Basis for -acetyllactosamine-mediated inhibition of enteropathogenic localized adherence Free

Abstract

In a previous article, the authors reported that exposing wild-type enteropathogenic (EPEC) to chemically synthesized -acetyllactosamine glycosides covalently coupled to BSA (LacNAc–BSA) inhibited localized adherence (LA) by these organisms and also caused them to lose their bundle-forming pili (BFP), the filamentous surface appendages responsible for their LA phenotype. This effect has now been further investigated by screening a panel of LacNAc–BSA-related glycosides for their ability to inhibit EPEC LA, which revealed that LacNAc–BSA retained its status as the most effective inhibitor of EPEC LA. It was also shown that LacNAc–BSA did not cause the loss of BFP in an EPEC strain containing a non-polar mutation in the gene and, as a consequence, unable to retract its BFP. LacNAc–BSA also effectively inhibited LA of the mutant EPEC. Taken together, these observations suggest that, as well as triggering BfpF-mediated BFP retraction, LacNAc–BSA likely functions as a competitive inhibitor of EPEC binding to LacNAc-related receptors on host cells. Moreover, transmission electron microscopy revealed that LacNAc conjugated to gold nanoparticles bound specifically to BFP. This observation indicated that either the major BFP structural subunit (BfpA) itself or, possibly, an accessory protein co-assembled with BfpA into the BFP filaments, contains a LacNAc-specific EPEC adhesin. The results suggest a mechanism whereby the initial binding of EPEC to LacNAc-like receptors on host cells triggers BfpF-mediated BFP retraction. This could then expedite the intimate adherence phase of the multi-step EPEC colonization process by drawing the organisms closer to the host-cell plasma membrane.

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2006-06-01
2024-03-28
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References

  1. Anantha R. P., Stone K. D., Donnenberg M. S. 1998; Role of BfpF, a member of the PilT family of putative nucleotide-binding proteins, in type IV pilus biogenesis and in interactions between enteropathogenic Escherichia coli and host cells. Infect Immun 66:122–131
    [Google Scholar]
  2. Anantha R. P., Stone K. D., Donnenberg M. S. 2000; Effects of bfp mutations on biogenesis of functional enteropathogenic Escherichia coli type IV pili. J Bacteriol 182:2498–2506 [CrossRef]
    [Google Scholar]
  3. Bieber D., Ramer S. W., Wu C. Y., Murray W. J., Tobe T., Fernandez R., Schoolnik G. K. 1998; Type IV pili, transient bacterial aggregates, and virulence of enteropathogenic Escherichia coli . Science 280:2114–2118 [CrossRef]
    [Google Scholar]
  4. Campellone K. G., Leong J. M. 2003; Tails of two Tirs: actin pedestal formation by enteropathogenic E. coli and enterohemorrhagic E. coli O157 : H7. Curr Opin Microbiol 6:82–90 [CrossRef]
    [Google Scholar]
  5. Cleary J., Lai L. C., Shaw R. K., Straatman-Iwanowska A., Donnenberg M. S., Frankel G., Knutton S. 2004; Enteropathogenic Escherichia coli (EPEC) adhesion to intestinal epithelial cells: role of bundle-forming pili (BFP), EspA filaments and intimin. Microbiology 150:527–538 [CrossRef]
    [Google Scholar]
  6. Cravioto A., Tello A., Villafan H., Ruiz J., del Vedovo S., Neeser J. R. 1991; Inhibition of localized adhesion of enteropathogenic Escherichia coli to HEp-2 cells by immunoglobulin and oligosaccharide fractions of human colostrum and breast milk. J Infect Dis 163:1247–1255 [CrossRef]
    [Google Scholar]
  7. Delahay R. M., Frankel G., Knutton S. 2001; Intimate interactions of enteropathogenic Escherichia coli at the host cell surface. Curr Opin Infect Dis 14:559–565 [CrossRef]
    [Google Scholar]
  8. Donnenberg M. S., Kaper J. B. 1992; Enteropathogenic Escherichia coli . Infect Immun 60:3953–3961
    [Google Scholar]
  9. Donnenberg M. S., Whittam T. S. 2001; Pathogenesis and evolution of virulence in enteropathogenic and enterohemorrhagic Escherichia coli . J Clin Invest 107:539–548 [CrossRef]
    [Google Scholar]
  10. Donnenberg M. S., Giron J. A., Nataro J. P., Kaper J. B. 1992; A plasmid-encoded type IV fimbrial gene of enteropathogenic Escherichia coli associated with localized adherence. Mol Microbiol 6:3427–3437 [CrossRef]
    [Google Scholar]
  11. Giron J. A., Ho A. S., Schoolnik G. K. 1991; An inducible bundle-forming pilus of enteropathogenic Escherichia coli . Science 254:710–713 [CrossRef]
    [Google Scholar]
  12. Giron J. A., Ho A. S., Schoolnik G. K. 1993; Characterization of fimbriae produced by enteropathogenic Escherichia coli . J Bacteriol 175:7391–7403
    [Google Scholar]
  13. Hart C. A., Batt R. M., Saunders J. R. 1993; Diarrhoea caused by Escherichia coli . Ann Trop Paediatr 13:121–131
    [Google Scholar]
  14. Hicks S., Frankel G., Kaper J. B., Dougan G., Phillips A. D. 1998; Role of intimin and bundle-forming pili in enteropathogenic Escherichia coli adhesion to pediatric intestinal tissue in vitro. Infect Immun 66:1570–1578
    [Google Scholar]
  15. Idota T., Kawakami H. 1995; Inhibitory effects of milk gangliosides on the adhesion of Escherichia coli to human intestinal carcinoma cells. Biosci Biotechnol Biochem 59:69–72 [CrossRef]
    [Google Scholar]
  16. Jagannatha H. M., Sharma U. K., Ramaseshan T., Surolia A., Balganesh T. S. 1991; Identification of carbohydrate structures as receptors for localised adherent enteropathogenic Escherichia coli. Microb Pathog 11:259–268 [CrossRef]
    [Google Scholar]
  17. Kenny B. 2002; Mechanism of action of EPEC type III effector molecules. Int J Med Microbiol 291:469–477
    [Google Scholar]
  18. Lemieux R. U., Baker A., Bundle D. R. 1977; A methodology for the production of carbohydrate-specific antibody. Can J Biochem 55:507–512 [CrossRef]
    [Google Scholar]
  19. Leverton L. Q., Kaper J. B. 2005; Temporal expression of enteropathogenic Escherichia coli virulence genes in an in vitro model of infection. Infect Immun 73:1034–1043 [CrossRef]
    [Google Scholar]
  20. Levine M. M., Nataro J. P., Karch H., Baldini M. M., Kaper J. B., Black R. E., Clements M. L., O'Brien A. D. 1985; The diarrheal response of humans to some classic serotypes of enteropathogenic Escherichia coli is dependent on a plasmid encoding an enteroadhesiveness factor. J Infect Dis 152:550–559 [CrossRef]
    [Google Scholar]
  21. Lin C. C., Yeh Y. C., Yang C. Y., Chen C. L., Chen G. F., Chen C. C., Wu Y. C. 2002; Selective binding of mannose-encapsulated gold nanoparticles to type 1 pili in Escherichia coli . J Am Chem Soc 124:3508–3509 [CrossRef]
    [Google Scholar]
  22. Marcato P., Mulvey G., Read R. J., Vander Helm K., Nation P. N., Armstrong G. D. 2001; Immunoprophylactic potential of cloned Shiga toxin 2 B subunit. J Infect Dis 183:435–443 [CrossRef]
    [Google Scholar]
  23. Raivio T. L. 2005; Envelope stress responses and Gram-negative bacterial pathogenesis. Mol Microbiol 56:1119–1128 [CrossRef]
    [Google Scholar]
  24. Ramer S. W., Schoolnik G. K., Wu C. Y., Hwang J., Schmidt S. A., Bieber D. 2002; The type IV pilus assembly complex: biogenic interactions among the bundle-forming pilus proteins of enteropathogenic Escherichia coli . J Bacteriol 184:3457–3465 [CrossRef]
    [Google Scholar]
  25. Tobe T., Sasakawa C. 2001; Role of bundle-forming pilus of enteropathogenic Escherichia coli in host cell adherence and in microcolony development. Cell Microbiol 3:579–585 [CrossRef]
    [Google Scholar]
  26. Vanmaele R. P., Finlayson M. C., Armstrong G. D. 1995; Effect of enteropathogenic Escherichia coli on adherent properties of Chinese hamster ovary cells. Infect Immun 63:191–198
    [Google Scholar]
  27. Vanmaele R. P., Heerze L. D., Armstrong G. D. 1999; Role of lactosyl glycan sequences in inhibiting enteropathogenic Escherichia coli attachment. Infect Immun 67:3302–3307
    [Google Scholar]
  28. Winther-Larsen H. C., Wolfgang M., Dunham S., van Putten J. P., Dorward D., Lovold C., Aas F. E., Koomey M. 2005; A conserved set of pilin-like molecules controls type IV pilus dynamics and organelle-associated functions in Neisseria gonorrhoeae . Mol Microbiol 56:903–917 [CrossRef]
    [Google Scholar]
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