Molecular basis of two subfamilies of immunoglobulin-like chaperones

EMBO Journal

Volumn 15, Issue 15, 1996, Pages 3792-3805

  Hung, Danielle L ^a   Knight, Stefan D ^b   Woods, Robert M ^c   Pinkner, Jerome S ^a   Hultgren, Scott J ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UPPSALA UNIVERSITY   (Sweden)

^c MEDIMMUNE   (United States)

Author keywords

Immunoglobulin like chaperones; Pathogenesis; Virulence associated pili; X ray crystallography

Indexed keywords

ADHESIN; CHAPERONE; IMMUNOGLOBULIN; PROTEIN SUBUNIT;

ARTICLE; BACTERIAL INFECTION; BACTERIAL VIRULENCE; BACTERIUM PILUS; CARBOXY TERMINAL SEQUENCE; CELL STRUCTURE; CYTOPLASM; FIMBRIA; GRAM NEGATIVE BACTERIUM; HYDROGEN BOND; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN STRUCTURE;

BACTERIA (MICROORGANISMS); NEGIBACTERIA;

EID: 0029738256     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1996.tb00753.x     Document Type: Article

References (68)

1. Ahrens, R., Ott, M., Ritter, A., Hoschützky, H., Bühler, T., Lottspeich, F., Boulnois, G.J., Jann, K. and Hacker, J. (1993) Genetic analysis of the gene cluster encoding nonfimbrial adhesin I from an Escherichia coli uropathogen. Infect. Immun., 61, 2505-2512.
2. Allen, B.L., Gerlach, G.F. and Clegg, S. (1991) Nucleotide sequence and functions of mrk determinants necessary for expression of type 3 fimbriae in Klebsiella pneumoniae. J. Bacteriol., 173, 916-920.
3. Amit, A.G., Marrizzua, R.A., Phillips, S.E. and Poljak, R.J. (1986) Three dimensional structure of an antibody-antigen complex at 2.8A resolution. Science, 233, 747-753.
4. Arnqvist, A., Olsén, A., Pfieffer, J., Russel, D.G. and Normark, S. (1992) The Crl protein activates cryptic genes for curli formation and fibronectin binding in Escherichia coli. Mol Microbiol., 6, 2443-2453.
5. Bahrani, F.K. and Mobley, H.L.T. (1994) Proteus mirabilis MR/P fimbrial operon: genetic organization, nucleotide sequence, and conditions for expression. J. Bacteriol., 176, 3412-3419.
6. Bahrani, F.K., Johnson, D.E., Robbins, D. and Mobley, H.L.T. (1991) Proteus mirabilis flagella and MR/P fimbriae: isolation, purification, N-terminal analysis and serum antibody response following experimental urinary tract infection. Infect. Immun., 59, 3574-3580.
7. Bahrani, F.K., Cook, S., Hull, R.A., Massad, G. and Mobley, H.L.T. (1993) Proteus mirabilis fimbriae: N-terminal amino acid sequence of a major fimbrial subunit and nucleotide sequences of the genes from two strains. Infect. Immun., 61, 884-891.
8. Bakker, D., Vader, C.E.M., Mooi, F.R., Oudega, B. and de Graaf, F.K. (1991) Structure and function of periplasmic chaperone-like proteins involved in the biosynthesis of K88 and K99 fimbriae in enterotoxigenic Escherichia coli. Mol. Microbiol., 5, 875-886.
9. Bäumler, A.J. and Heffron, F. (1995) Identification and sequence analysis of lpfABCDE, a putative fimbrial operon of Salmonella typhimurium. J. Bacteriol., 177, 2087-2097.
10. Bertin, Y., Girardeau, J.P., Vartanian, M.D. and Martin, C. (1993) The ClpE protein involved in biogenesis of the CS31A capsule-like antigen is a member of a periplasmic chaperone family in gram-negative bacteria. FEMS Microbiol. Lett., 108, 59-68.
11. Bullitt, E. and Makowski, L. (1995) Structural polymorphism of bacterial adhesion pili. Nature, 373, 164-167.
12. Clouthier, S.C., Müller, K.H., Doran, J.L., Collinson, S.K. and Kay, W.W. (1993) Characterization of three fimbrial genes, sefABC, of Salmonella enteritidis. J. Bacteriol., 175, 2523-2533.
13. Dodson, K.W., Jacob-Dubuisson, F., Striker, R.T. and Hultgren, S.J. (1993) Outer membrane PapC usher discriminately recognizes periplasmic chaperone-pilus subunit complexes. Proc. Natl Acad. Sci. USA, 90, 3670-3674.
14. Duchet-Suchaux, M., Bertin, A. and Dubray, G. (1988) Morphological description of surface structures on strain B41 of bovine enterotoxigenic Escherichia coli bearing both K99 and F41 antigens. J. Gen. Microbiol., 134, 983-995.
15. Foged, N.T., Klemm, P., Elling, F., Jorsal, S.E. and Zeuthen, J. (1986) Monoclonal antibodies to K88ab, K88ac and K88ad fimbriae from enterotoxigenic Escherichia coli. Microb. Pathogen., 1, 57-69.
16. Friedrich, M.J., Kinsey, N.E., Vila, J. and Kadner, R.J. (1993) Nucleotide sequence of a 13.9 kb segment of the 90 kb virulence plasmid of Salmonella typhimurium: the presence of a fimbrial biosynthetic gene. Mol. Microbiol., 8, 543-558.
17. Galyov, E.E., Karlishev, A.V., Chernovskaya, T.V., Dolgikh, D.A., Smirnov, O.Yu., Volkovoy, K.I., Abramov, V.M. and Zav'yalov, V.P. (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.
18. Garcia, M.I., Labigne, A. and LeBouguenec, C. (1994) Nucleotide sequence of the afimbrial-adhesin-encoding afa-3 gene cluster and its translocation via flanking IS1 insertion sequences. J. Bacteriol., 176, 7601-7613.
19. Girardeau, J.P., Vartanian, M.D., Ollier, J.L. and Contrepois, M. (1988) CS31A, a new K88-related fimbrial antigen on bovine enteropathogenic and septicemic Escherichia coli strains. Infect. Immun., 56, 2180-2188.
20. Goldhar, J., Perry, R., Golecki, J.R., Hoschutzky, H., Jann, B. and Jann, K. (1987) Nonfimbrial, mannose-resistant adhesins from uropathogenic Escherichia coli O83:K1:H4 and O14:K?:H11. Infect. Immun., 55, 1837-1842.
21. Hacker, J. and Morschhäuser, J. (1994) S and F1C fimbriae. In Klemm, P. (ed.), Fimbriae: Adhesion, Genetics, Biogenesis, and Vaccines. CRC Press, Boca Raton, FL, pp. 27-36.
22. Holmgren, A. and Brändén, C.-I. (1989) Crystal structure of chaperone protein PapD reveals an immunoglobulin fold. Nature, 342, 248-251.
23. Holmgren, A., Kuehn, M.J., Brändén, C.-I. and Hultgren, S.J. (1992) Conserved imunoglobulin-like features in a family of periplasmic pilus chaperones in bacteria. EMBO J., 11, 1617-1622.
24. 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.
25. Hultgren, S.J., Normark, S. and Abraham, S.N. (1991) Chaperone-assisted assembly and molecular architecture of adhesive pili. Annu. Rev. Microbiol., 45, 383-415.
26. Hultgren, S.J., Abraham, S.N., Caparon, M.G., Falk, P., St. Geme, J.W., III and Normark, S. (1993a) Pilus and non-pilus bacterial adhesins: assembly and function in cell recognition. Cell, 73, 887-901.
27. Hultgren, S.J., Jacob-Dubuisson, F., Jones, C.H. and Brändén, C.-I. (1993b) PapD and superfamily of periplasmic immunoglobulin-like pilus chaperones. Adv. Protein Chem., 44, 99-123.
28. Iriarte, M., Vanooteghem, J.C., Delor, I., Díaz, R., Knutton, S. and Cornelis, G.R. (1993) The Myf fibrillae of Yersinia enterocolitica. Mol. Microbiol., 9, 507-520.
29. Jacob-Dubuisson, F., Heuser, J., Dodson, K., Normark, S. and Hultgren, S.J. (1993a) Initiation of assembly and association of the structural elements of a bacterial pilus depend on two specialized tip proteins. EMBO J., 12, 837-847.
30. Jacob-Dubuisson, F., Kuehn, M. and Hultgren, S. (1993b) A novel secretion apparatus for the assembly of adhesive bacterial pili. Trends Microbiol., 1, 50-55.
31. Jalajakumari, M.B., Thomas, C.J., Halter, R. and Manning, P.A. (1989) Genes for biosynthesis and assembly of CS3 pili of CFA/II enterotoxigenic Escherichia coli: novel regulation of pilus production by bypassing an amber codon. Mol. Microbiol., 3, 1685-1695.
32. Jones, C.H., Pinkner, J.S., Nicholes, A.V., Slonim, L.N., Abraham, S.N. and Hultgren, S.J. (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.
33. Jones, C.H., Pinkner, J.S., Roth, R., Heuser, J., Nicholes, A.V., Abraham, S.N. and Hultgren, S.J. (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.
34. Jones, T.A., Zou, J.Y., Cowan, S.W. and Kjeldgaard, 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.
35. Karlyshev, A.V., Galyov, E.E., Smirnov, O.Y., Guzayev, A.P., Abramov, V.M. and Zav'yalov, V.P. (1992) A new gene of the f1 operon of Y. pestis involved in the capsule biogenesis. FEBS Lett., 297, 77-80.
36. Klemm, P. and Krogfelt, K.A. (1994) Type 1 fimbriae of Escherichia coli. In Klemm, P. (ed.), Fimbriae: Adhesion, Genetics, Biogenesis, and Vaccines. CRC Press, Boca Raton, FL, pp. 9-26.
37. Klemm, P., Christiansen, G., Kreft, B., Marre, R. and Bergmans, H. (1994) Reciprocal exchange of minor components of Type 1 and F1C fimbriae results in hybrid organelles with changed receptor specificities. J. Bacteriol., 176, 2227-2234.
38. Klemm, P., Jørgensen, B.J., Kreft, B. and Christiansen, G. (1995) The export systems of type 1 and F1C fimbriae are interchangeable but work in parental pairs. J. Bacteriol., 177, 621-627.
39. Knutton, S., McConnell, M.M., Rowe, B. and McNeish, A.S. (1989) Adhesion and ultrastructural properties of human enterotoxigenic Escherichia coli producing colonization factor antigens III and IV. Infect. Immun., 57, 3364-3371.
40. Kuehn, M.J., Normark, S. and Hultgren, S.J. (1991) Immunoglobulin-like PapD chaperone caps and uncaps interactive surfaces of nascently translocated pilus subunits. Proc. Natl Acad. Sci. USA, 88, 10586-10590.
41. 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.
42. 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.
43. Kuehn, M.J., Haslam, D., Normark, S. and Hultgren, S.J. (1994) Structure, function, and biogenesis of Escherichia coli P pili. In Klemm, P. (ed.), Fimbriae: Adhesion, Genetics, Biogenesis, and Vaccines. CRC Press, Boca Raton, FL, pp. 37-51.
44. Le Bouguenec, C., Garcia, M.I., Ouin, V., Desperrier, J.-M., Gounon, P. and Labigne, A. (1993) Characterization of plasmid bourne afa-3 gene clusters encoding afimbrial adhesins expressed by Escherichia coli strains associated with intestinal or urinary tract infections. Infect. Immun., 61, 5106-5114.
45. Levine, M.M. et al. (1984) Coli surface antigens 1 and 3 of colonization factor antigen II-positive enterotoxigenic Escherichia coli: morphology, purification, and immune responses in humans. Infect. Immun., 44, 409-420.
46. Lindberg, F., Tennent, J.M., Hultgren, S.J., Lund, B. and Normark, S. (1989) PapD, a periplasmic transport protein in P-pilus biogenesis. J. Bacteriol., 171, 6052-6058.
47. Lindler, L.E. and Tall, B.D. (1993) Yersinia pestis pH 6 antigen forms fimbriae and is induced by intracellular association with macrophages. Mol. Microbiol., 8, 311-324.
48. Lintermans, P.F. et al. (1988) Characterization and purification of the F17 adhesin on the surface of bovine enteropathogenic and septicemic Escherichia coli. Am. J. Vet. Res., 49, 1794-1799.
49. Massad, G. and Mobley, H.L.T. (1994) Genetic organization and complete sequence of the Proteus mirabilis pmf fimbrial operon. Gene, 150, 101-104.
50. Merrifield, R.B. (1963) Solid phase peptide synthesis. I. The synthesis of a tetrapeptide. J. Am. Chem. Soc., 85, 2149-2154.
51. Miller, S., Janin, J., Lesk, A.M. and Chothia, C. (1987) Interior and surface of monomeric proteins. J. Mol. Biol., 196, 641-656.
52. Müller, K.H., Collinson, S.K., Trust, T.J. and Kay, W.W. (1991) Type 1 fimbriae of Salmonella enteritidis. J. Bacteriol., 173, 4765-4772.
53. Nicholls, A. (1993) GRASP: Graphical Representation and Analysis of Surface Properties. Columbia University Press, New York.
54. Normark, S., Båga, M., Goransson, M., Lindberg, F.P., Lund, B., Norgren, M. and Uhlin, B.E. (1986) Genetics and biogenesis of Escherichia coli adhesins. In Mirelman, D. (ed.), Microbial Lectins and Agglutinins: Properties and Biological Activity. Wiley Interscience, New York, pp. 113-143.
55. Pugsley, A. (1993) The complete general secretory pathway in Gram negative bacteria. Microbiol. Rev., 57, 50-108.
56. Raina, S., Missiakas, D., Baird, L., Kumar, S. and Georgopoulos, C. (1993) Identification and transcriptional analysis of the Escherichia coli htrE operon which is homologous to pap related pilin operons. J. Bacteriol., 75, 5009-5021.
57. Roberts, J.A. et al. (1994) The Ga1 α(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.
58. Savarino, S.J., Fox, P., Yikang, D. and Nataro, J.P. (1994) Identification and characterization of a gene cluster mediating enteroaggregative Escherichia coli aggregative adherence fimbriae I biogenesis. J. Bacteriol., 176, 4949-4957.
59. Schmoll, T., Morschhauser, J., Ott, M., Ludwig, B., van Die, I. and Hacker, J. (1990) Complete genetic organization and functional aspects of the Escherichia coli S fimbrial adhesin determinant: nucleotide sequence of the genes sfa B, C, D, E, F. Microb. Pathogen., 9, 331-343.
60. Shapiro, L. et al. (1995) Structural basis of cell-cell adhesion by cadherins. Nature, 374, 327-337.
61. Simons, B., Rathman, P., Malij, C., Oudega, B. and de Graf, F.K. (1990) The penultimate tyrosine residue of the K99 fibrillar subunit is essential for the stability of the protein and its interaction with the periplasmic carrier protein. FEMS Microbiol. Lett., 67, 107-112.
62. Slonim, L.N., Pinkner, J.S., Brändén, C.I. 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.
63. Steven, A.C., Bisher, M.E., Trus, B.L., Thomas, D., Zhang, J.M. and Cowell, J.L. (1986) Helical structure of Bordetella pertussis fimbriae. J. Bacteriol., 167, 968-974.
64. Stirm, S., Ørskov, F., Ørskov, E. and Birch-Andersen, A. (1967) Episome-carried surface antigen K88 of Escherichia coli. J. Bacteriol., 93, 740-748.
65. Stull, T.L., Mendelman, P.M., Haas, J.E., Schoenborn, M.A., Mack, K.D. and Smith, A.L. (1984) Characterization of Haemophilus influence type b fimbriae. Infect. Immun., 46, 787-796.
66. Willems, R.J.L., van der Heide, H.G.J. and Mooi, F.R. (1992) Characterization of a Bordetella pertussis fimbrial gene cluster which is located directly downstream of the filamentous haemagglutinin gene. Mol. Microbiol., 6, 2661-2671.
67. Williams, A.F. and Barclay, A.N. (1988) The immunoglobulin superfamily-domains for cell surface recognition. Annu. Rev. Immunol., 6, 381-405.
68. Wolf, M.K., Andrews, G.P. Tall, B.D., McConnell, M.M., Levine, M.M. and Boedeker, E.C. (1989) Characterization of CS4 and CS6 antigenic components of PCF8775, a putative colonization factor complex from enterotoxigenic Escherichia coli E8775. Infect. Immun., 57, 164-173.