Periplasmic chaperone recognition motif of subunits mediates quaternary interactions in the pilus

EMBO Journal

Volumn 17, Issue 21, 1998, Pages 6155-6167

  Soto, Gabriel E ^a   Dodson, Karen W ^a   Ogg, Derek ^a   Liu, Christopher ^a   Heuser, John ^b   Knight, Stefan ^c   Kihlberg, Jan ^d   Jones, C Hal ^e   Hultgren, Scott J ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Structural Chemistry N626

^c SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^d UMEÅ UNIVERSITY   (Sweden)

^e SIGA Technologies Incorporated   (United States)

Author keywords

Bacterial fimbriae; Macromolecular systems; Molecular chaperones; Protein folding; X ray crystallography

Indexed keywords

CHAPERONE; PROTEIN SUBUNIT;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL MEMBRANE; BACTERIUM PILUS; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTALLOGRAPHY; CYTOPLASM; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN QUATERNARY STRUCTURE;

ADHESINS, BACTERIAL; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; ESCHERICHIA COLI; FIMBRIAE, BACTERIAL; MODELS, MOLECULAR; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PERIPLASM; PROTEIN BINDING; PROTEIN FOLDING;

BACTERIA (MICROORGANISMS); NEGIBACTERIA;

EID: 0032476662     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.21.6155     Document Type: Article

References (49)

1. Bacon, D.J. and Anderson, W.F. (1988) A fast algorithm for rendering space-filling molecular pictures. J. Mol Graph., 6, 219-220.
2. Baga, M., Norgren, M. and 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.
3. Boyer, H.W. and Roulland-Dussoix, D. (1969) A complementation analysis of the restriction and modification of DNA in Escherichia coli. J. Mol. Biol., 41, 459-472.
4. Brünger, A.T. (1992) X-PLOR Manual Version 3.1. Yale University Press, New Haven, CT.
5. Bullitt, E. and Makowski, L. (1993) Structural polymorphism of bacterial adhesion pili. Nature, 373, 164-167.
6. Bullitt, E., Jones, C.H., Striker, R., Soto, G., Jacob-Dubuisson, F., Pinkner, J., Wick, M.J., Makowski, L. and Hultgren, S.J. (1996) Development of pilus organelle subassemblies in vitro depends on chaperone uncapping of a β zipper. Proc. Natl Acad. Sci. USA, 93, 12890-12895.
7. CCP4 (1994) Collaborative computational project number 4. The CCP4 suite of programs for protein crystallography. Acta Crystallogr., D50, 760-763.
8. DasGupta, U., Weston-Hafer, K, and Berg, D.E. (1987) Local DNA sequence control of deletion formation in Escherichia coli plasmid pBR322. Genetics, 115, 41-49.
9. Derber, C.M. and Goto, N.K. (1996) Folding proteins into membranes. Nature Struct. Biol., 3, 815-818.
10. Dodson, K.W., Jacob-Dubuisson, F., Striker, R.T. and Hultgren, S.J. (1993) Outer-membrane PapC molecular usher discriminately recognizes periplasmic chaperone-pilux subunit complexes. Proc. Natl Acad. Sci. USA, 90, 3670-3674.
11. Engelman, D.M. and Steitz, T.A. (1981) The spontaneous insertion of proteins into and across membranes: the helical hairpin hypothesis. Cell, 23, 411-422.
12. Finkelstein, A.V. (1991) Rate of β-structure formation in polypeptides. Proteins, 9, 23-27.
13. Gong, M. and Makowski, L. (1992) Helical structure of P pili from Escherichia coli. J. Mol. Biol., 228, 735-742.
14. Hamada, D., Segawa, S. and Goto, Y. (1996) Non-native α-helical intermediate in the refolding of β-lactoglobulin, a predominantly β-sheet protein. Nature Struct. Biol., 3, 868-873.
15. Heuser, J. (1989) Protocol for 3-D visualization of molecules on mica via the quick-freeze, deep-etch technique. J. Electron Microsc. Tech., 13, 244-263.
16. Holmgren, A. and Brändén, C.I. (1989) Crystal structure of chaperone protein PapD reveals an immunoglobulin fold. Nature, 342, 248-251.
17. Holmgren, A., Brändén, C.I., Lindberg, F. and Tennent, J.M. (1988) Preliminary X-ray study of PapD crystals from uropathogenic Escherichia coli. J. Mol. Biol. 203, 279-280.
18. Holmgren, A., Kuehn, M.J., Brändén, C.I. and Hultgren, S.J. (1992) Conserved immunoglobulin-like features in a family of periplasmic pilus chaperones in bacteria. EMBO J., 11, 1617-1622.
19. Hultgren, S.J., Lindberg, F. Magnusson, G., Kihlberg, J., Tennent, J.M. and Normark, S. (1989) The PapG adhesin of uropathogenic Escherichia coli contains separate regions for receptor binding and for the incorporation into the pilus. Proc. Natl Acad. Sci. USA, 86, 4357-4361.
20. Hultgren, S.J., Jones, C.H. and Normark, S. (1996) Bacterial adhesins and their assembly. In Neidhardt, F.C. (ed.). Escherichia coli and Salmonella: Cellular and Molecular Biology. ASM Press, Washington DC, pp. 2730-2756.
21. Hung, D.L., Knight, S.D., Woods, R.M. Pinkner, J.S. and Hultgren, S.J. (1996) Molecular basis of two subfamilies of immunoglobulin-like chaperones. EMBO J., 15, 3792-3805.
22. Jacob-Dubuisson, F., Heuser, J., Dodson, K., Normark, S. and 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.
23. Jacob-Dubuisson, F., Striker, R. and Hultgren, S.J. (1994a) Chaperone-assisted self-assembly of pili independent of cellular energy. J. Biol. Chem., 269, 12447-12455.
24. Jacob-Dubuisson, F., Pinkner, J., Xu, Z., Striker, R., Padmanhaban, A. and Hultgren, S.J. (1994b) PapD chaperone function in pilus biogenesis depends on oxidant and chaperone-like activities of DsbA. Proc. Natl Acad. Sci. USA, 91, 11552-11556.
25. Jones, C.H., Dodson, K. and Hultgren S.J. (1996) Structure, function and assembly of adhesive P pili. In Mobley, H.L.T. and Warren, J.W. (eds), Urinary Tract Infections: Molecular Pathogenesis and Clinical Management. ASM Press, Washington DC, pp. 175-219.
26. Jones, C.H., Danese, P.N., Pinkner, J.S., Silhavy, T.J. and Hultgren, S.J. (1997) The chaperone-assisted membrane release and folding pathway is sensed by two signal transduction systems. EMBO J., 16, 6394-6406.
27. Jones, S. and Thornton, J.M. (1995) Protein-protein interactions: a review of protein dimer structures. Prog. Biophys. Mol. Biol., 63, 31-65.
28. Jones, S. and Thornton, J.M. (1996) Principles of protein-protein interactions. Proc. Natl Acad. Sci. USA, 93, 13-20.
29. Jones, T.A., Zou, J.Y., Cowan, S.W. and Kjelgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr., A47, 110-119.
30. Karlsson, K.F., Walse, B., Drakenberg, T. and Kihlberg, J. (1996) Synthesis and conformational studies of peptides from E.coli pilus proteins recognized by the chaperone PapD. Lett. Pept. Sci., 3, 143-156.
31. Kraulis, P.J. (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr., 24, 946-950.
32. Kuehn, M.J., Heuser, J., Normark, S. and Hultgren, S.J. (1992) P pili in uropathogenic E.coli are composite fibres with distinct fibrillar adhesive tips. Nature, 356, 252-255.
33. Kuehn, M.J., Ogg, D.J., Kihlberg, J., Slonim, L.N., Flemmer, K., Bergfors, T. and Hultgren, S.J. (1993) Structural basis of pilus subunit recognition by the PapD chaperone. Science, 262, 1234-1241.
34. Lech, K. and Brent, R. (1987) Selected topics from classical bacterial genetics. In Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman J.G., Smith, J.A. and Struhl, K. (eds), Current Protocols in Molecular Biology. Greene Publishing Associates and Wiley Interscience, New York, NY, unit 1.4.
35. Lee, B. and Richards, F.M. (1971) The interpretation of protein structures: estimation of static accessibility. J. Mol. Biol., 55, 379-400.
36. Merritt, E.A. and Murphy, M.E.P. (1994) Raster3D version 2.0: a program for photorealistic molecular graphics. Acta Crystallogr., D50, 869-873.
37. Minor, D.L.Jr and Kim, P.S. (1994) Context is a major determinant of β- sheet propensity. Nature, 371, 264-267.
38. Morrison, H.G. and Desrosiers, R.C. (1993) A PCR-based strategy for extensive mutagenesis of a target DNA sequence. BioTechniques. 14, 454-457.
39. Normark, S., Baga, M., Göransson, M., Lindberg, F.P., Lund, B., Norgren, M. and Uhlin, B. (1986) Genetics and biogenesis of Escherichia coli adhesins. In Mirelman, D. (ed.), Microbial Lectins and Agglutinins. John Wiley and Sons, New York, NY, pp. 113-143.
40. Oliver, D.B. (1996) Periplasm. In Neidhardt, F.C. (ed.), Escherichia coli and Salmonella: Cellular and Molecular Biology. ASM Press, Washington DC, pp. 88-103.
41. Otwinowski, Z. (1993) Data collection and processing. In Proceedings of CCP4 Study Weekend 29-30 January 1991. SERC Daresbury Laboratory, UK.
42. Saulino, E.T., Thanassi, D.G., Pinkner, J. and Hultgren, S.J. (1998) Ramifications of kinetic partitioning on usher-mediated pilus biogenesis. EMBO J., 17, 2177-2185.
43. Slonim, L.N., Pinkner, J.S., Brändén, C. and Hultgren, S.J. (1992) Interactive surface in the PapD chaperone cleft is conserved in pilus chaperone superfamily and essential in subunit recognition and assembly. EMBO J., 11, 4747-4756.
44. Stites, W.E. (1997) Protein-protein interactions: interface structure, binding thermodynamics and mutational analysis. Chem. Rev., 97, 1233-1250.
45. Strauch, K.L., Johnson, K. and Beckwith, J. (1989) Characterization of degP, a gene required for proteolysis in the cell envelope of Escherichia coli at high temperature. J. Bacteriol., 171, 2689-2696.
46. Striker, R., Jacob-Dubuisson, F., Frieden, C. and Hultgren, S.J. (1994) Stable fiber-forming and nonfiber-forming chaperone-subunit complexes in pilus biogenesis. J. Biol. Chem., 269, 12233-12239.
47. Thanassi, D.G., Saulino, E.T., Lombardo, M.J., Roth, R., Heuser, J. and 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.
48. Wimley, W.C. and White, S.H. (1996) Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nature Struct. Biol., 3, 842-848.
49. Xu, Z., Jones, C.H., Haslem, D., Pinkner, J.S., Dodson, K., Kihlberg, J. and Hultgren, S.J. (1995) Molecular dissection of PapD interaction with PapG reveals two chaperone-binding sites. Mol. Microbiol., 16, 1011-1020.