1887

Abstract

is a species that emerged recently from and gained an exceptional pathogenicity potential. Among the major genetic differences between the plague bacillus and its ancestor is the acquisition of the pPla plasmid, which has been associated with the increased virulence of . In a previous study, introduction of pPla into did not lead to any modification of the virulence of the host bacterium. However, it was subsequently demonstrated that the presence of smooth lipopolysaccharide (LPS) inhibits the activity of Pla. In this study, pPla was introduced into a strain expressing smooth LPS, and into a variant in which a mutation that abrogates the formation of O-antigen (O-Ag) repeats (as in natural isolates of ) was generated. It was found that in both strains, Pla was synthesized, exported to the bacterial membrane and processed as in . However, the ability of Pla to activate plasminogen was weak and observed only at 37 °C in the smooth strain, while this activity was similar to that of and expressed at both 28 and 37 °C in the O-Ag mutant strain. Similarly, Pla-mediated inactivation of the antiprotease -antiplasmin was not detected in the smooth strain grown at 28 °C, but was expressed at both temperatures in the O-Ag mutant strain. Despite the more efficient activity of Pla, the O-Ag mutant strain exhibited a lower pathogenicity upon subcutaneous infection of mice. The results thus indicate that, although abrogation of O side chain synthesis in a strain harbouring pPla potentiates the two proteolytic activities of Pla, this is not sufficient to confer to a higher pathogenicity potential. These results also suggest that acquisition of pPla may not have been sufficient to confer an immediate higher pathogenic potential to the ancestor strain.

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2005-11-01
2019-11-14
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References

  1. Achtman, M., Zurth, K., Morelli, C., Torrea, G., Guiyoule, A. & Carniel, E. ( 1999; ). Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis. Proc Natl Acad Sci U S A 96, 14043–14048.[CrossRef]
    [Google Scholar]
  2. Bengoechea, J. A., Brandenburg, K., Seydel, U., Diaz, R. & Moriyon, I. ( 1998; ). Yersinia pseudotuberculosis and Yersinia pestis show increased outer membrane permeability to hydrophobic agents which correlates with lipopolysaccharide acyl-chain fluidity. Microbiology 144, 1517–1526.[CrossRef]
    [Google Scholar]
  3. Chain, P. S., Carniel, E., Larimer, F. W. & 20 other authors ( 2004; ). Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis. Proc Natl Acad Sci U S A 101, 13826–13831.[CrossRef]
    [Google Scholar]
  4. Chung, S.-I., Kim, W.-Y., Kim, K.-J. & Choi, C.-S. ( 1997; ). Seropositive rate to Yersinia enterocolitica-pseudotuberculosis complex among patients with acute gastroenteritis in children, 1994-1997. J Korean Soc Microbiol 32, 701–715.
    [Google Scholar]
  5. Conchas, R. F. & Carniel, E. ( 1990; ). A highly efficient electroporation system for transformation of Yersinia. Gene 87, 133–137.[CrossRef]
    [Google Scholar]
  6. Darwin, A. ( 2004; ). Identification of Yersinia genes expressed during host infection. In Yersinia, Molecular and Cellular Biology, pp. 149–168. Edited by E. Carniel & B. J. Hinnebusch. Norfolk: Horizon Bioscience.
  7. Davis, K. J., Fritz, D. L., Pitt, M. L., Welkos, S. L., Worsham, P. L. & Friedlander, A. M. ( 1996; ). Pathology of experimental pneumonic plague produced by fraction 1-positive and fraction 1-negative Yersinia pestis in African green monkeys (Cercopithecus aethiops). Arch Pathol Lab Med 120, 156–163.
    [Google Scholar]
  8. Derbise, A., Lesic, B., Dacheux, D., Ghigo, J. M. & Carniel, E. ( 2003; ). A rapid and simple method for inactivating chromosomal genes in Yersinia. FEMS Immunol Med Microbiol 38, 113–116.[CrossRef]
    [Google Scholar]
  9. Friedlander, A. M., Welkos, S. L., Worsham, P. L., Andrews, G. P., Heath, D. G., Anderson, G. W., Pitt, M. L. M., Estep, J. & Davis, K. ( 1995; ). Relationship between virulence and immunity as revealed in recent studies of the F1 capsule of Yersinia pestis. Clin Infect Dis 21, S178–S181.[CrossRef]
    [Google Scholar]
  10. Hinnebusch, J., Cherepanov, P., Du, Y., Rudolph, A., Dixon, J. D., Schwan, T. & Forsberg, A. ( 2000; ). Murine toxin of Yersinia pestis shows phospholipase D activity but is not required for virulence in mice. Int J Med Microbiol 290, 483–487.[CrossRef]
    [Google Scholar]
  11. Hinnebusch, B. J., Rudolph, A. E., Cherepanov, P., Dixon, J. E., Schwan, T. G. & Forsberg, A. ( 2002; ). Role of Yersinia murine toxin in survival of Yersinia pestis in the midgut of the flea vector. Science 296, 733–735.[CrossRef]
    [Google Scholar]
  12. Korhonen, T. K., Kukkonen, M., Virkola, R., Lång, H., Suomalainen, M., Kyllonen, P. & Lähteenmäki, K. ( 2004; ). The plasminogen activator Pla of Yersinia pestis: localized proteolysis and systemic spread. In Yersinia, Molecular and Cellular Biology, pp. 349–362. Edited by E. Carniel & B. J. Hinnebusch. Norfolk: Horizon Bioscience.
  13. Kukkonen, M., Lähteenmäki, K., Suomalainen, M., Kalkkinen, N., Emödy, L., Lång, H. & Korhonen, T. K. ( 2001; ). Protein regions important for plasminogen activation and inactivation of α 2-antiplasmin in the surface protease Pla of Yersinia pestis. Mol Microbiol 40, 1097–1111.[CrossRef]
    [Google Scholar]
  14. Kukkonen, M., Suomalainen, M., Kyllonen, P., Lähteenmäki, K., Lång, H., Virkola, R., Helander, I. M., Holst, O. & Korhonen, T. K. ( 2004; ). Lack of O-antigen is essential for plasminogen activation by Yersinia pestis and Salmonella enterica. Mol Microbiol 51, 215–225.
    [Google Scholar]
  15. Kutyrev, V. V., Filippov, A. A., Shavina, N. & Protsenko, O. A. ( 1989; ). Genetic analysis and simulation of the virulence of Yersinia pestis. Mol Gen Mikrobiol Virusol 8, 42–47.
    [Google Scholar]
  16. Kutyrev, V., Mehigh, R. J., Motin, V. L., Pokrovskaya, M. S., Smirnov, G. B. & Brubaker, R. R. ( 1999; ). Expression of the plague plasminogen activator in Yersinia pseudotuberculosis and Escherichia coli. Infect Immun 67, 1359–1367.
    [Google Scholar]
  17. Lähteenmäki, K., Virkola, R., Saren, A., Emödy, L. & Korhonen, T. K. ( 1998; ). Expression of plasminogen activator Pla of Yersinia pestis enhances bacterial attachment to the mammalian extracellular matrix. Infect Immun 66, 5755–5762.
    [Google Scholar]
  18. Lähteenmäki, K., Kyllonen, P., Partanen, L. & Korhonen, T. K. ( 2005; ). Antiprotease inactivation by Salmonella enterica released from infected macrophages. Cell Microbiol 7, 529–538.
    [Google Scholar]
  19. Lesic, B. & Carniel, E. ( 2005; ). Horizontal transfer of the high-pathogenicity island of Yersinia pseudotuberculosis. J Bacteriol 187, 3352–3358.[CrossRef]
    [Google Scholar]
  20. Parkhill, J., Wren, B. W., Thomson, N. R. & 32 other authors ( 2001; ). Genome sequence of Yersinia pestis, the causative agent of plague. Nature 413, 523–527.[CrossRef]
    [Google Scholar]
  21. Plow, E. F., Ploplis, V. A., Carmeliet, P. & Collen, D. ( 1999; ). Plasminogen and cell migration in vivo. Fibrinol Proteol 13, 49–53.[CrossRef]
    [Google Scholar]
  22. Reed, L. J. & Muench, H. ( 1935; ). A simple method of estimation fifty per cent endpoints. Am J Hyg 27, 493–497.
    [Google Scholar]
  23. Rudolph, A. E., Stuckey, J. A., Zhao, Y., Matthews, H. R., Patton, W. A., Moss, J. & Dixon, J. E. ( 1999; ). Expression, characterization, and mutagenesis of the Yersinia pestis murine toxin, a phospholipase D superfamily member. J Biol Chem 274, 11824–11831.[CrossRef]
    [Google Scholar]
  24. Saksela, O. ( 1985; ). Plasminogen activation and regulation of pericellular proteolysis. Biochim Biophys Acta 823, 35–65.
    [Google Scholar]
  25. Samoilova, S. V., Samoilova, L. V., Yezhov, I. N., Drozdov, I. G. & Anisimov, A. P. ( 1996; ). Virulence of pPst(+) and pPst(-) strains of Yersinia pestis for guinea-pigs. J Med Microbiol 45, 440–444.[CrossRef]
    [Google Scholar]
  26. Schmidt, V. J. ( 1965; ). Untersuchungen über den fluoreszenzserologischen Nachweis von Pasteurella pseudotuberculosis-Antikörpenrn. Pathol Microbiol 28, 21–25.
    [Google Scholar]
  27. Sizaret, P. & Mollaret, H. H. ( 1968; ). Sensibilité et spécificité comparées des réactions d'agglutination et d'immunofluorescence indirecte vis-à-vis du bacille de Malassez et Vignal “Pasteurella pseudotuberculosis”. In International Symposium on Pseudotuberculosis, pp. 197–206. Edited by R. H. Regamey, A. de Barbieri, W. Hennessen, D. Ikié, F. T. Perkins & J. Ungar. Basel: S. Karger.
  28. Skurnik, M., Peippo, A. & Ervela, E. ( 2000; ). Characterization of the O-antigen gene clusters of Yersinia pseudotuberculosis and the cryptic O-antigen gene cluster of Yersinia pestis shows that the plague bacillus is most closely related to and has evolved from Yersinia pseudotuberculosis serotype O : 1b. Mol Microbiol 37, 316–330.[CrossRef]
    [Google Scholar]
  29. Sodeinde, O. A. & Goguen, J. D. ( 1988; ). Genetic analysis of the 9·5-kilobase virulence plasmid of Yersinia pestis. Infect Immun 56, 2743–2748.
    [Google Scholar]
  30. Sodeinde, O. A., Subrahmanyam, Y. V. B. K., Stark, K., Quan, T., Bao, Y. D. & Goguen, J. D. ( 1992; ). A surface protease and the invasive character of plague. Science 258, 1004–1007.[CrossRef]
    [Google Scholar]
  31. Splino, M., Kyntera, F., Peychl, L. & Kotrlik, J. ( 1969; ). Ein beitrag zur serologie und epidemiologie der humanen Pasteurella-Pseudotuberkulose. Pathol Anat Inst Med Fak der Karlssuniversität 209, 204–211.
    [Google Scholar]
  32. Welkos, S. L., Friedlander, A. M. & Davis, K. J. ( 1997; ). Studies on the role of plasminogen activator in systemic infection by virulent Yersinia pestis strain C092. Microb Pathog 23, 211–223.[CrossRef]
    [Google Scholar]
  33. World Health Organization ( 2003; ). Human plague in 2000 and 2001. Wkly Epidemiol Rec 78, 130–135.
    [Google Scholar]
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