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
2019-10-18
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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 Dis 166, 792–796.[CrossRef]
    [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 Immun 66, 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 Immun 57, 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 Immun 60, 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 Microbiol 6, 1539–1546.[CrossRef]
    [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 Microbiol 40, 1403–1413.[CrossRef]
    [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. Gut 38, 248–253.[CrossRef]
    [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 Bacteriol 171, 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 Biochem 72, 248–254.[CrossRef]
    [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 A 86, 3554–3558.[CrossRef]
    [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 A 93, 14851–14856.[CrossRef]
    [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 Med 185, 1557–1564.[CrossRef]
    [Google Scholar]
  13. Falk, P., Boren, T. & Normark, S. ( 1994; ). Characterization of microbial host receptors. Methods Enzymol 236, 353–374.
    [Google Scholar]
  14. Finlay, B. B. & Falkow, S. ( 1997; ). Common themes in microbial pathogenicity revisited. Microbiol Mol Biol Rev 61, 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 Biol 93, 97–103.[CrossRef]
    [Google Scholar]
  16. Garnier, J., Gibrat, J. F. & Robson, B. ( 1996; ). GOR method for predicting protein secondary structure from amino acid sequence. Methods Enzymol 266, 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 Biosci 11, 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 Immun 64, 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 Dis 163, 507–513.[CrossRef]
    [Google Scholar]
  20. Gottardi, C. J. & Caplan, M. J. ( 1992; ). Cell surface biotinylation in the determination of epithelial membrane polarity. J Tissue Cult Methods 14, 173–180.[CrossRef]
    [Google Scholar]
  21. Harlow, E. & Lane, D. ( 1988; ). Antibodies: a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  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 Med 183, 1037–1044.[CrossRef]
    [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 Microbiol 33, 693–703.[CrossRef]
    [Google Scholar]
  24. Henderson, I. R. & Nataro, J. P. ( 2001; ). Virulence functions of autotransporter proteins. Infect Immun 69, 1231–1243.[CrossRef]
    [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 Bacteriol 181, 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 Microbiol 6, 370–378.[CrossRef]
    [Google Scholar]
  27. Henderson, I. R., Capello, R. & Nataro, J. P. ( 2000; ). Autotransporter proteins, evolution and redefining protein secretion. Trends Microbiol 8, 529–532.[CrossRef]
    [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. Cell 73, 887–901.[CrossRef]
    [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. Cell 60, 861–871.[CrossRef]
    [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 Microbiol 145, 621–632.[CrossRef]
    [Google Scholar]
  31. Jose, J., Jähnig, F. & Meyer, T. F. ( 1995; ). Common structural features of IgA1 protease-like outer membrane protein autotransporters. Mol Microbiol 18, 377–382.[CrossRef]
    [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 Methods 168, 209–218.[CrossRef]
    [Google Scholar]
  33. Kaper, J. B. ( 1998; ). EPEC delivers the goods. Trends Microbiol 6, 169–172.[CrossRef]
    [Google Scholar]
  34. Karlsson, K. A. ( 1989; ). Animal glycosphingolipids as membrane attachment sites for bacteria. Annu Rev Biochem 58, 309–350.[CrossRef]
    [Google Scholar]
  35. Klemm, P. ( 1994; ). Fimbriae: Adhesion, Genetics, Biogenesis and Vaccines. Boca Raton, FL: CRC Press.
  36. Klemm, P. & Schembri, M. A. ( 2000; ). Bacterial adhesins: function and structure. Int J Med Microbiol 290, 27–35.[CrossRef]
    [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 Microbiol 27, 321–332.[CrossRef]
    [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 Leeuwenhoek 80, 19–34.[CrossRef]
    [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 Epidemiol 138, 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 Immun 59, 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 Biol 14, 113–123.[CrossRef]
    [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 Bacteriol 179, 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. Cell 84, 923–932.[CrossRef]
    [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 Biol 412, 109–123.
    [Google Scholar]
  45. Nataro, J. P. & Kaper, J. B. ( 1998; ). Diarrheagenic Escherichia coli. Clin Microbiol Rev 11, 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 Immunol 8, 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 Immun 58, 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. Nature 325, 458–462.[CrossRef]
    [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. Electrophoresis 18, 307–316.[CrossRef]
    [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 Biochem 116, 53–64.[CrossRef]
    [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 Immun 68, 3541–3547.[CrossRef]
    [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 T. E. Creighton. Oxford: IRL Press.
  53. Sharon, N. ( 1987; ). Bacterial lectins, cell–cell recognition and infectious disease. FEBS Lett 217, 145–157.[CrossRef]
    [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 Immun 67, 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 Immun 62, 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 Bacteriol 178, 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 Microbiol 22, 31–42.[CrossRef]
    [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 Microbiol 22, 941–950.[CrossRef]
    [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 Med 183, 991–999.[CrossRef]
    [Google Scholar]
  60. Westerlund, B. & Korhonen, T. K. ( 1993; ). Bacterial proteins binding to the mammalian extracellular matrix. Mol Microbiol 9, 687–694.[CrossRef]
    [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 Methods 78, 143–153.[CrossRef]
    [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 Immun 64, 3694–3702.
    [Google Scholar]
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