Exploring the 3D molecular architecture of Escherichia coli type 1 pili

Journal of Molecular Biology

Volumn 323, Issue 5, 2002, Pages 845-857

  Hahn, Erik ^a   Wild, Peter ^a   Hermanns, Uta ^b   Sebbel, Peter ^b   Glockshuber, Rudi ^b   Häner, Marcus ^c   Taschner, Nicole ^c   Burkhard, Peter ^c   Aebi, Ueli ^c   Müller, Shirley A ^c  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF BASEL   (Switzerland)

Author keywords

3D model; FimH; Immuno gold labeling; Pilus; Scanning transmission electron microscopy

Indexed keywords

PROTEIN; PROTEIN FIMA; PROTEIN FIMF; PROTEIN FIMG; PROTEIN FIMH; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

ARTICLE; BACTERIUM PILUS; BINDING SITE; BLADDER EPITHELIUM; CALCULATION; CONTROLLED STUDY; ESCHERICHIA COLI; FOURIER TRANSFORMATION; IMMUNOELECTRON MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STRUCTURE; SCANNING TRANSMISSION ELECTRON MICROSCOPY;

ESCHERICHIA COLI;

EID: 0036428752     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(02)01005-7     Document Type: Article

References (49)

1. Soto, G. E. & Hultgren, S. J. (1999). Bacterial adhesins: Common themes and variations in architecture and assembly. J. Bacteriol. 181, 1059-1071.
2. Beachey, E. H., Giampapa, C. S. & Abraham, S. N. (1988). Bacterial adherence. Adhesin receptor-mediated attachment of pathogenic bacteria to mucosal surfaces. Am. Rev. Respir. Dis. 138, 45-48.
3. Smyth, C. J., Marron, M. & Smyth, S. G. J. (1994). Fimbriae of Escherichia coli. In Escherichia coli in Domestic Animals and Humans (Gyles, C. L., ed.), pp. 399-435, CAB International, Wallingford, UK.
4. Kuehn, M. J., Haslam, D., Normak, S. & Hultgren, S. J. (1994). Structure, function, and biogenesis of Escherichia coli P-pili. In Fimbriae: Adhesion, Genetics, Biogenesis, and Vaccines (Klemm, P., ed.), pp. 37-51, CRC Press, Boca Raton, FL.
5. Klemm, P. & Krogfelt, K. A. (1994). Type 1-fimbriae of Escherichia coli. In Fimbriae: Adhesion, Genetics, Biogenesis, and Vaccines (Klemm, P., ed.), pp. 9-26, CRC Press, Boca Raton, FL.
6. Mulvey, M. A., Lopez-Boado, Y. S., Wilson, C. L., Roth, R., Parks, W. C., Heuser, J. & Hultgren, S. J. (1998). Induction and evasion of host defenses by type 1-piliated uropathogenic Escherichia coli. Science, 282, 1494-1497.
7. Min, G., Stolz, M., Zhou, G., Liang, F., Sebbel, P., Stoffler, D. et al. (2002). Localization of uroplakin 1a, the urothelial receptor for bacterial adhesin FimH, on the six inner domains of the 16 nm urothelial plaque particel. J. Mol. Biol. 317, 701-711.
8. Abraham, S. N., Sun, D., Dale, J. B. & Beachey, E. H. (1988). Conservation of the D-mannose-adhesion protein among type 1 fimbriated members of the family enterobacteriaceae. Nature, 336, 682-684.
9. Sokurenko, E. V., Chesnokova, V., Dykhuizen, D. E., Ofek, I., Wu, X. R., Krogfelt, K. A. et al. (1998). Pathogenic adaptation of Escherichia coli by natural variation of the FimH adhesin. Proc. Natl Acad. Sci. USA, 95, 8922-8926.
10. Thanassi, D. G., Saulino, E. T. & Hultgren, S. J. (1998). The chaperone/usher pathway: A major terminal branch of the general secretory pathway. Curr. Opin. Microbiol. 1, 223-231.
11. Thanassi, D. G., Saulino, E. T., Lombardo, M. J., Roth, R., Heuser, J. & Hultgren, S. J. (1998). The PapC usher forms an oligomeric channel: Implications for pilus biogenesis across the outer membrane. Proc. Natl Acad. Sci. USA, 95, 3146-3151.
12. Jones, C. H., Pinkner, J. S., Roth, R., Heuser, J., Nicholes, A. V., Abraham, S. N. & Hultgren, S. J. (1995). FimH adhesin of type 1 pili is assembled into a fibrillar tip structure in the enterobacteriaceae. Proc. Natl Acad. Sci. USA, 92, 2081-2085.
13. Brinton, C. C. J. (1965). The structure, functions, synthesis and genetic control of bacterial pili and a molecular model for DNA and RNA transport in gram negative bacteria. Trans. NY Acad. Sci. 27, 1003-1054.
14. Lindberg, F., Lund, B., Johansson, L. & Normark, S. (1987). Localization of the receptor-binding protein adhesin at the tip of the bacterial pilus. Nature, 328, 84-87.
15. Bullitt, E. & Makowski, L. (1995). Structural polymorphism of bacterial adhesion pili. Nature, 373, 164-167.
16. Choudhury, D., Thompson, A., Stojanoff, V., Langermann, S., Pinkner, J., Hultgren, S. J. & Knight, S. D. (1999). X-ray structure of the FimC-FimH chaperone-adhesin complex from uropathogenic Escherichia coli. Science, 285, 1061-1066.
17. Klemm, P. (1984). The fimA gene encoding the type-1 fimbrial subunit of Escherichia coli. Nucleotide sequence and primary structure of the protein. Eur. J. Biochem. 143, 395-399.
18. Klemm, P. & Christiansen, G. (1987). Three fim genes required for the regulation of length and mediation of adhesion of Escherichia coli type 1 fimbriae. Mol. Gen. Genet. 208, 439-445.
19. Smith, P. R. & Aebi, U. (1974). Computer-generated Fourier transforms of helical particles. J. Phys. 7, 1627-1633.
20. Baschong, W., Aebi, U., Baschong-Prescianotto, C., Dubochet, J., Landmann, L., Kellenberger, E. & Wurtz, M. (1988). Head structure of bacteriophages T2 and T4. J. Ultrastruct. Mol. Struct. Res. 99, 189-202.
21. Hahn, E., Wild, P., Schraner, E. M., Bertschinger, H. U., Häner, M., Müller, S. A. & Aebi, U. (2000). Structural analysis of F18 fimbriae expressed by porcine toxigenic Escherichia coli. J. Struct. Biol. 132, 241-250.
22. Henn, C., Teschner, M., Engel, A. & Aebi, U. (1996). Real-time isocontouring and texture mapping meet new challenges in interactive molecular graphics applications. J. Struct. Biol. 116, 86-92.
23. Giron, J. A., Ho, A. S. Y. & Schoolnik, G. K. (1991). An inducible bundle-forming pilus of enteropathogenic Escherichia coli. Science, 254, 710-713.
24. Donnenberg, M. S. (2000). Pathogenic strategies of enteric bacteria. Nature, 406, 768-774.
25. Simons, B. L., Mol, O., Van Breemen, J. F. L. & Oudega, B. (1994). Morphological appearances of K88 ab fimbriae and optical diffraction analysis of K88 paracrystalline structures. FEMS Microbiol. Letters, 118, 83-88.
26. Steven, A. C., Bisher, M. E., Trus, B. L., Thomas, D., Zhang, J. M. & Cowell, J. L. (1986). Helical structure of Bordetella pertussis fimbriae. J. Bacteriol. 167, 968-974.
27. Hamilton, R. C., Bennet, J., Drane, D., Pietrzykowski, E., Seddon, F., Stefancic, A. & Cox, J. (1994). Negative staining can cause clumping of Bordetella pertussis fimbriae. Micron, 25, 613-615.
28. Kuehn, M. J., Heuser, J., Normark, S. & Hultgren, S. J. (1992). P-pili in uropathogenic Escherichia coli are composite fibres with distinct fibrillar adhesive tips. Nature, 356, 252-255.
29. Saulino, E. T., Bullitt, E. & Hultgren, S. J. (2000). Snapshots of usher-mediated protein secretion and ordered pilus assembly. Proc. Natl Acad. Sci. USA, 97, 9240-9245.
30. Bork, P., Holm, L. & Sander, C. (1994). The immunoglobulin fold. Structural classification, sequence patterns and common core. J. Mol. Biol. 242, 309-320.
31. Sauer, F. G., Futterer, K., Pinkner, J. S., Dodson, K. W., Hultgren, S. J. & Waksman, G. (1999). Structural basis of chaperone function and pilus biogenesis. Science, 285, 1058-1061.
32. Barnhart, M. M., Pinkner, J. S., Soto, G. E., Sauer, F. G., Langermann, S., Waksman, G. et al. (2000). PapD-like chaperones provide the missing information for folding of pilin proteins. Proc. Natl Acad. Sci. USA, 97, 7709-7714.
33. Sauer, F. G., Knight, S. D., Waksman, G. & Hultgren, S. J. (2000). PapD-like chaperones and pilus biogenesis. Semin. Cell Dev. Biol. 11, 27-34.
34. Klemm, P. & Christiansen, G. (1990). The fimD gene required for cell surface localization of Escherichia coli type 1 fimbriae. Mol. Gen. Genet. 220, 334-338.
35. Mulvey, M. A., Schilling, J. D., Martinez, J. J. & Hultgren, S. J. (2000). Bad bugs and beleaguered bladders: Interplay between uropathogenic Escherichia coli and innate host defenses. Proc. Natl Acad. Sci. USA, 97, 8829-8835.
36. Merz, A. J., So, M. & Sheetz, M. P. (2000). Pilus retraction powers bacterial twitching motility. Nature, 407, 98-102.
37. Pellecchia, M., Sebbel, P., Hermanns, U., Wuthrich, K. & Glockshuber, R. (1999). Pilus chaperone FimC-adhesin FimH interactions mapped by TROSY-NMR. Nature Struct. Biol. 6, 336-339.
38. Blomfield, I. C., McClain, M. S. & Eisenstein, B. I. (1991). Type 1 fimbriae mutants of Escherichia coli K12: Characterization of recognized afimbriate strains and construction of new fim deletion mutants. Mol. Microbiol. 5, 1439-1445.
39. Orndorff, P. E. & Falkow, S. (1984). Organization and expression of genes responsible for type 1 piliation in Escherichia coli. J. Bacteriol. 159, 736-744.
40. Slot, J. W. & Geuze, H. J. (1985). A new method of preparing gold probes for multiple-labeling cytochemistry. Eur. J. Cell Biol. 38, 87-93.
41. Baschong, W. & Wrigley, N. G. (1990). Small colloidal gold conjugated to Fab fragments or to immunoglobulin G as high-resolution labels for electron microscopy: A technical overview. J. Electron Microsc. Technol. 14, 313-323.
42. Engel, A. (1978). Molecular weight determination by scanning transmission electron microscopy. Ultramicroscopy, 3, 273-281.
43. Müller, S. A., Goldie, K. N., Bürki, R., Häring, R. & Engel, A. (1992). Factors influencing the precision of quantitative scanning transmission electron microscopy. Ultramicroscopy, 46, 317-334.
44. Smith, P. R. & Gottesman, S. M. (1996). The micrograph data processing program. J. Struct. Biol. 116, 35-40.
45. Bremer, A., Henn, C., Goldie, K. N., Engel, A., Smith, P. R. & Aebi, U. (1994). Towards atomic interpretation of F-actin filament three-dimensional reconstructions. J. Mol. Biol. 242, 683-700.
46. Taylor, K. A. & Amos, L. A. (1981). A new model for the geometry of the binding of myosin crossbridges to muscle thin filaments. J. Mol. Biol. 147, 297-324.
47. Schwede, T., Diemand, A., Guex, N. & Peitsch, M. C. (2000). Protein structure computing in the genomic era. Res. Microbiol. 151, 107-112.
48. Collaborative Computing Project No. 4. (1994). The CCP4 suite: Programs for protein crystallography. Acta Crystallog. Sect. D, 50, 760-763.
49. Sanner, M. F., Olson, A. J. & Spehner, J. C. (1996). Reduced surface: An efficient way to compute molecular surfaces. Biopolymers, 38, 305-320.