Clathrin-mediated endocytosis and transcytosis of enterotoxigenic Escherichia coli F4 fimbriae in porcine intestinal epithelial cells

Veterinary Immunology and Immunopathology

Volumn 137, Issue 3-4, 2010, Pages 243-250

  Rasschaert, Kristien ^a   Devriendt, Bert ^a   Favoreel, Herman ^a   Goddeeris, Bruno M ^a   Cox, Eric ^a  

^a GHENT UNIVERSITY   (Belgium)

Author keywords

Clathrin; Enterotoxigenic Escherichia coli; F4 fimbriae; Intestinal epithelial cells; Transcytosis

Indexed keywords

CLATHRIN; F4 FIMBRIA PROTEIN; FIMBRIA PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; DOG; ENDOCYTOSIS; ENTEROTOXIGENIC ESCHERICHIA COLI; IN VITRO STUDY; INTERNALIZATION; INTESTINE EPITHELIUM CELL; NONHUMAN; PROTEIN PURIFICATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TRANSCYTOSIS;

ANIMALS; CELL LINE; CLATHRIN; ENDOCYTOSIS; ENTEROTOXIGENIC ESCHERICHIA COLI; FIMBRIAE, BACTERIAL; INTESTINAL MUCOSA; SWINE; TRANSCYTOSIS;

ANIMALIA; ESCHERICHIA COLI; SUS;

EID: 77956265587     PISSN: 01652427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vetimm.2010.05.016     Document Type: Article

References (41)

1. Bakker D., Willemsen P.T.J., Simons L.H., van Zijderveld F.G., de Graaf F.K. Characterization of the antigenic and adhesive properties of FaeG, the major subunit of K88 fimbriae. Mol. Microbiol. 1992, 6(2):247-255.
2. Bennett E.M., Chen C.Y., Engqvist-Goldstein A.E., Drubin D.G., Brodsky F.M. Clathrin hub expression dissociates the actin-binding protein Hip1 R from coated pits and disrupts their alignment with the actin cytoskeleton. Traffic 2001, 2:851-858.
3. Berschneider H.M. Development of normal cultured small intestinal epithelial cell line which transports Na and Cl. Gastroenterology 1989, 96:A41.
4. Bijlsma I.G., Bouw J. Inheritance of K88-mediated adhesion of Escherichia coli to jejunal brush borders in pigs: a genetic analysis. Vet. Res. Commun. 1987, 11:509-518.
5. Blanco M., Blanco J.E., Gonzales E.A., Mora A., Jansen W., Gomes T.A.T., Zerbini L.F., Yano T., Pestana de Castro A.F., Blanco J. Genes coding for enterotoxins and verotoxins in porcine Escherichia coli strains belonging to different O:K:H: serotypes: relationship with toxic phenotypes. J. Clin. Microbiol. 1997, 35:2958-2963.
6. Brodsky F.M., Chen C.Y., Knuehl C., Towler M.C., Wakeham D.E. Biological basket weaving: formation and function of clathrin-coated vesicles. Annu. Rev. Cell. Dev. Biol. 2001, 17:517-568.
7. Conner S.D., Schmid S.L. Regulated portals of entry into the cell. Nature 2003, 422:37-44.
8. De Greve H., wyns L., Bouckaert J. Combining sites of bacterial fimbriae. Curr. Opin. Struct. Biol. 2007, 17:506-512.
9. + intestinal antigen presenting cells and antigen-specific immune responses, leading to a prolonged intestinal ETEC infection. Vet. Res. 2009, 40:40.
10. Erickson A.K., Baker D.R., Bosworth B.T., Casey T.A., Benfield D.A., Francis D.H. Characterization of porcine intestinal receptors for the K88ac fimbrial adhesin of Escherichia coli as mucin-type sialoglycoproteins. Infect. Immun. 1994, 62:5404-5410.
11. Evans D.G., Evans D.J., Graham D.Y. Adherence and internalization of Helicobacter pylori by HEp-2 cells. Gastroenterology 1992, 102:1557-1567.
12. Francis D.H., Grange P.A., Zeman D.H., Baker D.R., Sun R., Erickson A.K. Expression of mucin-type glycoprotein K88 receptors strongly correlates with piglet susceptibility to K88(+) enterotoxigenic Escherichia coli, but adhesion of this bacterium to brush borders does not. Infect. Immun. 1998, 66:4050-4055.
13. Gibbons R.A., Sellwood R., Burrows M., Hunter P.A. Inheritance of resistance to neonatal E. coli diarrhoea in the pig. Theor. Appl. Gen. 1977, 51:65-70.
14. Grange P.A., Erickson A.K., Anderson T.J., Francis D.H. Characterization of the carbohydrate moiety of intestinal mucin-type sialoglycoprotein receptors for the K88ac fimbrial adhesin of Escherichia coli. Infect. Immun. 1998, 66:1613-1621.
15. Gyles C.L. Escherichia coli enterotoxins. Escherichia coli in Domestic Animals and Humans 1994, 337-364. CAB International, Wallingford, Oxon, UK. C.L. Gyles (Ed.).
16. Johnson A.M., Kaushik R.S., Francis D.H., Fleckenstein J.M., Hardwidge P.R. Heat-labile enterotoxin promotes Escherichia coli adherence to intestinal epithelial cells. J. Bacteriol. 2009, 191:178-186.
17. Koh S.Y., George S., Brözel V., Moxley R., Francis D., Kaushik R.S. Porcine intestinal epithelial cell lines as a new in vitro model for studying adherence and pathogenesis of enterotoxigenic Escherichia coli. Vet. Microbiol. 2008, 130:191-197.
18. Lamaze C., Fujimoto L.M., Yin H.L., Schmid S.L. The actin cytoskeleton is required for receptor-mediated endocytosis in mammalian cells. J. Biol. Chem. 1997, 272:20332-20335.
19. McOrist S., Jasni S., Mackie R.A., Berschneider H.M., Rowland A.C., Lawson G.H. Entry of the bacterium ileal symbiont intracellularis into cultured enterocytes and its subsequent release. Res. Vet. Sci. 1995, 59:255-260.
20. Oelschlaeger T.A., Barret T.J., Kopecko D.J. Some structures and processes of human epithelial cells involved in uptake of enterohemorrhagic Escherichia coli O157:H7 strains. Infect. Immun. 1994, 62:5142-5150.
21. Phonphok Y., Rosenthal K.S. Stabilization of clathrin coated vesicles by amantadine, tromantadine and other hydrophobic amines. FEBS Lett. 1991, 281:188-190.
22. Pitman R.S., Blumberg R.S. First line of defense: the role of the intestinal epithelium as an active component of the mucosal immune system. J. Gastroenterol. 2000, 35:805-814.
23. Rückert P., Bates S.R., Fisher A.B. Role of clathrin- and actin-dependent endocytotic pathways in lung phospholipid uptake. Am. J. Physiol. Lung Cell. Mol. Physiol. 2003, 284:L981-L989.
24. Russell-Jones G.J. The potential use of receptor-mediated endocytosis for oral drug delivery. Adv. Drug Deliv. Rev. 2001, 46:59-73.
25. Schierack P., Nordhoff M., Pollmann M., Weyrauch K.D., Amasheh S., Lodemann U., Jores J., Tachu B., Kleta S., Blikslager A., Tedin K., Wieler L.H. Characterization of a porcine intestinal epithelial cell line for in vitro studies of microbial pathogenesis in swine. Histochem. Cell Biol. 2006, 125:293-305.
26. Schmid S.L., McNiven M.A., De Camilli P. Dynamin and its parterns: a progress report. Curr. Opin. Cell Biol. 1998, 10:504-512.
27. Shahriar F., Ngeleka M., Gordon J.R., Simko E. Identification by mass spectroscopy of F4ac-fimbrial-binding proteins in porcine milk and characterization of lactadherin as an inhibitor of F4ac-positive Escherichia coli attachment to intestinal villi in vitro. Dev. Comp. Immunol. 2006, 30:723-734.
28. Skjolaas K.A., Burkey T.E., Dritz S.S., Minton J.E. Effects of Salmonella enterica serovars Typhimurium (ST) and Choleraesuis (SC) on chemokine and cytokine expression in swine ileum and jejunal epithelial cells. Vet. Immunol. Immunopathol. 2006, 111:199-209.
29. Snoeck V., Goddeeris B., Cox E. The role of enterocytes in the intestinal barrier function and antigen uptake. Microb. Infect. 2005, 7:997-1004.
30. Snoeck V., Van den Broeck W., De Colvenaer V., Verdonck F., Vanrompay D., Goddeeris B.M., Cox E. Transcytosis of F4 fimbriae by villous and dome epithelia in F4-receptor positive pigs supports importance of enterocyte targeting in oral immunizations. Vet. Immunol. Immunopathol. 2008, 124:29-40.
31. Söderlund G., Kihlström E. Effect of methylamine and monodansylcadaverine on the susceptibility of McCoy cells to Chlamydia trachomatis infection. Infect. Immun. 1983, 40:534-541.
32. Sonntag A.K., Bielaszewska M., Mellmann A., Dierksen N., Schierack P., Wieler L.H., Schmidt M.A., Karch H. Shiga toxin 2e-producing Escherichia coli isolates from humans and pigs differ in their virulence profiles and interactions with intestinal epithelial cells. Appl. Environ. Microbiol. 2005, 71:8855-8863.
33. Van den Broeck W., Cox E., Goddeeris B.M. Receptor-dependent immune responses in pigs after oral immunization with F4 fimbriae. Infect. Immun. 1999, 67:520-526.
34. Van den Broeck W., Cox E., Goddeeris B.M. Induction of immune responses in pigs following oral administration of purified F4 fimbriae. Vaccine 1999, 17:2020-2029.
35. Van den Broeck W., Cox E., Goddeeris B.M. Receptor-specific binding of purified F4 to isolated villi. Vet. Microbiol. 1999, 68:255-263.
36. Van den Broeck W., Cox E., Oudega B., Goddeeris B.M. The F4 fimbrial antigen of Escherichia coli and its receptors. Vet. Microbiol. 2000, 71:223-244.
37. Van den Broeck W., Bouchaut H., Cox E., Goddeeris B.M. F4 receptor-independent priming of the systemic immune system of pigs by low oral doses of F4 fimbriae. Vet. Immunol. Immunopathol. 2002, 85:171-178.
38. Verdonck F., Cox E., van Gog K., Van der stede Y., Duchateau L., Deprez P., Goddeeris B.M. Different kinetic of antibody responses following infection of newly weaned pigs with an F4 enterotoxigenic Escherichia coli strain or an F18 verotoxigenic Escherichia coli strain. Vaccine 2002, 20:2995-3004.
39. + Escherichia coli infection. Vet. Immunol. Immunopathol. 2007, 120(3-4):69-79.
40. Verfaillie T., Melkebeek V., Snoeck V., Douterlungne S., Verdonck F., Vanrompay D., Goddeeris B., Cox E. Priming of piglets against enterotoxigenic E. coli F4 fimbriae by immunization with FAEG DNA. Vaccine 2004, 22:1640-1647.
41. Wyrick P.B., Choong J., Davis C.H., Knight S.T., Royal M.O., Maslow A.S., Bagnell C.R. Entry of genital Chlamydia trachomatis into polarized human epithelial cells. Infect. Immun. 1989, 57:2378-2389.