Quality control of disulfide bond formation in pilus subunits by the chaperone FimC

Nature Chemical Biology

Volumn 8, Issue 8, 2012, Pages 707-713

  Crespo, Maria D ^a   Puorger, Chasper ^a   Schärer, Martin A ^b   Eidam, Oliv ^c,d   Grütter, Markus G ^c   Capitani, Guido ^b,c   Glockshuber, Rudi ^a  

^a ETH ZURICH   (Switzerland)

^b PAUL SCHERRER INSTITUTE   (Switzerland)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; PROTEIN FIMC; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL INFECTION; BACTERIAL VIRULENCE; BACTERIUM PILUS; CATALYSIS; COMPLEX FORMATION; CRYSTAL STRUCTURE; DISULFIDE BOND; ENZYME SUBUNIT; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; QUALITY CONTROL; URINARY TRACT INFECTION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 84864261756     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.1019     Document Type: Article

References (50)

1. Choudhury, D. et al. X-ray structure of the FimC-FimH chaperone-adhesin complex from uropathogenic Escherichia coli. Science 285, 1061-1066 (1999).
2. Hahn, E. et al. Exploring the 3D molecular architecture of Escherichia coli type 1 pili. J. Mol. Biol. 323, 845-857 (2002).
3. Jones, C.H. et al. FimH adhesin of type 1 pili is assembled into a fibrillar tip structure in the Enterobacteriaceae. Proc. Natl. Acad. Sci. USA 92, 2081-2085 (1995).
4. Le Trong, I. et al. Donor strand exchange and conformational changes during E. coli fimbrial formation. J. Struct. Biol. 172, 380-388 (2010).
5. Le Trong, I. et al. Structural basis for mechanical force regulation of the adhesin FimH via finger trap-like β-sheet twisting. Cell 141, 645-655 (2010).
6. Sauer, F.G. et al. Structural basis of chaperone function and pilus biogenesis. Science 285, 1058-1061 (1999).
7. Sauer, F.G., Pinkner, J.S., Waksman, G. & Hultgren, S.J. Chaperone priming of pilus subunits facilitates a topological transition that drives fiber formation. Cell 111, 543-551 (2002).
8. Hung, D.L., Knight, S.D., Woods, R.M., Pinkner, J.S. & Hultgren, S.J. Molecular basis of two subfamilies of immunoglobulin-like chaperones. EMBO J. 15, 3792-3805 (1996).
9. Jones, C.H. et al. FimC is a periplasmic PapD-like chaperone that directs assembly of type 1 pili in bacteria. Proc. Natl. Acad. Sci. USA 90, 8397-8401 (1993).
10. Nishiyama, M., Ishikawa, T., Rechsteiner, H. & Glockshuber, R. Reconstitution of pilus assembly reveals a bacterial outer membrane catalyst. Science 320, 376-379 (2008).
11. Phan, G. et al. Crystal structure of the FimD usher bound to its cognate FimC-FimH substrate. Nature 474, 49-53 (2011).
12. Saulino, E.T., Thanassi, D.G., Pinkner, J.S. & Hultgren, S.J. Ramifications of kinetic partitioning on usher-mediated pilus biogenesis. EMBO J. 17, 2177-2185 (1998).
13. Vetsch, M. et al. Pilus chaperones represent a new type of protein-folding catalyst. Nature 431, 329-333 (2004).
14. Vetsch, M. et al. Mechanism of fibre assembly through the chaperone-usher pathway. EMBO Rep. 7, 734-738 (2006).
15. Remaut, H. et al. Donor-strand exchange in chaperone-assisted pilus assembly proceeds through a concerted beta strand displacement mechanism. Mol. Cell 22, 831-842 (2006).
16. Zavialov, A.V. et al. Structure and biogenesis of the capsular F1 antigen from Yersinia pestis: Preserved folding energy drives fiber formation. Cell 113, 587-596 (2003).
17. Dodd, D.C. & Eisenstein, B.I. Kinetic analysis of the synthesis and assembly of type 1 fimbriae of Escherichia coli. J. Bacteriol. 160, 227-232 (1984).
18. Jacob-Dubuisson, F., Striker, R. & Hultgren, S.J. Chaperone-assisted self-assembly of pili independent of cellular energy. J. Biol. Chem. 269, 12447-12455 (1994).
19. Heras, B. et al. DSB proteins and bacterial pathogenicity. Nat. Rev. Microbiol. 7, 215-225 (2009).
20. Hiniker, A. & Bardwell, J.C. In vivo substrate specificity of periplasmic disulfide oxidoreductases. J. Biol. Chem. 279, 12967-12973 (2004).
21. Bardwell, J.C., McGovern, K. & Beckwith, J. Identification of a protein required for disulfide bond formation in vivo. Cell 67, 581-589 (1991).
22. Bringer, M.A., Rolhion, N., Glasser, A.L. & Darfeuille-Michaud, A. The oxidoreductase DsbA plays a key role in the ability of the Crohn's disease-associated adherent-invasive Escherichia coli strain LF82 to resist macrophage killing. J. Bacteriol. 189, 4860-4871 (2007).
23. Jacob-Dubuisson, F. et al. PapD chaperone function in pilus biogenesis depends on oxidant and chaperone-like activities of DsbA. Proc. Natl. Acad. Sci. USA 91, 11552-11556 (1994).
24. Totsika, M., Heras, B., Wurpel, D.J. & Schembri, M.A. Characterization of two homologous disulfide bond systems involved in virulence factor biogenesis in uropathogenic Escherichia coli CFT073. J. Bacteriol. 191, 3901-3908 (2009).
25. Nishiyama, M. et al. Structural basis of chaperone-subunit complex recognition by the type 1 pilus assembly platform FimD. EMBO J. 24, 2075-2086 (2005).
26. Eidam, O., Dworkowski, F.S., Glockshuber, R., Grutter, M.G. & Capitani, G. Crystal structure of the ternary FimC-FimFt-FimDN complex indicates conserved pilus chaperone-subunit complex recognition by the usher FimD. FEBS Lett. 582, 651-655 (2008).
27. Pellecchia, M., Sebbel, P., Hermanns, U., Wuthrich, K. & Glockshuber, R. Pilus chaperone FimC-adhesin FimH interactions mapped by TROSY-NMR. Nat. Struct. Biol. 6, 336-339 (1999).
28. Puorger, C., Vetsch, M., Wider, G. & Glockshuber, R. Structure, folding and stability of FimA, the main structural subunit of type 1 pili from uropathogenic Escherichia coli strains. J. Mol. Biol. 412, 520-535 (2011).
29. Wunderlich, M. & Glockshuber, R. Redox properties of protein disulfide isomerase (DsbA) from Escherichia coli. Protein Sci. 2, 717-726 (1993).
30. Wunderlich, M., Otto, A., Seckler, R. & Glockshuber, R. Bacterial protein disulfide isomerase: Efficient catalysis of oxidative protein folding at acidic pH. Biochemistry 32, 12251-12256 (1993).
31. Hennecke, J., Sillen, A., Huber-Wunderlich, M., Engelborghs, Y. & Glockshuber, R. Quenching of tryptophan fluorescence by the active-site disulfide bridge in the DsbA protein from Escherichia coli. Biochemistry 36, 6391-6400 (1997).
32. Schmid, F.X. Mechanism of folding of ribonuclease A. Slow refolding is a sequential reaction via structural intermediates. Biochemistry 22, 4690-4696 (1983).
33. Reimer, U. et al. Side-chain effects on peptidyl-prolyl cis/trans isomerisation. J. Mol. Biol. 279, 449-460 (1998).
34. Balbach, J. & Schmid, F.X. Prolyl isomerization and its catalysis in protein folding in Mechanisms of Protein Folding: FRONTIERS in Molecular Biology 2nd edn. (ed. Pain, R.H.) 212-249 (Oxford University Press, 2000).
35. Kobayashi, T. & Ito, K. Respiratory chain strongly oxidizes the CXXC motif of DsbB in the Escherichia coli disulfide bond formation pathway. EMBO J. 18, 1192-1198 (1999).
36. Barnhart, M.M. et al. PapD-like chaperones provide the missing information for folding of pilin proteins. Proc. Natl. Acad. Sci. USA 97, 7709-7714 (2000).
37. Krissinel, E. & Henrick, K. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797 (2007).
38. Diederichs, K. Structural superposition of proteins with unknown alignment and detection of topological similarity using a six-dimensional search algorithm. Proteins 23, 187-195 (1995).
39. McDonald, I.K. & Thornton, J.M. Satisfying hydrogen bonding potential in proteins. J. Mol. Biol. 238, 777-793 (1994).
40. Kuehn, M.J. et al. Structural basis of pilus subunit recognition by the PapD chaperone. Science 262, 1234-1241 (1993).
41. Kelley, L.A. & Sutcliffe, M.J. OLDERADO: On-line database of ensemble representatives and domains. On line database of ensemble representatives and domains. Protein Sci. 6, 2628-2630 (1997).
42. Kabsch, W. A solution for the best rotation to relate two sets of vectors. Acta Crystallogr. A 32, 922-923 (1976).
43. Łasica, A.M. & Jagusztyn-Krynicka, E.K. The role of Dsb proteins of Gram-negative bacteria in the process of pathogenesis. FEMS Microbiol. Rev. 31, 626-636 (2007).
44. Yu, J. & Kroll, J.S. DsbA: A protein-folding catalyst contributing to bacterial virulence. Microbes Infect. 1, 1221-1228 (1999).
45. Hiniker, A., Collet, J.F. & Bardwell, J.C. Copper stress causes an in vivo requirement for the Escherichia coli disulfide isomerase DsbC. J. Biol. Chem. 280, 33785-33791 (2005).
46. Missiakas, D., Georgopoulos, C. & Raina, S. The Escherichia coli dsbC (xprA) gene encodes a periplasmic protein involved in disulfide bond formation. EMBO J. 13, 2013-2020 (1994).
47. Thomas, W.E., Trintchina, E., Forero, M., Vogel, V. & Sokurenko, E.V. Bacterial adhesion to target cells enhanced by shear force. Cell 109, 913-923 (2002).
48. Bann, J.G., Pinkner, J.S., Frieden, C. & Hultgren, S.J. Catalysis of protein folding by chaperones in pathogenic bacteria. Proc. Natl. Acad. Sci. USA 101, 17389-17393 (2004).
49. Capitani, G., Eidam, O., Glockshuber, R. & Grütter, M.G. Structural and functional insights into the assembly of type 1 pili from. Escherichia coli. Microbes Infect. 8, 2284-2290 (2006).
50. Collaborative Computational Project, Number 4. The CCP4 suite: Programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763 (1994).