Regulation of tight junction permeability by intestinal bacteria and dietary components

Journal of Nutrition

Volumn 141, Issue 5, 2011, Pages 769-776

  Ulluwishewa, Dulantha ^a,c   Anderson, Rachel C ^a   McNabb, Warren C ^b,c   Moughan, Paul J ^c   Wells, Jerry M ^d   Roy, Nicole C ^a,c  

^a Agri Foods and Health Section   (New Zealand)

^b AGRESEARCH GRASSLANDS   (New Zealand)

^c MASSEY UNIVERSITY   (New Zealand)

^d WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CLAUDIN; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MYOSIN LIGHT CHAIN KINASE; OCCLUDIN; PROBIOTIC AGENT; PROTEIN KINASE C; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

BACTERIAL STRAIN; CELL MEMBRANE PERMEABILITY; COMMENSAL; CYTOSKELETON; DIETARY INTAKE; ENVIRONMENT; HUMAN; INTESTINE EPITHELIUM; INTESTINE FLORA; INTESTINE MUCOSA PERMEABILITY; LIGHT CHAIN; NONHUMAN; PATHOGENESIS; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN STRUCTURE; REGULATORY MECHANISM; REVIEW; TIGHT JUNCTION;

ANIMALS; CELL MEMBRANE PERMEABILITY; DIET; GRAM-NEGATIVE BACTERIA; GRAM-POSITIVE BACTERIA; HOST-PATHOGEN INTERACTIONS; HUMANS; INTESTINAL MUCOSA; PROBIOTICS; SIGNAL TRANSDUCTION; TIGHT JUNCTIONS;

EID: 79955518664     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.3945/jn.110.135657     Document Type: Review

References (106)

1. Ley RE, Peterson DA, Gordon JI. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell. 2006;124:837-48.
2. Wells JM, Rossi O, Meijerink M, van Baarlen P. Microbes and Health Sackler Colloquium: epithelial crosstalk at the microbiota-mucosal interface. Proc Natl Acad Sci USA. Epub 2010 Sep 8.
3. Suenaert P, Bulteel V, Lemmens L, Noman M, Geypens B, Van Assche G, Geboes K, Ceuppens JL, Rutgeerts P. Anti-tumor necrosis factor treatment restores the gut barrier in Crohn's disease. Am J Gastro-enterol. 2002;97:2000-4.
4. Vogelsang H, Schwarzenhofer M, Oberhuber G. Changes in gastrointestinal permeability in celiac disease. Dig Dis. 1998;16:333-6.
5. Damci T, Nuhoglu I, Devranoglu G, Osar Z, Demir M, Ilkova H. Increased intestinal permeability as a cause of fluctuating postprandial blood glucose levels in Type 1 diabetic patients. Eur J Clin Invest. 2003;33:397-401.
6. Watts T, Berti I, Sapone A, Gerarduzzi T, Not T, Zielke R, Fasano A. Role of the intestinal tight junction modulator zonulin in the pathogenesis of type I diabetes in BB diabetic-prone rats. Proc Natl Acad Sci USA. 2005;102:2916-21.
7. Davin JC, Forget P, Mahieu PR. Increased intestinal permeability to (51 Cr) EDTA is correlated with IgA immune complex-plasma levels in children with IgA-associated nephropathies. Acta Paediatr Scand. 1988;77:118-24.
8. Wigg AJ, Roberts-Thomson IC, Dymock RB, McCarthy PJ, Grose RH, Cummins AG. The role of small intestinal bacterial overgrowth, intestinal permeability, endotoxaemia, and tumour necrosis factor alpha in the pathogenesis of non-alcoholic steatohepatitis. Gut. 2001;48:206-11.
9. Yacyshyn B, Meddings J, Sadowski D, Bowen-Yacyshyn MB. Multiple sclerosis patients have peripheral blood CD45RO+ B cells and increased intestinal permeability. Dig Dis Sci. 1996;41:2493-8.
10. Liu Z, Li N, Neu J. Tight junctions, leaky intestines, and pediatric diseases. Acta Paediatr. 2005;94:386-93.
11. Mullin JM, Valenzano MC, Verrecchio JJ, Kothari R. Age- and diet-related increase in transepithelial colon permeability of Fischer 344 rats. Dig Dis Sci. 2002;47:2262-70.
12. Saunders PR, Kosecka U, McKay DM, Perdue MH. Acute stressors stimulate ion secretion and increase epithelial permeability in rat intestine. Am J Physiol. 1994;267:G794-9.
13. Farquhar MG, Palade GE. Junctional complexes in various epithelia. J Cell Biol. 1963;17:375-412.
14. van der Flier LG, Clevers H. Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu Rev Physiol. 2009;71:241-60.
15. Perez-Moreno M, Fuchs E. Catenins: keeping cells from getting their signals crossed. Dev Cell. 2006;11:601-12.
16. Madara JL. Intestinal absorptive cell tight junctions are linked to cytoskeleton. Am J Physiol. 1987;253:C171-5.
17. Garrod D, Chidgey M. Desmosome structure, composition and function. Biochim Biophys Acta. 2008;1778:572-87.
18. Sosinsky GE, Nicholson BJ. Structural organization of gap junction channels. Biochim Biophys Acta. 2005;1711:99-125.
19. Banan A, Choudhary S, Zhang Y, Fields JZ, Keshavarzian A. Ethanol-induced barrier dysfunction and its prevention by growth factors in human intestinal monolayers: evidence for oxidative and cytoskeletal mechanisms. J Pharmacol Exp Ther. 1999;291:1075-85.
20. Chiba H, Osanai M, Murata M, Kojima T, Sawada N. Transmembrane proteins of tight junctions. Biochim Biophys Acta. 2008;1778:588-600.
21. Fanning AS, Jameson BJ, Jesaitis LA, Anderson JM. The tight junction protein ZO-1 establishes a link between the transmembrane protein occludin and the actin cytoskeleton. J Biol Chem. 1998;273:29745-53.
22. Furuse M. Molecular basis of the core structure of tight junctions. Cold Spring Harb Perspect Biol. 2010;2:a002907.
23. 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;141:1539-50.
24. Furuse M, Hirase T, Itoh M, Nagafuchi A, Yonemura S, Tsukita S, Tsukita S. Occludin: a novel integral membrane protein localizing at tight junctions. J Cell Biol. 1993;123:1777-88.
25. Ikenouchi J, Furuse M, Furuse K, Sasaki H, Tsukita S, Tsukita S. Tricellulin constitutes a novel barrier at tricellular contacts of epithelial cells. J Cell Biol. 2005;171:939-45.
26. Balda MS, Matter K. Transmembrane proteins of tight junctions. Semin Cell Dev Biol. 2000;11:281-9.
27. Furuse M, Sasaki H, Fujimoto K, Tsukita S. A single gene product, claudin-1 or -2, reconstitutes tight junction strands and recruits occludin in fibroblasts. J Cell Biol. 1998;143:391-401.
28. Bücker R, Schumann M, Amasheh S, Schulzke J-D. Claudins in intestinal function and disease. In: Yu ASL, editor. Current topics in membranes. Bulington (MA): Academic Press; 2010. p. 195-227.
29. Balda MS, Whitney JA, Flores C, González S, Cereijido M, Matter K. Functional dissociation of paracellular permeability and transepithelial electrical resistance and disruption of the apical-basolateral intra-membrane diffusion barrier by expression of a mutant tight junction membrane protein. J Cell Biol. 1996;134:1031-49.
30. Bazzoni G. The JAM family of junctional adhesion molecules. Curr Opin Cell Biol. 2003;15:525-30.
31. Martin-Padura I, Lostaglio S, Schneemann M, Williams L, Romano M, Fruscella P, Panzeri C, Stoppacciaro A, Ruco L, et al. Junctional adhesion molecule, a novel member of the immunoglobulin superfam-ily that distributes at intercellular junctions and modulates monocyte transmigration. J Cell Biol. 1998;142:117-27.
32. Cohen CJ, Shieh JT, Pickles RJ, Okegawa T, Hsieh JT, Bergelson JM. The coxsackievirus and adenovirus receptor is a transmembrane component of the tight junction. Proc Natl Acad Sci USA. 2001;98: 15191-6.
33. Bazzoni G, Martinez-Estrada OM, Orsenigo F, Cordenonsi M, Citi S, Dejana E. Interaction of junctional adhesion molecule with the tight junction components ZO-1, cingulin, and occludin. J Biol Chem. 2000; 275:20520-6.
34. Liu Y, Nusrat A, Schnell FJ, Reaves TA, Walsh S, Pochet M, Parkos CA. Human junction adhesion molecule regulates tight junction resealing in epithelia. J Cell Sci. 2000;113:2363-74.
35. Fanning AS, Anderson JM. PDZ domains: fundamental building blocks in the organization of protein complexes at the plasma membrane. J Clin Invest. 1999;103:767-72.
36. Itoh M, Furuse M, Morita K, Kubota K, Saitou M, Tsukita S. Direct binding of three tight junction-associated MAGUKs, ZO-1, ZO-2, and ZO-3, with the COOH termini of claudins. J Cell Biol. 1999;147: 1351-63.
37. Utepbergenov DI, Fanning AS, Anderson JM. Dimerization of the scaffolding protein ZO-1 through the second PDZ domain. J Biol Chem. 2006;281:24671-7.
38. Itoh M, Sasaki H, Furuse M, Ozaki H, Kita T, Tsukita S. Junctional adhesion molecule (JAM) binds to PAR-3: a possible mechanism for the recruitment of PAR-3 to tight junctions. J Cell Biol. 2001;154:491-7.
39. Fanning AS, Ma TY, Anderson JM. Isolation and functional characterization of the actin binding region in the tight junction protein ZO-1. FASEB J. 2002;16:1835-7.
40. Linnemann T, Geyer M, Jaitner BK, Block C, Kalbitzer HR, Wittinghofer A, Herrmann C. Thermodynamic and kinetic characterization of the interaction between the Ras binding domain of AF6 and members of the Ras subfamily. J Biol Chem. 1999;274:13556-62.
41. Stevenson BR, Anderson JM, Braun ID, Mooseker MS. Phosphoryl-ation of the tight-junction protein ZO-1 in two strains of Madin-Darby canine kidney cells which differ in transepithelial resistance. Biochem J. 1989;263:597-9.
42. Findley MK, Koval M. Regulation and roles for claudin-family tight junction proteins. IUBMB Life. 2009;61:431-7.
43. Wong V. Phosphorylation of occludin correlates with occludin localization and function at the tight junction. Am J Physiol. 1997;273:C1859-67.
44. Farhadi A, Keshavarzian A, Ranjbaran Z, Fields JZ, Banan A. The role of protein kinase C isoforms in modulating injury and repair of the intestinal barrier. J Pharmacol Exp Ther. 2006;316:1-7.
45. Song JC, Hanson CM, Tsai V, Farokhzad OC, Lotz M, Matthews JB. Regulation of epithelial transport and barrier function by distinct protein kinase C isoforms. Am J Physiol Cell Physiol. 2001;281:C649-61.
46. Cario E, Gerken G, Podolsky DK. Toll-like receptor 2 enhances ZO-1-associated intestinal epithelial barrier integrity via protein kinase C. Gastroenterology. 2004;127:224-38.
47. Plotnikov A, Zehorai E, Procaccia S, Seger R. The MAPK cascades: signaling components, nuclear roles and mechanisms of nuclear translocation. Biochim Biophys Acta. Epub 2010 Dec 16.
48. Basuroy S, Seth A, Elias B, Naren AP, Rao R. MAPK interacts with occludin and mediates EGF-induced prevention of tight junction disruption by hydrogen peroxide. Biochem J. 2006;393:69-77.
49. Turner JR, Rill BK, Carlson SL, Carnes D, Kerner R, Mrsny RJ, Madara JL. Physiological regulation of epithelial tight junctions is associated with myosin light-chain phosphorylation. Am J Physiol. 1997;273:C1378-85.
50. Scott KG, Meddings JB, Kirk DR, Lees-Miller SP, Buret AG. Intestinal infection with Giardia spp. reduces epithelial barrier function in a myosin light chain kinase-dependent fashion. Gastroenterology. 2002;123:1179-90.
51. Shen L, Black ED, Witkowski ED, Lencer WI, Guerriero V, Schneeberger EE, Turner JR. Myosin light chain phosphorylation regulates barrier function by remodeling tight junction structure. J Cell Sci. 2006;119:2095-106.
52. Nusrat A, Giry M, Turner JR, Colgan SP, Parkos CA, Carnes D, Lemichez E, Boquet P, Madara JL. Rho protein regulates tight junctions and perijunctional actin organization in polarized epithelia. Proc Natl Acad Sci USA. 1995;92:10629-33.
53. Kimura K, Ito M, Amano M, Chihara K, Fukata Y, Nakafuku M, Yamamori B, Feng J, Nakano T, et al. Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science. 1996;273:245-8.
54. Walsh SV, Hopkins AM, Chen J, Narumiya S, Parkos CA, Nusrat A. Rho kinase regulates tight junction function and is necessary for tight junction assembly in polarized intestinal epithelia. Gastroenterology. 2001;121:566-79.
55. Bruewer M, Hopkins AM, Hobert ME, Nusrat A, Madara JL, Rho A. Rac1, and Cdc42 exert distinct effects on epithelial barrier via selective structural and biochemical modulation of junctional proteins and F-actin. Am J Physiol Cell Physiol. 2004;287:C327-35.
56. Madsen K, Cornish A, Soper P, McKaigney C, Jijon H, Yachimec C, Doyle J, Jewell L, De Simone C. Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterology. 2001;121:580-91.
57. Gupta P, Andrew H, Kirschner BS, Guandalini S. Is lactobacillus GG helpful in children with Crohn's disease? Results of a preliminary, open-label study. J Pediatr Gastroenterol Nutr. 2000;31:453-7.
58. Zareie M, Johnson-Henry K, Jury J, Yang PC, Ngan BY, McKay DM, Soderholm JD, Perdue MH, Sherman PM. Probiotics prevent bacterial translocation and improve intestinal barrier function in rats following chronic psychological stress. Gut. 2006;55:1553-60.
59. Zyrek AA, Cichon C, Helms S, Enders C, Sonnenborn U, Schmidt MA. Molecular mechanisms underlying the probiotic effects of Escherichia coli Nissle 1917 involve ZO-2 and PKCzeta redistribution resulting in tight junction and epithelial barrier repair. Cell Microbiol. 2007; 9:804-16.
60. Ukena SN, Singh A, Dringenberg U, Engelhardt R, Seidler U, Hansen W, Bleich A, Bruder D, Franzke A, et al. Probiotic Escherichia coli Nissle 1917 inhibits leaky gut by enhancing mucosal integrity. PLoS ONE. 2007;2:e1308.
61. Ewaschuk JB, Diaz H, Meddings L, Diederichs B, Dmytrash A, Backer J, Looijer-van Langen M, Madsen KL. Secreted bioactive factors from Bifidobacterium infantis enhance epithelial cell barrier function. Am J Physiol Gastrointest Liver Physiol. 2008;295:G1025-34.
62. Anderson RC, Cookson AL, McNabb WC, Park Z, McCann MJ, Kelly WJ, Roy NC. Lactobacillus plantarum MB452 enhances the function of the intestinal barrier by increasing the expression levels of genes involved in tight junction formation. BMC Microbiol. 2010;10:316.
63. Karczewski J, Troost FJ, Konings I, Dekker J, Kleerebezem M, Brummer RJ, Wells JM. Regulation of human epithelial tight junction proteins by Lactobacillus plantarum in vivo and protective effects on the epithelial barrier. Am J Physiol Gastrointest Liver Physiol. 2010;298:G851-9.
64. Cario E, Gerken G, Podolsky DK. Toll-like receptor 2 controls mucosal inflammation by regulating epithelial barrier function. Gastroenterol-ogy. 2007;132:1359-74.
65. Qin H, Zhang Z, Hang X, Jiang Y. L. plantarum prevents enter-oinvasive Escherichia coli-induced tight junction proteins changes in intestinal epithelial cells. BMC Microbiol. 2009;9:63.
66. Anderson RC, Cookson AL, McNabb WC, Kelly WJ, Roy NC. Lactobacillus plantarum DSM 2648 is a potential probiotic that enhances intestinal barrier function. FEMS Microbiol Lett. 2010;309:184-92.
67. Putaala H, Salusjarvi T, Nordstrom M, Saarinen M, Ouwehand AC, Bech Hansen E, Rautonen N. Effect of four probiotic strains and Escherichia coli O157:H7 on tight junction integrity and cyclo-oxygenase expression. Res Microbiol. 2008;159:692-8.
68. Hardt WD, Galan JE. A secreted Salmonella protein with homology to an avirulence determinant of plant pathogenic bacteria. Proc Natl Acad Sci USA. 1997;94:9887-92.
69. Liao AP, Petrof EO, Kuppireddi S, Zhao Y, Xia Y, Claud EC, Sun J. Salmonella type III effector AvrA stabilizes cell tight junctions to inhibit inflammation in intestinal epithelial cells. PLoS ONE. 2008;3: e2369.
70. Trivedi K, Barrett KE, Resta-Lenert SC. Probiotic inhibition of the entry of enteroinvasive E. coli into human intestinal epithelial cells involves both Rho-dependent and independent pathways. Gastroen-terology. 2003;124:A106.
71. Resta-Lenert S, Barrett KE. Probiotics and commensals reverse TNF-alpha- and IFN-gamma-induced dysfunction in human intestinal epithelial cells. Gastroenterology. 2006;130:731-46.
72. Ghadimi D, Vrese MD, Heller KJ, Schrezenmeir J. Effect of natural commensal-origin DNA on toll-like receptor 9 (TLR9) signaling cascade, chemokine IL-8 expression, and barrier integrity of polarized intestinal epithelial cells. Inflamm Bowel Dis. 2010;16:410-27.
73. Drago S, El Asmar R, Di Pierro M, Grazia Clemente M, Tripathi A, Sapone A, Thakar M, Iacono G, Carroccio A, et al. Gliadin, zonulin and gut permeability: effects on celiac and non-celiac intestinal mucosa and intestinal cell lines. Scand J Gastroenterol. 2006;41:408-19.
74. Wang W, Uzzau S, Goldblum SE, Fasano A. Human zonulin, a potential modulator of intestinal tight junctions. J Cell Sci. 2000;113: 4435-40.
75. Clemente MG, De Virgiliis S, Kang JS, Macatagney R, Musu MP, Di Pierro MR, Drago S, Congia M, Fasano A. Early effects of gliadin on enterocyte intracellular signalling involved in intestinal barrier function. Gut. 2003;52:218-23.
76. Lammers KM, Lu R, Brownley J, Lu B, Gerard C, Thomas K, Rallabhandi P, Shea-Donohue T, Tamiz A, et al. Gliadin induces an increase in intestinal permeability and zonulin release by binding to the chemokine receptor CXCR3. Gastroenterology. 2008;135:194-204 e3.
77. Hashimoto K, Matsunaga N, Shimizu M. Effect of vegetable extracts on the transepithelial permeability of the human intestinal Caco-2 cell monolayer. Biosci Biotechnol Biochem. 1994;58:1345-6.
78. Jensen-Jarolim E, Gajdzik L, Haberl I, Kraft D, Scheiner O, Graf J. Hot spices influence permeability of human intestinal epithelial monolayers. J Nutr. 1998;128:577-81.
79. Hashimoto K, Kawagishi H, Nakayama T, Shimizu M. Effect of capsianoside, a diterpene glycoside, on tight-junctional permeability. Biochim Biophys Acta. 1997;1323:281-90.
80. Konishi Y. Modulations of food-derived substances on intestinal permeability in Caco-2 cell monolayers. Biosci Biotechnol Biochem. 2003;67:2297-9.
81. Mine Y, Zhang JW. Surfactants enhance the tight-junction permeability of food allergens in human intestinal epithelial Caco-2 cells. Int Arch Allergy Immunol. 2003;130:135-42.
82. Narai A, Arai S, Shimizu M. Rapid decrease in transepithelial electrical resistance of human intestinal Caco-2 cell monolayers by cytotoxic membrane perturbents. Toxicol In Vitro. 1997;11:347-54.
83. Shi X, Gisolfi CV. Paracellular transport of water and carbohydrates during intestinal perfusion of protamine in the rat. Am J Med Sci. 1996;311:107-12.
84. Sadowski DC, Meddings JB. Luminal nutrients alter tight-junction permeability in the rat jejunum: an in vivo perfusion model. Can J Physiol Pharmacol. 1993;71:835-9.
85. Yasumatsu H, Tanabe S. The casein peptide Asn-Pro-Trp-Asp-Gln enforces the intestinal tight junction partly by increasing occludin expression in Caco-2 cells. Br J Nutr. 2010;104:951-6.
86. Visser JT, Lammers K, Hoogendijk A, Boer MW, Brugman S, Beijer-Liefers S, Zandvoort A, Harmsen H, Welling G, et al. Restoration of impaired intestinal barrier function by the hydrolysed casein diet contributes to the prevention of type 1 diabetes in the diabetes-prone BioBreeding rat. Diab tologia. 2010;53:2621-8.
87. Hashimoto K, Nakayama T, Shimizu M. Effects of beta-lactoglobulin on the tight-junctional stability of Caco-2-SF monolayer. Biosci Biotechnol Biochem. 1998;62:1819-21.
88. Madara JL, Carlson S. Supraphysiologic L-tryptophan elicits cytoskel-etal and macromolecular permeability alterations in hamster small intestinal epithelium in vitro. J Clin Invest. 1991;87:454-62.
89. Li N, DeMarco VG, West CM, Neu J. Glutamine supports recovery from loss of transepithelial resistance and increase of permeability induced by media change in Caco-2 cells. J Nutr Biochem. 2003;14:401-8.
90. Li N, Lewis P, Samuelson D, Liboni K, Neu J. Glutamine regulates Caco-2 cell tight junction proteins. Am J Physiol Gastrointest Liver Physiol. 2004;287:G726-33.
91. Rhoads JM, Argenzio RA, Chen W, Rippe RA, Westwick JK, Cox AD, Berschneider HM, Brenner DA. L-glutamine stimulates intestinal cell proliferation and activates mitogen-activated protein kinases. Am J Physiol. 1997;272:G943-53.
92. Finamore A, Massimi M, Conti Devirgiliis L, Mengheri E. Zinc deficiency induces membrane barrier damage and increases neutrophil transmigration in Caco-2 cells. J Nutr. 2008;138:1664-70.
93. Lindmark T, Kimura Y, Artursson P. Absorption enhancement through intracellular regulation of tight junction permeability by medium chain fatty acids in Caco-2 cells. J Pharmacol Exp Ther. 1998;284:362-9.
94. Usami M, Komurasaki T, Hanada A, Kinoshita K, Ohata A. Effect of gamma-linolenic acid or docosahexaenoic acid on tight junction permeability in intestinal monolayer cells and their mechanism by protein kinase C activation and/or eicosanoid formation. Nutrition. 2003;19:150-6.
95. Usami M, Muraki K, Iwamoto M, Ohata A, Matsushita E, Miki A. Effect of eicosapentaenoic acid (EPA) on tight junction permeability in intestinal monolayer cells. Clin Nutr. 2001;20:351-9.
96. Soderholm JD, Oman H, Blomquist L, Veen J, Lindmark T, Olaison G. Reversible increase in tight junction permeability to macromolecules in rat ileal mucosa in vitro by sodium caprate, a constituent of milk fat. Dig Dis Sci. 1998;43:1547-52.
97. Roche HM, Terres AM, Black IB, Gibney MJ, Kelleher D. Fatty acids and epithelial permeability: effect of conjugated linoleic acid in Caco-2 cells. Gut. 2001;48:797-802.
98. Thanou M, Verhoef JC, Junginger HE. Oral drug absorption enhancement by chitosan and its derivatives. Adv Drug Deliv Rev. 2001; 52:117-26.
99. Schipper NG, Olsson S, Hoogstraate JA, deBoer AG, Varum KM, Artursson P. Chitosans as absorption enhancers for poorly absorbable drugs 2: mechanism of absorption enhancement. Pharm Res. 1997;14: 923-9.
100. Amasheh M, Schlichter S, Amasheh S, Mankertz J, Zeitz M, Fromm M, Schulzke JD. Quercetin enhances epithelial barrier function and increases claudin-4 expression in Caco-2 cells. J Nutr. 2008;138:1067-73.
101. Suzuki T, Hara H. Quercetin enhances intestinal barrier function through the assembly of zonula occludens-2, occludin, and claudin-1 and the expression of claudin-4 in Caco-2 cells. J Nutr. 2009;139: 965-74.
102. Watson JL, Ansari S, Cameron H, Wang A, Akhtar M, McKay DM. Green tea polyphenol (-)-epigallocatechin gallate blocks epithelial barrier dysfunction provoked by IFN-gamma but not by IL-4. Am J Physiol Gastrointest Liver Physiol. 2004;287:G954-61.
103. Di Cagno R, Mazzacane F, Rizzello CG, Vincentini O, Silano M, Giuliani G, De Angelis M, Gobbetti M. Synthesis of isoflavone aglycones and equol in soy milks fermented by food-related lactic acid bacteria and their effect on human intestinal Caco-2 cells. J Agric Food Chem. 2010;58:10338-46.
104. Schmitz H, Fromm M, Bentzel CJ, Scholz P, Detjen K, Mankertz J, Bode H, Epple HJ, Riecken EO, et al. Tumor necrosis factor-alpha (TNFalpha) regulates the epithelial barrier in the human intestinal cell line HT-29/B6. J Cell Sci. 1999;112:137-46.
105. Peng L, Li ZR, Green RS, Holzman IR, Lin J. Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers. J Nutr. 2009;139:1619-25.
106. Gibson GR. Fibre and effects on probiotics (the prebiotic concept). Clin Nutr Suppl. 2004;1:25-31.