1887

Chapter 5 : The Chaperone-Usher Pathway of Pilus Fiber Biogenesis

Authors: Frederic G. Sauer1, Scott J. Hultgren2, Gabriel Waksman3
VIEW AFFILIATIONS HIDE AFFILIATIONS
Affiliations: 1: Section of Microbial Pathogenesis, Boyer Center for Molecular Medicine, Yale University School of Medicine, 295 Congress Ave., New Haven, CT 06536; 2: Departmentof Molecular Microbiology, Washington University School of Medicine, St. Louis, MO 63110; 3: Institute of Structural Molecular Biology, Birkbeck and University College London, Malet St., London WC1 7HX, United Kingdom
Content Type: Monograph
Publication Year: 2005

Category: Microbial Genetics and Molecular Biology; Bacterial Pathogenesis

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Preview Magnify
Zoom in
Zoomout

The Chaperone-Usher Pathway of Pilus Fiber Biogenesis, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555818395/9781555813017_Chap05-1.gif /docserver/preview/fulltext/10.1128/9781555818395/9781555813017_Chap05-2.gif

Abstract:

Many species of gram-negative bacteria employ a conserved protein secretion system termed the chaperone-usher pathway to assemble a diverse array of multisubunit protein fibers on their surfaces. Fibers assembled by the chaperone-usher pathway play critical roles in bacterially mediated disease: they mediate bacterial attachment to host tissues, often an essential early step in pathogenesis; they facilitate the evasion of host defenses; and they promote biofilm formation, a contributing factor both to the establishment of infection and to bacterial resistance to antibiotic treatment. Fibers assembled by the chaperone-usher pathway are typically encoded in individual gene clusters. The well-studied surface organelles, the capsular F1 antigen of and the hemagglutinating pilus of the human respiratory pathogen , highlight the structural diversity of fibers assembled by the chaperone-usher pathway. The periplasmic chaperones of the chaperone-usher pathway share conserved structural features first revealed in the crystal structure of PapD. Each chaperone consists of two domains that are oriented at an approximate right angle to each other to produce an L-shaped molecule. Donor strand exchange occurs very rapidly in vivo but only relatively slowly and inefficiently in vitro in the absence of the usher. This suggests that while the chaperone primes the subunit for donor strand exchange, additional interactions with the usher may facilitate subunit uncapping during fiber formation. The relative specificity of donor strand exchange determines, at least in part, the function of individual subunits and their order of incorporation into the fiber.

Citation: Sauer F, Hultgren S, Waksman G. 2005. The Chaperone-Usher Pathway of Pilus Fiber Biogenesis, p 69-80. In Waksman G, Caparon M, Hultgren S (ed), Structural Biology of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818395.ch5
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

References

/content/book/10.1128/9781555818395.chap5
1. Barnhart, M. M.,, J. S. Pinkner,, G. E. Soto,, F. G. Sauer,, S. Langermann,, G. Waksman,, C. Frieden,, and S. J. Hultgren. 2000. PapD-like chaperones provide the missing information for folding of pilin proteins. Proc. Natl. Acad. Sci. USA 97: 7709– 7714.
2. Barnhart, M. M.,, F. G. Sauer,, J. S. Pinkner,, and S. J. Hultgren. 2003. Chaperone-subunit-usher interactions required for donor strand exchange during bacterial pilus assembly. J. Bacteriol. 185: 2723– 2730.
3. Bullitt, E.,, C. H. Jones,, R. Striker,, G. Soto,, F. Jacob-Dubuisson,, J. Pinkner,, M. J. Wick,, L. Makowski,, and S. J. Hultgren. 1996. Development of pilus organelle subassemblies in vitro depends on chaperone uncapping of a beta zipper. Proc. Natl. Acad. Sci. USA 93: 12890– 12895.
4. Bullitt, E.,, and L. Makowski. 1995. Structural polymorphism of bacterial adhesion pili. Nature 373: 164– 167.
5. Carson, M. 1997. Ribbons. Methods Enzymol. 277: 493– 505.
6. Choudhury, D.,, A. Thompson,, V. Stojanoff,, S. Langermann,, J. Pinkner,, S. J. Hultgren,, and S. D. Knight. 1999. X-ray structure of the FimC-FimH chaperone-adhesin complex from uropathogenic Escherichia coli. Science 285: 1061– 1066.
7. Connell, H.,, W. Agace,, P. Klemm,, M. Schembri,, S. Marild,, and C. Svanborg. 1996. Type 1 fimbrial expression enhances Escherichia coli virulence for the urinary tract. Proc. Natl. Acad. Sci. USA 93: 9827– 9832.
8. Dodson, K. W.,, F. Jacob-Dubuisson,, R. T. Striker,, and S. J. Hultgren. 1993. Outer-membrane PapC molecular usher discriminately recognizes periplasmic chaperone-pilus subunit complexes. Proc. Natl. Acad. Sci. USA 90: 3670– 3674.
9. Du, Y.,, R. Rosqvist,, and A. Forsberg. 2002. Role of fraction 1 antigen of Yersinia pestis in inhibition of phagocytosis. Infect. Immun. 70: 1453– 1460.
10. Galyov, E. E.,, A. V. Karlishev,, T. V. Chernovskaya,, D. A. Dolgikh,, O. Smirnov,, K. I. Volkovoy,, V. M. Abramov,, and V. P. Zav’yalov. 1991. Expression of the envelope antigen F1 of Yersinia pestis is mediated by the product of caf1M gene having homology with the chaperone protein PapD of Escherichia coli. FEBS Lett. 286: 79– 82.
11. Gong, M.,, and L. Makowski. 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.
12. Hahn, E.,, P. Wild,, U. Hermanns,, P. Sebbel,, R. Glockshuber,, M. Haner,, N. Taschner,, P. Burkhard,, U. Aebi,, and S. A. Muller. 2002. Exploring the 3D molecular architecture of Escherichia coli type 1 pili. J. Mol. Biol. 323: 845– 857.
13. Holmgren, A.,, and C. I. Branden. 1989. Crystal structure of chaperone protein PapD reveals an immunoglobulin fold. Nature 342: 248– 251.
14. Hull, R. A.,, R. E. Gill,, P. Hsu,, B. H. Minshew,, and S. Falkow. 1981. 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: 933– 938.
15. Hultgren, S. J.,, F. Lindberg,, G. Magnusson,, J. Kihlberg,, J. M. Tennent,, and S. Normark. 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.
16. Hung, D. L.,, S. D. Knight,, and S. J. Hultgren. 1999. Probing conserved surfaces on PapD. Mol. Microbiol. 31: 773– 783.
17. Hung, D. L.,, S. D. Knight,, R. M. Woods,, J. S. Pinkner,, and S. J. Hultgren. 1996. Molecular basis of two subfamilies of immunoglobulin-like chaperones. EMBO J. 15: 3792– 3805.
18. Jacob-Dubuisson, F.,, J. Heuser,, K. Dodson,, S. Normark,, and S. J. Hultgren. 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.
19. Jacob-Dubuisson, F.,, R. Striker,, and S. J. Hultgren. 1994. Chaperone-assisted self-assembly of pili independent of cellular energy. J. Biol. Chem. 269: 12447– 12455.
20. Jones, C. H.,, P. N. Danese,, J. S. Pinkner,, T. J. Silhavy,, and S. J. Hultgren. 1997. The chaperone-assisted membrane release and folding pathway is sensed by two signal transduction systems. EMBO J. 16: 6394– 6406.
21. Jones, C. H.,, J. S. Pinkner,, A. V. Nicholes,, L. N. Slonim,, S. N. Abraham,, and S. J. Hultgren. 1993. FimC is a periplasmic PapD-like chaperone that directs assembly of type 1 pili in bacteria. Proc. Natl. Acad. Sci. USA 90: 8397– 8401.
22. Jones, C. H.,, J. S. Pinkner,, R. Roth,, J. Heuser,, A. V. Nicholes,, S. N. Abraham,, and S. J. Hultgren. 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.
23. Knight, S. D.,, D. Choudhury,, S. Hultgren,, J. Pinkner,, V. Stojanoff,, and A. Thompson. 2002. Structure of the S pilus periplasmic chaperone SfaE at 2.2 Å resolution. Acta Crystallogr. Ser. D 58: 1016– 1022.
24. Kuehn, M. J.,, J. Heuser,, S. Normark,, and S. J. Hultgren. 1992. P pili in uropathogenic E. coli are composite fibres with distinct fibrillar adhesive tips. Nature 356: 252– 255.
25. Kuehn, M. J.,, S. Normark,, and S. J. Hultgren. 1991. Immunoglobulin-like PapD chaperone caps and uncaps interactive surfaces of nascently translocated pilus subunits. Proc. Natl. Acad. Sci. USA 88: 10586– 10590.
26. Kuehn, M. J.,, D. J. Ogg,, J. Kihlberg,, L. N. Slonim,, K. Flemmer,, T. Bergfors,, and S. J. Hultgren. 1993. Structural basis of pilus subunit recognition by the PapD chaperone. Science 262: 1234– 1241.
27. Langermann, S.,, S. Palaszynski,, M. Barnhart,, G. Auguste,, J. S. Pinkner,, J. Burlein,, P. Barren,, S. Koenig,, S. Leath,, C. H. Jones,, and S. J. Hultgren. 1997. Prevention of mucosal Escherichia coli infection by FimHadhesin- based systemic vaccination. Science 276: 607– 611.
28. Lindberg, F.,, J. M. Tennent,, S. J. Hultgren,, B. Lund,, and S. Normark. 1989. PapD, a periplasmic transport protein in P-pilus biogenesis. J. Bacteriol. 171: 6052– 6058.
29. Lund, B.,, F. Lindberg,, B. I. Marklund,, and S. Normark. 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.
30. MacIntyre, S.,, I. M. Zyrianova,, T. V. Chernovskaya,, M. Leonard,, E. G. Rudenko,, V. P. Zav’yalov,, and D. A. Chapman. 2001. An extended hydrophobic interactive surface of Yersinia pestis Caf1M chaperone is essential for subunit binding and F1 capsule assembly. Mol. Microbiol. 39: 12– 25.
31. Manting, E. H.,, and A. J. Driessen. 2000. Escherichia coli translocase: the unravelling of a molecular machine. Mol. Microbiol. 37: 226– 238.
32. McCrea, K. W.,, W. J. Watson,, J. R. Gilsdorf,, and C. F. Marrs. 1994. Identification of hifD and hifE in the pilus gene cluster of Haemophilus influenzae type b strain Eagan. Infect. Immun. 62: 4922– 4928.
33. Mu, X.-Q.,, E. H. Egelman,, and E. Bullitt. 2002. Structure and function of Hib pili from Haemophilus influenzae type b. J. Bacteriol. 184: 4868– 4874.
34. Mulvey, M. A.,, Y. S. Lopez-Boado,, C. L. Wilson,, R. Roth,, W. C. Parks,, J. Heuser,, and S. J. Hultgren. 1998. Induction and evasion of host defenses by type 1-piliated uropathogenic Escherichia coli. Science 282: 1494– 1497. ( Erratum, 283:795, 1999.)
35. Nicholls, A.,, K. A. Sharp,, and B. Honig. 1991. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Protein Struct. Funct. Genet. 11: 281– 296.
36. Nishiyama, M.,, M. Vetsch,, C. Puorger,, I. Jelesarov,, and R. Glockshuber. 2003. Identification and characterization of the chaperone-subunit complex-binding domain from type 1 pilus assembly platform FimD. J. Mol. Biol. 330: 513– 525.
37. Pellecchia, M.,, P. Guntert,, R. Glockshuber,, and K. Wuthrich. 1998. NMR solution structure of the periplasmic chaperone FimC. Nat. Struct. Biol. 5: 885– 890.
38. Pratt, L. A.,, and R. Kolter. 1998. Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol. Microbiol. 30: 285– 293.
39. Roberts, J. A.,, B. I. Marklund,, D. Ilver,, D. Haslam,, M. B. Kaack,, G. Baskin,, M. Louis,, R. Mollby,, J. Winberg,, and S. Normark. 1994. The Gal(alpha 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.
40. Sable, N. S.,, E. M. Connor,, C. B. Hall,, and M. R. Loeb. 1985. Variable adherence of fimbriated Haemophilus influenzae type b to human cells. Infect. Immun. 48: 119– 123.
41. Sauer, F. G.,, K. Futterer,, J. S. Pinkner,, K. W. Dodson,, S. J. Hultgren,, and G. Waksman. 1999. Structural basis of chaperone function and pilus biogenesis. Science 285: 1058– 1061.
42. Sauer, F. G.,, S. D. Knight,, G. Waksman,, and S. J. Hultgren. 2000. PapD-like chaperones and pilus biogenesis. Semin. Cell Dev. Biol. 11: 27– 34.
43. Sauer, F. G.,, J. S. Pinkner,, G. Waksman,, and S. J. Hultgren. 2002. Chaperone priming of pilus subunits facilitates a topological transition that drives fiber formation. Cell 111: 543– 551.
44. Saulino, E. T.,, E. Bullitt,, and S. J. Hultgren. 2000. Snapshots of usher-mediated protein secretion and ordered pilus assembly. Proc. Natl. Acad. Sci. USA 97: 9240– 9245.
45. Saulino, E. T.,, D. G. Thanassi,, J. Pinkner,, and S. J. Hultgren. 1998. Ramifications of kinetic partitioning on usher-mediated pilus biogenesis. EMBO J. 17: 2177– 2185.
46. Slonim, L. N.,, J. S. Pinkner,, C. I. Branden,, and S. J. Hultgren. 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.
47. Soto, G. E.,, K. W. Dodson,, D. Ogg,, C. Liu,, J. Heuser,, S. Knight,, J. Kihlberg,, C. H. Jones,, and S. J. Hultgren. 1998. Periplasmic chaperone recognition motif of subunits mediates quaternary interactions in the pilus. EMBO J 17: 6155– 6167.
48. St. Geme,, J. W., III,, J. S. Pinkner,, G. P. Krasan,, J. Heuser,, E. Bullitt,, A. L. Smith,, and S. J. Hultgren. 1996. Haemophilus influenzae pili are composite structures assembled via the HifB chaperone. Proc. Natl. Acad. Sci. USA 93: 11913– 11918.
49. Striker, R.,, F. Jacob-Dubuisson,, C. Freiden,, and S. J. Hultgren. 1994. Stable fiber-forming and nonfiberforming chaperone-subunit complexes in pilus biogenesis. J. Biol. Chem. 269: 12233– 12239.
50. Thanassi, D. G.,, E. T. Saulino,, and S. J. Hultgren. 1998a. The chaperone/usher pathway: a major terminal branch of the general secretory pathway. Curr. Opin. Microbiol. 1: 223– 231.
51. Thanassi, D. G.,, E. T. Saulino,, M. J. Lombardo,, R. Roth,, J. Heuser,, and S. J. Hultgren. 1998b. The PapC usher forms an oligomeric channel: implications for pilus biogenesis across the outer membrane. Proc. Natl. Acad. Sci. USA 95: 3146– 3151.
52. Thanassi, D. G.,, C. Stathopoulos,, K. Dodson,, D. Geiger,, and S. J. Hultgren. 2002. Bacterial outer membrane ushers contain distinct targeting and assembly domains for pilus biogenesis. J. Bacteriol. 184: 6260– 6269.
53. Vallet, I.,, J. W. Olson,, S. Lory,, A. Lazdunski,, and A. Filloux. 2001. The chaperone/usher pathways of Pseudomonas aeruginosa: identification of fimbrial gene clusters ( cup) and their involvement in biofilm formation. Proc. Natl. Acad. Sci. USA 98: 6911– 6916.
54. Vetsch, M.,, P. Sebbel,, and R. Glockshuber. 2002. Chaperone-independent folding of type 1 pilus domains. J. Mol. Biol. 322: 827– 840.
55. Weber, A.,, R. Harris,, S. Lohrke,, L. Forney,, and A. L. Smith. 1991. Inability to express fimbriae results in impaired ability of Haemophilus influenzae b to colonize the nasopharynx. Infect. Immun. 59: 4724– 4728.
56. Zavialov, A. V.,, J. Berglund,, A. F. Pudney,, L. J. Fooks,, T. M. Ibrahim,, S. MacIntyre,, and S. D. Knight. 2003. Structure and biogenesis of the capsular F1 antigen from Yersinia pestis. Preserved folding energy drives fiber formation. Cell 113: 587– 596.
57. Zavialov, A. V.,, J. Kersley,, T. Korpela,, and V. P. Zav’yalov. 2002. Donor strand complementation mechanism in the biogenesis of non-pilus systems. Mol. Microbiol. 45: 983– 995.

Back to top
This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error