Primary bovine colonic cells: A model to study strain-specific responses to Escherichia coli

Veterinary Immunology and Immunopathology

Volumn 137, Issue 1-2, 2010, Pages 54-63

  Bridger, Philip Simon ^a   Mohr, Melanie ^a   Stamm, Ivonne ^a   Fröhlich, Julia ^a   Föllmann, Wolfram ^b   Birkner, Sascha ^b   Metcalfe, Hannah ^c   Werling, Dirk ^c   Baljer, Georg ^a   Menge, Christian ^a,d  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b TU DORTMUND UNIVERSITY   (Germany)

^c ROYAL VETERINARY COLLEGE   (United Kingdom)

^d FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

Author keywords

Bovine colon; Cytokine; E. coli; Epithelial cell; TLR

Indexed keywords

ACTIN; CYTOKERATIN; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 10; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 6; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR 9; TRANSFORMING GROWTH FACTOR BETA; VIMENTIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; BACTERIAL STRAIN; BACTERIUM ADHERENCE; COLON MUCOSA; COMMENSAL ESCHERICHIA COLI; CONTROLLED STUDY; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ENTEROPATHOGENIC ESCHERICHIA COLI; ESCHERICHIA COLI; HOST PARASITE INTERACTION; INTESTINE CELL; INTESTINE CRYPT; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION;

BACTERIA (MICROORGANISMS); BOS; BOVINAE; ESCHERICHIA COLI;

EID: 77955451758     PISSN: 01652427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vetimm.2010.04.010     Document Type: Article

References (47)

1. Aidar-Ugrinovich L., Blanco J., Blanco M., Blanco J.E., Leomil L., Dahbi G., Mora A., Onuma D.L., Silveira W.D., Pestana de Castro A.F. Serotypes, virulence genes, and intimin types of Shiga toxin-producing Escherichia coli (STEC) and enteropathogenic E. coli (EPEC) isolated from calves in Sao Paulo, Brazil. Int. J. Food Microbiol. 2007, 115:297-306.
2. Bambou J.C., Giraud A., Menard S., Begue B., Rakotobe S., Heyman M., Taddei F., Cerf-Bensussan N., Gaboriau-Routhiau V. In vitro and ex vivo activation of the TLR5 signaling pathway in intestinal epithelial cells by a commensal Escherichia coli strain. J. Biol. Chem. 2004, 279:42984-42992.
3. Behrendt J.H., Hermosilla C., Hardt M., Failing K., Zahner H., Taubert A.A. PMN-mediated immune reactions against Eimeria bovis. Vet. Parasitol. 2008, 151:97-109.
4. Dibb-Fuller M.P., Best A., Stagg D.A., Cooley W.A., Woodward M.J. An in-vitro model for studying the interaction of Escherichia coli O157:H7 and other enteropathogens with bovine primary cell cultures. J. Med. Microbiol. 2001, 50:759-769.
5. Dwinell M.B., Johanesen P.A., Smith J.M. Immunobiology of epithelial chemokines in the intestinal mucosa. Surgery 2003, 133:601-607.
6. Föllmann W., Birkner S. The use of cultured primary bovine colon epithelial cells as a screening model to detect genotoxic effects of heterocyclic aromatic amines in the comet assay. J. Toxicol. Environ. Health A 2008, 71:947-953.
7. Föllmann W., Weber S., Birkner S. Primary cell cultures of bovine colon epithelium: isolation and cell culture of colonocytes. Toxicol. In Vitro 2000, 14:435-445.
8. Frick J.S., Fink K., Niemiec K.M.J., Quitadamo M., Schenk K., Autenrieth I.B. Identification of commensal bacterial strains that modulate Yersinia enterocolitica and dextran sodium sulfate-induced inflammatory responses: implications for the development of probiotics. Infect. Immun. 2007, 75:3490-3497.
9. Gobert A.P., Vareille M., Glasser A.L., Hindre T., de Sablet T., Martin C. Shiga toxin produced by enterohemorrhagic Escherichia coli inhibits PI3K/NF-{kappa}B signaling pathway in globotriaosylceramide-3-negative human intestinal epithelial cells. J. Immunol. 2007, 178:8168-8174.
10. Gribar S.C., Anand R.J., Sodhi C.P., Hackam D.J. The role of epithelial Toll-like receptor signaling in the pathogenesis of intestinal inflammation. J. Leukoc. Biol. 2008, 83:493-498.
11. Grossmann J., Walther K., Artinger M., Kiessling S., Scholmerich J. Apoptotic signaling during initiation of detachment-induced apoptosis (" Anoikis" ) of primary human intestinal epithelial cells. Cell Growth Differ. 2001, 12:147-155.
12. Hauf N., Chakraborty T. Suppression of NF-{kappa}B activation and proinflammatory cytokine expression by Shiga toxin-producing Escherichia coli. J. Immunol. 2003, 170:2074-2082.
13. Hoey D.E.E., Sharp L., Currie C., Lingwood C.A., Gally D.L., Smith D.G.E. Verotoxin 1 binding to intestinal crypt epithelial cells results in localization to lysosomes and abrogation of toxicity. Cell. Microbiol. 2003, 5:85-97.
14. Hooper L.V., Wong M.H., Thelin A., Hansson L., Falk P.G., Gordon J.I. Molecular analysis of commensal host-microbial relationships in the intestine. Science 2001, 291:881-884.
15. Jerse A.E., Yu J., Tall B.D., Kaper J.B. A genetic locus of enteropathogenic Escherichia coli necessary for the production of attaching and effacing lesions on tissue culture cells. Proc. Natl. Acad. Sci. U.S.A. 1990, 87:7839-7843.
16. Jung H.C., Eckmann L., Yang S.K., Panja A., Fierer J., Morzyckawroblewska E., Kagnoff M.F. A distinct array of proinflammatory cytokines is expressed in human colon epithelial-cells in response to bacterial invasion. J. Clin. Invest. 1995, 95:55-65.
17. Kaeffer B. Mammalian intestinal epithelial cells in primary culture: a mini-review. In Vitro Cell. Dev. Biol. Anim. 2002, 38:123-134.
18. Kagnoff M.F., Eckmann L. Epithelial cells as sensors for microbial infection. J. Clin. Invest. 1997, 100:S51-S55.
19. Khalil N. TGF-[beta]: from latent to active. Microb. Infect. 1999, 1:1255-1263.
20. Knutton S., Baldwin T., Williams P.H., McNeish A.S. Actin accumulation at sites of bacterial adhesion to tissue culture cells: basis of a new diagnostic test for enteropathogenic and enterohemorrhagic Escherichia coli. Infect. Immun. 1989, 57:1290-1298.
21. Lammers K.M., Helwig U., Swennen E., Rizzello F., Venturi A., Caramelli E., Kamm M.A., Brigidi P., Gionchetti P., Campieri M. Effect of probiotic strains on interleukin 8 production by HT29/19A cells. Am. J. Gastroenterol. 2002, 97:1182-1186.
22. Lan J.G., Cruickshank S.M., Singh J.C., Farrar M., Lodge J.P., Felsburg P.J., Carding S.R. Different cytokine response of primary colonic epithelial cells to commensal bacteria. World J. Gastroenterol. 2005, 11:3375-3384.
23. Lee J.D., Mo J.H., Shen C., Rucker A.N., Raz E. Toll-like receptor signaling in intestinal epithelial cells contributes to colonic homoeostasis. Curr. Opin. Gastroenterol. 2007, 23:27-31.
24. Lotz M., Konig T., Menard S., Guetle D., Bogdan C., Hornef M.W. Cytokine-mediated control of lipopolysaccharide-induced activation of small intestinal epithelial cells. Immunology 2007, 122:306-315.
25. Moussay E., Stamm I., Taubert A., Baljer G., Menge C. Escherichia coli Shiga toxin 1 enhances il-4 transcripts in bovine ileal intraepithelial lymphocytes. Vet. Immunol. Immunopathol. 2006, 113:367-382.
26. Mundy R., Schuller S., Girard F., Fairbrother J.M., Phillips A.D., Frankel G. Functional studies of intimin in vivo and ex vivo: implications for host specificity and tissue tropism. Microbiology 2007, 153:959-967.
27. Nagalakshmi M.L., Rascle A., Zurawski S., Menon S., Waal Malefyt R. Interleukin-22 activates STAT3 and induces IL-10 by colon epithelial cells. Int. Immunopharmacol. 2004, 4:679-691.
28. Neish A.S., Gewirtz A.T., Zeng H., Young A.N., Hobert M.E., Karmali V., Rao A.S., Madara J.L. Prokaryotic regulation of epithelial responses by inhibition of Ikappa B-alpha ubiquitination. Science 2000, 289:1560-1563.
29. Otte J.M., Cario E., Podolsky D.K. Mechanisms of cross hyporesponsiveness to Toll-like receptor bacterial ligands in intestinal epithelial cells. Gastroenterology 2004, 126:1054-1070.
30. Parlesak A., Haller D., Brinz S., Baeuerlein A., Bode C. Modulation of cytokine release by differentiated CACO-2 cells in a compartmentalized coculture model with mononuclear leucocytes and nonpathogenic bacteria. Scand. J. Immunol. 2004, 60:477-485.
31. Paton J.C., Rogers T.J., Morona R., Paton A.W. Oral administration of formaldehyde-killed recombinant bacteria expressing a mimic of the Shiga toxin receptor protects mice from fatal challenge with Shiga-toxigenic Escherichia coli. Infect. Immun. 2001, 69:1389-1393.
32. Rashid R.A., Tabata T.A., Oatley M.J., Besser T.E., Tarr P.I., Moseley S.L. Expression of putative virulence factors of Escherichia coli O157: H7 differs in bovine and human infections. Infect. Immun. 2006, 74:4142-4148.
33. Rogers T.J., Paton A.W., McColl S.R., Paton J.C. Enhanced CXC chemokine responses of human colonic epithelial cells to locus of enterocyte effacement-negative Shiga-toxigenic Escherichia coli. Infect. Immun. 2003, 71:5623-5632.
34. Rusu D., Loret S., Peulen O., Mainil J., Dandrifosse G. Immunochemical, biomolecular and biochemical characterization of bovine epithelial intestinal primocultures. BMC Cell Biol. 2005, 6.
35. Sansonetti P.J. War and peace at mucosal surfaces. Nat. Rev. Immunol. 2004, 4:953-964.
36. Schlundt J., Toyofuku H., Jansen J., Herbst S.A. Emerging food-borne zoonoses. Rev. Sci. Technol. 2004, 23:513-533.
37. Schoepe H., Wieler L.H., Bauerfeind R., Schlapp T., Potschka H., Hehnen H.R., Baljer G. Neutralization of hemolytic and mouse lethal activities of C. perfringensalpha-toxin need simultaneous blockade of two epitopes by monoclonal antibodies. Microb. Pathog. 1997, 23:1-10.
38. Shibahara T., Wilcox J.N., Couse T., Madara J.L. Characterization of epithelial chemoattractants for human intestinal intraepithelial lymphocytes. Gastroenterology 2001, 120:60-70.
39. Skjolaas K.A., Burkey T.E., Dritz S.S., Minton J.E. Effects of Salmonella enterica serovar Typhimurium, or serovar Choleraesuis. Lactobacillus reuteri and Bacillus licheniformis on chemokine and cytokine expression in the swine jejunal epithelial cell line, IPEC-J2. Vet. Immunol. Immunopathol. 2007, 115:299-308.
40. Smith D.G., Naylor S.W., Gally D.L. Consequences of EHEC colonisation in humans and cattle. Int. J. Med. Microbiol. 2002, 292:169-183.
41. 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.
42. Stamm I., Mohr M., Bridger P.S., Schropfer E., Konig M., Stoffregen W.C., Dean-Nystrom E.A., Baljer G., Menge C. Epithelial and mesenchymal cells in the bovine colonic mucosa differ in their responsiveness to Escherichia coli Shiga toxin 1. Infect. Immun. 2008, 76:5381-5391.
43. Taubert A., Zahner H., Hermosilla C. Dynamics of transcription of immunomodulatory genes in endothelial cells infected with different coccidian parasites. Vet. Parasitol. 2006, 142:214-222.
44. Wakabayashi Y., Chua J., Larkin J.M., Lippincott-Schwartz J., Arias I.M. Four-dimensional imaging of filter-grown polarized epithelial cells. Histochem. Cell Biol. 2007, 127:463-472.
45. Werling D., Jungi T.W. Toll-like receptors linking innate and adaptive immune response. Vet. Immunol. Immunopathol. 2003, 91:1-12.
46. Wieler L.H., Vieler E., Erpenstein C., Schlapp T., Steinruck H., Bauerfeind R., Byomi A., Baljer G. Shiga toxin-producing Escherichia coli strains from bovines: association of adhesion with carriage of eae and other genes. J. Clin. Microbiol. 1996, 34:2980-2984.
47. Yang S.K., Eckmann L., Panja A., Kagnoff M.F. Differential and regulated expression of C-X-C, C-C, and C-chemokines by human colon epithelial cells. Gastroenterology 1997, 113:1214-1223.