Flagellin in combination with curli fimbriae elicits an immune response in the gastrointestinal epithelial cell line HT-29

Microbes and Infection

Volumn 8, Issue 8, 2006, Pages 2027-2033

  Rochon, Maike ^a   Römling, Ute ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Biofilm; Curli; Flagellin; IL 8

Indexed keywords

FLAGELLIN;

ARTICLE; BIOFILM; CELL STRAIN HT29; ENTEROBACTERIACEAE; EPITHELIUM CELL; FIMBRIA; HUMAN; HUMAN CELL; IMMUNE RESPONSE; NONHUMAN; PRIORITY JOURNAL; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM;

BACTERIAL PROTEINS; BIOFILMS; BLOTTING, WESTERN; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EPITHELIAL CELLS; ESCHERICHIA COLI; FLAGELLIN; HT29 CELLS; HUMANS; INTERLEUKIN-8; INTESTINAL MUCOSA; PROTEIN BINDING;

ENTEROBACTERIACEAE; ESCHERICHIA COLI; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

EID: 33748184696     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2006.03.003     Document Type: Article

References (42)

1. Felix G., Duran J.D., Volko S., and Boller T. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18 (1999) 265-276
2. Gewirtz A.T., Simon Jr. P.O., Schmitt C.K., Taylor L.J., Hagedorn C.H., O'Brien A.D., Neish A.S., and Madara J.L. Salmonella typhimurium translocates flagellin across intestinal epithelia, inducing a proinflammatory response. J. Clin. Invest. 107 (2001) 99-109
3. Smith K.D., Andersen-Nissen E., Hayashi F., Strobe K., Bergman M.A., Barrett S.L., Cookson B.T., and Aderem A. Toll-like receptor 5 recognizes a conserved site on flagellin required for protofilament formation and bacterial motility. Nat. Immunol. 4 (2003) 1247-1253
4. Applequist S.E., Rollman E., Wareing M.D., Liden M., Rozell B., Hinkula J., and Ljunggren H.G. Activation of innate immunity, inflammation, and potentiation of DNA vaccination through mammalian expression of the TLR5 agonist flagellin. J. Immunol. 175 (2005) 3882-3891
5. Pino O., Martin M., and Michalek S.M. Cellular mechanisms of the adjuvant activity of the flagellin component FljB of Salmonella enterica Serovar Typhimurium to potentiate mucosal and systemic responses. Infect. Immun. 73 (2005) 6763-6770
6. Strindelius L., Filler M., and Sjoholm I. Mucosal immunization with purified flagellin from Salmonella induces systemic and mucosal immune responses in C3H/HeJ mice. Vaccine 22 (2004) 3797-3808
7. Gewirtz A.T., Navas T.A., Lyons S., Godowski P.J., and Madara J.L. Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J. Immunol. 167 (2001) 1882-1885
8. Lyons S., Wang L., Casanova J.E., Sitaraman S.V., Merlin D., and Gewirtz A.T. Salmonella typhimurium transcytoses flagellin via an SPI2-mediated vesicular transport pathway. J. Cell. Sci. 117 (2004) 5771-5780
9. Römling U., Bian Z., Hammar M., Sierralta W.D., and Normark S. Curli fibers are highly conserved between Salmonella typhimurium and Escherichia coli with respect to operon structure and regulation. J. Bacteriol. 180 (1998) 722-731
10. Römling U., Bokranz W., Gerstel U., Lunsdorf H., Nimtz M., Rabsch W., Tschäpe H., and Zogaj X. Medical Implication of Biofilms. In: Wilson M., and Devin D. (Eds) (2003), Cambridge University Press, Cambridge 231-261
11. Gophna U., Barlev M., Seijffers R., Oelschlager T.A., Hacker J., and Ron E.Z. Curli fibers mediate internalization of Escherichia coli by eukaryotic cells. Infect. Immun. 69 (2001) 2659-2665
12. Uhlich G.A., Keen J.E., and Elder R.O. Variations in the csgD promoter of Escherichia coli O157:H7 associated with increased virulence in mice and increased invasion of HEp-2 cells. Infect. Immun. 70 (2002) 395-399
13. Hammar M., Arnqvist A., Bian Z., Olsen A., and Normark S. Expression of two csg operons is required for production of fibronectin- and congo red-binding curli polymers in Escherichia coli K-12. Mol. Microbiol. 18 (1995) 661-670
14. Römling U., Sierralta W.D., Eriksson K., and Normark S. Multicellular and aggregative behaviour of Salmonella typhimurium strains is controlled by mutations in the agfD promoter. Mol. Microbiol. 28 (1998) 249-264
15. Humphries A., Deridder S., and Baumler A.J. Salmonella enterica serotype Typhimurium fimbrial proteins serve as antigens during infection of mice. Infect. Immun. 73 (2005) 5329-5338
16. Tukel C., et al. CsgA is a pathogen-associated molecular pattern of Salmonella enterica serotype Typhimurium that is recognized by Toll-like receptor 2. Mol. Microbiol. 58 (2005) 289-304
17. Bonifield H.R., and Hughes K.T. Flagellar phase variation in Salmonella enterica is mediated by a posttranscriptional control mechanism. J. Bacteriol. 185 (2003) 3567-3574
18. Ciacci-Woolwine F., Blomfield I.C., Richardson S.H., and Mizel S.B. Salmonella flagellin induces tumor necrosis factor alpha in a human promonocytic cell line. Infect. Immun. 66 (1998) 1127-1134
19. Rogers T.J., Paton A.W., McColl S.R., and Paton J.C. Enhanced CXC chemokine responses of human colonic epithelial cells to locus of enterocyte effacement-negative Shiga-toxigenic Escherichia coli. Infect. Immun. 71 (2003) 5623-5632
20. Collinson S.K., Doig P.C., Doran J.L., Clouthier S., Trust T.J., and Kay W.W. Thin, aggregative fimbriae mediate binding of Salmonella enteritidis to fibronectin. J. Bacteriol. 175 (1993) 12-18
21. Olsen A., Jonsson A., and Normark S. Fibronectin binding mediated by a novel class of surface organelles on Escherichia coli. Nature 338 (1989) 652-655
22. Ben Nasr A., Olsen A., Sjobring U., Muller-Esterl W., and Bjorck L. Assembly of human contact phase proteins and release of bradykinin at the surface of curli-expressing Escherichia coli. Mol. Microbiol. 20 (1996) 927-935
23. Ramos H.C., Rumbo M., and Sirard J.C. Bacterial flagellins: mediators of pathogenicity and host immune responses in mucosa. Trends Microbiol. 12 (2004) 509-517
24. Tallant T., Deb A., Kar N., Lupica J., de Veer M.J., and DiDonato J.A. Flagellin acting via TLR5 is the major activator of key signaling pathways leading to NF-kappa B and proinflammatory gene program activation in intestinal epithelial cells. BMC Microbiol. 4 (2004) 33
25. Zogaj X., Bokranz W., Nimtz M., and Römling U. Production of cellulose and curli fimbriae by members of the family Enterobacteriaceae isolated from the human gastrointestinal tract. Infect. Immun. 71 (2003) 4151-4158
26. Römling U., Bokranz W., Rabsch W., Zogaj X., Nimtz M., and Tschäpe H. Occurrence and regulation of the multicellular morphotype in Salmonella serovars important in human disease. Int. J. Med. Microbiol. 293 (2003) 273-285
27. Olsen A., Wick M.J., Morgelin M., and Bjorck L. Curli, fibrous surface proteins of Escherichia coli, interact with major histocompatibility complex class I molecules. Infect. Immun. 66 (1998) 944-949
28. Zogaj X., Nimtz M., Rohde M., Bokranz W., and Römling U. The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol. Microbiol. 39 (2001) 1452-1463
29. Komoriya K., Shibano N., Higano T., Azuma N., Yamaguchi S., and Aizawa S.I. Flagellar proteins and type III-exported virulence factors are the predominant proteins secreted into the culture media of Salmonella typhimurium. Mol. Microbiol. 34 (1999) 767-779
30. Uhlen P., et al. Alpha-haemolysin of uropathogenic E. coli induces Ca2+ oscillations in renal epithelial cells. Nature 405 (2000) 694-697
31. Das M., Chopra A.K., Cantu J.M., and Peterson J.W. Antisera to selected outer membrane proteins of Vibrio cholerae protect against challenge with homologous and heterologous strains of V. cholerae. FEMS Immunol. Med. Microbiol. 22 (1998) 303-308
32. Asai Y., Ohyama Y., Gen K., and Ogawa T. Bacterial fimbriae and their peptides activate human gingival epithelial cells through Toll-like receptor 2. Infect. Immun. 69 (2001) 7387-7395
33. DiMango E., Zar H.J., Bryan R., and Prince A. Diverse Pseudomonas aeruginosa gene products stimulate respiratory epithelial cells to produce interleukin-8. J. Clin. Invest. 96 (1995) 2204-2210
34. Harrington S.M., Strauman M.C., Abe C.M., and Nataro J.P. Aggregative adherence fimbriae contribute to the inflammatory response of epithelial cells infected with enteroaggregative Escherichia coli. Cell. Microbiol. 7 (2005) 1565-1578
35. Samuelsson P., Hang L., Wullt B., Irjala H., and Svanborg C. Toll-like receptor 4 expression and cytokine responses in the human urinary tract mucosa. Infect. Immun. 72 (2004) 3179-3186
36. Backhed F., et al. Identification of target tissue glycosphingolipid receptors for uropathogenic, F1C-fimbriated Escherichia coli and its role in mucosal inflammation. J. Biol. Chem. 277 (2002) 18198-18205
37. Hedlund M., Frendeus B., Wachtler C., Hang L., Fischer H., and Svanborg C. Type 1 fimbriae deliver an LPS- and TLR4-dependent activation signal to CD14-negative cells. Mol. Microbiol. 39 (2001) 542-552
38. Cario E., Rosenberg I.M., Brandwein S.L., Beck P.L., Reinecker H.C., and Podolsky D.K. Lipopolysaccharide activates distinct signaling pathways in intestinal epithelial cell lines expressing Toll-like receptors. J. Immunol. 164 (2000) 966-972
39. Furrie E., Macfarlane S., Thomson G., and Macfarlane G.T. Toll-like receptors-2, -3 and -4 expression patterns on human colon and their regulation by mucosal-associated bacteria. Immunology 115 (2005) 565-574
40. Lindmark H., Johansson K.C., Stoven S., Hultmark D., Engstrom Y., and Soderhall K. Enteric bacteria counteract lipopolysaccharide induction of antimicrobial peptide genes. J. Immunol. 167 (2001) 6920-6923
41. Fischer L., Poeckel D., Buerkert E., Steinhilber D., and Werz O. Inhibitors of actin polymerisation stimulate arachidonic acid release and 5-lipoxygenase activation by upregulation of Ca2+ mobilisation in polymorphonuclear leukocytes involving Src family kinases. Biochim. Biophys. Acta 1736 (2005) 109-119
42. Ikewaki N., Yamada A., and Inoko H. Depolymerization of actin filament by cytochalasin E induces interleukin-8 production and up-regulates CD54 in the HeLa epithelial cell line. Microbiol. Immunol. 47 (2003) 775-783