuberculosis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Anderson, D.M., Ramamurthi, K.S., Tam, C. and Schneewind, O. (2002) YopD and LcrH regulate expression of Yersinia enterocolitica YopQ by a posttranscriptional mechanism and bind to yopQ RNA. J. Bacteriol. 184, 1287-1295.CrossRefPubMedPubMedCentralGoogle Scholar
  2. Bartra, S., Cherepanov, P., Forsberg, A. and Schesser, K. (2001) The Yersinia YopE and YopH type III effector proteins enhance bacterial proliferation following contact with eukaryotic cells. BMC Microbiol. 1, 22-33.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Ben-Gurion, R. and Shafferman, A. (1981) Essential virulence determinants of different Yersinia species are carried on a common plasmid. Plasmid 5, 183-187.CrossRefPubMedGoogle Scholar
  4. Callaghan, A.J., Marcaida, M.J., Stead, J.A., McDowall, K.J., Scott, W.G. and Luisi, B.F. (2005) Structure of Escherichia coli RNase E catalytic domain and implications for RNA turnover. Nature 437, 1187-1191.CrossRefPubMedGoogle Scholar
  5. Clements, M., Eriksson, S., Thompson, A., Lucchini, S., Hinton, J., Normark, S. and Rhen, M. (2002) Polynucleotide phosphorylase is a global regulator of virulence and persistency in Salmonella enterica. PNAS 99, 8784-8789.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Ferber, D.M. and Brubaker, R.R. (1981) Plasmids in Yersinia pestis. Infect. Immun. 2, 839-841.Google Scholar
  7. Francis, M.S., Lloyd, S.A. and Wolf-Watz, H. (2001) The type III secretion chaperone LcrH co-operates with YopD to establish a negative, regulatory loop for control of Yop synthe-sis in Yersinia pseudotuberculosis. Mol. Microbiol. 42, 1075-1093.CrossRefPubMedGoogle Scholar
  8. Fukui, G.M., Ogg, J.E., Wessman, G.E. and Surgalla, M.J. (1957) Studies on the relation of cultural conditions and virulence of Pasteurella pestis. J. Bacteriol. 74, 714-717.PubMedPubMedCentralGoogle Scholar
  9. Gemski, P., Lazere, J.R., Casey, T. and Wohlhieter, J.A. (1980) Presence of a virulence-associated plasmid in Yersinia pseudotuberculosis. Infect. Immun. 28, 1044-1047.PubMedPubMedCentralGoogle Scholar
  10. Higuchi, K. and Carlin, C.E. (1958) Studies on the nutrition and physiology of Pasteurella pestis. II. A defined medium for the growth of Pasteurella pestis. J. Bacteriol. 75, 409-413.PubMedPubMedCentralGoogle Scholar
  11. Higuchi, K., Kupferberg, L.L. and Smith, J.L. (1959) Studies on the nutrition and physiology of Pasteurella pestis. III. Effects of calcium ions on the growth of virulent and avirulent strains of Pasteurella pestis. J. Bacteriol. 77, 317-321.PubMedPubMedCentralGoogle Scholar
  12. Higuchi, K. and Smith, J.L. (1961) Studies on the nutrition and physiology of Pasteurella pestis. VI. A differential plating medium for the estimation of the mutation rate to aviru-lence. J. Bacteriol. 81, 605-608.PubMedPubMedCentralGoogle Scholar
  13. Hoe, N.P. and Goguen, J.D. (1993) Temperature sensing in Yersinia pestis: translation of the LcrF activator protein is thermally regulated. J. Bacteriol. 175, 7901-7909.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Jackson, M.W., Silva-Herzog, E. and Plano, G.V. (2004) The ATP-dependent ClpXP and Lon proteases regulate expression of the Yersinia pestis type III secretion system via regulated proteolysis of YmoA, a small histone-like protein. Mol. Microbiol. 54, 1364-1378.CrossRefPubMedGoogle Scholar
  15. Lambert de Rouvroit, C., Sluiters, C. and Cornelis, G.R. (1992) Role of the transcriptional activator, VirF, and temperature in the expression of the pYV plasmid genes of Yersinia enterocolitica. Mol. Microbiol 6, 395-409.CrossRefGoogle Scholar
  16. Pettersson, J., Nordfelth, R., Dubinina, E., Bergman, T., Gustafsson, M., Magnusson, K.E. and Wolf-Watz, H. (1996) Modulation of virulence factor expression by pathogen target cell contact. Science 273, 1231-1233.CrossRefPubMedGoogle Scholar
  17. Portnoy, D.A., Moseley, S.L. and Falkow, S. (1981) Characterization of plasmids and plas-mid-associated determinants of Yersinia enterocolitica pathogenesis. Infect. Immun. 31, 775-782.PubMedPubMedCentralGoogle Scholar
  18. Portnoy, D.A., Wolf-Watz, H., Bolin, I., Beeder, A.B. and Falkow, S. (1984) Characterization of common virulence plasmids in Yersinia species and their role in the expression of outer membrane proteins. Infect. Immun. 43, 108-114.PubMedPubMedCentralGoogle Scholar
  19. Rosenzweig, J.A., Weltman, G., Plano, G.V. and Schesser, K. (2005) Modulation of Yersinia type three secretion system by the S1 domain of polynucleotide phosphorylase. J. Biol. Chem. 280, 156-163.CrossRefPubMedGoogle Scholar
  20. Rosqvist, R., Magnusson, K.E. and Wolf-Watz, H. (1994) Target cell contact triggers expres-sion and polarized transfer of Yersinia YopE cytotoxin into mammalian cells. EMBO J. 13, 964-972.PubMedPubMedCentralGoogle Scholar
  21. Schubert, M., Edge, R.E., Lario, P., Cook, M.A., Strynadka, N.C., Mackie, G.A. and McIntosh, L.P. (2004) Structural characterization of the RNase E S1 domain and identifi-cation of its oligonucleotide-binding and dimerization interfaces. J. Mol. Biol. 341, 37-54.CrossRefPubMedGoogle Scholar
  22. Williams, A.W. and Straley, S.C. (1998) YopD of Yersinia pestis plays a role in negative regulation of the low-calcium response in addition to its role in translocation of Yops. J. Bacteriol. 180, 350-358.PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Jason A. Rosenzweig
    • 1
  • Kurt Schesser
    • 2
  1. 1.Division of Math Science and TechnologyNova Southeastern UniversityUSA
  2. 2.Department of Microbiology & Immunology, Miller School of MedicineUniversity of MiamiMiamiUSA

Personalised recommendations