Home LiteratureArticle Details
PMID: 7892228 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

FimH adhesin of type 1 pili is assembled into a fibrillar tip structure in the Enterobacteriaceae.

Jones CH, Pinkner JS, Roth R, Heuser J, Nicholes AV, Abraham SN, Hultgren SJ

Abstract

Type 1 pili are heteropolymeric mannosebinding fibers produced by all members of the Enterobacteriaceae family. The bulk of the fiber is composed of FimA. Two macromolecular complexes responsible for mediating an interaction with mannose-containing receptors were purified from fimA- Escherichia coli by mannose affinity chromatography and ion-exchange chromatography. One complex contained only the mannose-binding adhesin, FimH, associated with FimG, a minor component of the type 1 pilus. In the other complex the FimG-FimH moiety was loosely associated with a chaperone-minor subunit complex (FimC-FimF), possibly representing an intermediate in tip fibrilla assembly. The FimC chaperone has also been shown to form a preassembly complex with FimH that has been purified and characterized previously. Purified FimC did not bind to the FimG-FimH complex but did recognize FimH dissociated from the FimG-FimH complex. Quick-freeze deep-etch electron microscopy revealed that the FimG-FimH complex had a thin fibrillar architecture. High-resolution electron microscopy of type 1 pili revealed that a 16-nm fibrillar tip structure with an architecture identical to that of the FimG-FimH complex was joined end-to-end to the pilus rod. In a fimH- deletion mutant, the tip fibrillae joined to pilus rods were approximately 3 nm in length. The full-length tip fibrilla was restored by complementation with the fimH gene in trans. The bipartite nature of the type 1 pilus was also demonstrated on pili purified from clinical isolates of members of the Enterobacteriaceae family arguing that it is a conserved feature of the type 1 pilus.

MeSH Terms
Adhesins, Escherichia coli Bacterial Adhesion Bacterial Outer Membrane Proteins/isolation & purification,metabolism Bacterial Proteins/biosynthesis,isolation & purification Chromatography, Affinity Citrobacter freundii/genetics,isolation & purification,metabolism Enterobacter cloacae/genetics,isolation & purification,metabolism Enterobacteriaceae/genetics,metabolism Escherichia coli/genetics Escherichia coli Proteins Fimbriae Proteins Fimbriae, Bacterial/metabolism,ultrastructure Freeze Etching Humans Klebsiella pneumoniae/genetics,isolation & purification,metabolism Mannose Microscopy, Electron Recombinant Proteins/biosynthesis,isolation & purification,metabolism Urinary Tract Infections/microbiology
Chemicals
Adhesins, Escherichia coli Bacterial Outer Membrane Proteins Bacterial Proteins Escherichia coli Proteins Recombinant Proteins fimC protein, E coli fimH protein, E coli Fimbriae Proteins Mannose
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Jones C H
Department of Molecular Microbiology, Washington University School of Medicine, St. Louis, MO 63110.
Pinkner J S
Roth R
Heuser J
Nicholes A V
Abraham S N
Hultgren S J
References (28)
28 references, click to expand
  1. The structure, function, synthesis and genetic control of bacterial pili and a molecular model for DNA and RNA transport in gram negative bacteria.
    Trans N Y Acad Sci. 1965 Jun;27(8):1003-54 PMID: 5318403
  2. Stable fiber-forming and nonfiber-forming chaperone-subunit complexes in pilus biogenesis.
    J Biol Chem. 1994 Apr 22;269(16):12233-9 PMID: 7909317
  3. New knowledge on pathogenesis of bacterial enteric infections as applied to vaccine development.
    Microbiol Rev. 1983 Dec;47(4):510-50 PMID: 6363898
  4. Organization and expression of genes responsible for type 1 piliation in Escherichia coli.
    J Bacteriol. 1984 Aug;159(2):736-44 PMID: 6146599
  5. The genetic determinant of adhesive function in type 1 fimbriae of Escherichia coli is distinct from the gene encoding the fimbrial subunit.
    J Bacteriol. 1986 Mar;165(3):1033-6 PMID: 2419305
  6. Three fim genes required for the regulation of length and mediation of adhesion of Escherichia coli type 1 fimbriae.
    Mol Gen Genet. 1987 Jul;208(3):439-45 PMID: 2890081
  7. Identification of two ancillary subunits of Escherichia coli type 1 fimbriae by using antibodies against synthetic oligopeptides of fim gene products.
    J Bacteriol. 1987 Dec;169(12):5530-6 PMID: 2890622
  8. Identification and characterization of E. coli type-1 pilus tip adhesion protein.
    Nature. 1988 Mar 17;332(6161):265-8 PMID: 2894612
  9. Isolation and characterization of a receptor for type 1 fimbriae of Escherichia coli from guinea pig erythrocytes.
    J Biol Chem. 1988 Apr 15;263(11):5362-7 PMID: 2895767
  10. Conservation of the D-mannose-adhesion protein among type 1 fimbriated members of the family Enterobacteriaceae.
    Nature. 1988 Dec 15;336(6200):682-4 PMID: 2904657
  11. Identification and characterization of the genes encoding the type 3 and type 1 fimbrial adhesins of Klebsiella pneumoniae.
    J Bacteriol. 1989 Mar;171(3):1262-70 PMID: 2563996
  12. Protocol for 3-D visualization of molecules on mica via the quick-freeze, deep-etch technique.
    J Electron Microsc Tech. 1989 Nov;13(3):244-63 PMID: 2585121
  13. The fimD gene required for cell surface localization of Escherichia coli type 1 fimbriae.
    Mol Gen Genet. 1990 Jan;220(2):334-8 PMID: 1970114
  14. Mannose-sensitive haemagglutination in the absence of piliation in Escherichia coli.
    Mol Microbiol. 1990 Aug;4(8):1311-8 PMID: 1980711
  15. Fragmentation of Escherichia coli type 1 fimbriae exposes cryptic D-mannose-binding sites.
    J Bacteriol. 1991 Jul;173(13):4195-202 PMID: 1676398
  16. Identification of the leukocyte adhesion molecules CD11 and CD18 as receptors for type 1-fimbriated (mannose-specific) Escherichia coli.
    Infect Immun. 1991 Dec;59(12):4524-30 PMID: 1682263
  17. P pili in uropathogenic E. coli are composite fibres with distinct fibrillar adhesive tips.
    Nature. 1992 Mar 19;356(6366):252-5 PMID: 1348107
  18. A key role for type 1 pili in enterobacterial communicability.
    Mol Microbiol. 1992 Mar;6(6):697-701 PMID: 1349417
  19. Lesions in two Escherichia coli type 1 pilus genes alter pilus number and length without affecting receptor binding.
    J Bacteriol. 1992 Sep;174(18):5923-35 PMID: 1355769
  20. Interactive surface in the PapD chaperone cleft is conserved in pilus chaperone superfamily and essential in subunit recognition and assembly.
    EMBO J. 1992 Dec;11(13):4747-56 PMID: 1361168
  21. Neutrophil activation by nascent FimH subunits of type 1 fimbriae purified from the periplasm of Escherichia coli.
    J Biol Chem. 1993 Feb 5;268(4):3009-15 PMID: 8094080
  22. Basement membrane carbohydrate as a target for bacterial adhesion: binding of type I fimbriae of Salmonella enterica and Escherichia coli to laminin.
    Mol Microbiol. 1993 Jan;7(2):229-37 PMID: 8095317
  23. Initiation of assembly and association of the structural elements of a bacterial pilus depend on two specialized tip proteins.
    EMBO J. 1993 Mar;12(3):837-47 PMID: 8096174
  24. Outer-membrane PapC molecular usher discriminately recognizes periplasmic chaperone-pilus subunit complexes.
    Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3670-4 PMID: 8097321
  25. FimC is a periplasmic PapD-like chaperone that directs assembly of type 1 pili in bacteria.
    Proc Natl Acad Sci U S A. 1993 Sep 15;90(18):8397-401 PMID: 8104335
  26. Structural basis of pilus subunit recognition by the PapD chaperone.
    Science. 1993 Nov 19;262(5137):1234-41 PMID: 7901913
  27. FimH family of type 1 fimbrial adhesins: functional heterogeneity due to minor sequence variations among fimH genes.
    J Bacteriol. 1994 Feb;176(3):748-55 PMID: 7905476
  28. Type I Escherichia coli pili: characterization of binding to monkey kidney cells.
    J Exp Med. 1977 Nov 1;146(5):1182-94 PMID: 21933
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1995-03-14
Pages
2081-5
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC42427
Subset
IM
Grants
NIAID NIH HHS · R01AI29549 · United States
NIGMS NIH HHS · R01GM29647 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]