Claudin-related intestinal diseases

Seminars in Cell and Developmental Biology

Volumn 42, Issue , 2015, Pages 30-38

  Barmeyer, Christian ^a   Schulzke, Jörg D ^a   Fromm, Michael ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Claudin; Inflammatory bowel disease; Intestinal disease; Intestine; Tight junction

Indexed keywords

CLAUDIN; WATER;

CAMPYLOBACTER ENTERITIS; CELIAC DISEASE; CELL TRANSPORT; CHOLESTATIC LIVER DISEASE; CLOSTRIDIUM PERFRINGENS INFECTION; CROHN DISEASE; ENTEROPATHY; ENZYME INHIBITION; GALLSTONE; GENE MUTATION; HUMAN; IRRITABLE COLON; LIVER DISEASE; MACROMOLECULE; MICROSCOPIC COLITIS; MOLECULAR PATHOLOGY; NONHUMAN; PROTEIN FUNCTION; REVIEW; SOLUTE; ULCERATIVE COLITIS; WATER TRANSPORT; ANIMAL; CLOSTRIDIUM INFECTION; INTESTINE MUCOSA; METABOLISM; PATHOPHYSIOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; CLAUDINS; CLOSTRIDIUM INFECTIONS; HUMANS; INTESTINAL DISEASES; INTESTINAL MUCOSA;

EID: 84940895720     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2015.05.006     Document Type: Review

References (104)

1. Furuse M., Fujita K., Hiiragi T., Fujimoto K., Tsukita S. Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J Cell Biol 1998, 141:1539-1550.
2. Mineta K., Yamamoto Y., Yamazaki Y., Tanaka H., Tada Y., Saito K., et al. Predicted expansion of the claudin multigene family. FEBS Lett 2011, 585:606-612.
3. Günzel D., Yu A.S. Claudins and the modulation of tight junction permeability. Physiol Rev 2013, 93:525-569.
4. Krug S.M., Schulzke J.D., Fromm M. Tight junction, selective permeability, and related diseases. Semin Cell Dev Biol 2014, 36:166-176.
5. Stokes C.S., Krawczyk M., Lammert F. Gallstones: environment, lifestyle and genes. Dig Dis 2011, 29:191-201.
6. van Erpecum K.J., van Berge Henegouwen G.P., Stoelwinder B., Schmidt Y.M., Willekens F.L. Bile concentration is a key factor for nucleation of cholesterol crystals and cholesterol saturation index in gallbladder bile of gallstone patients. Hepatology 1990, 11:1-6.
7. Amasheh S., Meiri N., Gitter A.H., Schöneberg T., Mankertz J., Schulzke J.D., et al. Claudin-2 expression induces cation-selective channels in tight junctions of epithelial cells. J Cell Sci 2002, 115:4969-4976.
8. Furuse M., Furuse K., Sasaki H., Tsukita S. 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.
9. Rosenthal R., Milatz S., Krug S.M., Oelrich B., Schulzke J.D., Amasheh S., et al. Claudin-2, a component of the tight junction, forms a paracellular water channel. J Cell Sci 2010, 123:1913-1921.
10. Matsumoto K., Imasato M., Yamazaki Y., Tanaka H., Watanabe M., Eguchi H., et al. Claudin 2 deficiency reduces bile flow and increases susceptibility to cholesterol gallstone disease in mice. Gastroenterology 2014, 147:1134-1145.
11. Matsuzaki T., Tajika Y., Ablimit A., Aoki T., Hagiwara H., Takata K. Aquaporins in the digestive system. Med Electron Microsc 2004, 37:71-80.
12. Schmitz H., Barmeyer C., Fromm M., Runkel N., Foss H.D., Bentzel C.J., et al. Altered tight junction structure contributes to the impaired epithelial barrier function in ulcerative colitis. Gastroenterology 1999, 116:301-309.
13. Inai T., Kobayashi J., Shibata Y. Claudin-1 contributes to the epithelial barrier function in MDCK cells. Eur J Cell Biol 1999, 78:849-855.
14. Oshima T., Miwa H., Joh T. Changes in the expression of claudins in active ulcerative colitis. J Gastroenterol Hepatol 2008, 23(Suppl. 2):S146-S150.
15. Poritz L.S., Harris L.R., Kelly A.A., Koltun W.A. Increase in the tight junction protein claudin-1 in intestinal inflammation. Dig Dis Sci 2011, 56:2802-2809.
16. Weber C.R., Nalle S.C., Tretiakova M., Rubin D.T., Turner J.R. Claudin-1 and claudin-2 expression is elevated in inflammatory bowel disease and may contribute to early neoplastic transformation. Lab Investig 2008, 88:1110-1120.
17. Heller F., Florian P., Bojarski C., Richter J., Christ M., Hillenbrand B., et al. Interleukin-13 is the key effector Th2 cytokine in ulcerative colitis that affects epithelial tight junctions, apoptosis, and cell restitution. Gastroenterology 2005, 129:550-564.
18. Hering N.A., Schulzke J.D. Therapeutic options to modulate barrier defects in inflammatory bowel disease. Dig Dis 2009, 27:450-454.
19. Rosen M.J., Frey M.R., Washington M.K., Chaturvedi R., Kuhnhein L.A., Matta P., et al. STAT6 activation in ulcerative colitis: a new target for prevention of IL-13-induced colon epithelial cell dysfunction. Inflamm Bowel Dis 2011, 17:2224-2234.
20. Weber C.R., Raleigh D.R., Su L., Shen L., Sullivan E.A., Wang Y., et al. Epithelial myosin light chain kinase activation induces mucosal interleukin-13 expression to alter tight junction ion selectivity. J Biol Chem 2010, 285:12037-12046.
21. Prasad S., Mingrino R., Kaukinen K., Hayes K.L., Powell R.M., MacDonald T.T., et al. Inflammatory processes have differential effects on claudins 2, 3 and 4 in colonic epithelial cells. Lab Investig 2005, 85:1139-1162.
22. Suzuki T., Yoshinaga N., Tanabe S. Interleukin-6 (IL-6) regulates claudin-2 expression and tight junction permeability in intestinal epithelium. J Biol Chem 2011, 286:31263-31271.
23. Milatz S., Krug S.M., Rosenthal R., Günzel D., Müller D., Schulzke J.D., et al. Claudin-3 acts as a sealing component of the tight junction for ions of either charge and uncharged solutes. Biochim Biophys Acta 2010, 1798:2048-2057.
24. Thuijls G., Derikx J.P., de Haan J.J., Grootjans J., de Bruine A., Masclee A.A., et al. Urine-based detection of intestinal tight junction loss. J Clin Gastroenterol 2010, 44:e14-e19.
25. Zeissig S., Bürgel N., Günzel D., Richter J., Mankertz J., Wahnschaffe U., 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.
26. Lu Z., Ding L., Lu Q., Chen Y.H. Claudins in intestines: distribution and functional significance in health and diseases. Tissue Barriers 2013, 1:e24978.
27. Kucharzik T., Walsh S.V., Chen J., Parkos C.A., Nusrat A. Neutrophil transmigration in inflammatory bowel disease is associated with differential expression of epithelial intercellular junction proteins. Am J Pathol 2001, 159:2001-2009.
28. Goswami P., Das P., Verma A.K., Prakash S., Das T.K., Nag T.C., et al. Are alterations of tight junctions at molecular and ultrastructural level different in duodenal biopsies of patients with celiac disease and Crohn's disease?. Virchows Arch 2014, 465:521-530.
29. Yu A.S., Enck A.H., Lencer W.I., Schneeberger E.E. Claudin-8 expression in Madin-Darby canine kidney cells augments the paracellular barrier to cation permeation. J Biol Chem 2003, 278:17350-17359.
30. Fischer A., Gluth M., Weege F., Pape U.F., Wiedenmann B., Baumgart D.C., et al. Glucocorticoids regulate barrier function and claudin expression in intestinal epithelial cells via MKP-1. Am J Physiol Gastrointest Liver Physiol 2014, 306:G218-G228.
31. Bürgel N., Bojarski C., Mankertz J., Zeitz M., Fromm M., Schulzke J.D. Mechanisms of diarrhea in collagenous colitis. Gastroenterology 2002, 123:433-443.
32. Barmeyer C., Troeger H., Bojarski C., Siegmund B., Fromm M., Schulzke J.D. Lymphocytic colitis-related diarrhea is caused by both, ERK1/2-dependent inhibition of the epithelial sodium channel (ENaC) and a claudin-induced barrier defect. Gastroenterology 2014, 146:S-475.
33. Barmeyer C., Erko I., Fromm A., Bojarski C., Allers K., Moos V., et al. Ion transport and barrier function are disturbed in microscopic colitis. Ann N Y Acad Sci 2012, 1258:143-148.
34. Matysiak-Budnik T., Candalh C., Dugave C., Namane A., Cellier C., Cerf-Bensussan N., et al. Alterations of the intestinal transport and processing of gliadin peptides in celiac disease. Gastroenterology 2003, 125:696-707.
35. Schumann M., Richter J.F., Wedell I., Moos V., Zimmermann-Kordmann M., Schneider T., et al. Mechanisms of epithelial translocation of the alpha(2)-gliadin-33mer in coeliac sprue. Gut 2008, 57:747-754.
36. Ciccocioppo R., Finamore A., Ara C., Di Sabatino A., Mengheri E., Corazza G.R. Altered expression, localization, and phosphorylation of epithelial junctional proteins in celiac disease. Am J Clin Pathol 2006, 125:502-511.
37. Schumann M., Kamel S., Pahlitzsch M.L., Lebenheim L., May C., Krauss M., et al. Defective tight junctions in refractory celiac disease. Ann N Y Acad Sci 2012, 1258:43-51.
38. Szakál D.N., Gyorffy H., Arató A., Cseh A., Molnár K., Papp M., et al. Mucosal expression of claudins 2, 3 and 4 in proximal and distal part of duodenum in children with coeliac disease. Virchows Arch 2010, 456:245-250.
39. van Elburg R.M., Uil J.J., Mulder C.J., Heymans H.S. Intestinal permeability in patients with coeliac disease and relatives of patients with coeliac disease. Gut 1993, 34:354-357.
40. Ménard S., Lebreton C., Schumann M., Matysiak-Budnik T., Dugave C., Bouhnik Y., et al. Paracellular versus transcellular intestinal permeability to gliadin peptides in active celiac disease. Am J Pathol 2012, 180:608-615.
41. Schulzke J.D., Schulzke I., Fromm M., Riecken E.O. Epithelial barrier and ion transport in coeliac sprue: electrical measurements on intestinal aspiration biopsy specimens. Gut 1995, 37:777-782.
42. Schulzke J.D., Bentzel C.J., Schulzke I., Riecken E.O., Fromm M. Epithelial tight junction structure in the jejunum of children with acute and treated celiac sprue. Pediatr Res 1998, 43:435-441.
43. Schumann M., Günzel D., Buergel N., Richter J.F., Troeger H., May C., et al. Cell polarity-determining proteins Par-3 and PP-1 are involved in epithelial tight junction defects in coeliac disease. Gut 2012, 61:220-228.
44. Utech M., Ivanov A.I., Samarin S.N., Bruewer M., Turner J.R., Mrsny R.J., et al. Mechanism of IFN-gamma-induced endocytosis of tight junction proteins: myosin II-dependent vacuolarization of the apical plasma membrane. Mol Biol Cell 2005, 16:5040-5052.
45. Bodd M., Raki M., Tollefsen S., Fallang L.E., Bergseng E., Lundin K.E., et al. HLA-DQ2-restricted gluten-reactive T cells produce IL-21 but not IL-17 or IL-22. Mucosal Immunol 2010, 3:594-601.
46. Caruso R., Marafini I., Sedda S., Del Vecchio Blanco G., Giuffrida P., MacDonald T.T., et al. Analysis of the cytokine profile in the duodenal mucosa of refractory coeliac disease patients. Clin Sci 2014, 126:451-458.
47. Wisner D.M., Harris L.R., Green C.L., Poritz L.S. Opposing regulation of the tight junction protein claudin-2 by interferon-gamma and interleukin-4. J Surg Res 2008, 144:1-7.
48. Willemsen L.E., Hoetjes J.P., van Deventer S.J., van Tol E.A. Abrogation of IFN-gamma mediated epithelial barrier disruption by serine protease inhibition. Clin Exp Immunol 2005, 142:275-284.
49. Van Itallie C.M., Fanning A.S., Anderson J.M. Reversal of charge selectivity in cation or anion-selective epithelial lines by expression of different claudins. Am J Physiol Renal Physiol 2003, 285:F1078-F1084.
50. + deficiency and glucose malabsorption in mouse small intestine. Gastroenterology 2011, 140:913-923.
51. [No authors listed]. Systematic review on the management of irritable bowel syndrome in the European Union. Eur J Gastroenterol Hepatol 2007; 19(Suppl. 1):S11-37.
52. Dunlop S.P., Hebden J., Campbell E., Naesdal J., Olbe L., Perkins A.C., et al. Abnormal intestinal permeability in subgroups of diarrhea-predominant irritable bowel syndromes. Am J Gastroenterol 2006, 101:1288-1294.
53. Marshall J.K., Thabane M., Garg A.X., Clark W., Meddings J., Collins S.M., et al. Intestinal permeability in patients with irritable bowel syndrome after a waterborne outbreak of acute gastroenteritis in Walkerton, Ontario. Aliment Pharmacol Ther 2004, 20:1317-1322.
54. Zhou Q., Zhang B., Verne G.N. Intestinal membrane permeability and hypersensitivity in the irritable bowel syndrome. Pain 2009, 146:41-46.
55. Chadwick V.S., Chen W., Shu D., Paulus B., Bethwaite P., Tie A., et al. Activation of the mucosal immune system in irritable bowel syndrome. Gastroenterology 2002, 122:1778-1783.
56. Martínez C., Vicario M., Ramos L., Lobo B., Mosquera J.L., Alonso C., et al. The jejunum of diarrhea-predominant irritable bowel syndrome shows molecular alterations in the tight junction signaling pathway that are associated with mucosal pathobiology and clinical manifestations. Am J Gastroenterol 2012, 107:736-746.
57. Piche T., Barbara G., Aubert P., Bruley des Varannes S., Dainese R., Nano J.L., et al. Impaired intestinal barrier integrity in the colon of patients with irritable bowel syndrome: involvement of soluble mediators. Gut 2009, 58:196-201.
58. Gecse K., Róka R., Séra T., Rosztóczy A., Annaházi A., Izbéki F., et al. Leaky gut in patients with diarrhea-predominant irritable bowel syndrome and inactive ulcerative colitis. Digestion 2012, 85:40-46.
59. Kong W.M., Gong J., Dong L., Xu J.R. Changes of tight junction claudin-1, -3, -4 protein expression in the intestinal mucosa in patients with irritable bowel syndrome. Nan Fang Yi Ke Da Xue Xue Bao 2007, 27:1345-1347.
60. Bertiaux-Vandaële N., Youmba S.B., Belmonte L., Lecleire S., Antonietti M., Gourcerol G., et al. The expression and the cellular distribution of the tight junction proteins are altered in irritable bowel syndrome patients with differences according to the disease subtype. Am J Gastroenterol 2011, 106:2165-2173.
61. Martínez C., Lobo B., Pigrau M., Ramos L., González-Castro A.M., Alonso C., et al. Diarrhoea-predominant irritable bowel syndrome: an organic disorder with structural abnormalities in the jejunal epithelial barrier. Gut 2013, 62:1160-1168.
62. Aerssens J., Camilleri M., Talloen W., Thielemans L., Göhlmann H.W., Van Den Wyngaert I., et al. Alterations in mucosal immunity identified in the colon of patients with irritable bowel syndrome. Clin Gastroenterol Hepatol 2008, 6:194-205.
63. Sankaran S., George M.D., Reay E., Guadalupe M., Flamm J., Prindiville T., et al. Rapid onset of intestinal epithelial barrier dysfunction in primary human immunodeficiency virus infection is driven by an imbalance between immune response and mucosal repair and regeneration. J Virol 2008, 82:538-545.
64. Brenchley J.M., Schacker T.W., Ruff L.E., Price D.A., Taylor J.H., Beilman G.J., et al. CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med 2004, 200:749-759.
65. Brenchley J.M., Price D.A., Schacker T.W., Asher T.E., Silvestri G., Rao S., et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 2006, 12:1365-1371.
66. Epple H.J., Allers K., Troeger H., Kühl A., Erben U., Fromm M., et al. Acute HIV infection induces mucosal infiltration with CD4+ and CD8+ T cells, epithelial apoptosis, and a mucosal barrier defect. Gastroenterology 2010, 139:1289-1300.
67. Epple H.J., Schneider T., Troeger H., Kunkel D., Allers K., Moos V., et al. Impairment of the intestinal barrier is evident in untreated but absent in suppressively treated HIV-infected patients. Gut 2009, 58:220-227.
68. Nazli A., Chan O., Dobson-Belaire W.N., Ouellet M., Tremblay M.J., Gray-Owen S.D., et al. Exposure to HIV-1 directly impairs mucosal epithelial barrier integrity allowing microbial translocation. PLoS Pathogens 2010, 6:e1000852.
69. Fackler O.T., Schäfer M., Schmidt W., Zippel T., Heise W., Schneider T., et al. HIV-1 p24 but not proviral load is increased in the intestinal mucosa compared with the peripheral blood in HIV-infected patients. AIDS 1998, 12:139-146.
70. Mattapallil J.J., Douek D.C., Hill B., Nishimura Y., Martin M., Roederer M. Massive infection and loss of memory CD4+ T cells in multiple tissues during acute SIV infection. Nature 2005, 434:1093-1097.
71. Clayton F., Kotler D.P., Kuwada S.K., Morgan T., Stepan C., Kuang J., et al. Gp120-induced Bob/GPR15 activation: a possible cause of human immunodeficiency virus enteropathy. Am J Pathol 2001, 159:1933-1939.
72. Buccigrossi V., Laudiero G., Nicastro E., Miele E., Esposito F., Guarino A. The HIV-1 transactivator factor (Tat) induces enterocyte apoptosis through a redox-mediated mechanism. PLoS ONE 2011, 6:e29436.
73. Kim C.J., Nazli A., Rojas O.L., Chege D., Alidina Z., Huibner S., et al. A role for mucosal IL-22 production and Th22 cells in HIV-associated mucosal immunopathogenesis. Mucosal Immunol 2012, 5:670-680.
74. Friedman C.R., Neimann J., Wegener H.C., Tauxe R.V. Epidemiology of Campylobacter jejuni infections in the United States and other industrialized nations. Campylobacter 2000, 121-138. ASM Press, Washington, DC. 2nd ed. I. Nachamkin, M.J. Blaser (Eds.).
75. Young K.T., Davis L.M., Dirita V.J. Campylobacter jejuni: molecular biology and pathogenesis. Nat Rev Microbiol 2007, 5:665-679.
76. Reed R.P., Friedland I.R., Wegerhoff F.O., Khoosal M. Campylobacter bacteremia in children. Pediatr Infect Dis J 1996, 15:345-348.
77. Mishu B., Ilyas A.A., Koski C.L., Vriesendorp F., Cook S.D., Mithen F.A., et al. Serologic evidence of previous Campylobacter jejuni infection in patients with the Guillain-Barré syndrome. Ann Intern Med 1993, 118:947-953.
78. Neal K.R., Hebden J., Spiller R. Prevalence of gastrointestinal symptoms six months after bacterial gastroenteritis and risk factors for development of the irritable bowel syndrome: postal survey of patients. Br Med J 1997, 314:779-782.
79. Backert S., Boehm M., Wessler S., Tegtmeyer N. Transmigration route of Campylobacter jejuni across polarized intestinal epithelial cells: paracellular, transcellular or both?. Cell Commun Signal 2013, 11:72.
80. Chen M.L., Ge Z., Fox J.G., Schauer D.B. Disruption of tight junctions and induction of proinflammatory cytokine responses in colonic epithelial cells by Campylobacter jejuni. Infect Immun 2006, 74:6581-6589.
81. Wine E., Chan V.L., Sherman P.M. Campylobacter jejuni mediated disruption of polarized epithelial monolayers is cell-type specific, time dependent, and correlates with bacterial invasion. Pediatr Res 2008, 64:599-604.
82. Bras A.M., Ketley J.M. Transcellular translocation of Campylobacter jejuni across human polarised epithelial monolayers. FEMS Microbiol Lett 1999, 179:209-215.
83. MacCallum A., Hardy S.P., Everest P.H. Campylobacter jejuni inhibits the absorptive transport functions of Caco-2 cells and disrupts cellular tight junctions. Microbiology 2005, 151:2451-2458.
84. Nielsen H.L., Nielsen H., Ejlertsen T., Engberg J., Günzel D., Zeitz M., et al. Oral and fecal Campylobacter concisus strains perturb barrier function by apoptosis induction in HT-29/B6 intestinal epithelial cells. PLoS ONE 2011, 6:e23858.
85. Scallan E., Hoekstra R.M., Angulo F.J., Tauxe R.V., Widdowson M.A., Roy S.L., et al. Foodborne illness acquired in the United States - major pathogens. Emerg Infect Dis 2011, 17:7-15.
86. Fujita K., Katahira J., Horiguchi Y., Sonoda N., Furuse M., Tsukita S. Clostridium perfringens enterotoxin binds to the second extracellular loop of claudin-3, a tight junction integral membrane protein. FEBS Lett 2000, 476:258-261.
87. Winkler L., Gehring C., Wenzel A., Müller S.L., Piehl C., Krause G., et al. Molecular determinants of the interaction between Clostridium perfringens enterotoxin fragments and claudin-3. J Biol Chem 2009, 284:18863-18872.
88. Kimura J., Abe H., Kamitani S., Toshima H., Fukui A., Miyake M., et al. Clostridium perfringens enterotoxin interacts with claudins via electrostatic attraction. J Biol Chem 2010, 285:401-408.
89. Holmes J.L., Van Itallie C.M., Rasmussen J.E., Anderson J.M. Claudin profiling in the mouse during postnatal intestinal development and along the gastrointestinal tract reveals complex expression patterns. Gene Expr Patterns 2006, 6:581-588.
90. Fujita H., Chiba H., Yokozaki H., Sakai N., Sugimoto K., Wada T., et al. Differential expression and subcellular localization of claudin-7, -8, -12, -13, and -15 along the mouse intestine. J Histochem Cytochem 2006, 54:933-944.
91. Saitoh Y., Suzuki H., Tani K., Nishikawa K., Irie K., Ogura Y., et al. Tight junctions, Structural insight into tight junction disassembly by Clostridium perfringens enterotoxin. Science 2015, 347:775-778.
92. Veshnyakova A., Piontek J., Protze J., Waziri N., Heise I., Krause G. Mechanism of Clostridium perfringens enterotoxin interaction with claudin-3/-4 protein suggests structural modifications of the toxin to target specific claudins. J Biol Chem 2012, 287:1698-1708.
93. Sonoda N., Furuse M., Sasaki H., Yonemura S., Katahira J., Horiguchi Y., et al. Clostridium perfringens enterotoxin fragment removes specific claudins from tight junction strands: Evidence for direct involvement of claudins in tight junction barrier. J Cell Biol 1999, 147:195-204.
94. Lohrberg D., Krause E., Schumann M., Piontek J., Winkler L., Blasig I.E., et al. A strategy for enrichment of claudins based on their affinity to Clostridium perfringens enterotoxin. BMC Mol Biol 2009, 10:61.
95. Chakrabarti G., McClane B.A. The importance of calcium influx, calpain and calmodulin for the activation of CaCo-2 cell death pathways by Clostridium perfringens enterotoxin. Cell Microbiol 2005, 7:129-146.
96. Chakrabarti G., Zhou X., McClane B.A. Death pathways activated in CaCo-2 cells by Clostridium perfringens enterotoxin. Infect Immun 2003, 71:4260-4270.
97. Singh U., Van Itallie C.M., Mitic L.L., Anderson J.M., McClane B.A. CaCo-2 cells treated with Clostridium perfringens enterotoxin form multiple large complex species, one of which contains the tight junction protein occludin. J Biol Chem 2000, 275:18407-18417.
98. Veshnyakova A., Protze J., Rossa J., Blasig I.E., Krause G., Piontek J. On the interaction of Clostridium perfringens enterotoxin with claudins. Toxins 2010, 2:1336-1356.
99. Furuse M., Hirase T., Itoh M., Nagafuchi A., Yonemura S., Tsukita S., et al. Occludin: a novel integral membrane protein localizing at tight junctions. J Cell Biol 1993, 123:1777-1788.
100. Lameris A.L., Huybers S., Kaukinen K., Makela T.H., Bindels R.J., Hoenderop J.G., et al. Expression profiling of claudins in the human gastrointestinal tract in health and during inflammatory bowel disease. Scand J Gastroenterol 2013, 48:58-69.
101. Troeger H., Epple H.J., Schneider T., Wahnschaffe U., Ullrich R., Burchard G.D., et al. Effect of chronic Giardia lamblia infection on epithelial transport and barrier function in human duodenum. Gut 2007, 56:328-335.
102. Sanada Y., Oue N., Mitani Y., Yoshida K., Nakayama H., Yasui W. Down-regulation of the claudin-18 gene, identified through serial analysis of gene expression data analysis, in gastric cancer with an intestinal phenotype. J Pathol 2006, 208:633-642.
103. Amasheh S., Dullat S., Fromm M., Schulzke J.D., Buhr H.J., Kroesen A.J. Inflamed pouch mucosa possesses altered tight junctions indicating recurrence of inflammatory bowel disease. Int J Colorectal Dis 2009, 24:1149-1156.
104. Németh Z., Szász A.M., Tátrai P., Németh J., Gyorffy H., Somorácz A., et al. Claudin-1, -2, -3, -4, -7, -8, and -10 protein expression in biliary tract cancers. J Histochem Cytochem 2009, 57:113-121.