Structural Insight into Archaic and Alternative Chaperone-Usher Pathways Reveals a Novel Mechanism of Pilus Biogenesis

English version České info

Gram-negative pathogens depend on fibrous adhesive organelles to attach to target tissues and establish infection. The major class of these organelles is assembled via the classical, alternative and archaic chaperone-usher (CU) pathways. CU pathways are recognized as promising new targets for the next generation of antibacterial drugs. The recently discovered archaic and alternative systems are of particular interest, as they are implicated in biofilm formation of antibiotic resistant pathogens, have a wider phylogenetic distribution and are associated with a broader range of diseases than the classical systems. Here, we report an atomic-resolution insight into the structure and assembly mechanism of two such biofilm-forming organelles assembled via the archaic and alternative pathways. We show that the archaic and alternative systems are structurally related, but their assembly mechanism is strikingly different from the classical assembly pathway. Whereas the classical chaperones deliver folded subunits to the usher assembly platform, non-classical chaperones apply a unique binding mechanism to maintain subunits in substantially unfolded state. The open subunit core allows for a new mode of strand replacement during polymerisation, and also represents an attractive target for the rational design of antimicrobials.

Vyšlo v časopise: Structural Insight into Archaic and Alternative Chaperone-Usher Pathways Reveals a Novel Mechanism of Pilus Biogenesis. PLoS Pathog 11(11): e32767. doi:10.1371/journal.ppat.1005269
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1005269

Souhrn

Zdroje

1. Nuccio SP, Baumler AJ (2007) Evolution of the chaperone/usher assembly pathway: fimbrial classification goes Greek. Microbiol Mol Biol Rev 71 : 551–575. 18063717

2. Busch A, Waksman G (2012) Chaperone-usher pathways: diversity and pilus assembly mechanism. Philos Trans R Soc Lond B Biol Sci 367 : 1112–1122. doi: 10.1098/rstb.2011.0206 22411982

3. Zav'yalov V, Zavialov A, Zav'yalova G, Korpela T (2010) Adhesive organelles of Gram-negative pathogens assembled with the classical chaperone/usher machinery: structure and function from a clinical standpoint. FEMS Microbiol Rev 34 : 317–378. doi: 10.1111/j.1574-6976.2009.00201.x 20070375

4. Berry AA, Yang Y, Pakharukova N, Garnett JA, Lee WC, et al. (2014) Structural Insight into Host Recognition by Aggregative Adherence Fimbriae of Enteroaggregative Escherichia coli. PLoS Pathog 10: e1004404. doi: 10.1371/journal.ppat.1004404 25232738

5. Bao R, Nair MK, Tang WK, Esser L, Sadhukhan A, et al. (2013) Structural basis for the specific recognition of dual receptors by the homopolymeric pH 6 antigen (Psa) fimbriae of Yersinia pestis. Proc Natl Acad Sci U S A 110 : 1065–1070. doi: 10.1073/pnas.1212431110 23277582

6. Garnett JA, Martinez-Santos VI, Saldana Z, Pape T, Hawthorne W, et al. (2012) Structural insights into the biogenesis and biofilm formation by the Escherichia coli common pilus. Proc Natl Acad Sci U S A 109 : 3950–3955. doi: 10.1073/pnas.1106733109 22355107

7. Tomaras AP, Dorsey CW, Edelmann RE, Actis LA (2003) Attachment to and biofilm formation on abiotic surfaces by Acinetobacter baumannii: involvement of a novel chaperone-usher pili assembly system. Microbiology 149 : 3473–3484. 14663080

8. Tomaras AP, Flagler MJ, Dorsey CW, Gaddy JA, Actis LA (2008) Characterization of a two-component regulatory system from Acinetobacter baumannii that controls biofilm formation and cellular morphology. Microbiology 154 : 3398–3409. doi: 10.1099/mic.0.2008/019471-0 18957593

9. Rendon MA, Saldana Z, Erdem AL, Monteiro-Neto V, Vazquez A, et al. (2007) Commensal and pathogenic Escherichia coli use a common pilus adherence factor for epithelial cell colonization. Proc Natl Acad Sci U S A 104 : 10637–10642. 17563352

10. Pouttu R, Westerlund-Wikstrom B, Lang H, Alsti K, Virkola R, et al. (2001) matB, a common fimbrillin gene of Escherichia coli, expressed in a genetically conserved, virulent clonal group. J Bacteriol 183 : 4727–4736. 11466275

11. Choudhury D, Thompson A, Stojanoff V, Langermann S, Pinkner J, et al. (1999) X-ray structure of the FimC-FimH chaperone-adhesin complex from uropathogenic Escherichia coli. Science 285 : 1061–1066. 10446051

12. Sauer FG, Futterer K, Pinkner JS, Dodson KW, Hultgren SJ, et al. (1999) Structural basis of chaperone function and pilus biogenesis. Science 285 : 1058–1061. 10446050

13. Remaut H, Rose RJ, Hannan TJ, Hultgren SJ, Radford SE, et al. (2006) Donor-strand exchange in chaperone-assisted pilus assembly proceeds through a concerted beta strand displacement mechanism. Mol Cell 22 : 831–842. 16793551

14. Zavialov AV, Berglund J, Pudney AF, Fooks LJ, Ibrahim TM, et al. (2003) Structure and biogenesis of the capsular F1 antigen from Yersinia pestis: preserved folding energy drives fiber formation. Cell 113 : 587–596. 12787500

15. 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. 12437927

16. Nishiyama M, Ishikawa T, Rechsteiner H, Glockshuber R (2008) Reconstitution of pilus assembly reveals a bacterial outer membrane catalyst. Science 320 : 376–379. doi: 10.1126/science.1154994 18369105

17. Phan G, Remaut H, Wang T, Allen WJ, Pirker KF, et al. (2011) Crystal structure of the FimD usher bound to its cognate FimC-FimH substrate. Nature 474 : 49–53. doi: 10.1038/nature10109 21637253

18. Li YF, Poole S, Nishio K, Jang K, Rasulova F, et al. (2009) Structure of CFA/I fimbriae from enterotoxigenic Escherichia coli. Proc Natl Acad Sci U S A 106 : 10793–10798. doi: 10.1073/pnas.0812843106 19515814

19. Zavialov AV, Kersley J, Korpela T, Zav'yalov VP, MacIntyre S, et al. (2002) Donor strand complementation mechanism in the biogenesis of non-pilus systems. Mol Microbiol 45 : 983–995. 12180918

20. Bao R, Fordyce A, Chen YX, McVeigh A, Savarino SJ, et al. (2014) Structure of CfaA suggests a new family of chaperones essential for assembly of class 5 fimbriae. PLoS Pathog 10: e1004316. doi: 10.1371/journal.ppat.1004316 25122114

21. Hung DL, Knight SD, Woods RM, Pinkner JS, Hultgren SJ (1996) Molecular basis of two subfamilies of immunoglobulin-like chaperones. EMBO J 15 : 3792–3805. 8670884

22. Pellecchia M, Sebbel P, Hermanns U, Wuthrich K, Glockshuber R (1999) Pilus chaperone FimC-adhesin FimH interactions mapped by TROSY-NMR. Nat Struct Biol 6 : 336–339. 10201401

23. Bann JG, Pinkner JS, Frieden C, Hultgren SJ (2004) Catalysis of protein folding by chaperones in pathogenic bacteria. Proc Natl Acad Sci U S A 101 : 17389–17393. 15583129

24. Zavialov AV, Tischenko VM, Fooks LJ, Brandsdal BO, Aqvist J, et al. (2005) Resolving the energy paradox of chaperone/usher-mediated fibre assembly. Biochem J 389 : 685–694. 15799718

25. Yu XD, Fooks LJ, Moslehi-Mohebi E, Tischenko VM, Askarieh G, et al. (2012) Large is fast, small is tight: determinants of speed and affinity in subunit capture by a periplasmic chaperone. J Mol Biol 417 : 294–308. doi: 10.1016/j.jmb.2012.01.020 22321795

26. Verger D, Rose RJ, Paci E, Costakes G, Daviter T, et al. (2008) Structural determinants of polymerization reactivity of the P pilus adaptor subunit PapF. Structure 16 : 1724–1731. doi: 10.1016/j.str.2008.08.012 19000824

27. Pinkner JS, Remaut H, Buelens F, Miller E, Aberg V, et al. (2006) Rationally designed small compounds inhibit pilus biogenesis in uropathogenic bacteria. Proc Natl Acad Sci U S A 103 : 17897–17902. 17098869

28. Pakharukova N, Tuittila M, Paavilainen S, Zavialov A (2015) Crystallization and preliminary X-ray diffraction analysis of the Csu pili CsuC-CsuA/B chaperone-major subunit pre-assembly complex from Acinetobacter baumannii. Acta Crystallogr F Struct Biol Commun 71 : 770–774. doi: 10.1107/S2053230X15007955 26057810

29. Garnett JA, Diallo M, Matthews S (2015) X-ray diffraction analysis of the E. coli common pilus chaperone EcpB. Crystallogr Sect F Struct Biol Cryst Commun in press.

30. Marchant J, Sawmynaden K, Saouros S, Simpson P, Matthews S (2008) Complete resonance assignment of the first and second apple domains of MIC4 from Toxoplasma gondii, using a new NMRView-based assignment aid. Biomolecular Nmr Assignments 2 : 119–121. doi: 10.1007/s12104-008-9100-1 19636884

31. Yu X, Dubnovitsky A, Pudney AF, Macintyre S, Knight SD, et al. (2012) Allosteric Mechanism Controls Traffic in the Chaperone/Usher Pathway. Structure 20 : 1861–1871. doi: 10.1016/j.str.2012.08.016 22981947