1887

Abstract

The AIDA-I autotransporter adhesin, as a prototype of the AIDA adhesin family, represents a tripartite antigen consisting of the functional adhesin AIDA-I (-domain), which mediates the specific attachment of bacteria to target cells, and a two-domain translocator (AIDA) organized in the - and -domains. Cellular receptor moieties for the adhesin AIDA-I have not been identified. Here, it is demonstrated that the purified adhesin binds specifically to a high-affinity class of receptors on HeLa cells. Additionally, the adhesin was found to bind to a variety of mammalian cell types, indicating a broad tissue distribution of the receptor moiety. By using complementary techniques, including co-immunoprecipitation and one- and two-dimensional gel electrophoresis, the AIDA-I binding protein on HeLa cells was identified as a surface glycoprotein of about 119 kDa (gp119). The gp119 AIDA-I cellular receptor protein was characterized biochemically and found to be an integral -glycosylated membrane protein with a pI of 5·2.

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2003-07-01
2020-10-23
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References

  1. Baqui A. H., Sack R. B., Black R. E., Haider K., Hossain A., Alim A. R., Yunus M., Chowdhury H. R., Siddique A. K.. 1992; Enteropathogens associated with acute and persistent diarrhea in Bangladeshi children less than 5 years of age. J Infect Dis166:792–796
    [Google Scholar]
  2. Beinke C., Laarmann S., Wachter C., Karch H., Greune L., Schmidt M. A.. 1998; Diffusely adhering Escherichia coli strains induce attaching and effacing phenotypes and secrete homologs of Esp proteins. Infect Immun66:528–539
    [Google Scholar]
  3. Benz I., Schmidt M. A.. 1989; Cloning and expression of an adhesin (AIDA-I) involved in diffuse adherence of enteropathogenic Escherichia coli . Infect Immun57:1506–1511
    [Google Scholar]
  4. Benz I., Schmidt M. A.. 1992a; Isolation and serologic characterization of AIDA-I, the adhesin mediating the diffuse adherence phenotype of the diarrhea-associated Escherichia coli strain 2787 (O126 : H27). Infect Immun60:13–18
    [Google Scholar]
  5. Benz I., Schmidt M. A.. 1992b; AIDA-I, the adhesin involved in diffuse adherence of the diarrheagenic Escherichia coli strain 2787 (O126 : H27), is synthesized via a precursor molecule. Mol Microbiol6:1539–1546
    [Google Scholar]
  6. Benz I., Schmidt M. A.. 2001; Glycosylation with heptose residues mediated by the aah gene product is essential for adherence of the AIDA-I adhesin. Mol Microbiol40:1403–1413
    [Google Scholar]
  7. Bernet-Camard M. F., Coconnier M. H., Hudault S., Servin A. L.. 1996; Differential expression of complement proteins and regulatory decay accelerating factor in relation to differentiation of cultured human colon adenocarcinoma cell lines. Gut38:248–253
    [Google Scholar]
  8. Bilge S. S., Clausen C. R., Lau W., Moseley S. L.. 1989; Molecular characterization of a fimbrial adhesin, F1845, mediating diffuse adherence of diarrhea-associated Escherichia coli to HEp-2 cells. J Bacteriol171:4281–4289
    [Google Scholar]
  9. Bradford M. M.. 1976; A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem72:248–254
    [Google Scholar]
  10. Charles I. G., Dougan G., Pickard D., Chatfield S., Smith M., Novotny P., Morissey P., Fairweather N. F.. 1989; Molecular cloning and characterization of a protective outer membrane protein P. 69 from Bordetella pertussis . Proc Natl Acad Sci U S A86:3554–3558
    [Google Scholar]
  11. Chen T., Gotschlich E. C.. 1996; CGM1a antigen of neutrophils, a receptor of gonococcal opacity proteins. Proc Natl Acad Sci U S A93:14851–14856
    [Google Scholar]
  12. Chen T., Grunert F., Medina Marino A., Gotschlich E. C.. 1997; Several carcinoembryonic antigens (CD66) serve as receptors for gonococcal opacity proteins. J Exp Med185:1557–1564
    [Google Scholar]
  13. Falk P., Boren T., Normark S.. 1994; Characterization of microbial host receptors. Methods Enzymol236:353–374
    [Google Scholar]
  14. Finlay B. B., Falkow S.. 1997; Common themes in microbial pathogenicity revisited. Microbiol Mol Biol Rev61:136–169
    [Google Scholar]
  15. Fujiki Y., Hubbard A. L., Fowler S., Lazarow P. B.. 1982; Isolation of intracellular membranes by means of sodium carbonate treatment. J Cell Biol93:97–103
    [Google Scholar]
  16. Garnier J., Gibrat J. F., Robson B.. 1996; GOR method for predicting protein secondary structure from amino acid sequence. Methods Enzymol266:540–553
    [Google Scholar]
  17. Geourjon C., Deleage G.. 1995; SOPMA: significant improvements in protein secondary structure prediction by consensus prediction from multiple alignments. Comput Appl Biosci11:681–684
    [Google Scholar]
  18. Giannasca K. T., Giannasca P. J., Neutra M. R.. 1996; Adherence of Salmonella typhimurium to Caco-2 cells: identification of a glycoconjugate receptor. Infect Immun64:135–145
    [Google Scholar]
  19. Giron J. A., Jones T., Millan-Velasco F.. 9 other authors 1991; Diffuse-adhering Escherichia coli (DAEC) as a putative cause of diarrhea in Mayan children in Mexico. J Infect Dis163:507–513
    [Google Scholar]
  20. Gottardi C. J., Caplan M. J.. 1992; Cell surface biotinylation in the determination of epithelial membrane polarity. J Tissue Cult Methods14:173–180
    [Google Scholar]
  21. Harlow E., Lane D.. 1988; Antibodies: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  22. Hedlund M., Svensson M., Nilsson A., Duan R. D., Svanborg C.. 1996; Role of the ceramide-signaling pathway in cytokine responses to P-fimbriated Escherichia coli . J Exp Med183:1037–1044
    [Google Scholar]
  23. Hedlund M., Wachtler C., Johansson E., Hang L., Somerville J. E., Darveau R. P., Svanborg C.. 1999; P fimbriae-dependent, lipopolysaccharide-independent activation of epithelial cytokine responses. Mol Microbiol33:693–703
    [Google Scholar]
  24. Henderson I. R., Nataro J. P.. 2001; Virulence functions of autotransporter proteins. Infect Immun69:1231–1243
    [Google Scholar]
  25. Henderson I. R., Owen P.. 1999; The major phase-variable outer membrane protein of Escherichia coli structurally resembles the immunoglobulin A1 protease class of exported protein and is regulated by a novel mechanism involving Dam and OxyR. J Bacteriol181:2132–2141
    [Google Scholar]
  26. Henderson I. R., Navarro-Garcia F., Nataro J. P.. 1998; The great escape: structure and function of the autotransporter proteins. Trends Microbiol6:370–378
    [Google Scholar]
  27. Henderson I. R., Capello R., Nataro J. P.. 2000; Autotransporter proteins, evolution and redefining protein secretion. Trends Microbiol8:529–532
    [Google Scholar]
  28. Hultgren S. J., Abraham S., Capron M., Falk P., St Geme J. W., Normark S.. 1993; Pilus and non-pilus bacterial adhesins: assembly and function in cell recognition. Cell73:887–901
    [Google Scholar]
  29. Isberg R. R., Leong J. M.. 1990; Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell60:861–871
    [Google Scholar]
  30. Jallat C., Darfeuille Michaud A., Rich C., Joly B.. 1994; Survey of clinical isolates of diarrheagenic Escherichia coli : diffusely adhering E. coli strains with multiple adhesive factors. Res Microbiol145:621–632
    [Google Scholar]
  31. Jose J., Jähnig F., Meyer T. F.. 1995; Common structural features of IgA1 protease-like outer membrane protein autotransporters. Mol Microbiol18:377–382
    [Google Scholar]
  32. Kähne T., Ansorge S.. 1994; Non-radioactive labelling and immunoprecipitation analysis of leukocyte surface proteins using different methods of protein biotinylation. J Immunol Methods168:209–218
    [Google Scholar]
  33. Kaper J. B.. 1998; EPEC delivers the goods. Trends Microbiol6:169–172
    [Google Scholar]
  34. Karlsson K. A.. 1989; Animal glycosphingolipids as membrane attachment sites for bacteria. Annu Rev Biochem58:309–350
    [Google Scholar]
  35. Klemm P.. 1994; Fimbriae: Adhesion, Genetics, Biogenesis and Vaccines Boca Raton, FL: CRC Press;
    [Google Scholar]
  36. Klemm P., Schembri M. A.. 2000; Bacterial adhesins: function and structure . Int. J Med Microbiol290:27–35
    [Google Scholar]
  37. Konieczny M. P., Suhr M., Noll A., Autenrieth I. B., Schmidt M. A.. 2000; Cell surface presentation of recombinant (poly-) peptides including functional T-cell epitopes by the AIDA autotransporter system. FEMS Immunol Med Microbiol27:321–332
    [Google Scholar]
  38. Konieczny M. P. J., Benz I., Hollinderbäumer B., Beinke C., Niederweis M., Schmidt M. A.. 2001; Modular structure of the AIDA autotransporter translocator: evidence for a transmembrane β -sheet core stabilized by a surface-exposed N-terminal domain. Antonie van Leeuwenhoek80:19–34
    [Google Scholar]
  39. Levine M. M., Ferreccio C., Prado V.. 39 other authors 1993; Epidemiologic studies of Escherichia coli diarrheal infections in a low socioeconomic level peri-urban community in Santiago, Chile. Am J Epidemiol138:849–869
    [Google Scholar]
  40. Lindstedt R., Larson G., Falk P., Jodal U., Leffler H., Svanborg C.. 1991; The receptor repertoire defines the host range for attaching Escherichia coli strains that recognize globo-A. Infect Immun59:1086–1092
    [Google Scholar]
  41. Loveless B. J., Saier M. H. Jr. 1997; A novel family of channel-forming, autotransporting, bacterial virulence factors. Mol Membr Biol14:113–123
    [Google Scholar]
  42. Maurer J., Jose J., Meyer T. F.. 1997; Autodisplay: one-component system for efficient surface display and release of soluble recombinant proteins from Escherichia coli . J Bacteriol179:794–804
    [Google Scholar]
  43. Mengaud J., Ohayon H., Gounon P., Mege R. M., Cossart P.. 1996; E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell84:923–932
    [Google Scholar]
  44. Mouricout M.. 1997; Interactions between the enteric pathogen and the host. An assortment of bacterial lectins and a set of glycoconjugate receptors. Adv Exp Med Biol412:109–123
    [Google Scholar]
  45. Nataro J. P., Kaper J. B.. 1998; Diarrheagenic Escherichia coli . Clin Microbiol Rev11:142–201
    [Google Scholar]
  46. Niewerth U., Voss T., Frey A., le Bouguénec C., Baljer G., Franke S., Schmidt M. A.. 2001; The AIDA autotransporter system is associated with F18 and Stx2e in E. coli isolates derived from pigs suffering from edema disease and postweaning diarrhea. Clin Diagn Lab Immunol8:143–149
    [Google Scholar]
  47. Nowicki B., Labigne A., Moseley S., Hull R., Hull S., Moulds J.. 1990; The Dr hemagglutinin, afimbrial adhesins AFA-I and AFA-III, and F1845 fimbriae of uropathogenic and diarrhea-associated Escherichia coli belong to a family of hemagglutinins with Dr receptor recognition. Infect Immun58:279–281
    [Google Scholar]
  48. Pohlner J., Halter R., Beyreuther K., Meyer T. F.. 1987; Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease. Nature325:458–462
    [Google Scholar]
  49. Rabilloud T., Adessi C., Giraudel A., Lunardi J.. 1997; Improvement of the solubilization of proteins in two-dimensional electrophoresis with immobilized pH gradients. Electrophoresis18:307–316
    [Google Scholar]
  50. Read S. M., Northcote D. H.. 1981; Minimization of variation in the response to different proteins of the Coomassie blue G dye-binding assay for protein. Anal Biochem116:53–64
    [Google Scholar]
  51. Salam Khan A., Kniep B., Ölschläger T. A., van Die I., Korhonen T., Hacker J.. 2000; Receptor structure for F1C fimbriae of uropathogenic Escherichia coli . Infect Immun68:3541–3547
    [Google Scholar]
  52. Schmid F. X.. 1989; Spectral methods of characterizing protein conformation and conformational changes. In Protein Structure – a Practical Approach pp 251–285 Edited by Creighton T. E. Oxford: IRL Press;
    [Google Scholar]
  53. Sharon N.. 1987; Bacterial lectins, cell–cell recognition and infectious disease. FEBS Lett217:145–157
    [Google Scholar]
  54. Stathopoulos C., Provence D. L., Curtiss R. III. 1999; Characterization of the avian pathogenic Escherichia coli hemagglutinin Tsh, a member of the immunoglobulin A protease-type family of autotransporters. Infect Immun67:772–781
    [Google Scholar]
  55. St Geme J. W. III. 1994; The HMW1 adhesin of nontypeable Haemophilus influenzae recognizes sialylated glycoprotein receptors on cultured human epithelial cells. Infect Immun62:3881–3889
    [Google Scholar]
  56. St Geme J. W. III, Cutter D., Barenkamp S. J.. 1996; Characterization of the genetic locus encoding Haemophilus influenzae type b surface fibrils. J Bacteriol178:6281–6287
    [Google Scholar]
  57. Suhr M., Benz I., Schmidt M. A.. 1996; Processing of the AIDA-I precursor: removal of AIDAC and evidence for the outer membrane anchoring as a β -barrel structure. Mol Microbiol22:31–42
    [Google Scholar]
  58. Virji M., Makepeace K., Ferguson D. J., Watt S. M.. 1996; Carcinoembryonic antigens (CD66) on epithelial cells and neutrophils are receptors for Opa proteins of pathogenic Neisseriae . Mol Microbiol22:941–950
    [Google Scholar]
  59. Watarai M., Funato S., Sasakawa C.. 1996; Interaction of Ipa proteins of Shigella flexneri with α 5 β 1-integrin promotes entry of the bacteria into mammalian cells. J Exp Med183:991–999
    [Google Scholar]
  60. Westerlund B., Korhonen T. K.. 1993; Bacterial proteins binding to the mammalian extracellular matrix. Mol Microbiol9:687–694
    [Google Scholar]
  61. Woodward M. P., Young W. W. Jr, Bloodgood R. A.. 1985; Detection of monoclonal antibodies specific for carbohydrate epitopes using periodate oxidation. J Immunol Methods78:143–153
    [Google Scholar]
  62. Yamamoto T., Wakisaka N., Nakae T., Kamano T., Serichantalergs O., Echeverria P.. 1996; Characterization of a novel hemagglutinin of diarrhea associated Escherichia coli that has characteristics of diffusely adhering E. coli and enteroaggregative E. coli . Infect Immun64:3694–3702
    [Google Scholar]
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