Pilus biogenesis via the chaperone/usher pathway: An integration of structure and function

Journal of Structural Biology

Volumn 124, Issue 2-3, 1998, Pages 201-220

  Hung, Danielle L ^a   Hultgren, Scott J ^a  

^a WASHINGTON UNIVERSITY   (United States)

Author keywords

Chaperone; P pili; Urinary tract infections; Usher

Indexed keywords

CHAPERONE;

ARTICLE; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BACTERIUM PILUS; BACTERIUM TRANSDUCTION; ESCHERICHIA COLI; IMMUNOGLOBULIN STRUCTURE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FOLDING; STRUCTURE ACTIVITY RELATION;

EID: 0032461831     PISSN: 10478477     EISSN: None     Source Type: Journal    
DOI: 10.1006/jsbi.1998.4049     Document Type: Article

References (119)

1. Adams L. M., Simmons C. P., Rezmann L., Strugnell R. A., Robins-Browne R. M. Identification and characterization of a K88- and CS31A-like operon of a rabbit enteropathogenicEscherichia coli. Infect. Immun. 65:1997;5222-5230.
2. Ahrens R., Ott M., Ritter A., Hoschutzkky H., Buhler T., Lottspeich F., Boulnois G. J., Jann K., Hacker J. Genetic analysis of the gene cluster encoding nonfimbrial adhesin I from anEscherichia coli. Infect. Immun. 61:1993;2505-2512.
3. Allen B. L., Gerlach G. F., Cleff S. Nucleotide sequence and functions ofmrkKlebsiella pneumoniae. J. Bacteriol. 173:1991;916-920.
4. Amit A. G., Marrizzua R. A., Phillips S. E., Poljak R. J. Three dimensional structure of an antibody-antigen complex at 2.8A resolution. Science. 233:1986;747-753.
5. Båga M., Norgren, Normark S. Biogenesis of E. coli Pap pili: PapH, a minor pilin subunit involved in cell anchoring and length modulation. Cell. 49:1987;241-251.
6. Båga M., Goransson M., Normark S., Uhlin B. E. Transcriptional activation of a Pap pilus virulence operon from uropathogenicEscherichia coli. EMBO J. 4:1985;3887-3893.
7. Båga M., Normark S., Hardy J., O'Hanley P., Lark D., Olsson O., Schoolnik G., Falkow S. Nucleotide sequence of the gene encoding thepapAEscherichia coli. J. Bacteriol. 157:1984;330-333.
8. Bahrani F. K., Mobley H. L. T. Proteus mirabilis. J. Bacteriol. 176:1994;3412-3419.
9. Bahrani F. K., Cook S., Hull R., Massad G., Mobley H. L. T. Proteus mirabilis. Infect. Immun. 61:1993;884-891.
10. Bahrani F. K., Johnson D. E., Robbins D., Mobley H. L. T. Proteus mirabilis. Infect. Immun. 59:1991;3574-3580.
11. Bakker D., Vader C. E., Roosendall B., Mooi F. R., Oudega B., de Graaf F. K. Structure and function of periplasmic chaperone-like proteins involved in the biosynthesis of K88 and K99 fimbriae in enterotoxigenicEscherichia coli. Mol. Microbiol. 5:1991;875-886.
12. Baumler A. J., Heffron F. Identification and sequence analysis oflpfABCDE,Salmonella typhimurium. J. Bacteriol. 177:1995;2087-2097.
13. Barza M. Urinary Tract. Mechanisms of Microbial Disease. 1993;Williams & Wilkins, Baltimore. p. 735-747.
14. Bertin Y., Girardeau J. P., Vartanian M. D., Martin C. 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. 108:1993;59-68.
15. Blum G., Ott M., Lischewski A., Ritter A., Imrich H., Tschape H., Hacker J. Excision of large DNA regions termed pathogenicity islands from tRNA-specific loci in the chromosome of anEscherichia coli. Infect. Immun. 62:1994;606-614.
16. Blyn L. B., Braaten B. A., White Z. C., Rolfson D. H., Low D. A. Phase-variation of pyelonephritis-associated pili in Escherichia coli: Evidence for transcriptional regulation. EMBO J. 8:1989;613-620.
17. Bock K., Breimer M. E., Brignole A., Hansson G. C., Karlsson K.-A., Larson G., Leffler H., Samuelsson B. E., Strömberg N., Svanborg-Edén C., Thurin J. Specificity of binding of a strain of uropathogenicEscherichia coli. J. Biol. Chem. 260:1985;8545-8551.
18. Brinton C. C. Jr. The structure, function, synthesis, and genetic control of bacterial pili and a model for DNA and RNA transport in gram negative bacteria. Trans. N.Y. Acad. Sci. 27:1965;1003-1165.
19. Bullitt E., Jones C. H., Striker R., Soto G., Jacob-Dubuisson F., Pinkner J., Wick M. J., Makowski L., Hultgren S. J. Development of pilus organelle subassembliesin vitro. Proc. Natl. Acad. Sci. USA. 93:1996;12890-12895.
20. Bullitt E., Makowski L. Structural polymorphism of bacterial adhesion pili. Nature. 373:1995;164-167.
21. Cao J., Chan A. S., Bayer M. E., Schifferli D. M. Ordered translocation of 987P fimbrial subunits through the outer membrane ofEscherichia coli. J. Bacteriol. 177:1995;3704-3713.
22. Clouthier S. C., Muller K. H., Doran J. L., Collinson S. K., Kay W. W. Characterization of three fimbrial genes,sefABC,Salmonella enteriditis. J. Bacteriol. 175:1993;2523-2533.
23. Connell H., Agace W., Klemm P., Schembri M., Marild S., Svanborg C. Type 1 fimbrial expression enhancesEscherichia coli. Proc. Natl. Acad. Sci. USA. 93:1996;9827-9832.
24. Danese P. N., Silhavy T. J. The σE and the Cpx signal transduction systems control the synthesis of periplasmic protein-folding systems inEscherichia coli. Genes Dev. 11:1997;1183-1193.
25. Davies D. R., Padlan E. A. Antibody-antigen complexes. Annu. Rev. Biochem. 59:1990;439-473.
26. Dodson K. W., Jacob-Dubuisson F., Striker R. T., Hultgren S. J. Outer membrane PapC usher discriminately recognizes periplasmic chaperone-pilus subunit complexes. Proc. Natl. Acad. Sci. USA. 90:1993;3670-3674.
27. Dong J., Iuchi S., Kwan H.-S., Lu Z., Lin E. C. C. The deduced amino-acid sequence of the clonedcpxREscherichia coli. Gene. 136:1993;227-230.
28. Duchet-Suchaux M., Bertin A., Dubray G. Morphological description of surface structures on strain B41 of bovine enterotoxigenicEscherichia coli. J. Gen. Microbiol. 134:1988;983-995.
29. Duguid J. P., Smith I. W., Dempster G., Edmunds P. N. Non-flagellar filamentous appendages ("fimbriae") and hemagglutinating activity inbacterium coli. J. Pathol. Bacteriol. 70:1955;335-348.
30. Edwards R. A., Cao J., Schifferli D. M. Identification of major and minor chaperone proteins involved in the export of 987P fimbriae. J. Bacteriol. 178:1996;3426-3433.
31. Foged N. T., Klemm P., Ellilng F., Jorsal S. E., Zeuthen J. Monoclonal antibodies to K88ab, K88ac, and K88ad fimbriae from enterotoxigenicEscherichia coli. Microb. Pathog. 1:1986;57-69.
32. Forsman K., Goransson M., Uhlin B. E. Autoregulation and multiple DNA interactions by a transcriptional regulatory protein in E. coli pili biogenesis. EMBO J. 8:1989;1271-1277.
33. Forsman K., Sonden B., Goransson M., Uhlin B. E. Antirepression function inEscherichia coli. Proc. Natl. Acad. Sci. U.S.A. 89:1992;9880-9884.
34. Friedich M. J., Kinsey N. E., Vila J., Kadner R. J. Nucleotide sequence of a 13.9 kb segment of the 90kb virulence plasmid ofSalmonella typhimurium. Mol. Microbiol. 8:1993;543-558.
35. Galyov E. E., Karlishev A. V., Chernovskaya T. V., Dolgikh D. A., Smirnov O. Y., Volkovoy K. I., Abramov V. M., Zav'yalov V. P. Expression of the envelope antigen F1 ofYersinia pestiscal1MEscherichia coli. FEBS Lett. 286:1991;79-82.
36. Garcia M. I., Labigne A., LeBouguenec C. Nucleotide sequence of the afimbrial-adhesin-encodingafa-3. J. Bacteriol. 176:1994;7601-7613.
37. Girdeau J. P., Vartanian M. D., Ollier J. L., Contrepois M. CS31A, a new K88-related fimbrial antigen on bovine enteropathogenic and septicemicEscherichia coli. Infect. Immun. 56:1988;2180-2188.
38. Goldhar J., Perry R., Golecki J. R., Hoschutzky H., Jann B., Jann K. Nonfimbrial, mannose-resistant adhesins from uropathogenicEscherichia coli. Infect. Immun. 55:1987;1837-1842.
39. Gong M., Makowski L. Helical structure of Pap adhesion pili fromEscherichia Coli. J. Mol. Biol. 228:1992;735-742.
40. Gruneberg R. N., Brumfitt W. Single-dose treatment of acute urinary tract infection: A controlled trial. Br. Med. J. 9:1967;649-651.
41. Hacker J., Blum-Oehler G., Muhldorfer I., Tschape H. Pathogenicity islands of virulent bacteria: Structure, function and impact on microbial evolution. Mol. Microbiol. 23:1997;1089-1097.
42. Hacker J., Morschhauser J. S and F1C Fimbriae. Klemm P. Fimbriae: Adhesion, Genetics, Biogenesis, and Vaccines. 1994;27-36 CRC Press, Boca Raton.
43. Hacker J., Bender L., Ott M., Wingender J., Lund B., Marre R., Goebel W. Deletions and chromosomal regions coding for fimbriae and hemolysins occurin vitroin vivoEscherichia coli. Microb. Pathog. 8:1990;213-225.
44. Hartl U. F., Martin J. Molecular chaperones in cellular protein folding. Curr. Opin. Struct. Biol. 5:1995;92-102.
45. Holmgren A., Brändén C. Crystal structure of chaperone protein PapD reveals an immunoglobulin fold. Nature. 342:1989;248-251.
46. Holmgren A., Kuehn M. J., Brändén C.-I., Hultgren S. J. Conserved immunoglobulin-like features in a family of periplasmic pilus chaperones in bacteria. EMBO J. 11:1992;1617-1622.
47. Hull R. A., Gill R. E., Hsu P., Minshaw B. H., Falkow S. Construction and expression of recombinant plasmids encoding type 1 and D-mannose-resistant pili from a urinary tract infectionEscherichia coli. Infect. Immun. 33:1981;933-938.
48. Hultgren S. J., Abraham S. N., Caparon M. G., Falk P., St. Geme J. W. III, Normark S. Pilus and non-pilus bacterial adhesins: Assembly and function in cell recognition. Cell. 73:1993a;887-901.
49. Hultgren S. J., Jacob-Dubuisson F., Jones C. H., Brändén C.-I. PapD and superfamily of periplasmic immunoglobulin-like pilus chaperones. Lorimer G. Advances in Protein Chemistry. 1993b;99-123 Academic Press, San Diego.
50. Hultgren S. J., Normark S., Abraham S. N. Chaperone-assisted assembly and molecular architecture of adhesive pili. Annu. Rev. Microbiol. 45:1991;383-415.
51. Hultgren S. J., Lindberg F., Magnusson G., Kihlberg J., Tennent J. M., Normark S. The PapG adhesin of uropathogenicEscherichia coli. Proc. Natl. Acad. Sci. USA. 86:1989;4357-4361.
52. Hung D. L., Knight S. D., Hultgren S. J. Probing conserved surfaces on PapD. Mol. Microbiol. 1999.
53. 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.
54. Iriate M., Vanooteghem C., Delor I., Diaz R., Knutton S., Cornelis G. R. The Myf fimbriallae ofYersinia enterocolitica. Mol. Microbiol. 9:1993;507-520.
55. 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. 12:1993a;837-847.
56. Jacob-Dubuisson F., Kuehn M. J., Hultgren S. J. A novel secretion apparatus for the assembly of adhesive bacterial pili. Trends Microbiol. 1:1993b;50-55.
57. Jacob-Dubuisson F., Striker R., Hultgren S. J. Chaperone-assisted self-assembly of pili independent of cellular energy. J. Biol. Chem. 269:1994a;12447-12455.
58. Jacob-Dubuisson F., Pinkner J., Xu Z., Striker R., Padmanhaban A., Hultgren S. J. PapD chaperone function in pilus biogenesis depends on oxidant and chaperone-like activities of DsbA. Proc. Natl. Acad. Sci. USA. 91:1994b;11552-11556.
59. Jalajakumari M. B., Thomas C. J., Halter R., Manning P. A. Genes for biosynthesis and assembly of CS3 pili of CFA/II enterotoxigenicEscherichia coli: Mol. Microbiol. 3:1989;1685-1695.
60. Johnson J. R. Virulence factors inEscherichia coli. Clin. Microbiol. Rev. 4:1991;80-128.
61. 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.
62. Jones C. H., Pinkner J. S., Roth R., Heuser J., Nicholas A. V., Abraham S. N., Hultgren S. J. FimH adhesin of type 1 pili is assembled into a fibrillar tip structure is theEnterobacteriaceae. Proc. Natl. Acad. Sci. USA. 92:1995;2081-2085.
63. Jones C. H., Pinkner J. S., Nicholes A. V., Slonim L. N., Abraham S. N., Hultgren S. J. FimC is a periplasmic PapD-like chaperone that directs assembly of type 1 pili in bacteria. Proc. Natl. Acad. Sci. USA. 90:1993;8397-8401.
64. Kallenius G., Svenson S. B., Hultberg H., Molby R., Helin I., Cedergen B., Windberg J. Occurrence of P fimbriatedEscherichia coli. Lancet. ii:1981;1369-1372.
65. Kaltenbach L. S., Braaten B. A., Low D. A. Specific binding of PapI to Lrp-pap. J. Bacteriol. 177:1995;6449-6455.
66. Kao J. S., Stucker D. M., Warren J. W., Mobley H. L. Pathogenicity island sequences of pyelonephrogenicEscherichia coli. Infect. Immun. 65:1997;2812-2820.
67. Kaper J. B. Molecular pathogenesis of enteropathogenicEscherichia coli. Miller V., Kaper J., Portnoy D., Isberg R. Molecular Genetics of Bacterial Pathogenesis: A Tribute to Stanley Falkow. 1994;173-197 ASM Press, Washington.
68. Karlsson K. F., Walse B., Drakenberg T., Kihlberg J. Synthesis and conformational studies of peptides fromE. coli. Lett. Pept. Sci. 3:1996;143-156.
69. Karlyshev A. V., Galyov E. E., Smirnov O. Y., Guzayev A. P., Abramov V. M., Zav'yalov V. P. A new gene of thef1Y. pestis. FEBS. 297:1992;77-80.
70. Klemm P., Jorgensen B. J., Kreft B., Christiansen G. The export of type 1 and F1C fimbriae are interchangeable by work in parental pairs. J. Bacteriol. 177:1995;621-627.
71. Klemm P., Krogfelt K. A. Type 1 fimbriae ofEscherichia coli. Klemm P. Fimbriae: Adhesion, Genetics, Biogenesis, and Vaccines. 1994;9-26 CRC Press, Boca Raton.
72. Knutton S., McConnel M. M., Rowe B., McNeish A. S. Adhesion and ultrastructural properties of human enterotoxigenicEscherichia coli. Infect. Immun. 57:1989;3364-3371.
73. 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.
74. Kuehn M. J., Heuser J., Normark S., Hultgren S. J. P pili in uropathogenicE. coli. Nature. 356:1992;252-255.
75. 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.
76. Langermann S., Palaszynski S., Barnhart M., Auguste G., Pinkner J. S., Burlein J., Barren P., Koenig S., Leath S., Jones C. H., Hultgren S. J. Prevention of mucosalEscherichia coli. Science. 262:1997;1234-1241.
77. Le Bouguenec C., Garcia M. I., Ouin V., Desperrier J-M., Gounon P., Labigne A. Characterization of plasmid bourne afa-3 gene clusters encoding afimbrial adhesins expressed byEscherichia coli. Infect. Immun. 61:1993;5106-5114.
78. Leffler H., Svanborg-Eden C. Chemical identification of a glycosphingolipid receptor forEscherichia coli. FEMS Microbiol. Lett. 8:1980;127-134.
79. Levine M. M., Ristaino P., Marley G., Smyth C., Knutton S., Boedeker E., Black R., Young C., Clements M. L., Cheney C., Patnaik R. Coli surface antigens 1 and 3 of colonization factor antigen II-positive enteritoxigenicEscherichia coli. Infect. Immun. 44:1984;409-429.
80. Lindler L. E., Tall B. D. Yersinia pestis. Mol. Microbiol. 8:1993;311-324.
81. Lintermans P. F., Pohl P., Bertels A., Charlier G., Vandekerckhove J., Van Damme J., Shoup J., Schlicker C., Korhonen T., De Greve H., Van Montagu M. Characterization and purification of the F7 adhesin on the surface of bovine enteropathogenic and septicemicEscherichia coli. Am. J. Vet. Res. 49:1988;1794-1799.
82. 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.
83. Massad G., Fulkerson J. F. Jr., Watson D. C., Mobley H. L. T. Proteus mirabilisaft. Infect. Immun. 64:1996;4390-4395.
84. Massad G., Lockatell C. V., Johnson D. E., Mobley H. L. T. Proteus mirabilispmfA. Infect. Immun. 62:1994a;536-542.
85. Massad G., Bahrani F. K., Mobley H. L. T. Proteus mirabilis. Infect. Immun. 62:1994b;1989-1994.
86. Muller K. H., Collinson S. K., Trust T. J., Kay W. W. Type 1 fimbriae ofSalmonella enteriditis. J. Bacteriol. 173:1991;454-457.
87. 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 uropathogenicEscherichia coli. Science. 282:1998;1494-1497.
88. Normark, S. Båga, M. Goransson, M. Lindberg, F. P. Lund, B. Norgren, M. Uhlin, B. E. 1986, Genetics and Biogenesis ofEscherichia coli, in, Mirelman, D. Microbial Lectins and Agglutinins: Properties and Biological Activity, 113, 143, Wiley-Interscience, New York.
89. Norgren M., Baga M., Tennent J. M., Normark S. Nucleotide sequence, regulation and functional analysis of thepapCEscherichia coli. Mol. Microbiol. 1:1987;169-178.
90. Norrby S. R. Opening remarks. Infection. 22:1994;S3.
91. Overduin M., Harvey T. S., Bagby S., Tong K. I., Yau P., Takeichi M., Ikura M. Solution structure of the epithelial cadherin domain responsible for selective cell adhesion. Science. 267:1995;386-389.
92. Pogliano J., Lynch A. S., Belin D., Lin E. C. C., Beckwith J. Regulation ofEscherichia coli. Genes Dev. 11:1997;1169-1182.
93. Raina S., Missiakas D., Baird L., Kumar S., Georgopoulos C. Identification and transcriptional analysis ofEscherichia coli htrE. J. Bacteriol. 175:1993;5009-5021.
94. Raivio T. L., Silhavy T. J. Transduction of envelope stress inEscherichia coli. J. Bacteriol. 179:1997;7724-7733.
95. Read T. D., Dowdell M., Satola S. W., Farley M. M. Duplication of pilus gene complexes ofHaemophilus influenzae. J. Bacteriol. 178:1996;6564-6570.
96. Ritter A., Blum G., Emody L., Kerenyi M., Bock A., Neuhierl B., Rabsch W., Scheutz F., Hacker J. tRNA genes and pathogenicity islands: Influence on virulence and metabolic properties of uropathogenicEscherichia coli. Mol. Microbiol. 17:1995;109-121.
97. Roberts J. A., Marklund B.-I., Ilver D., Haslam D., Kaack M. B., Baskin G., Louis M., Mollby R., Winberg J., Normark S. The Galα(1-4)Gal-specific tip adhesin ofEscherichia coli. Proc. Natl. Acad. Sci. USA. 91:1994;11889-11893.
98. Saulino E. T., Thanassi D. G., Pinkner J., Hultgren S. J. Ramifications of kinetic partitioning on usher-mediated pilus biogenesis. EMBO J. 17:1998;2177-2185.
99. Savarino S., Fox P., Yikang D., Nataro J. P. Identification and characterization of a gene cluster mediating enteroaggregativeEscherichia coli. J. Bacteriol. 176:1994;4949-4957.
100. Schmoll T., Morschhauser J., Ott M., Ludwig B., van Die I., Hacker J. Complete genetic organization and functional aspects of theEscherichia colisfa B, C, D, E, F. Microb. Pathog. 9:1990;331-343.
101. Shapiro L., Fannon A. M., Kwong P. D., Thompson A., Lehmann M. S., Grubel G., Legrand J. F., Als-Nielsen J., Colman D. R., Hendrickson W. A. Structural basis of cell-cell adhesion by cadherins. Nature. 374:1995;327-337.
102. Simons B., Rathman P., Malij C., Oudega B., de Graf F. K. 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. 67:1990;107-112.
103. 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.
104. Snyder W. B., Davis L. J., Danese P. N., Cosma C. L., Silhavy T. J. Overproduction of NlpE, a new outer membrane lipoprotein, suppresses the toxicity of periplasmic LacZ by activation of the Cpx signal transduction pathway. J. Bacteriol. 177:1995;4216-4223.
105. 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.
106. Steven A. C., Bisher M. E., Trus B. L., Thomas D., Zhang J. M., Covell J. L. Helical structure ofBordetella pertussis. J. Bacteriol. 167:1986;968-974.
107. Stirm S., Orskov F., Orskov E., Birch-Andersen A. Episome-carried surface antigen K88 ofEscherichia coli. J. Bacteriol. 93:1967;740-748.
108. Stromberg N., Nyholm P.-G., Pascher I., Normark S. Saccharide orientation at the cell surface affects glycolipid receptor function. Proc. Natl. Acad. Sci. USA. 88:1991;9340-9344.
109. Stromberg N., Marklund B. I., Lund B., Ilver D., Hamers A., Gaastra W., Karlsson K. A., Normark S. Host-specificity of uropathogenicEscherichia coli. EMBO J. 9:1990;2001-2010.
110. Stull T. L., Mendelman P. M., Haas J. E., Schoenborn M. A., Mack K. D., Smith A. L. Characterization ofHaemophilus influenzae. Infect. Immun. 46:1984;787-796.
111. Swenson D. L., Bukanov N. O., Berg D. E., Welch R. A. Two pathogenicity islands in uropathogenicEscherichia coli. Infect. Immun. 64:1996;3736-3743.
112. 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. 1:1998a;223-231.
113. 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. 95:1998b;3146-3151.
114. van der Woude M., Braaten B., Low D. Epigenetic phase variation of thepapEscherichia coli. Trends Microbiol. 4:1996;5-9.
115. van der Woude M. W., Braaten B. A., Low D. A. Evidence of global regulatory control of pilus expression inEscherichia coli. Mol. Microbiol. 6:1992;2429-2435.
116. Winberg J., Mollby R., Bergstrom J., Karlsson K. A., Leonardsson I., Milh M. A., Teneberg S., Haslam D., Marklund B. I., Normark S. The PapG-adhesin at the tip of P-fimbriae providesEscherichia coli. J. Exp. Med. 182:1995;1695-1702.
117. Willems R. J. L., van der Heide H. G. J., Mooi F. R. Characterization of aBordetella pertussis. Mol. Microbiol. 6:1992;2661-2671.
118. Wolf M. K., Andrews G. P., Tall B. D., McConnell M. M., Levine M. M., Boedeker E. C. Characterization of CS4 and CS6 antigenic components of PCF8775, a putative colonization factor complex from enterotoxigenicEscherichia coli. Infect. Immun. 57:1989;164-173.
119. Xu Z., Jones C. H., Haslam D., Dodson K., Kihlberg J., Hultgren S. J. Molecular dissection of PapD interaction with PapG reveals two chaperone binding sites. Mol. Microbiol. 16:1995;1011-1020.