Home LiteratureArticle Details
PMID: 8670884 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Molecular basis of two subfamilies of immunoglobulin-like chaperones.

The EMBO journal ·Vol. 15 ·No. 15 ·1996-08-01 ·Pages 3792-805

Hung DL, Knight SD, Woods RM, Pinkner JS, Hultgren SJ

Abstract

The initial encounter of a microbial pathogen with the host often involves the recognition of host receptors by different kinds of bacterial adhesive organelles called pili, fimbriae, fibrillae or afimbrial adhesins. The development of over 26 of these architecturally diverse adhesive organelles in various Gram-negative pathogens depends on periplasmic chaperones that are comprised of two immunoglobulin-like domains. All of the chaperones possess a highly conserved sheet in domain 1 and a conserved interdomain hydrogen-bonding network. Chaperone-subunit complex formation depends on the anchoring of the carboxylate group of the subunit into the conserved crevice of the chaperone cleft and the subsequent positioning of the COOH terminus of subunits along the exposed edge of the conserved sheet of the chaperone. We discovered that the chaperones can be divided into two distinct subfamilies based upon conserved structural differences that occur in the conserved sheet. Interestingly, a subdivision of the chaperones based upon whether they assemble rod-like pili or non-pilus organelles that have an atypical morphology defines the same two subgroups. The molecular dissection of the two chaperone subfamilies and the adhesive fibers that they assemble has advanced our understanding of the development of virulence-associated organelles in pathogenic bacteria.

MeSH Terms
Amino Acid Sequence Bacterial Proteins/chemistry,classification Conserved Sequence Crystallography, X-Ray Enzyme-Linked Immunosorbent Assay Models, Molecular Molecular Chaperones/chemistry,classification Molecular Sequence Data Protein Conformation
Chemicals
Bacterial Proteins Molecular Chaperones
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Hung D L
Department of Molecular Microbiology, Washington University School of Medicine, St Louis, MO 63110, USA.
Knight S D
Woods R M
Pinkner J S
Hultgren S J
References (62)
62 references, click to expand
  1. 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. 1991 Jul 29;286(1-2):79-82 PMID: 1677900
  2. Characterization of three fimbrial genes, sefABC, of Salmonella enteritidis.
    J Bacteriol. 1993 May;175(9):2523-33 PMID: 8097515
  3. Immunoglobulin-like PapD chaperone caps and uncaps interactive surfaces of nascently translocated pilus subunits.
    Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10586-90 PMID: 1683704
  4. Chaperone-assisted assembly and molecular architecture of adhesive pili.
    Annu Rev Microbiol. 1991;45:383-415 PMID: 1683764
  5. A new gene of the f1 operon of Y. pestis involved in the capsule biogenesis.
    FEBS Lett. 1992 Feb 3;297(1-2):77-80 PMID: 1551441
  6. P pili in uropathogenic E. coli are composite fibres with distinct fibrillar adhesive tips.
    Nature. 1992 Mar 19;356(6366):252-5 PMID: 1348107
  7. Conserved immunoglobulin-like features in a family of periplasmic pilus chaperones in bacteria.
    EMBO J. 1992 Apr;11(4):1617-22 PMID: 1348692
  8. The Crl protein activates cryptic genes for curli formation and fibronectin binding in Escherichia coli HB101.
    Mol Microbiol. 1992 Sep;6(17):2443-52 PMID: 1357528
  9. Characterization of a Bordetella pertussis fimbrial gene cluster which is located directly downstream of the filamentous haemagglutinin gene.
    Mol Microbiol. 1992 Sep;6(18):2661-71 PMID: 1360139
  10. 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
  11. Proteus mirabilis fimbriae: N-terminal amino acid sequence of a major fimbrial subunit and nucleotide sequences of the genes from two strains.
    Infect Immun. 1993 Mar;61(3):884-91 PMID: 8094384
  12. Pilus and nonpilus bacterial adhesins: assembly and function in cell recognition.
    Cell. 1993 Jun 4;73(5):887-901 PMID: 8098994
  13. Genetic analysis of the gene cluster encoding nonfimbrial adhesin I from an Escherichia coli uropathogen.
    Infect Immun. 1993 Jun;61(6):2505-12 PMID: 8099066
  14. Yersinia pestis pH 6 antigen forms fimbriae and is induced by intracellular association with macrophages.
    Mol Microbiol. 1993 Apr;8(2):311-24 PMID: 8100346
  15. PapD and superfamily of periplasmic immunoglobulin-like pilus chaperones.
    Adv Protein Chem. 1993;44:99-123 PMID: 8100380
  16. Nucleotide sequence of a 13.9 kb segment of the 90 kb virulence plasmid of Salmonella typhimurium: the presence of fimbrial biosynthetic genes.
    Mol Microbiol. 1993 May;8(3):543-58 PMID: 8100983
  17. Identification and transcriptional analysis of the Escherichia coli htrE operon which is homologous to pap and related pilin operons.
    J Bacteriol. 1993 Aug;175(16):5009-21 PMID: 8102362
  18. 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
  19. Episome-carried surface antigen K88 of Escherichia coli. 3. Morphology.
    J Bacteriol. 1967 Feb;93(2):740-8 PMID: 5335971
  20. Coli surface antigens 1 and 3 of colonization factor antigen II-positive enterotoxigenic Escherichia coli: morphology, purification, and immune responses in humans.
    Infect Immun. 1984 May;44(2):409-20 PMID: 6370866
  21. Characterization of Haemophilus influenzae type b fimbriae.
    Infect Immun. 1984 Dec;46(3):787-96 PMID: 6150012
  22. Three-dimensional structure of an antigen-antibody complex at 2.8 A resolution.
    Science. 1986 Aug 15;233(4765):747-53 PMID: 2426778
  23. Helical structure of Bordetella pertussis fimbriae.
    J Bacteriol. 1986 Sep;167(3):968-74 PMID: 2875062
  24. Nonfimbrial, mannose-resistant adhesins from uropathogenic Escherichia coli O83:K1:H4 and O14:K?:H11.
    Infect Immun. 1987 Aug;55(8):1837-42 PMID: 2886432
  25. Interior and surface of monomeric proteins.
    J Mol Biol. 1987 Aug 5;196(3):641-56 PMID: 3681970
  26. The immunoglobulin superfamily--domains for cell surface recognition.
    Annu Rev Immunol. 1988;6:381-405 PMID: 3289571
  27. CS31A, a new K88-related fimbrial antigen on bovine enterotoxigenic and septicemic Escherichia coli strains.
    Infect Immun. 1988 Aug;56(8):2180-8 PMID: 2899553
  28. Morphological description of surface structures on strain B41 of bovine enterotoxigenic Escherichia coli bearing both K99 and F41 antigens.
    J Gen Microbiol. 1988 Apr;134(4):983-95 PMID: 2903218
  29. Characterization of CS4 and CS6 antigenic components of PCF8775, a putative colonization factor complex from enterotoxigenic Escherichia coli E8775.
    Infect Immun. 1989 Jan;57(1):164-73 PMID: 2491834
  30. Monoclonal antibodies to K88ab, K88ac and K88ad fimbriae from enterotoxigenic Escherichia coli.
    Microb Pathog. 1986 Feb;1(1):57-69 PMID: 2907768
  31. Characterization and purification of the F17 adhesin on the surface of bovine enteropathogenic and septicemic Escherichia coli.
    Am J Vet Res. 1988 Nov;49(11):1794-9 PMID: 2907846
  32. The PapG adhesin of uropathogenic Escherichia coli contains separate regions for receptor binding and for the incorporation into the pilus.
    Proc Natl Acad Sci U S A. 1989 Jun;86(12):4357-61 PMID: 2567514
  33. Adhesion and ultrastructural properties of human enterotoxigenic Escherichia coli producing colonization factor antigens III and IV.
    Infect Immun. 1989 Nov;57(11):3364-71 PMID: 2572550
  34. PapD, a periplasmic transport protein in P-pilus biogenesis.
    J Bacteriol. 1989 Nov;171(11):6052-8 PMID: 2572580
  35. Crystal structure of chaperone protein PapD reveals an immunoglobulin fold.
    Nature. 1989 Nov 16;342(6247):248-51 PMID: 2478891
  36. 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. 1989 Dec;3(12):1685-95 PMID: 2576094
  37. The penultimate tyrosine residue of the K99 fibrillar subunit is essential for stability of the protein and its interaction with the periplasmic carrier protein.
    FEMS Microbiol Lett. 1990 Jan 15;55(1-2):107-12 PMID: 1970318
  38. Nucleotide sequence and functions of mrk determinants necessary for expression of type 3 fimbriae in Klebsiella pneumoniae.
    J Bacteriol. 1991 Jan;173(2):916-20 PMID: 1670938
  39. Improved methods for building protein models in electron density maps and the location of errors in these models.
    Acta Crystallogr A. 1991 Mar 1;47 ( Pt 2):110-9 PMID: 2025413
  40. Complete genetic organization and functional aspects of the Escherichia coli S fimbrial adhesion determinant: nucleotide sequence of the genes sfa B, C, D, E, F.
    Microb Pathog. 1990 Nov;9(5):331-43 PMID: 1983079
  41. Type 1 fimbriae of Salmonella enteritidis.
    J Bacteriol. 1991 Aug;173(15):4765-72 PMID: 1677356
  42. Structure and function of periplasmic chaperone-like proteins involved in the biosynthesis of K88 and K99 fimbriae in enterotoxigenic Escherichia coli.
    Mol Microbiol. 1991 Apr;5(4):875-86 PMID: 1713284
  43. The Myf fibrillae of Yersinia enterocolitica.
    Mol Microbiol. 1993 Aug;9(3):507-20 PMID: 8105362
  44. Characterization of plasmid-borne afa-3 gene clusters encoding afimbrial adhesins expressed by Escherichia coli strains associated with intestinal or urinary tract infections.
    Infect Immun. 1993 Dec;61(12):5106-14 PMID: 7901162
  45. Structural basis of pilus subunit recognition by the PapD chaperone.
    Science. 1993 Nov 19;262(5137):1234-41 PMID: 7901913
  46. Reciprocal exchange of minor components of type 1 and F1C fimbriae results in hybrid organelles with changed receptor specificities.
    J Bacteriol. 1994 Apr;176(8):2227-34 PMID: 7908902
  47. Proteus mirabilis MR/P fimbrial operon: genetic organization, nucleotide sequence, and conditions for expression.
    J Bacteriol. 1994 Jun;176(11):3412-9 PMID: 7910820
  48. A novel secretion apparatus for the assembly of adhesive bacterial pili.
    Trends Microbiol. 1993 May;1(2):50-5 PMID: 7913856
  49. Identification and characterization of a gene cluster mediating enteroaggregative Escherichia coli aggregative adherence fimbria I biogenesis.
    J Bacteriol. 1994 Aug;176(16):4949-57 PMID: 7914189
  50. Genetic organization and complete sequence of the Proteus mirabilis pmf fimbrial operon.
    Gene. 1994 Dec 2;150(1):101-4 PMID: 7959033
  51. 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 U S A. 1994 Dec 6;91(25):11889-93 PMID: 7991552
  52. Nucleotide sequence of the afimbrial-adhesin-encoding afa-3 gene cluster and its translocation via flanking IS1 insertion sequences.
    J Bacteriol. 1994 Dec;176(24):7601-13 PMID: 8002584
  53. Structural polymorphism of bacterial adhesion pili.
    Nature. 1995 Jan 12;373(6510):164-7 PMID: 7816100
  54. The export systems of type 1 and F1C fimbriae are interchangeable but work in parental pairs.
    J Bacteriol. 1995 Feb;177(3):621-7 PMID: 7836295
  55. Structural basis of cell-cell adhesion by cadherins.
    Nature. 1995 Mar 23;374(6520):327-37 PMID: 7885471
  56. FimH adhesin of type 1 pili is assembled into a fibrillar tip structure in the Enterobacteriaceae.
    Proc Natl Acad Sci U S A. 1995 Mar 14;92(6):2081-5 PMID: 7892228
  57. Identification and sequence analysis of lpfABCDE, a putative fimbrial operon of Salmonella typhimurium.
    J Bacteriol. 1995 Apr;177(8):2087-97 PMID: 7721701
  58. 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
  59. The complete general secretory pathway in gram-negative bacteria.
    Microbiol Rev. 1993 Mar;57(1):50-108 PMID: 8096622
  60. 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. 1993 Mar 15;108(1):59-67 PMID: 8097176
  61. 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
  62. Proteus mirabilis flagella and MR/P fimbriae: isolation, purification, N-terminal analysis, and serum antibody response following experimental urinary tract infection.
    Infect Immun. 1991 Oct;59(10):3574-80 PMID: 1680106
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1996-08-01
Pages
3792-805
Language
English
Region
England
NLM ID
8208664
PMCID
PMC452060
Subset
IM
Grants
NIAID NIH HHS · AI07172-16 · United States
NIAID NIH HHS · R01AI29549 · 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]