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.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
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.
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.
Ben-Gurion, R. and Shafferman, A. (1981) Essential virulence determinants of different Yersinia species are carried on a common plasmid. Plasmid 5, 183-187.
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.
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.
Ferber, D.M. and Brubaker, R.R. (1981) Plasmids in Yersinia pestis. Infect. Immun. 2, 839-841.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2007 Springer Science+Business Media, LLC
About this chapter
Cite this chapter
Rosenzweig, J.A., Schesser, K. (2007). Polynucleotide Phosphorylase and the T3SS. In: Perry, R.D., Fetherston, J.D. (eds) The Genus Yersinia. Advances In Experimental Medicine And Biology, vol 603. Springer, New York, NY. https://doi.org/10.1007/978-0-387-72124-8_19
Download citation
DOI: https://doi.org/10.1007/978-0-387-72124-8_19
Publisher Name: Springer, New York, NY
Print ISBN: 978-0-387-72123-1
Online ISBN: 978-0-387-72124-8
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)