Chaperone priming of pilus subunits facilitates a topological transition that drives fiber formation

Cell

Volumn 111, Issue 4, 2002, Pages 543-551

  Sauer, Frederic G ^a   Pinkner, Jerome S ^a   Waksman, Gabriel ^a,b,c   Hultgren, Scott J ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF LONDON   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; PROTEIN SUBUNIT;

AMINO TERMINAL SEQUENCE; ARTICLE; CRYSTAL STRUCTURE; CRYSTALLIZATION; CYTOPLASM; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN PURIFICATION;

BACTERIA (MICROORGANISMS); PHOCIDAE;

EID: 0037112164     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(02)01050-4     Document Type: Article

References (46)

1. Barnhart M.M., Pinkner J.S., Soto G.E., Sauer F.G., Langermann S., Waksman G., Frieden C., Hultgren S.J. PapD-like chaperones provide the missing information for folding of pilin proteins. Proc. Natl. Acad. Sci. USA. 97:2000;7709-7714.
2. Brünger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S.et al. Crystallography and NMR system. a new software suite for macromolecular structure determination Acta Crystallogr. D. 54:1998;905-921.
3. Bullitt E., Makowski L. Structural polymorphism of bacterial adhesion pili. Nature. 373:1995;164-167.
4. Carson M. Ribbons. Methods Enzymol. 277:1997;493-505.
5. Choudhury D., Thompson A., Stojanoff V., Langermann S., Pinkner J., Hultgren S.J., Knight S.D. X-ray structure of the FimC-FimH chaperone-adhesin complex from uropathogenic Escherichia coli. Science. 285:1999;1061-1066.
6. Connell H., Agace W., Klemm P., Schembri M., Marild S., Svanborg C. Type 1 fimbrial expression enhances Escherichia coli virulence for the urinary tract. Proc. Natl. Acad. Sci. USA. 93:1996;9827-9832.
7. Dodson K.W., Pinkner J.S., Rose T., Magnusson G., Hultgren S.J., Waksman G. Structural basis of the interaction of the pyelonephritic E. coli adhesin to its human kidney receptor. Cell. 105:2001;733-743.
8. Gong M., Makowski L. Helical structure of P pili from Escherichia coli. Evidence from X-ray fiber diffraction and scanning transmission electron microscopy. J. Mol. Biol. 228:1992;735-742.
9. Hardy J., Selkoe D.J. The amyloid hypothesis of Alzheimer's disease. progress and problems on the road to therapeutics Science. 297:2002;353-356.
10. Hartl F.U., Hayer-Hartl M. Molecular chaperones in the cytosol. from nascent chain to folded protein Science. 295:2002;1852-1858.
11. Hooton T.M. Epidemiology. Stanton S.L., Dwyer P.L. Urinary Tract Infection in the Female. 2000;Martin Dunitz, London. 1-14.pp.
12. Hull R.A., Gill R.E., Hsu P., Minshew B.H., Falkow S. Construction and expression of recombinant plasmids encoding type 1 or D-mannose-resistant pili from a urinary tract infection Escherichia coli isolate. Infect. Immun. 33:1981;933-938.
13. Hultgren S.J., Jones C.H., Normark S.N. Bacterial adhesins and their assembly. Neidhardt F.C. Escherichia Coli and Salmonella; Cellular and Molecular Biology. 1996;ASM Press, Washington, DC. 2730-2756.pp.
14. 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. 15:1996;3792-3805.
15. Hung D.L., Raivio T.L., Jones C.H., Silhavy T.J., Hultgren S.J. Cpx signaling pathway monitors biogenesis and affects assembly and expression of P pili. EMBO J. 20:2001;1508-1518.
16. Jacob-Dubuisson F., Heuser J., Dodson K., Normark S., Hultgren S.J. Initiation of assembly and association of the structural elements of a bacterial pilus depend on two specialized tip proteins. EMBO J. 12:1993;837-847.
17. Jones T.A., Zou J.Y., Cowan S.W., Kjelgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A. 47:1991;110-119.
18. Jones C.H., Danese P.N., Pinkner J.S., Silhavy T.J., Hultgren S.J. The chaperone-assisted membrane release and folding pathway is sensed by two signal transduction systems. EMBO J. 16:1997;6394-6406.
19. Kuehn M.J., Normark S., Hultgren S.J. Immunoglobulin-like PapD chaperone caps and uncaps interactive surfaces of nascently translocated pilus subunits. Proc. Natl. Acad. Sci. USA. 88:1991;10586-10590.
20. Kuehn M.J., Heuser J., Normark S., Hultgren S.J. P pili in uropathogenic E. coli are composite fibres with distinct fibrillar adhesive tips. Nature. 356:1992;252-255.
21. Kuehn M.J., Ogg D.J., Kihlberg J., Slonim L.N., Flemmer K., Bergfors T., Hultgren S.J. Structural basis of pilus subunit recognition by the PapD chaperone. Science. 262:1993;1234-1241.
22. Lindberg F., Tennent J.M., Hultgren S.J., Lund B., Normark S. PapD, a periplasmic transport protein in P-pilus biogenesis. J. Bacteriol. 171:1989;6052-6058.
23. Lund B., Lindberg F., Marklund B.I., Normark S. The PapG protein is the α-D-galactopyranosyl-(1-4)-β-D-galactopyranose-binding adhesin of uropathogenic Escherichia coli. Proc. Natl. Acad. Sci. USA. 84:1987;5898-5902.
24. Martinez J.J., Mulvey M.A., Schilling J.D., Pinkner J.S., Hultgren S.J. Type 1 pilus-mediated bacterial invasion of bladder epithelial cells. EMBO J. 19:2000;2803-2812.
25. Muhldorfer I., Ziebuhr W., Hacker J. Escherichia coli in urinary tract infections. Sussman M. Molecular Medical Microbiology. 2001;Academic Press, San Diego. 1515-1540.pp.
26. Mulvey M.A., Lopez-Boado Y.S., Wilson C.L., Roth R., Parks W.C., Heuser J., Hultgren S.J. Induction and evasion of host defenses by type 1-piliated uropathogenic Escherichia coli. Science. 282:1998;1494-1497.
27. Navaza J. AMoRe. an automated package for molecular replacement Acta Crystallogr. A. 50:1994;157-163.
28. Nicholls A., Sharp K.A., Honig B. Protein folding and association. insights from the interfacial and thermodynamic properties of hydrocarbons Proteins. 11:1991;281-296.
29. Otwinowski Z. Oscillation data reduction program. Sawyers L., Isaacs N., Bailey S. Proceedings of the CCP4 study weekend. data collection and processing:1993;SERC Daresbury Laboratory, Warrington. 56-62.pp.
30. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:1997;307-326.
31. Roberts J.A., Marklund B.I., Ilver D., Haslam D., Kaack M.B., Baskin G., Louis M., Mollby R., Winberg J., Normark S. The Gal(α1-4)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. 91:1994;11889-11893.
32. Sauer F.G., Futterer K., Pinkner J.S., Dodson K.W., Hultgren S.J., Waksman G. Structural basis of chaperone function and pilus biogenesis. Science. 285:1999;1058-1061.
33. Sauer F.G., Knight S.D., Waksman G., Hultgren S.J. PapD-like chaperones and pilus biogenesis. Semin. Cell Dev. Biol. 11:2000;27-34.
34. Saulino E.T., Bullitt E., Hultgren S.J. Snapshots of usher-mediated protein secretion and ordered pilus assembly. Proc. Natl. Acad. Sci. USA. 97:2000;9240-9245.
35. Slonim L.N., Pinkner J.S., Branden C.I., Hultgren S.J. Interactive surface in the PapD chaperone cleft is conserved in pilus chaperone superfamily and essential in subunit recognition and assembly. EMBO J. 11:1992;4747-4756.
36. Soto G.E., Hultgren S.J. Bacterial adhesins. common themes and variations in architecture and assembly J. Bacteriol. 181:1999;1059-1071.
37. Soto G.E., Dodson K.W., Ogg D., Liu C., Heuser J., Knight S., Kihlberg J., Jones C.H., Hultgren S.J. Periplasmic chaperone recognition motif of subunits mediates quaternary interactions in the pilus. EMBO J. 17:1998;6155-6167.
38. Stanton S.L., Dwyer P.L. Preface. Stanton S.L., Dwyer P.L. Urinary Tract Infection in the Female. 2000;Martin Dunitz, London. xi-xii.pp.
39. Stebbins C.E., Galan J.E. Maintenance of an unfolded polypeptide by a cognate chaperone in bacterial type III secretion. Nature. 414:2001;77-81.
40. Striker R., Jacob-Dubuisson F., Freiden C., Hultgren S.J. Stable fiber-forming and nonfiber-forming chaperone-subunit complexes in pilus biogenesis. J. Biol. Chem. 269:1994;12233-12239.
41. Sussman M. Urinary tract infections. a clinical overview Sussman M. Molecular Medical Microbiology. 2001;Academic Press, San Diego. 1507-1513.pp.
42. Terwilliger T.C. Maximum likelihood density modification. Acta Crystallogr. D Biol. Crystallogr. 56:2000;965-972.
43. Terwilliger T.C., Berendzen J. Automated MAD and MIR structure solution. Acta Crystallogr. D Biol. Crystallogr. 55:1999;849-861.
44. Thanassi D.G., Saulino E.T., Hultgren S.J. The chaperone/usher pathway. a major terminal branch of the general secretory pathway Curr. Opin. Microbiol. 1:1998;223-231. a.
45. Thanassi D.G., Saulino E.T., Lombardo M.J., Roth R., Heuser J., Hultgren S.J. The PapC usher forms an oligomeric channel. implications for pilus biogenesis across the outer membrane Proc. Natl. Acad. Sci. USA. 95:1998;3146-3151. b.
46. Warren J. Clinical presentations and epidemiology of urinary tract infections. Mobley H.L.T., Warren J.W. Urinary Tract Infections. Molecular Pathogenesis and Clinical Management:1996;ASM Press, Washington, DC. 3-27.pp.