Modulation of tight junction integrity by food components

Food Research International

Volumn 54, Issue 1, 2013, Pages 951-960

  Kosińska, Agnieszka ^a,b   Andlauer, Wilfried ^a  

^a University of Applied Sciences Valais   (Switzerland)

^b INSTITUTE OF ANIMAL REPRODUCTION AND FOOD RESEARCH   (Poland)

Author keywords

Epithelial barrier modulation; Food components; Paracellular transport; Phenolic compounds; Tight junction

Indexed keywords

EPITHELIAL BARRIER; FOOD COMPONENTS; PARACELLULAR TRANSPORT; PHENOLIC COMPOUNDS; TIGHT JUNCTIONS;

COMPLEX NETWORKS; DISEASES; LIVING SYSTEMS STUDIES; MODULATION; MONOLAYERS; SCAFFOLDS (BIOLOGY);

PROTEINS;

EID: 84886297700     PISSN: 09639969     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.foodres.2012.12.038     Document Type: Review

References (108)

1. Aaby K., Ekeberg D., Skrede G. Characterization of phenolic compounds in strawberry (Fragaria×ananassa) fruits by different HPLC detectors and contribution of individual compounds to total antioxidant capacity. Journal of Agricultural and Food Chemistry 2007, 55:4395-4406.
2. Al Sadi R.M., Ma T.Y. IL-1 beta causes an increase in intestinal epithelial tight junction permeability. The Journal of Immunology 2007, 178:4641-4649.
3. Al-Sadi R., Khatib K., Guo S.H., Ye D.M., Youssef M., Ma T. Occludin regulates macromolecule flux across the intestinal epithelial tight junction barrier. American Journal of Physiology - Gastrointestinal and Liver Physiology 2011, 300:G1054-G1064.
4. Amasheh M., Schlichter S., Amasheh S., Mankertz J., Zeitz M., Fromm M., et al. Quercetin enhances epithelial barrier function and increases claudin-4 expression in Caco-2 cells. The Journal of Nutrition 2008, 138:1067-1073.
5. Anderson J.M., Van Itallie C.M. Physiology and function of the tight junction. Cold Spring Harbor Perspectives in Biology 2009, 1:1-16.
6. Appeldoorn M.M., Vincken J.P., Gruppen H., Hollman P.C.H. Procyanidin dimers A1, A2, and B2 are absorbed without conjugation or methylation from the small intestine of rats. The Journal of Nutrition 2009, 139:1469-1473.
7. Assimakopoulos S.F., Papageorgiou I., Charonis A. Enterocytes' tight junctions: From molecules to diseases. World Journal of Gastrointestinal Pathophysiology 2011, 2:123-137.
8. Balda M.S., Matter K. Tight junctions at a glance. Journal of Cell Science 2008, 121:3677-3682.
9. Ballard S.T., Hunter J.H., Taylor A.E. Regulation of tight-junction permeability during nutrient absorption across the intestinal epithelium. Annual Review of Nutrition 1995, 15:35-55.
10. Bergmann H., Rogoll D., Scheppach W., Melcher R., Richling E. The Ussing type chamber model to study the intestinal transport and modulation of specific tight-junction genes using a colonic cell line. Molecular Nutrition & Food Research 2009, 53:1211-1225.
11. Blomhoff R., Carlsen M.H., Andersen L.F., Jacobs D.R. Health benefits of nuts: Potential role of antioxidants. The British Journal of Nutrition 2006, 96:S52-S60.
12. Borchardt R. Hidalgo, I. J., Raub, T. J., and Borchardt, R. T.: Characterization of the human colon carcinoma cell line (Caco-2) as a model system for intestinal epithelial permeability, Gastroenterology, 96, 736-749, 1989, The backstory. The AAPS Journal 2011, 13:323-327.
13. Boyer J., Liu R. Apple phytochemicals and their health benefits. Nutrition Journal 2004, 3:5.
14. Chan K.Y., Zhang L., Zuo Z. Intestinal efflux transport kinetics of green tea catechins in Caco-2 monolayer model. The Journal of Pharmacy and Pharmacology 2007, 59:395-400.
15. Chen W.Y., Lu Z.L., Viljoen A., Hamman J. Intestinal drug transport enhancement by Aloe vera. Planta Medica 2009, 75:587-595.
16. Cho S., Kim J., Li H., Shim C., Linhardt R., Kim Y. Enhancement of paracellular transport of heparin disaccharide across Caco-2 cell monolayers. Archives of Pharmacal Research 2002, 25:86-92.
17. Christensen J., El Gebali S., Natoli M., Sengstag T., Delorenzi M., Bentz S., et al. Defining new criteria for selection of cell-based intestinal models using publicly available databases. BMC Genomics 2012, 13:274.
18. Colegio O.R., Van Itallie C.M., Mccrea H.J., Rahner C., Anderson J.M. Claudins create charge-selective channels in the paracellular pathway between epithelial cells. American Journal of Physiology. Cell Physiology 2002, 283:C142-C147.
19. Deli M.A. Potential use of tight junction modulators to reversibly open membranous barriers and improve drug delivery. Biochimica et Biophysica Acta (BBA)-Biomembranes 2009, 1788:892-910.
20. Déprez S., Mila I., Huneau J.F., Tome D., Scalbert A. Transport of proanthocyanidin dimer, trimer, and polymer across monolayers of human intestinal epithelial Caco-2 cells. Antioxidants & Redox Signaling 2001, 3:957-967.
21. Eguchi A., Murakami A., Ohigashi H. Novel bioassay system for evaluating anti-oxidative activities of food items: Use of basolateral media from differentiated Caco-2 cells. Free Radical Research 2005, 39:1367-1375.
22. Epriliati I., D'Arcy B., Gidley M. Nutriomic analysis of fresh and processed fruit products. 2. During in vitro simultaneous molecular passages using Caco-2 cell monolayers. Journal of Agricultural and Food Chemistry 2009, 57:3377-3388.
23. Erlejman A.G., Fraga C.G., Oteiza P.I. Procyanidins protect Caco-2 cells from bile acid- and oxidant-induced damage. Free Radical Biology & Medicine 2006, 41:1247-1256.
24. Farquhar M.G., Palade G.E. Junctional complexes in various epithelia. The Journal of Cell Biology 1963, 17:375-412.
25. Fihn B.M., Sjoqvist A., Jodal M. Permeability of the rat small intestinal epithelium along the villus-crypt axis: Effects of glucose transport. Gastroenterology 2000, 119:1029-1036.
26. Fogh J., Fogh J.M., Orfeo T. 127 cultured human tumor-cell lines producing tumors in nude mice. Journal of the National Cancer Institute 1977, 59:221-226.
27. Förster C. Tight junctions and the modulation of barrier function in disease. Histochemistry and Cell Biology 2008, 130:55-70.
28. Fuller E., Duckham C., Wood E. Disruption of epithelial tight junctions by yeast enhances the paracellular delivery of a model protein. Pharmaceutical Research 2007, 24:37-47.
29. Furuse M. Molecular basis of the core structure of tight junctions. Cold Spring Harbor Perspectives in Biology 2010, 2:1-14.
30. Gonzalez R., Ballester I., Lopez-Posadas R., Suarez M., Zarzuelo A., Martinez-Augustin O., et al. Effects of flavonoids and other polyphenols on inflammation. Critical Reviews in Food Science and Nutrition 2011, 51:331-362.
31. González-Mariscal L., Tapia R., Chamorro D. Crosstalk of tight junction components with signaling pathways. Biochimica et Biophysica Acta (BBA)-Biomembranes 2008, 1778:729-756.
32. Gropper S.S., Smith J.J., Groff J.L. Advanced Nutrition and Human Metabolism 2009, Wadsworth/Cengage Learning, Australia; United States. 5th edition.
33. Groschwitz K.R., Hogan S.P. Intestinal barrier function: Molecular regulation and disease pathogenesis. The Journal of Allergy and Clinical Immunology 2009, 124:3-20.
34. Grube S., Wolfrurn U., Langguth P. Characterization of the epithelial permeation enhancing effect of basic butylated methacrylate copolymer-In vitro studies. Biomacromolecules 2008, 9:1398-1405.
35. Hamazaki Y., Itoh M., Sasaki H., Furuse M., Tsukita S. Multi-PDZ domain protein 1 (MUPP1) is concentrated at tight junctions through its possible interaction with claudin-1 and junctional adhesion molecule. The Journal of Biological Chemistry 2002, 277:455-461.
36. Harmidy K., Tufenkji N., Gruenheid S. Perturbation of host cell cytoskeleton by cranberry proanthocyanidins and their effect on enteric infections. PLoS One 2011, 6:1-9.
37. Hartsock A., Nelson W.J. Adherens and tight junctions: Structure, function and connections to the actin cytoskeleton. Biochimica et Biophysica Acta (BBA)-Biomembranes 2008, 1778:660-669.
38. Hashimoto K., Matsunaga N., Shimizu M. Effect of vegetable extracts on the transepithelial permeability of the human intestinal Caco-2 cell monolayer. Bioscience, Biotechnology, and Biochemistry 1994, 58:1345-1346.
39. Hilgendorf C., Spahn-Langguth H., Regårdh C.G., Lipka E., Amidon G.L., Langguth P. Caco-2 versus Caco-2/HT29-MTX co-cultured cell lines: Permeabilities via diffusion, inside- and outside-directed carrier-mediated transport. Journal of Pharmaceutical Sciences 2000, 89:63-75.
40. Hilgers A.R., Conradi R.A., Burton P.S. Caco-2 cell monolayers as a model for drug transport across the intestinal mucosa. Pharmaceutical Research 1990, 7:902-910.
41. Isoda H., Han J.Y., Tominaga M., Maekawa T. Effects of capsaicin on human intestinal cell line Caco-2. Cytotechnology 2001, 36:155-161.
42. Juuti-Uusitalo K., Klunder L.J., Sjollema K.A., Mackovicova K., Ohgaki R., Hoekstra D., et al. Differential effects of TNF (TNFSF2) and IFN-gamma on intestinal epithelial cell morphogenesis and barrier function in three-dimensional culture. PLoS One 2011, 6.
43. Kang M.J., Cho J.Y., Shim B.H., Kim D.K., Lee J. Bioavailability enhancing activities of natural compounds from medicinal plants. Journal of Medicinal Plants Research 2009, 3:1204-1211.
44. Konishi Y. Modulations of food-derived substances on intestinal permeability in Caco-2 cell monolayers. Bioscience, Biotechnology, and Biochemistry 2003, 67:2297-2299.
45. Kosińska A., Andlauer W. Cocoa polyphenols are absorbed in Caco-2 cell model of intestinal epithelium. Food Chemistry 2012, 135:999-1005.
46. Kosińska A., Karamać M., Estrella I., Hernandez T., Bartolome B., Dykes G.A. Phenolic compound profiles and antioxidant capacity of Persea americana Mill. peels and seeds of two varieties. Journal of Agricultural and Food Chemistry 2012, 60:4613-4619.
47. Kumar N.M., Gilula N.B. The gap junction communication channel. Cell 1996, 84:381-388.
48. Laitinen L.A., Tammela P.S.M., Galkin A., Vuorela H.J., Marvola M.L.A., Vuorela P.M. Effects of extracts of commonly consumed food supplements and food fractions on the permeability of drugs across Caco-2 cell monolayers. Pharmaceutical Research 2004, 21:1904-1916.
49. Lal-Nag M., Morin P. The claudins. Genome Biology 2009, 10:235.
50. Langerholc T., Maragkoudakis P.A., Wollgast J., Gradisnik L., Cencic A. Novel and established intestinal cell line models-An indispensable tool in food science and nutrition. Trends in Food Science & Technology 2011, 22:S11-S20.
51. Lebitsa T., Viljoen A., Lu Z.L., Hamman J. In vitro drug permeation enhancement potential of aloe gel materials. Current Drug Delivery 2012, 9:297-304.
52. Li N., Lewis P., Samuelson D., Liboni K., Neu J. Glutamine regulates Caco-2 cell tight junction proteins. American Journal of Physiology - Gastrointestinal and Liver Physiology 2004, 287:G726-G733.
53. Linnankoski J., Mäkelä J., Palmgren J., Mauriala T., Vedin C., Ungell A.L., et al. Paracellular porosity and pore size of the human intestinal epithelium in tissue and cell culture models. Journal of Pharmaceutical Sciences 2010, 99:2166-2175.
54. Lowe P.J., Miyai K., Steinbach J.H., Hardison W.G.M. Hormonal regulation of hepatocyte tight junctional permeability. The American Journal of Physiology 1988, 255:G454-G461.
55. Lu Z.L., Chen W.Y., Viljoen A., Hamman J.H. Effect of sinomenine on the in vitro intestinal epithelial transport of selected compounds. Phytotherapy Research 2010, 24:211-218.
56. Madara J.L. Functional morphology of epithelium of the small intestine. Comprehensive Physiology 2011, 83-120.
57. Mariano C., Sasaki H., Brites D., Brito M.A. A look at tricellulin and its role in tight junction formation and maintenance. European Journal of Cell Biology 2011, 90:787-796.
58. Martín-Padura I., Lostaglio S., Schneemann M., Williams L., Romano M., Fruscella P., et al. Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration. The Journal of Cell Biology 1998, 142:117-127.
59. Noda S., Tanabe S., Suzuki T. Differential effects of flavonoids on barrier integrity in human intestinal Caco-2 cells. Journal of Agricultural and Food Chemistry 2012, 60:4628-4633.
60. Ohno Y., Naganuma T., Ogawa T., Muramoto K. Effect of lectins on the transport of food factors in Caco-2 cell monolayers. Journal of Agricultural and Food Chemistry 2006, 54:548-553.
61. Ou K., Percival S.S., Zou T., Khoo C., Gu L. Transport of cranberry A-type procyanidin dimers, trimers, and tetramers across monolayers of human intestinal epithelial Caco-2 cells. Journal of Agricultural and Food Chemistry 2012, 60:1390-1396.
62. Pinto M., Robineleon S., Appay M.D., Kedinger M., Triadou N., Dussaulx E., et al. Enterocyte-like differentiation and polarization of the human-colon carcinoma cell-line Caco-2 in culture. Biology of the Cell 1983, 47:323-330.
63. Raleigh D.R., Boe D.M., Yu D., Weber C.R., Marchiando A.M., Bradford E.M., et al. Occludin S408 phosphorylation regulates tight junction protein interactions and barrier function. The Journal of Cell Biology 2011, 193:565-582.
64. Rapin J.R., Wiernsperger N. Possible links between intestinal permeability and food processing: A potential therapeutic niche for glutamine. Clinics 2010, 65:635-643.
65. Rodgers L.S., Fanning A.S. Regulation of epithelial permeability by the actin cytoskeleton. Cytoskeleton 2011, 68:653-660.
66. Runswick S.K., O'Hare M.J., Jones L., Streuli C.H., Garrod D.R. Desmosomal adhesion regulates epithelial morphogenesis and cell positioning. Nature Cell Biology 2001, 3:823-830.
67. Sadowski D.C., Meddings J.B. Luminal nutrients alter tight-junction permeability in the rat jejunum-An in-vivo perfusion model. Canadian Journal of Physiology and Pharmacology 1993, 71:835-839.
68. Salama N.N., Eddington N.D., Fasano A. Tight junction modulation and its relationship to drug delivery. Advanced Drug Delivery Reviews 2006, 58:15-28.
69. Sambuy Y., De Angelis I., Ranaldi G., Scarino M.L., Stammati A., Zucco F. The Caco-2 cell line as a model of the intestinal barrier: Influence of cell and culture-related factors on Caco-2 cell functional characteristics. Cell Biology and Toxicology 2005, 21:1-26.
70. Scalbert A., Deprez S., Mila I., Albrecht A.M., Huneau J.F., Rabot S. Proanthocyanidins and human health: Systemic effects and local effects in the gut. Biofactors 2000, 13:115-120.
71. Schonhoff S.E., Giel-Moloney M., Leiter A.B. Minireview: Development and differentiation of gut endocrine cells. Endocrinology 2004, 145:2639-2644.
72. Schulzke J.D., Gunzel D., John L.J., Fromm M. Perspectives on tight junction research. Annals of the New York Academy of Sciences 2012, 1257:1-19.
73. Seeram N.P. Berry fruits for cancer prevention: Current status and future prospects. Journal of Agricultural and Food Chemistry 2008, 56:630-635.
74. Seeram N.P., Adams L.S., Zhang Y., Lee R., Sand D., Scheuller H.S., et al. Blackberry, black raspberry, blueberry, cranberry, red raspberry, and strawberry extracts inhibit growth and stimulate apoptosis of human cancer cells in vitro. Journal of Agricultural and Food Chemistry 2006, 54:9329-9339.
75. Sharma M., Li L.Y., Celver J., Killian C., Kovoor A., Seeram N.P. Effects of fruit ellagitannin extracts, ellagic acid, and their colonic metabolite, urolithin A, on Wnt signaling. Journal of Agricultural and Food Chemistry 2010, 58:3965-3969.
76. Shen L., Weber C.R., Raleigh D.R., Yu D., Tumer J.R. Tight junction pore and leak pathways: A dynamic duo. Annual Reviews of Physiology 2011, 73:283-309.
77. Shimizu M. Modulation of intestinal functions by food substances. Nahrung-Food 1999, 43:154-158.
78. Shoji T., Masumoto S., Moriichi N., Akiyama H., Kanda T., Ohtake Y., et al. Apple procyanidin oligomers absorption in rats after oral administration: Analysis of procyanidins in plasma using the porter method and high-performance liquid chromatography/tandem mass spectrometry. Journal of Agricultural and Food Chemistry 2006, 54:884-892.
79. Soderholm J.D., 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. Digestive Diseases and Sciences 1998, 43:1547-1552.
80. Son T.G., Camandola S., Mattson M.P. Hormetic dietary phytochemicals. Neuromolecular Medicine 2008, 10:236-246.
81. Steed E., Balda M.S., Matter K. Dynamics and functions of tight junctions. Trends in Cell Biology 2010, 20:142-149.
82. Sun H., Chow E.C., Liu S., Du Y., Pang K.S. The Caco-2 cell monolayer: Usefulness and limitations. Expert Opinion on Drug Metabolism & Toxicology 2008, 4:395-411.
83. Suzuki T., Hara H. Various nondigestible saccharides open a paracellular calcium transport pathway with the induction of intracellular calcium signalling in human intestinal Caco-2 cells. The Journal of Nutrition 2004, 134:1935-1941.
84. Suzuki T., Nishimukai M., Takechi M., Taguchi H., Hamada S., Yokota A., et al. The nondigestible disaccharide epilactose increases paracellular Ca sbsorption via Rho-associated kinase- and myosin light chain kinase-dependent mechanisms in rat small intestines. Journal of Agricultural and Food Chemistry 2010, 58:1927-1932.
85. Suzuki T., Hara H. Quercetin enhances intestinal barrier function through the assembly of zonnula occludens-2, occludin, and claudin-1 and the expression of claudin-4 in Caco-2 cells. The Journal of Nutrition 2009, 139:965-974.
86. Suzuki T., Tanabe S., Hara H. Kaempferol enhances intestinal barrier function through the cytoskeletal association and expression of tight junction proteins in Caco-2 cells. The Journal of Nutrition 2011, 141:87-94.
87. Terry S., Nie M., Matter K., Balda M.S. Rho signaling and tight junction functions. Physiology 2010, 25:16-26.
88. Tsukamoto T., Nigam S.K. Role of tyrosine phosphorylation in the reassembly of occludin and other tight junction proteins. American Journal of Physiology. Renal Physiology 1999, 276:F737-F750.
89. Tsukura Y., Mori M., Hirotani Y., Ikeda K., Amano F., Kato R., et al. Effects of capsaicin on cellular damage and monolayer permeability in human intestinal Caco-2 cells. Biological & Pharmaceutical Bulletin 2007, 30:1982-1986.
90. Turner J.R. Show me the pathway! Regulation of paracellular permeability by Na(+)-glucose cotransport. Advanced Drug Delivery Reviews 2000, 41:265-281.
91. Ulluwishewa D., Anderson R.C., McNabb W.C., Moughan P.J., Wells J.M., Roy N.C. Regulation of tight junction permeability by intestinal bacteria and dietary components. The Journal of Nutrition 2011, 141:769-776.
92. Vaidyanathan J.B., Walle T. Cellular uptake and efflux of the tea flavonoid (-)-epicatechin-3-gallate in the human intestinal cell line Caco-2. The Journal of Pharmacology and Experimental Therapeutics 2003, 307:745-752.
93. Van Itallie C.M., Anderson J.M. Claudins and epithelial paracellular transport. Annual Reviews of Physiology 2006, 68:403-429.
94. Van Itallie C.M., Fanning A.S., Bridges A., Anderson J.M. ZO-1 stabilizes the tight junction solute barrier through coupling to the perijunctional cytoskeleton. Molecular Biology of the Cell 2009, 20:3930-3940.
95. Van Itallie C.M., Holmes J., Bridges A., Gookin J.L., Coccaro M.R., Proctor W., et al. The density of small tight junction pores varies among cell types and is increased by expression of claudin-2. Journal of Cell Science 2008, 121:298-305.
96. Van Itallie C.M., Fanning A.S., Holmes J., Anderson J.M. Occludin is required for cytokine-induced regulation of tight junction barriers. Journal of Cell Science 2010, 123:2844-2852.
97. Vreeburg R.A.M., Bastiaan-Net S., Mes J.J. Normalization genes for quantitative RT-PCR in differentiated Caco-2 cells used for food exposure studies. Food & Function 2011, 2:124-129.
98. Vreeburg R.A., van Wezel E.E., Ocana-Calahorro F., Mes J.J. Apple extract induces increased epithelial resistance and claudin 4 expression in Caco-2 cells. Journal of the Science of Food and Agriculture 2012, 92:439-444.
99. Ward P.D., Tippin T.K., Thakker D.R. Enhancing paracellular permeability by modulating epithelial tight junctions. Pharmaceutical Science & Technology Today 2000, 3:346-358.
100. Weinreb O., Amit T., Mandel S., Youdim M.B.H. Neuroprotective molecular mechanisms of (-)-epigallocatechin-3-gallate: A reflective outcome of its antioxidant, iron chelating and neuritogenic properties. Genes and Nutrition 2009, 4:283-296.
101. Wu C., Xu H., Héritier J., Andlauer W. Determination of catechins and flavonol glycosides in Chinese tea varieties. Food Chemistry 2012, 132:144-149.
102. Xie Y., Kosińska A., Xu H., Andlauer W. Milk enhances intestinal absorption of green tea catechins in in vitro digestion/Caco-2 cells model. Food Research International 2012, 10.1016/j.foodres.2012.07.063.
103. Xu J.G., Go M.L., Lim L.Y. Modulation of digoxin transport across Caco-2 cell monolayers by citrus fruit juices: Lime, lemon, grapefruit, and pummelo. Pharmaceutical Research 2003, 20:169-176.
104. Yamazaki Y., Tokumasu R., Kimura H., Tsukita S. Role of claudin species-specific dynamics in reconstitution and remodeling of the zonula occludens. Molecular Biology of the Cell 2011, 22:1495-1504.
105. 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. The British Journal of Nutrition 2010, 104:951-956.
106. Yu A.S.L. Molecular basis for cation selectivity in claudin-2-based pores. Annals of the New York Academy of Sciences 2009, 1165:53-57.
107. Zhang L., Chow M.S.S., Zuo Z. Effect of the co-occurring components from green tea on the intestinal absorption and disposition of green tea polyphenols in Caco-2 monolayer model. The Journal of Pharmacy and Pharmacology 2006, 58:37-44.
108. Zweibaum A., Laburthe M., Grasset E., Louvard D. Use of cultured cell lines in studies of intestinal cell differentiation and function. Comprehensive Physiology 2011, 223-255.