FimH family of type 1 fimbrial adhesins: functional heterogeneity due to minor sequence variations among fimH genes

We recently reported that the type 1-fimbriated Escherichia coli strains CSH-50 and HB101(pPKL4), both K-12 derivatives, have different patterns of adhesion to yeast mannan, human plasma fibronectin, and fibronectin derivatives, suggesting functional heterogeneity of type 1 fimbriae. In this report, we provide evidence that this functional heterogeneity is due to variations in the fimH genes. We also investigated functional heterogeneity among clinical isolates and whether variation in fimH genes accounts for differences in receptor specificity. Twelve isolates obtained from human urine were tested for their ability to adhere to mannan, fibronectin, periodate-treated fibronectin, and a synthetic peptide copying the 30 amino-terminal residues of fibronectin. CSH-50 and HB101(pPKL4) were tested for comparison. Selected isolates were also tested for adhesion to purified fragments spanning the entire fibronectin molecule. Three distinct functional classes, designated M, MF, and MFP, were observed. The fimH genes were amplified by PCR from chromosomal DNA obtained from representative strains and expressed in a delta fim strain (AAEC191A) transformed with a recombinant plasmid containing the entire fim gene cluster but with a translational stop-linker inserted into the fimH gene (pPKL114). Cloned fimH genes conferred on AAEC191A(pPKL114) receptor specificities mimicking those of the parent strains from which the fimH genes were obtained, demonstrating that the FimH subunits are responsible for the functional heterogeneity. Representative fimH genes were sequenced, and the deduced amino acid sequences were compared with the previously published FimH sequence. Allelic variants exhibiting >98% homology and encoding proteins differing by as little as a single amino acid substitution confer distinct adhesive phenotypes. This unexpected adhesive diversity within the FimH family broadens the scope of potential receptors for enterobacterial adhesion and may lead to a fundamental change in our understanding of the role(s) that type 1 fimbriae may play in enterobacterial ecology or pathogenesis.

[1]  S. Hultgren,et al.  Neutrophil activation by nascent FimH subunits of type 1 fimbriae purified from the periplasm of Escherichia coli. , 1993, The Journal of biological chemistry.

[2]  E. Sokurenko,et al.  Functional heterogeneity of type 1 fimbriae of Escherichia coli , 1992, Infection and immunity.

[3]  C. Bloch,et al.  A key role for type 1 pili in enterobacterial communicability , 1992, Molecular microbiology.

[4]  H. Lockman,et al.  Virulence of non-type 1-fimbriated and nonfimbriated nonflagellated Salmonella typhimurium mutants in murine typhoid fever , 1992, Infection and immunity.

[5]  B. Westerlund,et al.  Multifunctional nature of P fimbriae of uropathogenic Escherichia coli: mutations in fsoE and feoF influence fimbrial binding to renal tubuli and immobilized fibronectin , 1991, Molecular microbiology.

[6]  S. Normark,et al.  Saccharide orientation at the cell surface affects glycolipid receptor function. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[7]  S. Clegg,et al.  Fimbrial types among respiratory isolates belonging to the family Enterobacteriaceae , 1991, Journal of clinical microbiology.

[8]  S. Harris,et al.  Isolation and characterization of mutants with lesions affecting pellicle formation and erythrocyte agglutination by type 1 piliated Escherichia coli , 1990, Journal of bacteriology.

[9]  R. Ikeda,et al.  Reassessment of Antigenic Determinant of Saccharomyces cerevisiae Serotype Ia , 1990, Microbiology and immunology.

[10]  S. Normark,et al.  Host‐specificity of uropathogenic Escherichia coli depends on differences in binding specificity to Gal alpha 1‐4Gal‐containing isoreceptors. , 1990, The EMBO journal.

[11]  B. McCormick,et al.  Type 1 pili are not necessary for colonization of the streptomycin-treated mouse large intestine by type 1-piliated Escherichia coli F-18 and E. coli K-12 , 1989, Infection and immunity.

[12]  S. Clegg,et al.  Identification and characterization of the genes encoding the type 3 and type 1 fimbrial adhesins of Klebsiella pneumoniae , 1989, Journal of bacteriology.

[13]  B. Westerlund,et al.  A novel lectin‐independent interaction of P fimbriae of Escherichia coli with immobilized fibronectin , 1989, FEBS letters.

[14]  E. Beachey,et al.  Conservation of the D-mannose-adhesion protein among type 1 fimbriated members of the family Enterobacteriaceae , 1988, Nature.

[15]  E. Hounsell,et al.  NEW TYPE OF ADHESIVE SPECIFICITY REVEALED BY OLIGOSACCHARIDE PROBES IN ESCHERICHIA COLI FROM PATIENTS WITH URINARY TRACT INFECTION , 1988, The Lancet.

[16]  S. Barondes.  Bifunctional properties of lectins: lectins redefined. , 1988, Trends in biochemical sciences.

[17]  M. Hanson,et al.  Purification of the Escherichia coli type 1 pilin and minor pilus proteins and partial characterization of the adhesin protein , 1988, Journal of bacteriology.

[18]  D. Ohman,et al.  Experiments in Gene Manipulation , 1988 .

[19]  E. Beachey,et al.  Identification of two ancillary subunits of Escherichia coli type 1 fimbriae by using antibodies against synthetic oligopeptides of fim gene products , 1987, Journal of bacteriology.

[20]  L. Maurer,et al.  Identification and characterization of genes determining receptor binding and pilus length of Escherichia coli type 1 pili , 1987, Journal of bacteriology.

[21]  B. Koellreutter,et al.  Oligomannoside-type glycopeptides inhibiting adhesion of Escherichia coli strains mediated by type 1 pili: preparation of potent inhibitors from plant glycoproteins , 1986, Infection and immunity.

[22]  E. Beachey,et al.  The genetic determinant of adhesive function in type 1 fimbriae of Escherichia coli is distinct from the gene encoding the fimbrial subunit , 1986, Journal of bacteriology.

[23]  A. Schaeffer,et al.  Role of type 1 pili and effects of phase variation on lower urinary tract infections produced by Escherichia coli , 1985, Infection and immunity.

[24]  I. Ofek,et al.  Population shift in mannose-specific fimbriated phase of Klebsiella pneumoniae during experimental urinary tract infection in mice , 1985, Infection and immunity.

[25]  W. Simpson,et al.  Protection against Escherichia coli-induced urinary tract infections with hybridoma antibodies directed against type 1 fimbriae or complementary D-mannose receptors , 1985, Infection and immunity.

[26]  K. Yamada,et al.  The interaction of plasma fibronectin with fibroblastic cells in suspension. , 1985, The Journal of biological chemistry.

[27]  E. Ruoslahti,et al.  Structure of the carbohydrate units of human amniotic fluid fibronectin. , 1985, The Journal of biological chemistry.

[28]  L. Zardi,et al.  Elution of fibronectin proteolytic fragments from a hydroxyapatite chromatography column. A simple procedure for the purification of fibronectin domains. , 1985, European journal of biochemistry.

[29]  S. Falkow,et al.  Organization and expression of genes responsible for type 1 piliation in Escherichia coli , 1984, Journal of bacteriology.

[30]  R. Gibbons.  Microbial Ecology Adherent Interactions Which May Affect Microbial Ecology in the Mouth , 1984, Journal of dental research.

[31]  W. Simpson,et al.  Antiadhesive properties of a quaternary structure-specific hybridoma antibody against type 1 fimbriae of Escherichia coli , 1983, The Journal of experimental medicine.

[32]  D. Goldmann,et al.  The role of pili and capsule in the pathogenesis of neonatal infection with Escherichia coli K1. , 1983, The Journal of infectious diseases.

[33]  N. Firon,et al.  Carbohydrate specificity of the surface lectins of Escherichia coli, Klebsiella pneumoniae, and Salmonella typhimurium. , 1983, Carbohydrate research.

[34]  B. Eisenstein,et al.  Antigenic quantitation of type 1 fimbriae on the surface of Escherichia coli cells by an enzyme-linked immunosorbent inhibition assay , 1982, Infection and immunity.

[35]  E. Beachey,et al.  Bacterial adherence: adhesin-receptor interactions mediating the attachment of bacteria to mucosal surface. , 1981, The Journal of infectious diseases.

[36]  K. Suzuki,et al.  The sugar chains of cold-insoluble globulin. A protein related to fibronectin. , 1979, The Journal of biological chemistry.

[37]  E. Beachey,et al.  Mannose Binding and Epithelial Cell Adherence of Escherichia coli , 1978, Infection and immunity.

[38]  F. Sanger,et al.  DNA sequencing with chain-terminating inhibitors. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[39]  E. Engvall,et al.  Binding of soluble form of fibroblast surface protein, fibronectin, to collagen , 1977, International journal of cancer.

[40]  N. Sharon,et al.  Adherence of Escherichia coli to human mucosal cells mediated by mannose receptors , 1977, Nature.

[41]  D. Old.  Inhibition of the interaction between fimbrial haemagglutinins and erythrocytes by D-mannose and other carbohydrates. , 1972, Journal of general microbiology.

[42]  C. Brinton.  The structure, function, synthesis and genetic control of bacterial pili and a molecular model for DNA and RNA transport in gram negative bacteria. , 1965, Transactions of the New York Academy of Sciences.

[43]  I. Smith,et al.  Non-flagellar filamentous appendages (fimbriae) and haemagglutinating activity in Bacterium coli. , 1955, The Journal of pathology and bacteriology.

[44]  N. Sharon,et al.  Adhesins as lectins: specificity and role in infection. , 1990, Current topics in microbiology and immunology.

[45]  K. Vibe-Pedersen,et al.  Primary Structure of Fibronectin , 1989 .

[46]  F A Quiocho,et al.  Carbohydrate-binding proteins: tertiary structures and protein-sugar interactions. , 1986, Annual review of biochemistry.

[47]  J. Duguid,et al.  Adhesive Properties of Enterobacteriaceae , 1980 .

[48]  Jeffrey H. Miller.  Experiments in molecular genetics , 1972 .