Epithelial barriers in intestinal inflammation

Antioxidants and Redox Signaling

Volumn 15, Issue 5, 2011, Pages 1255-1270

  John, Lena J ^a   Fromm, Michael ^a   Schulzke, Jörg Dieter ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADALIMUMAB; ANTIOXIDANT; BERBERINE; BUDESONIDE; BUTYRIC ACID; CYTOKINE; GLUTATHIONE; INFLIXIMAB; MESALAZINE; NITRIC OXIDE; PHOSPHATASE; PLACEBO; PROBIOTIC AGENT; QUERCETIN; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG; WIP1 ENZYME; ZINC;

CELIAC DISEASE; CELL PERMEABILIZATION; COLLAGENOUS COLITIS; COLON ABSORPTION; CROHN DISEASE; DIARRHEA; ELECTRIC RESISTANCE; GASTROINTESTINAL INFECTION; HUMAN; INTESTINE EPITHELIUM; MICROSCOPIC COLITIS; NEUTROPHIL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW; TIGHT JUNCTION; ULCERATIVE COLITIS; ZINC DEFICIENCY;

ANIMALS; CYTOKINES; DIARRHEA; GASTROENTERITIS; HUMANS; INTESTINAL MUCOSA; OXIDATIVE STRESS; TIGHT JUNCTIONS;

EID: 79960772834     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2011.3892     Document Type: Review

References (136)

1. Aggarwal BB and Eessalu TE. Induction of receptors for tumor necrosis factor-alpha by interferons is not a major mechanism for their synergistic cytotoxic response. J Biol Chem 262: 10000-10007, 1987. (Pubitemid 17103058)
2. Alexandre MD, Lu Q, and Chen YH. Overexpression of claudin-7 decreases the paracellular Cl-conductance and increases the paracellular Na+ conductance in LLC-PK1 cells. J Cell Sci 118: 2683-2693, 2005. (Pubitemid 40932893)
3. Amasheh M, Schlichter S, Amasheh S, Mankertz J, Zeitz M, Fromm M, and Schulzke JD. Quercetin enhances epithelial barrier function and increases claudin-4 expression in Caco-2 cells. J Nutr 138: 1067-1073, 2008. (Pubitemid 351769130)
4. Amasheh S, Fromm M, and Günzel D. Claudins of intestine and nephron. A correlation of molecular tight junction structure and barrier function. Acta Physiol (Oxf) 201: 133-140, 2011.
5. Amasheh S, Meiri N, Gitter AH, Schöneberg T, Mankertz J, Schulzke JD, and Fromm M. Claudin-2 expression induces cation-selective channels in tight junctions of epithelial cells. J Cell Sci 115: 4969-4976, 2002. (Pubitemid 36061180)
6. Andresen L, Jørgensen VL, Perner A, Hansen A, Eugen-Olsen J, and Rask-Madsen J. Activation of nuclear factor kappaB in colonic mucosa from patients with collagenous and ulcerative colitis. Gut 54: 503-509, 2005. (Pubitemid 40395502)
7. Anezaki K, Asakura H, Honma T, Ishizuka K, Funakoshi K, Tsukada Y, and Narisawa R. Correlations between interleukin-8, and myeloperoxidase or luminol-dependent chemiluminescence in inflamed mucosa of ulcerative colitis. Intern Med 37: 253-258, 1998. (Pubitemid 128518589)
8. Atisook K, Carlson S, and Madara J. Effects of phlorizin and sodium on glucose-elicited alterations of cell junctions in intestinal epithelia. Am J Physiol 258: C77-85, 1990. (Pubitemid 20053598)
9. 2-producing enzyme of human neutrophils. J Biol Chem 256: 2321-2323, 1981.
10. Banan A, Fields JZ, Zhang Y, and Keshavarzian A. iNOS upregulation mediates oxidant-induced disruption of Factin and barrier of intestinal monolayers. Am J Physiol Gastrointest Liver Physiol 280: G1234-1246, 2001.
11. Bazzoni G. Pathobiology of junctional adhesion molecules. Antioxid Redox Signal 15: 1221-1234, 2011.
12. Berkes J, Viswanathan VK, Savkovic SD, and Hecht G. Intestinal epithelial responses to enteric pathogens: Effects on the tight junction barrier, ion transport, and inflammation. Gut 52: 439-451, 2003. (Pubitemid 36253638)
13. Blasig IE, Bellmann C, Cording J, del Vecchio G, Zwanziger D, Huber O, and Haseloff RF. Occludin protein family: oxidative stress and reducing conditions. Antioxid Redox Signal 15: 1195-1219, 2011.
14. Bonderup OK, Hansen JB, Birket-Smith L, Vestergaard V, Teglbjaerg PS, and Fallingborg J. Budesonide treatment of collagenous colitis: A randomised, double blind, placebo controlled trial with morphometric analysis. Gut 52: 248-251, 2003. (Pubitemid 36115067)
15. Bonderup OK, Hansen JB, Madsen P, Vestergaard V, Fallingborg J, and Teglbjaerg PS. Budesonide treatment and expression of inducible nitric oxide synthase mRNA in colonic mucosa in collagenous colitis. Eur J Gastroenterol Hepatol 18: 1095-1099, 2006. (Pubitemid 44379363)
16. Bruewer M, Luegering A, Kucharzik T, Parkos CA, Madara JL, Hopkins AM, and Nusrat A. Proinflammatory cytokines disrupt epithelial barrier function by apoptosis-independent mechanisms. J Immunol 171: 6164-6172, 2003. (Pubitemid 37467239)
17. Bruewer M, Utech M, Ivanov AI, Hopkins AM, Parkos CA, and Nusrat A. Interferon-gamma induces internalization of epithelial tight junction proteins via a macropinocytosislike process. FASEB J 19: 923-933, 2005. (Pubitemid 40827713)
18. Bücker R, Troeger H, Kleer J, Fromm M, and Schulzke JD. Arcobacter butzleri induces barrier dysfunction in intestinal HT-29/B6 cells. J Infect Dis 200: 756-764, 2009.
19. Bürgel N, Bojarski C, Mankertz J, Zeitz M, Fromm M, and Schulzke JD. Mechanisms of diarrhea in collagenous colitis. Gastroenterology 123: 433-443, 2002.
20. Cario E, Jung S, Harder D'Heureuse J, Schulte C, Sturm A, Wiedenmann B, Goebell H, and Dignass AU. Effects of exogenous zinc supplementation on intestinal epithelial repair in vitro. Eur J Clin Invest 30: 419-428, 2000. (Pubitemid 30251399)
21. Chang J, Rao NV,Markewitz BA, Hoidal JR, andMichael JR. Nitric oxide donor prevents hydrogen peroxide-mediated endothelial cell injury. Am J Physiol 270: L931-940, 1996.
22. Chapman MA, Grahn MF, Boyle MA, Hutton M, Rogers J, and Williams NS. Butyrate oxidation is impaired in the colonic mucosa of sufferers of quiescent ulcerative colitis. Gut 35: 73-76, 1994. (Pubitemid 24059476)
23. 2+ absorption during lactation by long-term prolactin exposure and suckling-induced prolactin surge. Am J Physiol Endocrinol Metab 297: E609-619, 2009.
24. Chavez AM, Menconi MJ, Hodin RA, and Fink MP. Cytokine-induced intestinal epithelial hyperpermeability: Role of nitric oxide. Crit Care Med 27 :2246-2251, 1999. (Pubitemid 29508346)
25. Ciccocioppo R, Finamore A, Ara C, Di Sabatino A, Mengheri E, and Corazza GR. Altered expression, localization, and phosphorylation of epithelial junctional proteins in celiac disease. Am J Clin Pathol 125: 502-511, 2006.
26. Clark E, Hoare C, Tanianis-Hughes J, Carlson GL, and Warhurst G. Interferon gamma induces translocation of commensal Escherichia coli across gut epithelial cells via a lipid raft-mediated process. Gastroenterology 128: 1258-1267, 2005. (Pubitemid 40712177)
27. Clark EC, Patel SD, Chadwick PR, Warhurst G, Curry A, and Carlson GL. Glutamine deprivation facilitates tumour necrosis factor-induced bacterial translocation in Caco-2 cells by depletion of enterocyte fuel substrate. Gut 52: 224-230, 2003. (Pubitemid 36115063)
28. Cohen CJ, Shieh JT, Pickles RJ, Okegawa T, Hsieh JT, and Bergelson JM. The coxsackievirus and adenovirus receptor is a transmembrane component of the tight junction. Proc Natl Acad Sci USA 98: 15191-15196, 2001. (Pubitemid 34013991)
29. Coisne C and Engelhardt B. Tight junctions in brain barriers during CNS inflammation. Antioxid Redox Signal 15: 1285-1303, 2011.
30. Czerucka D, Dahan S, Mograbi B, Rossi B, and Rampal P. Saccharomyces boulardii preserves the barrier function and modulates the signal transduction pathway induced in enteropathogenic Escherichia coli-infected T84 cells. Infect Immun 68: 5998-6004, 2000.
31. D'Haens G, Van Deventer S, Van Hogezand R, Chalmers D, Kothe C, Baert F, Braakman T, Schaible T, Geboes K, and Rutgeerts P. Endoscopic and histological healing with infliximab anti-tumor necrosis factor antibodies in Crohn's disease: A European multicenter trial. Gastroenterology 116: 1029-1034, 1999. (Pubitemid 29203012)
32. Epple HJ, Schneider T, Troeger H, Kunkel D, Allers K, Moos V, Amasheh M, Loddenkemper C, Fromm M, Zeitz M, and Schulzke JD. Impairment of the intestinal barrier is evident in untreated but absent in suppressively treated HIV-infected patients. Gut 58: 220-227, 2009.
33. Escaffit F, Boudreau F, and 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 203: 15-26, 2005. (Pubitemid 40328168)
34. Farber JL. Mechanisms of cell injury by activated oxygen species. Environ Health Perspect 102 Suppl 10: 17-24, 1994.
35. Fernández-Bañares F, Hinojosa J, Sánchez- Lombraña JL, Navarro E, Martínez-Salmerón JF, García-Pugés A, González-Huix F, Riera J, González-Lara V, Domínguez-Abascal F, Giné JJ, Moles J, Gomollón F, and Gassull MA. Randomized clinical trial of Plantago ovata seeds (dietary fiber) as compared with mesalamine in maintaining remission in ulcerative colitis. Spanish Group for the Study of Crohn's Disease and Ulcerative Colitis (GETECCU). Am J Gastroenterol 94: 427-433, 1999.
36. Finamore A, Massimi M, Conti Devirgiliis L, and Mengheri E. Zinc deficiency induces membrane barrier damage and increases neutrophil transmigration in Caco-2 cells. J Nutr 138: 1664-1670, 2008.
37. Fink MP. Intestinal epithelial hyperpermeability: Update on the pathogenesis of gut mucosal barrier dysfunction in critical illness. Curr Opin Crit Care 9: 143-151, 2003. (Pubitemid 36408134)
38. Fiscella M, Zhang H, Fan S, Sakaguchi K, Shen S, Mercer WE, Vande Woude GF, O'Connor PM, and Appella E. Wip1, a novel human protein phosphatase that is induced in response to ionizing radiation in a p53-dependent manner. Proc Natl Acad Sci USA 94: 6048-6053, 1997. (Pubitemid 27270633)
39. Frey T and Antonetti DA. Alterations to the blood-retinal barrier in diabetes: cytokines and reactive oxygen species. Antioxid Redox Signal 15: 1271-1284, 2011.
40. Fujita H, Chiba H, Yokozaki H, Sakai N, Sugimoto K, Wada T, Kojima T, Yamashita T, and Sawada N. Differential expression and subcellular localization of claudin-7,-8,-12,-13, and-15 along the mouse intestine. J Histochem Cytochem 54: 933-944, 2006. (Pubitemid 44106871)
41. 2+ absorption between enterocytes. Mol Biol Cell 19: 1912-1921, 2008.
42. Fuxe J, Vincent T, and de Herreros AG. Transcriptional crosstalk between TGFbeta and stem cell pathways in tumor cell invasion: Role of EMT promoting Smad complexes. Cell Cycle 9: 2363-2374, 2010.
43. Gitter AH, Bendfeldt K, Schulzke JD, and Fromm M. Leaks in the epithelial barrier caused by spontaneous and TNFalpha-induced single-cell apoptosis. FASEB J 14: 1749-1753, 2000.
44. Gitter AH, Wullstein F, Fromm M, and Schulzke JD. Epithelial barrier defects in ulcerative colitis: Characterization and quantification by electrophysiological imaging. Gastroenterology 121: 1320-1328, 2001. (Pubitemid 33140449)
45. Gloire G, Legrand-Poels S, and Piette J. NF-kappaB activation by reactive oxygen species: Fifteen years later. Biochem Pharmacol 72: 1493-1505, 2006. (Pubitemid 44666727)
46. González-Mariscal L, Quirós M, and Díaz- Coránguez M. ZO proteins and redox-dependent processes. Antioxid Redox Signal 15: 1235-1253, 2011.
47. Gow AJ and Ischiropoulos H. Nitric oxide chemistry and cellular signaling. J Cell Physiol 187: 277-282, 2001. (Pubitemid 32378352)
48. Greenberg GR, Feagan BG, Martin F, Sutherland LR, Thomson AB, Williams CN, Nilsson LG, and Persson T. Oral budesonide for active Crohn's disease. Canadian Inflammatory Bowel Disease Study Group. N Engl J Med 331: 836-841, 1994. (Pubitemid 24289710)
49. Greenberg GR, Feagan BG, Martin F, Sutherland LR, Thomson AB, Williams CN, Nilsson LG, and Persson T. Oral budesonide as maintenance treatment for Crohn's disease: A placebo-controlled, dose-ranging study. Canadian Inflammatory Bowel Disease Study Group. Gastroenterology 110: 45-51, 1996. (Pubitemid 26021603)
50. Hamer HM, Jonkers DM, Bast A, Vanhoutvin SA, Fischer MA, Kodde A, Troost FJ, Venema K, and Brummer RJ. Butyrate modulates oxidative stress in the colonic mucosa of healthy humans. Clin Nutr 28: 88-93, 2009.
51. Han X, Fink MP, and Delude RL. Proinflammatory cytokines cause NO$-dependent and-independent changes in expression and localization of tight junction proteins in intestinal epithelial cells. Shock 19: 229-237, 2003.
52. Hancock JT, Desikan R, and Neill SJ. Role of reactive oxygen species in cell signalling pathways. Biochem Soc Trans 29: 345-350, 2001. (Pubitemid 32587530)
53. Hayashi Y, Aoyagi K, Morita I, Yamamoto C, and Sakisaka S. Oral administration of mesalazine protects against mucosal injury and permeation in dextran sulfate sodiuminduced colitis in rats. Scand J Gastroenterol 44: 1323-1331, 2009.
54. 2 cytokine in ulcerative colitis that affects epithelial tight junctions, apoptosis, and cell restitution. Gastroenterology 129: 550-564, 2005. (Pubitemid 41096643)
55. Hendricks KM and Walker WA. Zinc deficiency in inflammatory bowel disease. Nutr Rev 46: 401-408, 1988.
56. Holmes JL, van Itallie CM, Rasmussen JE, and Anderson JM. Claudin profiling in the mouse during postnatal intestinal development and along the gastrointestinal tract reveals complex expression patterns. Gene Expr Patterns 6: 581-588, 2006.
57. Howe KL, Reardon C, Wang A, Nazli A, and McKay DM. Transforming growth factor-beta regulation of epithelial tight junction proteins enhances barrier function and blocks enterohemorrhagic Escherichia coli O157:H7-induced increased permeability. Am J Pathol 167: 1587-1597, 2005. (Pubitemid 41713312)
58. Katahira J, Sugiyama H, Inoue N, Horiguchi Y, Matsuda M, and Sugimoto N. Clostridium perfringens enterotoxin utilizes two structurally related membrane proteins as functional receptors in vivo. J Biol Chem 272: 26652-26658, 1997. (Pubitemid 27458889)
59. Katsube T, Tsuji H, and Onoda M. Nitric oxide attenuates hydrogen peroxide-induced barrier disruption and protein tyrosine phosphorylation in monolayers of intestinal epithelial cell. Biochim Biophys Acta 1773: 794-803, 2007. (Pubitemid 46829436)
60. Keshavarzian A, Banan A, Farhadi A, Komanduri S, Mutlu E, Zhang Y, and Fields JZ. Increases in free radicals and cytoskeletal protein oxidation and nitration in the colon of patients with inflammatory bowel disease. Gut 52: 720-728, 2003. (Pubitemid 36528876)
61. Kruidenier L, Kuiper I, Lamers CB, and Verspaget HW. Intestinal oxidative damage in inflammatory bowel disease: Semi-quantification, localization, and association with mucosal antioxidants. J Pathol 201: 28-36, 2003. (Pubitemid 37121200)
62. Kruidenier L, Kuiper I, van Duijn W, Marklund SL, van Hogezand RA, Lamers CB, and Verspaget HW. Differential mucosal expression of three superoxide dismutase isoforms in inflammatory bowel disease. J Pathol 201: 7-16, 2003. (Pubitemid 37121198)
63. Le'Negrate G, Selva E, Auberger P, Rossi B, and Hofman P. Sustained polymorphonuclear leukocyte transmigration induces apoptosis in T84 intestinal epithelial cells. J Cell Biol 150: 1479-1488, 2000.
64. Li N, Gu L, Qu L, Gong J, Li Q, Zhu W, and Li J. Berberine attenuates pro-inflammatory cytokine-induced tight junction disruption in an in vitro model of intestinal epithelial cells. Eur J Pharm Sci 40: 1-8, 2010.
65. Linehan JD, Kolios G, Valatas V, Robertson DA, and Westwick J. Effect of corticosteroids on nitric oxide production in inflammatory bowel disease: Are leukocytes the site of action? Am J Physiol Gastrointest Liver Physiol 288: G261-267, 2005. (Pubitemid 40129577)
66. MacDonald TT, Hutchings P, Choy MY, Murch S, and Cooke A. Tumour necrosis factor-alpha and interferongamma production measured at the single cell level in normal and inflamed human intestine. Clin Exp Immunol 81: 301-305, 1990. (Pubitemid 20242538)
67. Mankertz J, Amasheh M, Krug SM, Fromm A, Amasheh S, Hillenbrand B, Tavalali S, Fromm M, and Schulzke JD. TNFalpha up-regulates claudin-2 expression in epithelial HT-29/B6 cells via phosphatidylinositol-3-kinase signaling. Cell Tissue Res 336: 67-77, 2009.
68. Mankertz J, Tavalali S, Schmitz H, Mankertz A, Riecken EO, Fromm M, and Schulzke JD. Expression from the human occludin promoter is affected by tumor necrosis factor alpha and interferon gamma. J Cell Sci 113: 2085-2090, 2000. (Pubitemid 30386512)
69. Markov AG, Veshnyakova A, Fromm M, Amasheh M, and Amasheh S. Segmental expression of claudin proteins correlates with tight junction barrier properties in rat intestine. J Comp Physiol B 180: 591-598, 2010.
70. McKaig BC, Makh SS, Hawkey CJ, Podolsky DK, and Mahida YR. Normal human colonic subepithelial myofibroblasts enhance epithelial migration (restitution) via TGF-beta3. Am J Physiol 276: G1087-1093, 1999. (Pubitemid 29251906)
71. Mennigen R, Nolte K, Rijcken E, Utech M, Loeffler B, Senninger N, and Bruewer M. Probiotic mixture VSL#3 protects the epithelial barrier by maintaining tight junction protein expression and preventing apoptosis in a murine model of colitis. Am J Physiol Gastrointest Liver Physiol 296: G1140-1149, 2009.
72. Miralles-Barrachina O, Savoye G, Belmonte-Zalar L, Hochain P, Ducrotté P, Hecketsweiler B, Lerebours E, and Déchelotte P. Low levels of glutathione in endoscopic biopsies of patients with Crohn's colitis: The role of malnutrition. Clin Nutr 18: 313-317, 1999. (Pubitemid 29527742)
73. Montalto M, Cuoco L, Ricci R, Maggiano N, Vecchio FM, and Gasbarrini G. Immunohistochemical analysis of ZO-1 in the duodenal mucosa of patients with untreated and treated celiac disease. Digestion 65: 227-233, 2002.
74. Münch A, Söderholm JD, Wallon C, Ost A, Olaison G, and Ström M. Dynamics of mucosal permeability and inflammation in collagenous colitis before, during, and after loop ileostomy. Gut 54: 1126-1128, 2005.
75. Muza-Moons MM, Schneeberger EE, and Hecht GA. Enteropathogenic Escherichia coli infection leads to appearance of aberrant tight junctions strands in the lateral membrane of intestinal epithelial cells. Cell Microbiol 6: 783-793, 2004. (Pubitemid 39077384)
76. Naito Y, Takagi T, and Yoshikawa T. Molecular fingerprints of neutrophil-dependent oxidative stress in inflammatory bowel disease. J Gastroenterol 42: 787-798, 2007. (Pubitemid 47617456)
77. Nathan C. Nitric oxide as a secretory product of mammalian cells. FASEB J 6: 3051-3064, 1992.
78. Nusrat A, von Eichel-Streiber C, Turner JR, Verkade P, Madara JL, and Parkos CA. Clostridium difficile toxins disrupt epithelial barrier function by altering membrane microdomain localization of tight junction proteins. Infect Immun 69: 1329-1336, 2001. (Pubitemid 32187577)
79. Olesen M, Middelveld R, Bohr J, Tysk C, Lundberg JO, Eriksson S, Alving K, and Jä rnerot G. Luminal nitric oxide and epithelial expression of inducible and endothelial nitric oxide synthase in collagenous and lymphocytic colitis. Scand J Gastroenterol 38: 66-72, 2003. (Pubitemid 36152867)
80. Oliveira-Brett AM and Diculescu VC. Electrochemical study of quercetin-DNA interactions: Part I. Analysis in incubated solutions. Bioelectrochemistry 64: 133-141, 2004. (Pubitemid 39013957)
81. Oshima T, Sasaki M, Kataoka H, Miwa H, Takeuchi T, and Joh T. Wip1 protects hydrogen peroxide-induced colonic epithelial barrier dysfunction. Cell Mol Life Sci 64: 3139-3147, 2007. (Pubitemid 351152235)
82. Overgaard CE, Daugherty BL, Mitchell LA, and Koval M. Claudins: control of barrier function and regulation in response to oxidant stress. Antioxid Redox Signal 15: 1179-1193, 2011.
83. Pandey MK, Sung B, Kunnumakkara AB, Sethi G, Chaturvedi MM, and Aggarwal BB. Berberine modifies cysteine 179 of IkappaBalpha kinase, suppresses nuclear factor-kappaB-regulated antiapoptotic gene products, and potentiates apoptosis. Cancer Res 68: 5370-5379, 2008.
84. Pizzuti D, Bortolami M, Mazzon E, Buda A, Guariso G, D'Odorico A, Chiarelli S, D'Incà R, De Lazzari F, and Martines D. Transcriptional downregulation of tight junction protein ZO-1 in active coeliac disease is reversed after a gluten-free diet. Dig Liver Dis 36: 337-341, 2004. (Pubitemid 41115464)
85. Place RF, Noonan EJ, and Giardina C. HDAC inhibition prevents NF-kappa B activation by suppressing proteasome activity: Down-regulation of proteasome subunit expression stabilizes I kappa B alpha. Biochem Pharmacol 70: 394-406, 2005. (Pubitemid 40905111)
86. Planchon SM, Martins CA, Guerrant RL, and Roche JK. Regulation of intestinal epithelial barrier function by TGFbeta 1. Evidence for its role in abrogating the effect of a T cell cytokine. J Immunol 153: 5730-5739, 1994. (Pubitemid 24377709)
87. Plein K and Hotz J. Therapeutic effects of Saccharomyces boulardii on mild residual symptoms in a stable phase of Crohn's disease with special respect to chronic diarrhea-A pilot study. Z Gastroenterol 31: 129-134, 1993. (Pubitemid 23087390)
88. Prasad AS, Bao B, Beck FW, Kucuk O, and Sarkar FH. Antioxidant effect of zinc in humans. Free Radic Biol Med 37:1182-1190, 2004. (Pubitemid 39296743)
89. Prasad S, Mingrino R, Kaukinen K, Hayes KL, Powell RM, MacDonald TT, and Collins JE. Inflammatory processes have differential effects on claudins 2, 3, and 4 in colonic epithelial cells. Lab Invest 85: 1139-1162, 2005. (Pubitemid 43073987)
90. Rahner C, Mitic LL, and Anderson JM. Heterogeneity in expression and subcellular localization of claudins 2, 3, 4, and 5 in the rat liver, pancreas, and gut. Gastroenterology 120: 411-422, 2001. (Pubitemid 32147639)
91. Rao RK, Basuroy S, Rao VU, Karnaky Jr KJ, and Gupta A. Tyrosine phosphorylation and dissociation of occludin-ZO-1 and E-cadherin-beta-catenin complexes from the cytoskeleton by oxidative stress. Biochem J 368: 471-481, 2002. (Pubitemid 35454525)
92. Rembacken BJ, Snelling AM, Hawkey PM, Chalmers DM, and Axon AT. Non-pathogenic Escherichia coli versus mesalazine for the treatment of ulcerative colitis: A randomised trial. Lancet 354: 635-639, 1999. (Pubitemid 29391428)
93. Rice-Evans CA, Miller NJ, and Paganga G. Structureantioxidant activity relationships of flavonoids and phenolic acids. Free Radic Biol Med 20: 933-956, 1996. (Pubitemid 26157509)
94. Rodríguez-Cabezas ME, Gálvez J, Lorente MD, Concha A, Camuesco D, Azzouz S, Osuna A, Redondo L, and Zarzuelo A. Dietary fiber down-regulates colonic tumor necrosis factor alpha and nitric oxide production in trinitrobenzenesulfonic acid-induced colitic rats. J Nutr 132: 3263-3271, 2002.
95. Rosenthal R, Milatz S, Krug SM, Oelrich B, Schulzke JD, Amasheh S, Günzel D, and Fromm M. Claudin-2, a component of the tight junction, forms a paracellular water channel. J Cell Sci 123: 1913-1921, 2010.
96. Rosignoli P, Fabiani R, De Bartolomeo A, Spinozzi F, Agea E, Pelli MA, and Morozzi G. Protective activity of butyrate on hydrogen peroxide-induced DNA damage in isolated human colonocytes and HT29 tumour cells. Carcinogenesis 22: 1675-1680, 2001. (Pubitemid 32952146)
97. Ruan EA, Rao S, Burdick JS, Stryker SJ, Telford GL, Otterson MF, Opara EC, and Koch TR. Glutathione levels in chronic inflammatory disorders of the human colon. Nutr Res 17: 463-463, 1997.
98. Rutgeerts P, Sandborn WJ, Feagan BG, Reinisch W, Olson A, Johanns J, Travers S, Rachmilewitz D, Hanauer SB, Lichtenstein GR, de Villiers WJ, Present D, Sands BE, and Colombel JF. Infliximab for induction and maintenance therapy for ulcerative colitis. N Engl J Med 353: 2462-2476, 2005. (Pubitemid 41770166)
99. Sander GR, Cummins AG, Henshall T, and Powell BC. Rapid disruption of intestinal barrier function by gliadin involves altered expression of apical junctional proteins. FEBS Lett 579: 4851-4855, 2005. (Pubitemid 41218674)
100. Schmitz H, Barmeyer C, Fromm M, Runkel N, Foss HD, Bentzel CJ, Riecken EO, and Schulzke JD. Altered tight junction structure contributes to the impaired epithelial barrier function in ulcerative colitis. Gastroenterology 116: 301-309, 1999. (Pubitemid 29055352)
101. Schreck R, Rieber P, and Baeuerle PA. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-.1. EMBO J 10: 2247-2258,1991. (Pubitemid 21905698)
102. Schulzke JD, Bentzel CJ, Schulzke I, Riecken EO, and Fromm M. Epithelial tight junction structure in the jejunum of children with acute and treated celiac sprue. Pediatr Res 43: 435-441, 1998. (Pubitemid 28157949)
103. Schulzke JD, Bojarski C, Zeissig S, Heller F, Gitter AH, and Fromm M. Disrupted barrier function through epithelial cell apoptosis. Ann NY Acad Sci 1072: 288-299, 2006. (Pubitemid 44448461)
104. Schulzke JD, Schulzke I, Fromm M, and Riecken EO. Epithelial barrier and ion transport in coeliac sprue: Electrical measurements on intestinal aspiration biopsy specimens. Gut 37: 777-782, 1995.
105. Schürmann G, Brüwer M, Klotz A, Schmid KW, Senninger N, and Zimmer KP. Transepithelial transport processes at the intestinal mucosa in inflammatory bowel disease. Int J Colorectal Dis 14: 41-46, 1999. (Pubitemid 29295302)
106. Segain JP, Raingeard de la Blétière D, Bourreille A, Leray V, Gervois N, Rosales C, Ferrier L, Bonnet C, Blottière HM, and Galmiche JP. Butyrate inhibits inflammatory responses through NFkappaB inhibition: Implications for Crohn's disease. Gut 47: 397-403, 2000.
107. Sempértegui F, Díaz M, Mejía R, Rodríguez- Mora OG, Rentería E, Guarderas C, Estrella B, Recalde R, Hamer DH, and Reeves PG. Low concentrations of zinc in gastric mucosa are associated with increased severity of Helicobacter pylori-induced inflammation. Helicobacter 12: 43-48, 2007.
108. Seth A, Yan F, Polk DB, and Rao RK. Probiotics ameliorate the hydrogen peroxide-induced epithelial barrier disruption by a PKC-and MAP kinase-dependent mechanism. Am J Physiol Gastrointest Liver Physiol 294: G1060-1069, 2008. (Pubitemid 351520059)
109. Shirwaikar A, Shirwaikar A, Rajendran K, and Punitha IS. In vitro antioxidant studies on the benzyl tetra isoquinoline alkaloid berberine. Biol Pharm Bull 29: 1906-1910, 2006. (Pubitemid 44338416)
110. Simonovic I, Rosenberg J, Koutsouris A, and Hecht G. Enteropathogenic E. coli dephosphorylates and dissociates occludin from intestinal epithelial tight junctions. Cell Microbiol 2: 305-315, 2000. (Pubitemid 30612940)
111. Söderholm JD, Streutker C, Yang PC, Paterson C, Singh PK, McKay DM, Sherman PM, Croitoru K, and Perdue MH. Increased epithelial uptake of protein antigens in the ileum of Crohn's disease mediated by tumour necrosis factor alpha. Gut 53: 1817-1824, 2004. (Pubitemid 39556903)
112. Sträter J, Wellisch I, Riedl S, Walczak H, Koretz K, Tandara A, Krammer PH, and Möller P. CD95 (APO-1/Fas)-mediated apoptosis in colon epithelial cells: A possible role in ulcerative colitis. Gastroenterology 113:160-167, 1997.
113. Sturniolo GC, Di Leo V, Ferronato A, D'Odorico A, and D'Incà R. Zinc supplementation tightens "leaky gut" in Crohn's disease. Inflamm Bowel Dis 7: 94-98, 2001. (Pubitemid 32998495)
114. Sutherland LR, Martin F, Bailey RJ, Fedorak RN, Poleski M, Dallaire C, Rossman R, Saibil F, and Lariviere L. A randomized, placebo-controlled, double-blind trial of mesalamine in the maintenance of remission of Crohn's disease. The Canadian Mesalamine for Remission of Crohn's Disease Study Group. Gastroenterology 112: 1069-1077, 1997. (Pubitemid 27157516)
115. Szakál DN, Gyorffy H, Arató A, Cseh A, Molnár K, Papp M, Dezsofi A, and Veres G. Mucosal expression of claudins 2, 3, and 4 in proximal and distal part of duodenum in children with coeliac disease. Virchows Arch 456: 245-250, 2010.
116. Tagkalidis PP, Gibson PR, and Bhathal PS. Microscopic colitis demonstrates a T helper cell type 1 mucosal cytokine profile. J Clin Pathol 60: 382-387, 2007. (Pubitemid 46596556)
117. Troeger H, Epple HJ, Schneider T, Wahnschaffe U, Ullrich R, Burchard GD, Jelinek T, Zeitz M, Fromm M, and Schulzke JD. Effect of chronic Giardia lamblia infection on epithelial transport and barrier function in human duodenum. Gut 56: 328-335, 2007. (Pubitemid 46579759)
118. Troeger H, Loddenkemper C, Schneider T, Schreier E, Epple HJ, Zeitz M, Fromm M, and Schulzke JD. Structural and functional changes of the duodenum in human norovirus infection. Gut 58: 1070-1077, 2009.
119. Troeger H, Richter JF, Beutin L, Gü nzel D, Dobrindt U, Epple HJ, Gitter AH, Zeitz M, Fromm M, and Schulzke JD. Escherichia coli a-haemolysin induces focal leaks in colonic epithelium: A novel mechanism of bacterial translocation. Cell Microbiol 9: 2530-2540, 2007. (Pubitemid 47365655)
120. Unno N, Menconi MJ, Smith M, and Fink MP. Nitric oxide mediates interferon-gamma-induced hyperpermeability in cultured human intestinal epithelial monolayers. Crit Care Med 23: 1170-1176, 1995.
121. Venturi A, Gionchetti P, Rizzello F, Johansson R, Zucconi E, Brigidi P, Matteuzzi D, and Campieri M. Impact on the composition of the faecal flora by a new probiotic preparation: Preliminary data on maintenance treatment of patients with ulcerative colitis. Aliment Pharmacol Ther 13: 1103-1108, 1999. (Pubitemid 29374113)
122. Vogelsang H, Schwarzenhofer M, and Oberhuber G. Changes in gastrointestinal permeability in celiac disease. Dig Dis 16: 333-336, 1998. (Pubitemid 128525938)
123. Waetzig GH, Seegert D, Rosenstiel P, Nikolaus S, and Schreiber S. p38 mitogen-activated protein kinase is activated and linked to TNF-alpha signaling in inflammatory bowel disease. J Immunol 168: 5342-5351, 2002. (Pubitemid 34496003)
124. Waeytens A, De Vos M, and Laukens D. Evidence for a potential role of metallothioneins in inflammatory bowel diseases. Mediators Inflamm 2009 Article ID: 729172, 2009.
125. Wang N, Yu H, Ma J, Wu W, Zhao D, Shi X, Tian H, and Jiang H. Evidence for tight junction protein disruption in intestinal mucosa of malignant obstructive jaundice patients. Scand J Gastroenterol 45: 191-199, 2010.
126. van der Wouden EJ, Karrenbeld A, Kleibeuker JH, and Dijkstra G. Microscopic colitis: An unfamiliar but treatable disease. Neth J Med 67: 41-45, 2009.
127. Wu Z, Nybom P, and Magnusson KE. Distinct effects of Vibrio cholerae haemagglutinin/protease on the structure and localization of the tight junction-associated proteins occludin and ZO-1. Cell Microbiol 2: 11-17, 2000. (Pubitemid 30225063)
128. Yamada T and Grisham MB. Role of neutrophil-derived oxidants in the pathogenesis of intestinal inflammation. Klin Wochenschr 69: 988-994, 1991.
129. Yan F and Polk DB. Probiotic bacterium prevents cytokineinduced apoptosis in intestinal epithelial cells. J Biol Chem 277: 50959-50965, 2002. (Pubitemid 36042264)
130. Youakim A and Ahdieh M. Interferon-gamma decreases barrier function in T84 cells by reducing ZO-1 levels and disrupting apical actin. Am J Physiol 276: G1279-1288, 1999. (Pubitemid 29251928)
131. Yuan H, Gong A, and Young CY. Involvement of transcription factor Sp1 in quercetin-mediated inhibitory effect on the androgen receptor in human prostate cancer cells. Carcinogenesis 26: 793-801, 2005. (Pubitemid 41214342)
132. Zeissig S, Bojarski C, Buergel N, Mankertz J, Zeitz M, Fromm M, and Schulzke JD. Downregulation of epithelial apoptosis and barrier repair in active Crohn's disease by tumour necrosis factor alpha antibody treatment. Gut 53: 1295-1302, 2004. (Pubitemid 39120115)
133. Zeissig S, Bürgel N, Günzel D, Richter J, Mankertz J, Wahnschaffe U, Kroesen AJ, Zeitz M, Fromm M, and Schulzke JD. 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 56: 61-72, 2007. (Pubitemid 46044890)
134. Zhang B and Guo Y. Supplemental zinc reduced intestinal permeability by enhancing occludin and zonula occludens protein-1 (ZO-1) expression in weaning piglets. Br J Nutr 102: 687-693, 2009.
135. Zhou H and Mineshita S. The effect of berberine chloride on experimental
136. Zhou L, Wang X, Shao L, Yang Y, Shang W, Yuan G, Jiang B, Li F, Tang J, Jing H, and Chen M. Berberine acutely inhibits insulin secretion from beta-cells through 3',5'-cyclic adenosine 5'-monophosphate signaling pathway. Endocrinology 149: 4510-4518, 2008.