The chaperone-usher pathway of bacterial adhesin biogenesis - From molecular mechanism to strategies of anti-bacterial prevention and modern vaccine design

Acta Biochimica Polonica

Volumn 52, Issue 3, 2005, Pages 639-646

  Pia̧tek, Rafał ^a   Zalewska, Beata ^a   Bury, Katarzyna ^a   Kur, Józef ^a  

^a GDANSK UNIVERSITY OF TECHNOLOGY   (Poland)

Author keywords

Adhesion; Chaperone usher pathway; Fimbriae; Pili

Indexed keywords

BACTERIA (MICROORGANISMS); NEGIBACTERIA;

EID: 27644552925     PISSN: 0001527X     EISSN: None     Source Type: Journal    
DOI: 10.18388/abp.2005_3424     Document Type: Conference Paper

References (57)

1. Anderson KL, Billington J, Pettigrew D, Cota E, Simpson P, Roversi P, Chen HA, Urvil P, du Merle L, Barlow PN, Medof ME, Smith RA, Nowicki B, Le Bouguenec C, Lea SM, Matthews S (2004) An atomic resolution model for assembly, architecture, and function of the Dr adhesins. Mol Cell 15: 647-657.
2. Barnhart MM, Sauer FG, Pinkner JS, Hultgren SJ (2003) Chaperone-subunit-usher interactions required for donor strand exchange during bacterial pilus assembly. J Bacteriol 185: 2723-2730.
3. Barnett BJ, Stephens DS (1997) Urinary tract infection: an overview. Am J Med Sci 314: 245-249.
4. Bullitt E, Makowski L (1995) Structural polymorphism of bacterial adhesion pili. Nature 373: 164-167.
5. Choudhury D, Thompson A, Stojanoff V, Langermann S, Pinkner J, Hultgren SJ, Knight SD (1999) X-ray structure of the FimC-FimH chaperone-adhesin complex from uropathogenic Escherichia coli. Science 285: 1061-1066.
6. Donnenberg MS (2000) Pathogenic strategies of enteric bacteria. Nature 406: 768-774.
7. El Mazouari K, Oswald E, Hernalsteens JP, Lintermans P, De Greve H (1994) F17-like fimbriae from an invasive Escherichia coli strain producing cytotoxic necrotizing factor type 2 toxin. Infect Immun 62: 2633-2638.
8. Finlay BB, Falkow S (1997) Common themes in microbial pathogenicity revisited. Microbiol Mol Biol Rev 61: 136-169.
9. Goluszko P, Goluszko E, Nowicki B, Nowicki S, Popov V, Wang HQ (2005) Vaccination with purified Dr fimbriae reduces mortality associated with chronic urinary tract infection due to Escherichia coli bearing Dr adhesin. Infect Immun 73: 627-631.
10. Gong M, Makowski L (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.
11. Hahn E, Wild P, Hermanns U, Sebbel P, Glockshuber R, Haner M, Taschner N, Burkhard P, Aebi U, Muller SA (2002) Exploring the 3D molecular architecture of Escherichia coli type 1 pili. J Mol Biol 323: 845-857.
12. Henderson NS, So SS, Martin C, Kulkarni R, Thanassi DG (2004) Topology of the outer membrane usher PapC determined by site-directed fluorescence labeling. J Biol Chem 279: 53747-53754.
13. Hedegaard L, Klemm P (1989) Type 1 fimbriae of Escherichia coli as carriers of heterologous antigenic sequences. Gene 85: 115-124.
14. Holmgren A, Branden CI (1989) Crystal structure of chaperone protein PapD reveals an immunoglobulin fold. Nature 342: 248-251.
15. 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.
16. Hung DL, Knight SD, Hultgren SJ (1999) Probing conserved surfaces on PapD. Mol Microbiol 31: 773-783.
17. Jacob-Dubuisson F, Heuser J, Dodson K, Normark S, Hultgren SJ (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.
18. Jacob-Dubuisson F, Striker R, Hultgren SJ (1994) Chaperone-assisted self-assembly of pili independent of cellular energy. J Biol Chem 269: 12447-12455.
19. Jones CH, Pinkner JS, Roth R, Heuser J, Nicholes AV, Abraham SN, Hultgren SJ (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.
20. Jones CH, Danese PN, Pinkner JS, Silhavy TJ, Hultgren SJ (1997) The chaperone-assisted membrane release and folding pathway is sensed by two signal transduction systems. EMBO J 16: 6394-6406.
21. Knight SD, Choudhury D, Hultgren S, Pinkner J, Stojanoff V, Thompson A (2002) Structure of the S pilus periplasmic chaperone SfaE at 2.2 Å resolution. Acta Crystallog, D Biol Crystallogr 58: 1016-1022.
22. Klemm P, Schembri MA (2000a) Fimbrial surface display systems in bacteria: from vaccines to random libraries. Microbiol 146: 3025-3032.
23. Klemm P, Schembri MA (2000b) Fimbriae-assisted bacterial surface display of heterologous peptides. Int J Med Microbiol 290: 215-221.
24. Krogfelt KA, Bergmans H, Klemm P (1990) Direct evidence that FimH protein is the mannose-specific adhesin of Escherichia coli type 1 fimbriae. Infect Immun 58: 1995-1998.
25. Kuehn MJ, Heuser J, Normark S, Hultgren SJ (1992) P pili in uropathogenic E. coli are composite fibers with distinct fibrillar adhesive tips. Nature 356: 252-255.
26. Kuehn MJ, Ogg DJ, Kihlberg J, Slonim LN, Flemmer K, Bergfors T, Hultgren SJ (1993) Structural basis of pilus subunit recognition by the PapD chaperone. Science 262: 1234-1241.
27. Li H, Qian L, Chen Z, Thibault D, Liu G, Liu T, Thanassi DG (2004) The outer membrane usher forms a twin-pore secretion complex. J Mol Biol 344: 1397-1407.
28. Langermann S, Palaszynski S, Barnhart M, Auguste G, Pinkner JS, Burlein J, Barren P, Koenig S, Leath S, Jones CH, Hultgren SJ (1997) Prevention of mucosal Escherichia coli infection by FimH-adhesinbased systemic vaccination. Science 276: 607-611.
29. Langermann S, Mollby R, Burlein JE, Palaszynski SR, Auguste CG, DeFusco A, Strouse R, Schenerman MA, Hultgren SJ, Pinkner JS, Winberg J, Guldevall L, Soderhall M, Ishikawa K, Normark S, Koenig S (2000) Vaccination with FimH adhesin protects cynomolgus monkeys from colonization and infection by uropathogenic Escherichia coli. J Infect Dis 181: 774-778.
30. Levine MM, Giron J, Noriega F (1994) Fimbrial vaccines. In Fimbriae, Adhesion, Genetics, Biogenesis and Vaccine. Klemm P, ed, pp 271-286. Boca Raton, FL:CRC Press.
31. Lund B, Lindberg F, Marklund BI, Normark S (1987) The PapG protein is the β-D-galactopyranosyl-(1-4)-β-D-galactopyranose-binding adhesin of uropathogenic Escherichia coli. Proc Natl Acad Sci USA 84: 5898-5902.
32. Miller J, Williamson ED, Lakey JH, Pearce MJ, Jones SM, Titball RW (1998) Macromolecular organisation of recombinant Yersinia pestis F1 antigen and the effect of structure on immunogenicity. FEMS Immunol Med Microbiol 21: 213-221.
33. Moon HW, Bunn TO (1993) Vaccines for preventing enterotoxigenic Escherichia coli infections in farm animals. Vaccine 11: 213-220.
34. Mulvey MA (2002) Adhesion and entry of uropathogenic Escherichia coli. Cell Microbiol 4: 257-271.
35. Ng TW, Akman L, Osisami M, Thanassi DG (2004) The usher N terminus is the initial targeting site for chaperone-subunit complexes and participates in subsequent pilus biogenesis events. J Bacteriol 186: 5321-5331.
36. Nowicki B, Svanborg-Edén C, Hull R, Hull S (1989) Molecular analysis and epidemiology of the Dr hemagglutinin of uropathogenic Escherichia coli. Infect Immun 57: 446-451.
37. Nowicki B, Labigne A, Moseley S, Hull R, Hull S, Moulds J (1990) The Dr hemagglutinin, afimbrial adhesins AFA-I and AFA-III, and F1845 fimbriae of uropathogenic and diarrhea-associated Escherichia coli belong to a family of hemagglutinins with Dr receptor recognition. Infect Immun 58: 279-281.
38. Pettigrew D, Anderson KL, Billington J, Cota E, Simpson P, Urvil P, Rabuzin F, Roversi P, Nowicki B, du Merle L, Le Bouguenec C, Matthews S, Lea SM (2004) High resolution studies of the Afa/Dr adhesin DraE and its interaction with chloramphenicol. J Biol Chem 279: 46851-46857.
39. Pia̧tek R, Zalewska B, Kolaj O, Ferens M, Nowicki B, Kur J (2005) Molecular aspects of biogenesis of Escherichia coli Dr Fimbriae: characterization of DraB-DraE complexes. Infect Immun 73: 135-145.
40. Pouttu R, Puustinen T, Virkola R, Hacker J, Klemm P, Korhonen TK (1999) Amino acid residue Ala-62 in the FimH fimbrial adhesin is critical for the adhesiveness of meningitis-associated Escherichia coli to collagens. Mol Microbiol 31: 1747-1757.
41. Saulino ET, Bullitt E, Hultgren SJ (2000) Snapshots of usher-mediated protein secretion and ordered pilus assembly. Proc Natl Acad Sci USA 97: 9240-9245.
42. Sauer FG, Fütterer K, Pinkner JS, Dodson KW, Hultgren SJ, Waksman G (1999) Structural basis of chaperone function and pilus biogenesis. Science 285: 1058-1061.
43. 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.
44. Sauer FG, Remaut H, Hultgren SJ, Waksman G (2004) Fiber assembly by the chaperone-usher pathway. Biochim Biophys Acta 1694: 259-267.
45. Selvarangan R, Goluszko P, Singhal J, Carnoy C, Moseley S, Hudson B, Nowicki S, Nowicki B (2004) Interaction of Dr adhesin with collagen type IV is a critical step in Escherichia coli renal persistence. Infect Immun 72: 4827-4835.
46. Slonim LN, Pinkner JS, Branden CI, Hultgren SJ (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. Sokurenko EV, Courtney HS, Ohman DE, Klemm P, Hasty DL (1994) FimH family of type 1 fimbrial adhesins: functional heterogeneity due to minor sequence variations among fimH genes. J Bacteriol 176: 748-755.
48. Stentebjerg-Olesen B, Pallesen L, Jensen LB, Christiansen G, Klemm P (1997) Authentic display of a cholera toxin epitope by chimeric type 1 fimbriae: effects of insert position and host background. Microbiol 143: 2027-2038.
49. Svensson A, Larsson A, Emtenas H, Hedenstrom M, Fex T, Hultgren SJ, Pinkner JS, Almqvist F, Kihlberg J (2001) Design and evaluation of pilicides: potential novel antibacterial agents directed against uropathogenic Escherichia coli. Chembiochem 2: 915-918.
50. Van Loy CP, Sokurenko EV, Samudrala R, Moseley SL (2002a) Identification of amino acids in the Dr adhesin required for binding to decay-accelerating factor. Mol Microbiol 45: 439-452.
51. Van Loy CP, Sokurenko EV, Moseley SL (2002b) The major structural subunits of Dr and F1845 fimbriae are adhesins. Infect Immun 70: 1694-1702.
52. Westerlund B, Kuusela P, Risteli J, Vartio T, Rauvala H, Virkola R, Korhonen TK (1989) The O75X adhesin of uropathogenic Escherichia coli is a type IV collagen-binding protein. Mol Microbiol 3: 329-337.
53. Westerlund B, van Die I, Kramer C, Kuusela P, Holthöfer H, Tarkkanen AM, Virkola R, Riegman N, Bergmans H, Hoekstra W, Korhonen TK (1991) Multifunctional nature of P fimbriae of uropathogenic Escherichia coli: mutations in fsoE and fsoF influence fimbrial binding to renal tubuli and immobilized fibronectin. Mol Microbiol 5: 2965-2975.
54. Zalewska B, Pia̧tek R, Konopa G, Nowicki B, Nowicki S, Kur J (2003) Chimeric Dr fimbriae with a herpes simplex virus type 1 epitope as a model for a recombinant vaccine. Infect Immun 71: 5505-5513.
55. Zavialov AV, Kersley J, Korpela T, Zav'yalov VP, MacIntyre S, Knight SD (2002) Donor strand complementation mechanism in the biogenesis of non-pilus systems. Mol Microbiol 45: 983-995.
56. Zavialov AV, Berglund J, Pudney AF, Fooks LJ, Ibrahim TM, MacIntyre S, Knight SD (2003) Structure and biogenesis of the capsular F1 antigen from Yersinia pestis: preserved folding energy drives fiber formation. Cell 113: 587-596.
57. Zav'yalov VP, Chernovskaya TV, Chapman DA, Karlyshev AV, MacIntyre S, Zavialov AV, Vasiliev AM, Denesyuk AI, Zav'yalova GA, Dudich IV, Korpela T, Abramov VM (1997) Influence of the conserved disulphide bond, exposed to the putative binding pocket, on the structure and function of the immunoglobulin-like molecular chaperone Caf1M of Yersinia pestis. Biochem J 32: 571-578.