Structure and Assembly of Yersinia pestis F1 Antigen

  • Stefan D. Knight
Part of the Advances In Experimental Medicine And Biology book series (AEMB, volume 603)

Most Gram negative pathogens express surface located fibrillar organelles that are used for adhesion to host epithelia and/or for protection. The assembly of many such organelles is managed by a highly conserved periplasmic chaperone/usher assembly pathway. During the last few years, considerable progress has been made in understanding how periplasmic chaperones mediate folding, targeting, and assembly of F1 antigen subunits into the F1 capsular antigen. In particular, structures representing snapshots of several of the steps involved in assembly have allowed us to begin to draw a detailed molecular-level picture of F1 assembly specifically, and of chaperone/usher-mediated assembly in general. Here, a brief summary of these new results will be presented.


Fiber Module Yersinia Pestis Circular Permutation Folding Energy Pilus Assembly 
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  1. Ahting, U., Thieffry, M., Engelhardt, H., Hegerl, R., Neupert, W. and Nussberger, S. (2001) Tom40, the pore-forming component of the protein-conducting tom channel in the outer membrane of mitochondria. J Cell Biol 153, 1151-1160.CrossRefPubMedPubMedCentralGoogle Scholar
  2. Barnhart, M. M., Sauer, F. G., Pinkner, J. S. and Hultgren, S. J. (2003) Chaperone-subunit-usher interactions required for donor strand exchange during bacterial pilus assembly. J Bacteriol 185, 2723-2730.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Berglund, J. and Knight, S. D. (2003) Structural basis for bacterial adhesion in the urinary tract. Adv Exp Med Biol 535, 33-52.CrossRefPubMedGoogle Scholar
  4. Bernier, C., Gounon, P. and Le Bouguenec, C. (2002) Identification of an aggregative adhesion fimbria (AAF) type III-encoding operon in enteroaggregative Escherichia coli as a sensitive probe for detecting the AAF-encoding operon family. Infect Immun 70, 4302-4311.CrossRefPubMedPubMedCentralGoogle Scholar
  5. Brandts, J. F. and Lin, L. N. (1990) Study of strong to ultratight protein interactions using differential scanning calorimetry. Biochemistry 29, 6927-6940.CrossRefPubMedGoogle Scholar
  6. Chalton, D. A., Musson, J. A., Flick-Smith, H., Walker, N., McGregor, A., Lamb, H. K., Williamson, E. D., Miller, J., Robinson, J. H. and Lakey, J. H. (2006) Immunogenicity of a Yersinia pestis vaccine antigen monomerized by circular permutation. Infect Immun 74, 6624-6631.CrossRefPubMedPubMedCentralGoogle Scholar
  7. Chen, T. H. and Elberg, S. S. (1977) Scanning electron microscopic study of virulent Yersinia pestis and Yersinia pseudotuberculosis type 1. Infect Immun 15, 972-977.PubMedPubMedCentralGoogle Scholar
  8. Choudhury, D., Thompson, A., Stojanoff, V., Langermann, S., Pinkner, J., Hultgren, S. J. and Knight, S. D. (1999) X-ray structure of the FimE-FimH chaperone-adhesin complex from uropathogenic Escherichia coli [see comments]. Science 285, 1061-1066.CrossRefPubMedGoogle Scholar
  9. Davis, K. J., Fritz, D. L., Pitt, M. L., Welkos, S. L., Worsham, P. L. and 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.PubMedGoogle Scholar
  10. Drozdov, I. G., Anisimov, A. P., Samoilova, S. V., Yezhov, I. N., Yeremin, S. A., Karlyshev, A. V., Krasilnikova, V. M. and Kravchenko, V. I. (1995) Virulent non-capsulate Yersinia pestis variants constructed by insertion mutagenesis. J Med Microbiol 42, 264-268.CrossRefPubMedGoogle Scholar
  11. Du, Y., Galyov, E. and Forsberg, A. (1995) Genetic analysis of virulence determinants unique to Yersinia pestis. Contrib Microbiol Immunol 13, 321-324.PubMedGoogle Scholar
  12. Du, Y., Rosqvist, R. and Forsberg, A. (2002) Role of fraction 1 antigen of Yersinia pestis in inhibition of phagocytosis. Infect Immun 70, 1453-1460.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Friedlander, A. M., Welkos, S. L., Worsham, P. L., Andrews, G. P., Heath, D. G., Anderson, G. W., Jr., Pitt, M. L., Estep, J. and Davis, K. (1995) Relationship between virulence and immunity as revealed in recent studies of the F1 capsule of Yersinia pestis. Clin Infect Dis 21 Suppl 2, S178-181.CrossRefPubMedGoogle Scholar
  14. Galyov, E. E., Smirnov, O., Karlishev, A. V., Volkovoy, K. I., Denesyuk, A. I., Nazimov, I. V., Rubtsov, K. S., Abramov, V. M., Dalvadyanz, S. M. and Zav’yalov, V. P. (1990) Nucleotide sequence of the Yersinia pestis gene encoding F1 antigen and the primary structure of the protein. Putative T and B cell epitopes. FEBS Lett 277, 230-232.CrossRefPubMedGoogle Scholar
  15. Henderson, N. S., So, S. S., Martin, C., Kulkarni, R. and Thanassi, D. G. (2004) Topology of the outer membrane usher PapE determined by site-directed fluorescence labeling. J Biol Chem 279, 53747-53754.CrossRefPubMedGoogle Scholar
  16. Hung, D. L. and Hultgren, S. J. (1998) Pilus biogenesis via the chaperone/usher pathway: An integration of structure and function. J Struct Biol 124, 201-220.CrossRefPubMedGoogle Scholar
  17. Hung, D. L., Knight, S. D., Woods, R. M., Pinkner, J. S. and Hultgren, S. J. (1996) Molecular basis of two subfamilies of immunoglobulin-like chaperones. EMBO J. 15, 3792-3805.PubMedPubMedCentralGoogle Scholar
  18. Jacob-Dubuisson, F., Striker, R. and Hultgren, S. J. (1994) Chaperone-assisted self-assembly of pili independent of cellular energy. J Biol Chem 269, 12447-12455.PubMedGoogle Scholar
  19. Karlyshev, A. V., Galyov, E. E., Smirnov, O. Y., Abramov, V. M. and Zav’yalov, V. P. (1994) Structure and regulation of a gene cluster involved in capsule formation of Yersinia pestis. In J. A. F. O. d. Kamp, (Ed.) Biological membranes: Structure, biogenesis and dynamics. Springer-Verlag, Berlin, pp. 321-330.CrossRefGoogle Scholar
  20. Knight, S. D., Berglund, J. and Choudhury, D. (2000) Bacterial adhesins: Structural studies reveal chaperone function and pilus biogenesis. Curr Opin Chem Biol 4, 653-660.CrossRefPubMedGoogle Scholar
  21. Li, H., Qian, L., Chen, Z., Thibault, D., Liu, G., Liu, T. and Thanassi, D. G. (2004) The outer membrane usher forms a twin-pore secretion complex. J Mol Biol 344, 1397-1407.CrossRefPubMedGoogle Scholar
  22. MacIntyre, S., Knight, S. D. and Fooks, L. J. (2004) Structure assembly and applications of the polymeric F1 antigen of Yersinia pestis. In E. Carniel and J. Hinnebusch, (Eds.), Molecular and cellular biology of pathogenic yersinia. Horizon Press, U.K.Google Scholar
  23. MacIntyre, S., Zyrianova, I. M., Chernovskaya, T. V., Leonard, M., Rudenko, E. G., Zav’yalov, V. P. and Chapman, D. A. G. (2001) An extended hydrophobic interactive surface of Yersinia pestis caf1m chaperone is essential for subunit binding and F1 capsule assembly. Mol Microbiol 39, 12-25.CrossRefPubMedGoogle Scholar
  24. Makhatadze, G. I. and Privalov, P. L. (1995) Energetics of protein structure. Adv Protein Chem 47, 307-425.CrossRefPubMedGoogle Scholar
  25. Mulvey, M. A. (2002) Adhesion and entry of uropathogenic Escherichia coli. Cell Microbiol 4, 257-271.CrossRefPubMedGoogle Scholar
  26. Ng, T. W., Akman, L., Osisami, M. and Thanassi, D. G. (2004) The usher N terminus is the initial targeting site for chaperone-subunit complexes and participates in subsequent pilus biogenesis events. J Bacteriol 186, 5321-5331.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Nishiyama, M., Horst, R., Eidam, O., Herrmann, T., Ignatov, O., Vetsch, M., Bettendorff, P., Jelesarov, I., Grutter, M. G., Wuthrich, K., Glockshuber, R. and Capitani, G. (2005) Structural basis of chaperone-subunit complex recognition by the type 1 pilus assembly platform FimD. Embo J 24, 2075-2086.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Nishiyama, M., Vetsch, M., Puorger, C., Jelesarov, I. and Glockshuber, R. (2003) Identification and characterization of the chaperone-subunit complex-binding domain from the type 1 pilus assembly platform FimD. J Mol Biol 330, 513-525.CrossRefPubMedGoogle Scholar
  29. Perry, R. D. and Fetherston, J. D. (1997) Yersinia pestis--etiologic agent of plague. Clin. Microbiol. Rev. 10, 35-66.PubMedPubMedCentralGoogle Scholar
  30. Sauer, F. G., Barnhart, M., Choudhury, D., Knight, S. D., Waksman, G. and Hultgren, S. J. (2000a) Chaperone-assisted pilus assembly and bacterial attachment. Curr Opin Struc Biol 10, 548-556.CrossRefGoogle Scholar
  31. Sauer, F. G., Futterer, K., Pinkner, J. S., Dodson, K. W., Hultgren, S. J. and Waksman, G. (1999) Structural basis of chaperone function and pilus biogenesis. Science 285, 1058-1061.CrossRefPubMedGoogle Scholar
  32. Sauer, F. G., Knight, S. D., and Hultgren, S. J. (2000b) PapD-like chaperones and pilus biogenesis. Semin Cell Dev Biol 11, 27-34.CrossRefPubMedGoogle Scholar
  33. Sauer, F. G., Pinkner, J. S., Waksman, G. and Hultgren, S. J. (2002) Chaperone priming of pilus subunits facilitates a topological transition that drives fiber formation. Cell 111, 543-551.CrossRefPubMedGoogle Scholar
  34. So, S. S. and Thanassi, D. G. (2006) Analysis of the requirements for pilus biogenesis at the outer membrane usher and the function of the usher C-terminus. Mol Microbiol 60, 364-375.CrossRefPubMedGoogle Scholar
  35. Soto, G. E., Dodson, K. W., Ogg, D., Liu, C., Heuser, J., Knight, S., Kihlberg, J., Jones, C. H. and Hultgren, S. J. (1998) Periplasmic chaperone recognition motif of subunits mediates quaternary interactions in the pilus. Embo J 17, 6155-6167.CrossRefPubMedPubMedCentralGoogle Scholar
  36. Soto, G. E. and Hultgren, S. J. (1999) Bacterial adhesins: Common themes and variations in architecture and assembly. J Bacteriol 181, 1059-1071.PubMedPubMedCentralGoogle Scholar
  37. Stathopoulos, C., Hendrixson, D. R., Thanassi, D. G., Hultgren, S. J., St Geme, J. W., 3rd and Curtiss, R., 3rd (2000) Secretion of virulence determinants by the general secretory pathway in gram-negative pathogens: An evolving story. Microbes Infect 2, 1061-1072.CrossRefPubMedGoogle Scholar
  38. Thanassi, D. G. and Hultgren, S. J. (2000) Assembly of complex organelles: Pilus biogenesis in gram-negative bacteria as a model system. Methods 20, 111-126.CrossRefPubMedGoogle Scholar
  39. Thanassi, D. G., Stathopoulos, C., Dodson, K., Geiger, D. and Hultgren, S. J. (2002) Bacterial outer membrane ushers contain distinct targeting and assembly domains for pilus biogenesis. J Bacteriol 184, 6260-6269.CrossRefPubMedPubMedCentralGoogle Scholar
  40. Titball, R. W. and Williamson, E. D. (2001) Vaccination against bubonic and pneumonic plague. Vaccine 19, 4175-4184.CrossRefPubMedGoogle Scholar
  41. Titball, R. W. and Williamson, E. D. (2004) Yersinia pestis (plague) vaccines. Expert Opin Biol Ther 4, 965-973.CrossRefPubMedGoogle Scholar
  42. Vetsch, M., Erilov, D., Moliere, N., Nishiyama, M., Ignatov, O. and Glockshuber, R. (2006) Mechanism of fibre assembly through the chaperone-usher pathway. EMBO Rep 7, 734-738.CrossRefPubMedPubMedCentralGoogle Scholar
  43. Vetsch, M., Puorger, C., Spirig, T., Grauschopf, U., Weber-Ban, E. U. and Glockshuber, R. (2004) Pilus chaperones represent a new type of protein-folding catalyst. Nature 431, 329-333.CrossRefPubMedGoogle Scholar
  44. Vetsch, M., Sebbel, P. and Glockshuber, R. (2002) Chaperone-independent folding of type 1 pilus domains. J Mol Biol 322, 827-840.CrossRefPubMedGoogle Scholar
  45. Worsham, P. L., Stein, M. P. and Welkos, S. L. (1995) Construction of defined F1 negative mutants of virulent Yersinia pestis. Contrib Microbiol Immunol 13, 325-328.PubMedGoogle Scholar
  46. Zav’yalov, V. P., Chernovskaya, T. V., Chapman, D. A., Karlyshev, A. V., MacIntyre, S., Zavialov, A. V., Vasiliev, A. M., Denesyuk, A. I., Zav’yalova, G. A., Dudich, I. V., Korpela, T. and Abramov, V.M. (1997) Influence of the conserved disulphide bond, exposed to the putative binding pocket, on the structure and function of the immunoglobulin-like molecular chaperone Caf1M of Yersinia pestis. Biochem J 324 (Pt 2), 571-578.CrossRefPubMedPubMedCentralGoogle Scholar
  47. Zavialov, A. V., Berglund, J., Pudney, A. F., Fooks, L. J., Ibrahim, T. M., MacIntyre, S. and Knight, S. D. (2003) Structure and biogenesis of the capsular F1 antigen from Yersinia pestis: Preserved folding energy drives fiber formation. Cell 113, 587-596.CrossRefPubMedGoogle Scholar
  48. Zavialov, A. V., Kersley, J., Korpela, T., Zav’yalov, V. P., MacIntyre, S. and Knight, S. D. (2002) Donor strand complementation mechanism in the biogenesis of non-pilus systems. Mol Microbiol 45, 983-995.CrossRefPubMedGoogle Scholar
  49. Zavialov, A. V., Tischenko, V. M., Fooks, L. J., Brandsdal, B. O., Aqvist, J., Zav’yalov, V. P., Macintyre, S. and Knight, S. D. (2005) Resolving the energy paradox of chaperone/usher-mediated fibre assembly. Biochem J 389, 685-694.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Stefan D. Knight
    • 1
  1. 1.Department of Molecular BiologySwedish University of Agricultural SciencesSweden

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