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Bacterial Adhesion pp 159–174Cite as

Crystallography and Electron Microscopy of Chaperone/Usher Pilus Systems

Part of the Advances in Experimental Medicine and Biology book series (AEMB,volume 715)

Abstract

Among bacteria, the chaperone-usher (CU) pathway is a widespread conserved assembly and translocation system for adhesive protein fibres, called pili or fimbriae. Pili are large linear polymers that protrude from the outer bacterial surface and consist of several subunits. Pili contain adhesin proteins at the tip that are used by pathogenic bacteria to mediate attachment to host cells and initiate infections. Well studied examples of CU pili are P and type 1 pili of uropathogenic Escherichia coli (UPEC), which are responsible for kidney and bladder infections, respectively. Upon secretion into the periplasm, pilus subunits are stabilized by periplasmic chaperones and the resulting chaperone:subunit complexes are guided to the usher located in the outer membrane. The usher catalyzes the ordered assembly of pilus subunits while releasing the chaperones and translocating the growing pilus stepwise to the outer surface. Here we review the structural biology of the chaperone-usher pathway that has helped to understand the mechanisms by which biogenesis of an important class of bacterial organelles occurs.

Keywords

  • Pilus Assembly
  • Periplasmic Chaperone
  • Pilus Biogenesis
  • Pilus Subunit
  • Plug Domain

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.

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References

  • Baga M, Norgren M, Normark S (1987) Biogenesis of E. coli pap pili: papH, a minor pilin subunit involved in cell anchoring and length modulation. Cell 49:241–251

    PubMed  CrossRef  CAS  Google Scholar 

  • Barnhart MM, Pinkner JS, Soto GE, Sauer FG, Langermann S, Waksman G, Frieden C, Hultgren SJ (2000) PapD-like chaperones provide the missing information for folding of pilin proteins. Proc Natl Acad Sci USA 97:7709–7714

    PubMed  CrossRef  CAS  Google Scholar 

  • Bullitt E, Makowski L (1995) Structural polymorphism of bacterial adhesion pili. Nature 373: 164–167

    PubMed  CrossRef  CAS  Google Scholar 

  • Buts L, Bouckaert J, De Genst E, Loris R, Oscarson S, Lahmann M, Messens J, Brosens E, Wyns L, De Greve H (2003) The fimbrial adhesin F17-G of enterotoxigenic Escherichia coli has an immunoglobulin-like lectin domain that binds N-acetylglucosamine. Mol Microbiol 49: 705–715

    PubMed  CrossRef  CAS  Google Scholar 

  • Capitani G, Eidam O, Grütter MG (2006) Evidence for a novel domain of bacterial outer membrane ushers. Proteins 65:816–823

    PubMed  CrossRef  CAS  Google Scholar 

  • Choudhury D, Thompson A, Stojanoff V, Langermann S, Pinkner J, Hultgren SJ, Knight SD (1999) X-ray structure of the FimC-FimH chaperone-adhesin complex from uropathogenic Escherichia coli. Science 285:1061–1066

    PubMed  CrossRef  CAS  Google Scholar 

  • Dodson KW, Pinkner JS, Rose T, Magnusson G, Hultgren SJ, Waksman G (2001) Structural basis of the interaction of the pyelonephritic E. coli adhesin to its human kidney receptor. Cell 105:733–743

    PubMed  CrossRef  CAS  Google Scholar 

  • Eidam O, Dworkowski FS, Glockshuber R, Grütter MG, Capitani G (2008) Crystal structure of the ternary FimC-FimF(t)-FimD(N) complex indicates conserved pilus chaperone-subunit complex recognition by the usher FimD. FEBS Lett 582:651–655

    PubMed  CrossRef  CAS  Google Scholar 

  • Ford B, Rego AT, Ragan TJ, Pinkner J, Dodson K, Driscoll PC, Hultgren S, Waksman G (2010) Structural homology between the C-terminal domain of the Papc usher and its plug. J Bacteriol 192:1824–1831

    PubMed  CrossRef  CAS  Google Scholar 

  • Gong M, Makowski L (1992) Helical structure of P pili from Escherichia coli. Evidence from X-ray fiber diffraction and scanning transmission electron microscopy. J Mol Biol 228:735–742

    PubMed  CrossRef  CAS  Google Scholar 

  • Hahn E, Wild P, Hermanns U, Sebbel P, Glockshuber R, Haner M, Taschner N, Burkhard P, Aebi U, Müller SA (2002) Exploring the 3D molecular architecture of Escherichia coli type 1 pili. J Mol Biol 323:845–857

    PubMed  CrossRef  CAS  Google Scholar 

  • Holmgren A, Brändén C-I (1989) Crystal structure of chaperone protein PapD reveals an immunoglobulin fold. Nature 342:248–251

    PubMed  CrossRef  CAS  Google Scholar 

  • Hooton TM, Scholes D, Hughes JP, Winter C, Roberts PL, Stapleton AE, Stergachis A, Stamm WE (1996) A prospective study of risk factors for symptomatic urinary tract infection in young women. N Engl J Med 335:468–474

    PubMed  CrossRef  CAS  Google Scholar 

  • Huang Y, Smith BS, Chen LX, Baxter RH, Deisenhofer J (2009) Insights into pilus assembly and secretion from the structure and functional characterization of usher PapC. Proc Natl Acad Sci USA 106:7403–7407

    PubMed  CrossRef  CAS  Google Scholar 

  • Hung CS, Bouckaert J, Hung D, Pinkner J, Widberg C, DeFusco A, Auguste CG, Strouse R, Langermann S, Waksman G, Hultgren SJ (2002) Structural basis of tropism of Escherichia coli to the bladder during urinary tract infection. Mol Microbiol 44:903–915

    PubMed  CrossRef  CAS  Google Scholar 

  • Jacob-Dubuisson F, Heuser J, Dodson K, Normark S, Hultgren S (1993) Initiation of assembly and association of the structural elements of a bacterial pilus depend on two specialized tip proteins. EMBO J 12:837–847

    PubMed  CAS  Google Scholar 

  • Jacob-Dubuisson F, Striker R, Hultgren SJ (1994) Chaperone-assisted self-assembly of pili independent of cellular energy. J Biol Chem 269:12447–12455

    PubMed  CAS  Google Scholar 

  • Jones CH, Danese PN, Pinkner JS, Silhavy TJ, Hultgren SJ (1997) The chaperone-assisted membrane release and folding pathway is sensed by two signal transduction systems. EMBO J 16:6394–6406

    PubMed  CrossRef  CAS  Google Scholar 

  • Jones CH, Pinkner JS, Roth R, Heuser J, Nicholes AV, Abraham SN, Hultgren SJ (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

    PubMed  CrossRef  CAS  Google Scholar 

  • Justice SS, Hunstad DA, Seed PC, Hultgren SJ (2006) Filamentation by Escherichia coli subverts innate defenses during urinary tract infection. Proc Natl Acad Sci USA 103:19884–19889

    PubMed  CrossRef  CAS  Google Scholar 

  • Krogfelt KA, Bergmans H, Klemm P (1990) Direct evidence that the FimH protein is the mannose-specific adhesin of Escherichia coli type 1 fimbriae. Infect Immun 58:1995–1998

    PubMed  CAS  Google Scholar 

  • Kuehn MJ, Heuser J, Normark S, Hultgren SJ (1992) P pili in uropathogenic E. coli are composite fibres with distinct fibrillar adhesive tips. Nature 356:252–255

    PubMed  CrossRef  CAS  Google Scholar 

  • Kuehn MJ, Normark S, Hultgren SJ (1991) Immunoglobulin-like PapD chaperone caps and uncaps interactive surfaces of nascently translocated pilus subunits. Proc Natl Acad Sci USA 88:10586–10590

    PubMed  CrossRef  CAS  Google Scholar 

  • Kuehn MJ, Ogg DJ, Kihlberg J, Slonim LN, Flemmer K, Bergfors T, Hultgren SJ (1993) Structural basis of pilus subunit recognition by the PapD chaperone. Science 262:1234–1241

    PubMed  CrossRef  CAS  Google Scholar 

  • Li H, Qian L, Chen Z, Thibault D, Liu G, Liu T, Thanassi DG (2004) The outer membrane usher forms a twin-pore secretion complex. J Mol Biol 344:1397–1407

    PubMed  CrossRef  CAS  Google Scholar 

  • 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

    PubMed  CrossRef  CAS  Google Scholar 

  • Lund B, Lindberg F, Marklund BI, Normark S (1987) The PapG protein is the alpha-D-galactopyranosyl-(1—4)-beta-D-galactopyranose-binding adhesin of uropathogenic Escherichia coli. Proc Natl Acad Sci USA 84:5898–5902

    PubMed  CrossRef  CAS  Google Scholar 

  • Martinez JJ, Mulvey MA, Schilling JD, Pinkner JS, Hultgren SJ (2000) Type 1 pilus-mediated bacterial invasion of bladder epithelial cells. EMBO J 19:2803–2812

    PubMed  CrossRef  CAS  Google Scholar 

  • Merckel MC, Tanskanen J, Edelman S, Westerlund-Wikström B, Korhonen TK, Goldman A (2003) The structural basis of receptor-binding by Escherichia coli associated with diarrhea and septicemia. J Mol Biol 331:897–905

    PubMed  CrossRef  CAS  Google Scholar 

  • Mulvey MA, Lopez-Boado YS, Wilson CL, Roth R, Parks WC, Heuser J, Hultgren SJ (1998) Induction and evasion of host defenses by type 1-piliated uropathogenic Escherichia coli. Science 282:1494–1497

    PubMed  CrossRef  CAS  Google Scholar 

  • Munera D, Hultgren S, Fernandez LA (2007) Recognition of the N-terminal lectin domain of FimH adhesin by the usher FimD is required for type 1 pilus biogenesis. Mol Microbiol 64:333–346

    PubMed  CrossRef  CAS  Google Scholar 

  • Munera D, Palomino C, Fernandez LA (2008) Specific residues in the N-terminal domain of FimH stimulate type 1 fimbriae assembly in Escherichia coli following the initial binding of the adhesin to FimD usher. Mol Microbiol 69:911–925

    PubMed  CrossRef  CAS  Google Scholar 

  • Ng TW, Akman L, Osisami M, Thanassi DG (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

    PubMed  CrossRef  CAS  Google Scholar 

  • Nishiyama M, Glockshuber R (2010) The outer membrane usher guarantees the formation of functional pili by selectively catalyzing donor-strand exchange between subunits that are adjacent in the mature pilus. J Mol Biol 396:1–8

    PubMed  CrossRef  CAS  Google Scholar 

  • Nishiyama M, Horst R, Eidam O, Herrmann T, Ignatov O, Vetsch M, Bettendorff P, Jelesarov I, Grütter MG, Wüthrich K, Glockshuber R, Capitani G (2005) Structural basis of chaperone-subunit complex recognition by the type 1 pilus assembly platform FimD. EMBO J 24: 2075–2086

    PubMed  CrossRef  CAS  Google Scholar 

  • Nishiyama M, Ishikawa T, Rechsteiner H, Glockshuber R (2008) Reconstitution of pilus assembly reveals a bacterial outer membrane catalyst. Science 320:376–379

    PubMed  CrossRef  CAS  Google Scholar 

  • Nishiyama M, Vetsch M, Puorger C, Jelesarov I, 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

    PubMed  CrossRef  CAS  Google Scholar 

  • Nuccio SP, Baumler AJ (2007) Evolution of the chaperone/usher assembly pathway: fimbrial classification goes Greek. Microbiol Mol Biol Rev 71:551–575

    PubMed  CrossRef  CAS  Google Scholar 

  • Pellecchia M, Guntert P, Glockshuber R, Wüthrich K (1998) NMR solution structure of the periplasmic chaperone FimC. Nat Struct Biol 5:885–890

    PubMed  CrossRef  CAS  Google Scholar 

  • Pinkner JS, Remaut H, Buelens F, Miller E, Aberg V, Pemberton N, Hedenstrom M, Larsson A, Seed P, Waksman G, Hultgren SJ, Almqvist F (2006) Rationally designed small compounds inhibit pilus biogenesis in uropathogenic bacteria. Proc Natl Acad Sci USA 103:17897–17902

    PubMed  CrossRef  CAS  Google Scholar 

  • Remaut H, Rose RJ, Hannan TJ, Hultgren SJ, Radford SE, Ashcroft AE, Waksman G (2006) Donor-strand exchange in chaperone-assisted pilus assembly proceeds through a concerted βßstrand displacement mechanism. Mol Cell 22:831–842

    PubMed  CrossRef  CAS  Google Scholar 

  • Remaut H, Tang C, Henderson NS, Pinkner JS, Wang T, Hultgren SJ, Thanassi DG, Waksman G, Li H (2008) Fiber formation across the bacterial outer membrane by the chaperone/usher pathway. Cell 133:640–652

    PubMed  CrossRef  CAS  Google Scholar 

  • Roberts JA, Marklund BI, Ilver D, Haslam D, Kaack MB, Baskin G, Louis M, Mollby R, Winberg J, Normark S (1994) The Gal(ά 1–4)Gal-specific tip adhesin of Escherichia coli P-fimbriae is needed for pyelonephritis to occur in the normal urinary tract. Proc Natl Acad Sci USA 91:11889–11893

    PubMed  CrossRef  CAS  Google Scholar 

  • Rose RJ, Verger D, Daviter T, Remaut H, Paci E, Waksman G, Ashcroft AE, Radford SE (2008) Unraveling the molecular basis of subunit specificity in P pilus assembly by mass spectrometry. Proc Natl Acad Sci USA 105:12873–12878

    PubMed  CrossRef  CAS  Google Scholar 

  • Sauer FG, Futterer K, Pinkner JS, Dodson KW, Hultgren SJ, Waksman G (1999) Structural basis of chaperone function and pilus biogenesis. Science 285:1058–1061

    PubMed  CrossRef  CAS  Google Scholar 

  • Sauer FG, Pinkner JS, Waksman G, Hultgren SJ (2002) Chaperone priming of pilus subunits facilitates a topological transition that drives fiber formation. Cell 111:543–551

    PubMed  CrossRef  CAS  Google Scholar 

  • Saulino ET, Thanassi DG, Pinkner JS, Hultgren SJ (1998) Ramifications of kinetic partitioning on usher-mediated pilus biogenesis. EMBO J 17:2177–2185

    PubMed  CrossRef  CAS  Google Scholar 

  • So SS, Thanassi DG (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

    PubMed  CrossRef  CAS  Google Scholar 

  • Thanassi DG, Stathopoulos C, Dodson K, Geiger D, Hultgren SJ (2002) Bacterial outer membrane ushers contain distinct targeting and assembly domains for pilus biogenesis. J Bacteriol 184:6260–6269

    PubMed  CrossRef  CAS  Google Scholar 

  • Verger D, Miller E, Remaut H, Waksman G, Hultgren S (2006) Molecular mechanism of P pilus termination in uropathogenic Escherichia coli. EMBO Rep 7:1228–1232

    PubMed  CrossRef  CAS  Google Scholar 

  • Verger D, Rose RJ, Paci E, Costakes G, Daviter T, Hultgren S, Remaut H, Ashcroft AE, Radford SE, Waksman G (2008) Structural determinants of polymerization reactivity of the P pilus adaptor subunit PapF. Structure 16:1724–1731

    PubMed  CrossRef  CAS  Google Scholar 

  • Vetsch M, Puorger C, Spirig T, Grauschopf U, Weber-Ban EU, Glockshuber R (2004) Pilus chaperones represent a new type of protein-folding catalyst. Nature 431:329–333

    PubMed  CrossRef  CAS  Google Scholar 

  • Wright KJ, Seed PC, Hultgren SJ (2007) Development of intracellular bacterial communities of uropathogenic Escherichia coli depends on type 1 pili. Cell Microbiol 9:2230–2241

    PubMed  CrossRef  CAS  Google Scholar 

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Authors and Affiliations

  1. Institute of Structural Molecular Biology, Birkbeck and University College London, London, UK

    Sebastian Geibel & Gabriel Waksman

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  1. Sebastian Geibel
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  2. Gabriel Waksman
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Correspondence to Gabriel Waksman .

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Editors and Affiliations

  1. , Department I, Protein Evolution, Max-Planck Institute for Developmental B, Spemannstr. 35, Tübingen, 72076, Germany

    Dirk Linke

  2. , Institute of Biotechnology, University of Helsinki, Viikinkaari 1, Helsinki, FIN-00014, Finland

    Adrian Goldman

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Geibel, S., Waksman, G. (2011). Crystallography and Electron Microscopy of Chaperone/Usher Pilus Systems. In: Linke, D., Goldman, A. (eds) Bacterial Adhesion. Advances in Experimental Medicine and Biology, vol 715. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-0940-9_10

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