Enterohemorrhagic E. coli alters murine intestinal epithelial tight junction protein expression and barrier function in a Shiga toxin independent manner

Laboratory Investigation

Volumn 90, Issue 8, 2010, Pages 1152-1168

  Roxas, Jennifer L ^a   Koutsouris, Athanasia ^a   Bellmeyer, Amy ^a   Tesfay, Samuel ^a   Royan, Sandhya ^a   Falzari, Kanakeshwari ^a   Harris, Antoneicka ^a   Cheng, Hao ^a   Rhee, Ki Jong ^a   Hecht, Gail ^a,b  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b JESSE BROWN VA MEDICAL CENTER   (United States)

Author keywords

claudin 2; claudin 3; EHEC; mice; microvilli effacement; occludin; transmucosal electrical resistance

Indexed keywords

CLAUDIN 2; CLAUDIN 3; EOSIN; FLUORESCEIN ISOTHIOCYANATE DEXTRAN; HEMATOXYLIN; MESSENGER RNA; OCCLUDIN; PROTEIN ZO1; SHIGA TOXIN; STREPTOMYCIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BIOLUMINESCENCE; CECUM; CLDN2 GENE; CLDN3 GENE; COLON; CONTROLLED STUDY; DIARRHEA; ELECTRIC RESISTANCE; ENTEROHEMORRHAGIC ESCHERICHIA COLI; GENE; HEMOLYTIC UREMIC SYNDROME; HEMORRHAGIC COLITIS; ILEUM; IMMUNOFLUORESCENCE MICROSCOPY; INTESTINE EPITHELIUM; INTESTINE MUCOSA PERMEABILITY; LAMINA PROPRIA; LEUKOCYTE; MALE; MICROVILLUS; MOUSE; NONHUMAN; OCLN GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RNA TRANSCRIPTION; SYMPTOM; TIGHT JUNCTION; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; COLON; DEXTRANS; DIARRHEA; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; FLUORESCEIN-5-ISOTHIOCYANATE; HEMOLYTIC-UREMIC SYNDROME; ILEUM; INTESTINAL MUCOSA; INTESTINES; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; PERMEABILITY; SHIGA TOXIN; TIGHT JUNCTIONS;

EID: 77955124560     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2010.91     Document Type: Article

References (58)

1. Frankel G, Phillips AD, Rosenshine I, et al. Enteropathogenic and enterohaemorrhagic Escherichia coli: more subversive elements. Mol Microbiol 1998;30:911-921.
2. McDaniel TK, Kaper JB. A cloned pathogenicity island from enteropathogenic Escherichia coli confers the attaching and effacing phenotype on E. coli K-12. Mol Microbiol 1997;23:399-407.
3. Bielaszewska M, Karch H. Consequences of enterohaemorrhagic Escherichia coli infection for the vascular endothelium. Thromb Haemost 2005;94:312-318.
4. Nataro JP, Kaper JB. Diarrheagenic Escherichia coli. Clin Microbiol Rev 1998;11:142-201.
5. Viswanathan VK, Koutsouris A, Lukic S, et al. Comparative analysis of EspF from enteropathogenic and enterohemorrhagic Escherichia coli in alteration of epithelial barrier function. Infect Immun 2004;72:3218-3227.
6. Hecht G, Marrero JA, Danilkovich A, et al. Pathogenic Escherichia coli increase Cl-secretion from intestinal epithelia by upregulating galanin-1 receptor expression. J Clin Invest 1999;104:253-262.
7. Beery JT, Doyle MP, Schoeni JL. Colonization of chicken cecae by Escherichia coli associated with hemorrhagic colitis. Appl Environ Microbiol 1985;49:310-315.
8. Potter ME, Kaufmann AF, Thomason BM, et al. Diarrhea due to Escherichia coli O157:H7 in the infant rabbit. J Infect Dis 1985;152:1341-1343.
9. Pai CH, Kelly JK, Meyers GL. Experimental infection of infant rabbits with verotoxin-producing Escherichia coli. Infect Immun 1986;51: 16-23.
10. Francis DH, Moxley RA, Andraos CY. Edema disease-like brain lesions in gnotobiotic piglets infected with Escherichia coli serotype O157:H7. Infect Immun 1989;57:1339-1342.
11. Tzipori S, Gunzer F, Donnenberg MS, et al. The role of the eaeA gene in diarrhea and neurological complications in a gnotobiotic piglet model of enterohemorrhagic Escherichia coli infection. Infect Immun 1995;63:3621-3627.
12. Isogai E, Isogai H, Takeshi K, et al. Protective effect of Japanese green tea extract on gnotobiotic mice infected with an Escherichia coli O157:H7 strain. Microbiol Immunol 1998;42:125-128. (Pubitemid 28101046)
13. Kurioka T, Yunou Y, Kita E. Enhancement of susceptibility to Shiga toxin-producing Escherichia coli O157:H7 by protein calorie malnutrition in mice. Infect Immun 1998;66:1726-1734.
14. Ogawa M, Shimizu K, Nomoto K, et al. Protective effect of Lactobacillus casei strain Shirota on Shiga toxin-producing Escherichia coli O157:H7 infection in infant rabbits. Infect Immun 2001;69:1101-1108.
15. Nagano K, Taguchi K, Hara T, et al. Adhesion and colonization of enterohemorrhagic Escherichia coli O157:H7 in cecum of mice. Microbiol Immunol 2003;47:125-132.
16. Tzipori S, Karch H, Wachsmuth KI, et al. Role of a 60-megadalton plasmid and Shiga-like toxins in the pathogenesis of infection caused by enterohemorrhagic Escherichia coli O157:H7 in gnotobiotic piglets. Infect Immun 1987;55:3117-3125.
17. Myhal ML, Laux DC, Cohen PS. Relative colonizing abilities of human fecal and K 12 strains of Escherichia coli in the large intestines of streptomycin-treated mice. Eur J Clin Microbiol 1982;1:186-192.
18. Morin CE, Kaper JB. Use of stabilized luciferase-expressing plasmids to examine in vivo-induced promoters in the Vibrio cholerae vaccine strain CVD 103-HgR. FEMS Immunol Med Microbiol 2009;57:69-79.
19. Wiles S, Pickard KM, Peng K, et al. In vivo bioluminescence imaging of the murine pathogen Citrobacter rodentium. Infect Immun 2006;74:5391-5396.
20. Savkovic SD, Villanueva J, Turner JR, et al. Mouse model of enteropathogenic Escherichia coli infection. Infect Immun 2005;73:1161-1170.
21. Shifflett DE, Clayburgh DR, Koutsouris A, et al. Enteropathogenic E. coli disrupts tight junction barrier function and structure in vivo. Lab Invest 2005;85:1308-1324.
22. Mead PS, Griffin PM. Escherichia coli O157:H7. Lancet 1998;352: 1207-1212.
23. Shimizu K, Asahara T, Nomoto K, et al. Development of a lethal Shiga toxin-producing Escherichia coli-infection mouse model using multiple mitomycin C treatment. Microb Pathog 2003;35:1-9.
24. Wadolkowski EA, Burris JA, O'Brien AD. Mouse model for colonization and disease caused by enterohemorrhagic Escherichia coli O157:H7. Infect Immun 1990;58:2438-2445.
25. Mundy R, Girard F, FitzGerald AJ, et al. Comparison of colonization dynamics and pathology of mice infected with enteropathogenic Escherichia coli, enterohaemorrhagic E. coli and Citrobacter rodentium. FEMS Microbiol Lett 2006;265:126-132.
26. Que JU, Hentges DJ. Effect of streptomycin administration on colonization resistance to Salmonella typhimurium in mice. Infect Immun 1985;48:169-174.
27. Que JU, Casey SW, Hentges DJ. Factors responsible for increased susceptibility of mice to intestinal colonization after treatment with streptomycin. Infect Immun 1986;53:116-123.
28. Lye DJ. A mouse model for characterization of gastrointestinal colonization rates among environmental Aeromonas isolates. Curr Microbiol 2009;58:454-458.
29. Bohnhoff M, Miller CP, Martin WR. Resistance of the mouse's intestinal tract to experimental Salmonella infection. I. Factors which interfere with the initiation of infection by oral inoculation. J Exp Med 1964;120:805-816.
30. Bohnhoff M, Miller CP, Martin WR. Resistance of the mouse's intestinal tract to experimental Salmonella infection. Ii. Factors responsible for its loss following streptomycin treatment. J Exp Med 1964;120: 817-828.
31. Karch H, Heesemann J, Laufs R, et al. A plasmid of enterohemorrhagic Escherichia coli O157:H7 is required for expression of a new fimbrial antigen and for adhesion to epithelial cells. Infect Immun 1987;55: 455-461.
32. Zhao S, Meng J, Doyle MP, et al. A low molecular weight outer-membrane protein of Escherichia coli O157:H7 associated with adherence to INT407 cells and chicken caeca. J Med Microbiol 1996;45:90-96.
33. Tarr PI, Bilge SS, Vary Jr JC, et al. Iha: a novel Escherichia coli O157:H7 adherence-conferring molecule encoded on a recently acquired chromosomal island of conserved structure. Infect Immun 2000;68:1400-1407.
34. Judge NA, Mason HS, O'Brien AD. Plant cell-based intimin vaccine given orally to mice primed with intimin reduces time of Escherichia coli O157:H7 shedding in feces. Infect Immun 2004;72:168-175.
35. Sinclair JF, Dean-Nystrom EA, O'Brien AD. The established intimin receptor Tir and the putative eucaryotic intimin receptors nucleolin and beta1 integrin localize at or near the site of enterohemorrhagic Escherichia coli O157:H7 adherence to enterocytes in vivo. Infect Immun 2006;74:1255-1265.
36. Mundy R, MacDonald TT, Dougan G, et al. Citrobacter rodentium of mice and man. Cell Microbiol 2005;7:1697-1706.
37. Klapproth JM, Sasaki M, Sherman M, et al. Citrobacter rodentium lifA/efa1 is essential for colonic colonization and crypt cell hyperplasia in vivo. Infect Immun 2005;73:1441-1451.
38. Dean-Nystrom EA, Melton-Celsa AR, Pohlenz JF, et al. Comparative pathogenicity of Escherichia coli O157 and intimin-negative non-O157 Shiga toxin-producing E coli strains in neonatal pigs. Infect Immun 2003;71:6526-6533.
39. Sherman P, Soni R, Karmali M. Attaching and effacing adherence of Vero cytotoxin-producing Escherichia coli to rabbit intestinal epithelium in vivo. Infect Immun 1988;56:756-761.
40. Furuse M, Furuse K, Sasaki H, et al. Conversion of zonulae occludentes from tight to leaky strand type by introducing claudin-2 into Madin-Darby canine kidney I cells. J Cell Biol 2001;153:263-272.
41. Amasheh S, Meiri N, Gitter AH, et al. Claudin-2 expression induces cation-selective channels in tight junctions of epithelial cells. J Cell Sci 2002;115:4969-4976.
42. Weber CR, Nalle SC, Tretiakova M, et al. Claudin-1 and claudin-2 expression is elevated in inflammatory bowel disease and may contribute to early neoplastic transformation. Lab Invest 2008;88:1110-1120.
43. Zeissig S, Burgel N, Gunzel D, et al. Changes in expression and distribution of claudin 2, 5 and 8 lead to discontinuous tight junctions and barrier dysfunction in active Crohn's disease. Gut 2007;56:61-72.
44. Van Itallie CM, Holmes J, Bridges A, et al. The density of small tight junction pores varies among cell types and is increased by expression of claudin-2. J Cell Sci 2008;121:298-305.
45. Inai T, Sengoku A, Hirose E, et al. Comparative characterization of mouse rectum CMT93-I and-II cells by expression of claudin isoforms and tight junction morphology and function. Histochem Cell Biol 2008;129:223-232.
46. Van Itallie CM, Colegio OR, Anderson JM. The cytoplasmic tails of claudins can influence tight junction barrier properties through effects on protein stability. J Membr Biol 2004;199:29-38.
47. Sakaguchi T, Gu X, Golden HM, et al. Cloning of the human claudin-2 5-flanking region revealed a TATA-less promoter with conserved binding sites in mouse and human for caudal-related homeodomain proteins and hepatocyte nuclear factor-1alpha. J Biol Chem 2002;277:21361-21370.
48. Mankertz J, Hillenbrand B, Tavalali S, et al. Functional crosstalk between Wnt signaling and Cdx-related transcriptional activation in the regulation of the claudin-2 promoter activity. Biochem Biophys Res Commun 2004;314:1001-1007.
49. Escaffit F, Boudreau F, Beaulieu JF. Differential expression of claudin-2 along the human intestine: implication of GATA-4 in the maintenance of claudin-2 in differentiating cells. J Cell Physiol 2005;203:15-26.
50. Mankertz J, Amasheh M, Krug SM, et al. TNFalpha up-regulates claudin-2 expression in epithelial HT-29/B6 cells via phosphatidylinositol-3-kinase signaling. Cell Tissue Res 2009;336:67-77.
51. De Oliveira SS, de Oliveira IM, De Souza W, et al. Claudins upregulation in human colorectal cancer. FEBS Lett 2005;579:6179-6185.
52. Mees ST, Mennigen R, Spieker T, et al. Expression of tight and adherens junction proteins in ulcerative colitis associated colorectal carcinoma: upregulation of claudin-1, claudin-3, claudin-4, and beta-catenin. Int J Colorectal Dis 2009;24:361-368.
53. Hashimoto K, Oshima T, Tomita T, et al. Oxidative stress induces gastric epithelial permeability through claudin-3. Biochem Biophys Res Commun 2008;376:154-157.
54. 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.
55. Sharma R, Tesfay S, Tomson FL, et al. Balance of bacterial pro-and anti-inflammatory mediators dictates net effect of enteropathogenic Escherichia coli on intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 2006;290:G685-G694.
56. Bellmeyer A, Cotton C, Kanteti R, et al. Enterohemorrhagic Escherichia coli suppresses inflammatory response to cytokines and its own toxin. Am J Physiol Gastrointest Liver Physiol 2009;297: G576-G581.
57. Ritchie JM, Thorpe CM, Rogers AB, et al. Critical roles for stx2, eae, and tir in enterohemorrhagic Escherichia coli-induced diarrhea and intestinal inflammation in infant rabbits. Infect Immun 2003;71: 7129-7139.
58. Yamasaki C, Natori Y, Zeng XT, et al. Induction of cytokines in a human colon epithelial cell line by Shiga toxin 1 (Stx1) and Stx2 but not by non-toxic mutant Stx1 which lacks N-glycosidase activity. FEBS Lett 1999;442:231-234.