Advertisement

Using Every Trick in the Book: The Pla Surface Protease of Yersinia pestis

  • Marjo Suomalainen
  • Johanna Haiko
  • Maini Kukkonen
  • Timo K. Korhonen
  • Kaarina Lähteenmäki
  • Ritva Virkola
  • Benita Westerlund-Wikström
  • Leandro Lobo
  • Päivi Ramu
Part of the Advances In Experimental Medicine And Biology book series (AEMB, volume 603)

The Pla surface protease of Yersinia pestis, encoded by the Y. pestis-specific plasmid pPCP1, is a versatile virulence factor. In vivo studies have shown that Pla is essential in the establishment of bubonic plague, and in vitro studies have demonstrated various putative virulence functions for the Pla molecule. Pla is a surface protease of the omptin family, and its proteolytic targets include the abundant, circulating human zymogen plasminogen, which is activated by Pla to the serine protease plasmin. Plasmin is important in cell migration, and Pla also proteolytically inactivates the main circulating inhibitor of plasmin, α2-antiplasmin. Pla also is an adhesin with affinity for laminin, a major glycoprotein of mammalian basement membranes, which is degraded by plasmin but not by Pla. Together, these functions create uncontrolled plasmin proteolysis targeted at tissue barriers. Other proteolytic targets for Pla include complement proteins.

Keywords

Catalytic Residue Yersinia Pestis Tissue Barrier MEROPS Database Surface Protease 
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. Beesley, E.D., Brubaker, R.R., Janssen, W.A. and Surgalla, M.J. (1967) Pesticins. III. Expres-sion of coagulase and mechanisms of fibrinolysis. J. Bacteriol. 94, 19-26.PubMedPubMedCentralGoogle Scholar
  2. Cowan, C., Jones, H.A., Kaya, Y.H., Perry, R.D. and Straley, S.C. (2000) Invasion of epithe-lial cells by Yersinia pestis: evidence for a Y. pestis-specific invasion. Infect. Immun. 68, 4523-4530.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Egile, C., Hauteville, H., Parsot, C., and Sansonetti, P.J. (1997) SopA, the outer membrane protease responsible for polar localization of IcsA in Shigella flexneri. Mol. Microbiol. 23, 1063-1073.CrossRefPubMedGoogle Scholar
  4. Ferber, D.M. and Brubaker, R.R. (1981) Plasmids in Yersinia pestis. Infect. Immun. 31, 839-841.PubMedPubMedCentralGoogle Scholar
  5. Ferguson, A.D., Welte, W., Hofmann, E., Lindner, B., Holst, O., Coulton, J.W. and Diedrerichs, K. (2000) A conserved structural motif for lipopolysaccharide recognition by prokaryotic and eukaryotic proteins. Struct. Fold. Des. 8, 585-592.CrossRefGoogle Scholar
  6. Goguen, J.D., Bugge, T. and Degen, J.L. (2000) Role of the pleiotropic effects of plasminogen deficiency in infection experiments with plasminogen-deficient mice. Methods 21, 179-183.CrossRefPubMedGoogle Scholar
  7. Grodberg, J., Lundrigan, M.D., Toledo, D.L., Mangel, W.F. and Dunn, J.J. (1988) Complete nucleotide sequence and deduced amino acid sequence of the ompT gene of E. coli K-12. Nucleic Acids Res. 16, 1209.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Guina, T., Yi, E.C., Wang, H., Hackett, M. and Miller, S.I. (2000) A PhoP-regulated outer membrane protease of Salmonella enterica serovar Typhimurium promotes resistance to alpha-helical antimicrobial peptides. J. Bacteriol. 182, 4077-4086.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Kienle, Z., Emödy, L., Svanborg, C. and O´Toole, P.W. (1992) Adhesive properties conferred by the plasminogen activator of Yersinia pestis. J. Gen. Microbiol. 138, 1679-1687.CrossRefPubMedGoogle Scholar
  10. Kramer, R.A., Zandwijken, D., Egmond, M.R. and Dekker, N. (2001) In vitro folding, purifi-cation and characterization of E. coli outer membrane protease OmpT. Eur. J. Biochem. 267, 885-893.CrossRefGoogle Scholar
  11. Kukkonen, M., Lähteenmäki, K., Suomalainen, M., Kalkkinen, N., Emödy, L., Lång, H. and Korhonen T.K. (2001) Protein regions important for plasminogen activation and inactiva-tion of α2-antiplasmin in the surface protease Pla of Yersinia pestis. Mol. Microbiol. 40, 1097-1111.CrossRefPubMedGoogle Scholar
  12. Kukkonen, M., Suomalainen, M., Kyllönen, P., Lähteenmäki, K., Lång, H., Virkola, R., Helander, I.M., Holst, O. and Korhonen, T.K. (2004) Lack of O-antigen is essential for plasminogen activation by Yersinia pestis and Salmonella enterica. Mol. Microbiol. 51, 215-225.CrossRefPubMedGoogle Scholar
  13. Lähteenmäki, K., Kukkonen, M. and Korhonen, T.K. (2001) The Pla surface protease/adhesin of Yersinia pestis mediates bacterial invasion into human endothelial cells. FEBS Lett. 504, 69-72.CrossRefPubMedGoogle Scholar
  14. Lähteenmäki, K., Virkola, R., Sarén, A., Emödy, L. and Korhonen, T.K. (1998) Expression of plasminogen activator Pla of Yersinia pestis enhances bacterial attachment to the mammal-ian extracellular matrix. Infect. Immun. 66, 5755-5762.PubMedPubMedCentralGoogle Scholar
  15. Lähteenmäki, K., Edelman, S. and Korhonen, T.K. (2005a) Bacterial metastasis: the host plasminogen system in bacterial invasion. Trends Microbiol. 13, 79-85.CrossRefPubMedGoogle Scholar
  16. Lähteenmäki, K., Kyllönen, P., Partanen, L. and Korhonen, T.K. (2005b) Antiprotease inacti-vation by Salmonella enterica released from infected macrophages. Cell. Microbiol. 7, 529-538.CrossRefPubMedGoogle Scholar
  17. Lobo, L.A. (2006) Adhesive properties of the purified plasminogen activator Pla of Yersinia pestis. FEMS Microbiol. Lett. 262, 158-162.CrossRefPubMedGoogle Scholar
  18. Lijnen, H.R. and Collen, D. (1995) Mechanisms of physiological fibrinolysis. Bailliere´s Clinical Haematology 8, 277-290.CrossRefPubMedGoogle Scholar
  19. Matsuo, E., Sampei, G., Mizobuchi, K. and Ito, K. (1999) The plasmid F OmpP protease, a homolue of OmpT, as a potential obstacle to E. coli-based protein production. FEBS Lett. 461, 6-8.CrossRefPubMedGoogle Scholar
  20. McGhee, G.C., Schnabel, E.L., Maxson-Stein, K., Jones, B., Stromberg, V.K., Lacy, G.H. and Jones A.L. (2002) Relatedness of chromosomal and plasmid DNAs of Erwinia pyrifoliae and Erwinia amylovora. Appl. Environ. Microbiol. 68, 6182-6192.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Myöhänen, H. and Vaheri, A. (2004) Regulation and interactions in the activation of cell-associated plasminogen. Cell. Mol. Life Sci. 61, 2840-2858.CrossRefPubMedGoogle Scholar
  22. Ngampasutadol, J., Ram, S., Blom, A.M., Jarva, H., Jerse, A.E., Lien, E., Goguen, J., Gulati, S. and Rice, P.A. (2005) Human C4b-binding protein selectively interacts with Neisseria gonorrhoeae and results in species-specific infection. Proc. Natl. Acad. Sci. USA 102, 17142-17147.CrossRefPubMedPubMedCentralGoogle Scholar
  23. Perry, R.D. and Fetherston, J.D. (1997) Yersinia pestis - etiological agent of plague. Clin. Microbiol. Rev. 10, 35-66.PubMedPubMedCentralGoogle Scholar
  24. Plow, E.F., Ploplis, V.A. , Carmeliet, P. and Collen D. (1999) Plasminogen and cell migration in vivo. Fibrinol. Proteol. 13, 49-53.CrossRefGoogle Scholar
  25. Schulz, G.E. (2000) Aβ-barrel membrane protens. Curr. Opin. Struct. Biol. 10, 443-462.CrossRefPubMedGoogle Scholar
  26. Sebbane, F., Jarrett, C.O., Gardner, D., Long, D. and Hinnebusch, B.J. (2006a). Role of the Yersinia pestis plasminogen activator in the incidence of distinct septicemic and bubonic forms of flea-borne plague. Proc. Natl. Acad. Sci. USA 103, 5526-5530.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Sebbane, F., Lemaite, N., Sturdevant, D.E., Rebeil, R., Virtaneva, K., Porcella, S.F. and Hinnebusch, B.J. (2006b) Adaptive response of Yersinia pestis to extracellular effectors of innate immunity during bubonic plague. Proc. Natl. Acad. Sci. USA 103, 11766-11771.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Skurnik, M., Peippo, A. and Ervelä, E. (2000) Characterization of the O-antigen gene clusters of Yersinia pseudotuberculosis and the cryptic O-antigen cluster of Yersinia pestis shows that the plague bacillus is most closely related to and has evolved from Y. pseudotubercu-losis serotype O1b. Mol. Microbiol. 37, 316-330.CrossRefPubMedGoogle Scholar
  29. Sodeinde, O.A. and Goguen J.D. (1989) Nucleotide sequence of the plasminogen activator gene of Yersinia pestis: relationship to ompT of E. coli and gene E of Salmonella typhi-murium. Infect. Immun. 57, 1517-1523.PubMedPubMedCentralGoogle Scholar
  30. Sodeinde, O.A., Subrahmanyam, Y.V.B.K., Stark, K., Quan, T., Bao, Y. and Goguen, J.D. (1992) A surface protease and the invasive character of plague. Science 258, 1004-1007.CrossRefPubMedGoogle Scholar
  31. Stumpe, S., Schmid, R., Stephens, D.L., Georgiu, G. and Bakker, E.P. (1998) Identification of OmpT as the protease that hydrolyzes the antimicrobial peptide protamine before it enters growing cells of E. coli. J. Bacteriol. 180,4002-4006.PubMedPubMedCentralGoogle Scholar
  32. Vandeputte-Rutten, L., Kramer, R.A., Kroon, J., Dekker, N., Egmond, M.R. and Gros, P. (2001) Crystal structure of the outer membrane protease OmpT from E. coli suggests a novel catalytic site. EMBO J. 20, 5033-5039.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Yu, C.Q. and Hong, J.S. (1986) Identification and nucleotide sequence of the activator gene of the externally induced phosphoglycerate transport system of Salmonella typhimurium. Gene 45, 51-57.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Marjo Suomalainen
    • 1
  • Johanna Haiko
    • 2
  • Maini Kukkonen
    • 1
  • Timo K. Korhonen
    • 1
  • Kaarina Lähteenmäki
    • 1
  • Ritva Virkola
    • 1
  • Benita Westerlund-Wikström
    • 1
  • Leandro Lobo
    • 1
  • Päivi Ramu
    • 1
  1. 1.Faculty of Biosciences, General MicrobiologyUniversity of HelsinkiFinland
  2. 2.Department of Biological and Environmental SciencesUniversity of HelsinkiFinland

Personalised recommendations