Polyphenols protect the epithelial barrier function of Caco-2 cells exposed to indomethacin through the modulation of occludin and zonula occludens-1 expression

Journal of Agricultural and Food Chemistry

Volumn 61, Issue 22, 2013, Pages 5291-5297

  Carrasco Pozo, Catalina ^a,b   Morales, Pamela ^a,b   Gotteland, Martin ^a,b  

^a UNIVERSITY OF CHILE   (Chile)

^b UNIVERSITY OF CHILE   (Chile)

Author keywords

indomethacin; occludin; polyphenols; quercetin; rotenone; tight junction; transepithelial electrical resistance; ZO 1

Indexed keywords

INDOMETHACIN; OCCLUDIN; POLYPHENOLS; QUERCETIN; ROTENONE; TIGHT JUNCTIONS; TRANSEPITHELIAL ELECTRICAL RESISTANCES; ZO-1;

ALCOHOLS; CELLS; ELECTRIC RESISTANCE; FATTY ACIDS; MONOLAYERS; PHENOLS;

FLAVONOIDS;

ANTIOXIDANT; CATECHIN; DRUG DERIVATIVE; EPIGALLOCATECHIN GALLATE; INDOMETACIN; NONSTEROID ANTIINFLAMMATORY AGENT; OCCLUDIN; OCLN PROTEIN, HUMAN; POLYPHENOL; PROTEIN ZO1; QUERCETIN; RESVERATROL; STILBENE DERIVATIVE; TJP1 PROTEIN, HUMAN;

ARTICLE; CACO 2 CELL LINE; COMPARATIVE STUDY; DRUG ANTAGONISM; DRUG EFFECT; DRUG POTENTIATION; FUNCTIONAL FOOD; GENE EXPRESSION REGULATION; GENETICS; HUMAN; INTESTINE CELL; METABOLISM; PERMEABILITY; PROTEIN TRANSPORT; TIGHT JUNCTION;

ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ANTIOXIDANTS; CACO-2 CELLS; CATECHIN; ENTEROCYTES; FUNCTIONAL FOOD; GENE EXPRESSION REGULATION; HUMANS; INDOMETHACIN; OCCLUDIN; PERMEABILITY; POLYPHENOLS; PROTEIN TRANSPORT; QUERCETIN; STILBENES; TIGHT JUNCTIONS; ZONULA OCCLUDENS-1 PROTEIN;

EID: 84878664357     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf400150p     Document Type: Article

References (54)

1. Scarpignato, C.; Hunt, R. H. Nonsteroidal antiinflammatory drug-related injury to the gastrointestinal tract: Clinical picture, pathogenesis, and prevention Gastroenterol. Clin. North Am. 2010, 39, 433-464
2. Carrasco-Pozo, C.; Gotteland, M.; Speisky, H. Protection by apple peel polyphenols against indomethacin-induced oxidative stress, mitochondrial damage and cytotoxicity in Caco-2 cells J. Pharm. Pharmacol. 2010, 62, 943-950
3. Carrasco-Pozo, C.; Gotteland, M.; Speisky, H. Apple peel polyphenol extract protects against indomethacin-induced damage in Caco-2 cells by preventing mitochondrial complex I inhibition J. Agric. Food Chem. 2011, 59, 11501-11508
4. Carrasco-Pozo, C.; Speisky, H.; Brunser, O.; Pastene, E.; Gotteland, M. Apple peel polyphenols protect against gastrointestinal mucosa alterations induced by indomethacin in rats J. Agric. Food. Chem. 2011, 59, 6459-6666
5. Carrasco-Pozo, C.; Mizgier, M. L.; Speisky, H.; Gotteland, M. Differential protective effects of quercetin, resveratrol, rutin and epigallocatechin gallate against mitochondrial dysfunction induced by indomethacin in Caco-2 cells Chem. Biol. Interact. 2012, 195, 199-205
6. Carrasco-Pozo, C.; Pastene, E.; Vergara, C.; Zapata, M.; Sandoval, C.; Gotteland, M. Stimulation of cytosolic and mitochondrial calcium mobilization by indomethacin in Caco-2 cells: Modulation by the polyphenols quercetin, resveratrol and rutin Biochim. Biophys. Acta 2012, 1820, 2052-2061
7. Somasundaram, S.; Sigthorsson, G.; Simpson, R. J.; Watts, J.; Jacob, M.; Tavares, I. A.; Rafi, S.; Roseth, A.; Foster, R.; Price, A. B.; Wrigglesworth, J. M.; Bjarnason, I. Uncoupling of intestinal mitochondrial oxidative phosphorylation and inhibition of cyclooxygenase are required for the development of NSAID-enteropathy in the rat Aliment. Pharmacol. Ther. 2000, 14, 639-650 (Pubitemid 30240758)
8. Colpaert, S.; Liu, Z.; De Greef, B.; Rutgeerts, P.; Ceuppens, J. L.; Geboes, K. Effects of anti-tumour necrosis factor, interleukin-10 and antibiotic therapy in the indometacin-induced bowel inflammation rat model Aliment. Pharmacol. Ther. 2001, 15, 1827-1836 (Pubitemid 33001147)
9. Bernardes-Silva, C. F.; Damiao, A. O.; Sipahi, A. M.; Laurindo, F. R.; Iriya, K.; Lopasso, F. P.; Buchpiguel, C. A.; Lordello, M. L.; Agostinho, C. L.; Laudanna, A. A. Ursodeoxycholic acid ameliorates experimental ileitis counteracting intestinal barrier dysfunction and oxidative stress Dig. Dis. Sci. 2004, 49, 1569-1574 (Pubitemid 39335536)
10. Meddings, J. B.; Gibbons, I. Discrimination of site-specific alterations in gastrointestinal permeability in the rat Gastroenterology 1998, 114, 83-92 (Pubitemid 28020958)
11. Gotteland, M.; Cruchet, S.; Verbeke, S. Effect of Lactobacillus ingestion on the gastrointestinal mucosal barrier alterations induced by indometacin in humans Aliment. Pharmacol. Ther. 2001, 15, 11-17 (Pubitemid 32055581)
12. van Wijck, K.; Verlinden, T. J.; van Eijk, H. M.; Dekker, J.; Buurman, W. A.; Dejong, C. H.; Lenaerts, K. Novel multi-sugar assay for site-specific gastrointestinal permeability analysis: A randomized controlled crossover trial Clin. Nutr. 2013, 32, 245-251
13. van Itallie, C. M.; Fanningm, A. S.; Bridges, A.; Anderson, J. M. ZO-1 stabilizes the tight junction solute barrier through coupling to the perijunctional cytoskeleton Mol. Biol. Cell 2009, 20, 3930-3940
14. Manna, C.; Galletti, P.; Cucciolla, V.; Moltedo, O.; Leone, A.; Zappia, V. The protective effect of the olive oil polyphenol (3,4-dihydroxyphenyl)- ethanol counteracts reactive oxygen metabolite-induced cytotoxicity in Caco-2 cells J. Nutr. 1997, 127, 286-292 (Pubitemid 27079958)
15. Rao, R. K.; Baker, R. D.; Baker, S. S.; Gupta, A.; Holycross, M. Oxidant-induced disruption of intestinal epithelial barrier function: Role of protein tyrosine phosphorylation Am. J. Physiol. 1997, 273, G812-G823
16. Rao, R.; Baker, R. D.; Baker, S. S. Inhibition of oxidant-induced barrier disruption and protein tyrosine phosphorylation in Caco-2 cell monolayers by epidermal growth factor Biochem. Pharmacol. 1999, 57, 685-695 (Pubitemid 29080760)
17. Banan, A.; Fields, J. Z.; Farhadi, A.; Talmage, D. A.; Zhang, L.; Keshavarzian, A. Activation of delta-isoform of protein kinase C is required for oxidant-induced disruption of both the microtubule cytoskeleton and permeability barrier of intestinal epithelia J. Pharmacol. Exp. Ther. 2002, 303, 17-28
18. Rao, R. K.; Basuroy, S.; Rao, V. U.; Karnaky, K. J., Jr.; Gupta, A. Tyrosine phosphorylation and dissociation of occludin-ZO-1 and E-cadherin-beta-catenin complexes from the cytoskeleton by oxidative stress Biochem. J. 2002, 368, 471-481 (Pubitemid 35454525)
19. Tsukamoto, T.; Nigam, S. K. Tight junction proteins form large complexes and associate with the cytoskeleton in an ATP depletion model for reversible junction assembly J. Biol. Chem. 1997, 272, 16133-16139 (Pubitemid 27276427)
20. Gopalakrishnan, S.; Hallett, M. A.; Atkinson, S. J.; Marrs, J. A. aPKC-PAR complex dysfunction and tight junction disassembly in renal epithelial cells during ATP depletion Am. J. Physiol. Cell. Physiol. 2007, 292, C1094-1102
21. Wagner, M. C.; Rhodes, G.; Wang, E.; Pruthi, V.; Arif, E.; Saleem, M. A.; Wean, S. E.; Garg, P.; Verma, R.; Holzman, L. B.; Gattone, V.; Molitoris, B. A.; Nihalani, D. Ischemic injury to kidney induces glomerular podocyte effacement and dissociation of slit diaphragm proteins Neph1 and ZO-1 J. Biol. Chem. 2008, 283, 35579-35589
22. Rasmussen, S. E.; Frederiksen, H.; Krogholm, K. S.; Poulsen, L. Dietary proanthocyanidins: Occurrence, dietary intake, bioavailability, and protection against cardiovascular disease Mol. Nutr. Food Res. 2005, 49, 159-174 (Pubitemid 40379813)
23. Ramassamy, C. Emerging role of polyphenolic compounds in the treatment of neurodegenerative diseases: A review of their intracellular targets Eur. J. Pharmacol. 2006, 545, 51-64
24. Kerem, Z.; Chetrit, D.; Shoseyov, O.; Regev-Shoshani, G. Protection of lipids from oxidation by epicatechin, trans -resveratrol, and gallic and caffeic acids in intestinal model systems J. Agric. Food Chem. 2006, 54, 10288-10293 (Pubitemid 46159040)
25. Alarcón de la Lastra, C.; Martín, V. Antiulcer and gastroprotective effects of quercetin: A gross and histologic study Pharmacology 1994, 48, 56-62
26. Dey, A.; Guha, P.; Chattopadhyay, S.; Bandyopadhyay, S. K. Biphasic activity of resveratrol on indomethacin-induced gastric ulcers Biochem. Biophys. Res. Commun. 2009, 381, 90-95
27. Abdel-Raheem, I. T. Gastroprotective effect of rutin against indomethacin induced ulcers in rats Basic Clin. Pharmacol. Toxicol. 2010, 107, 742-750
28. Li, K.; Guo, D.; Zhu, H.; Hering-Smith, K. S.; Hamm, L. L.; Ouyang, J.; Dong, Y. Interleukin-6 stimulates epithelial sodium channels in mouse cortical collecting duct cells Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010, 299, R590-R595
29. Penes, M. C.; Li, X.; Nagy, J. I. Expression of zonula occludens-1 (ZO-1) and the transcription factor ZO-1-associated nucleic acid-binding protein (ZONAB)-MsY3 in glial cells and colocalization at oligodendrocyte and astrocyte gap junctions in mouse brain Eur. J. Neurosci. 2005, 22, 404-418 (Pubitemid 41097614)
30. Piche, T.; Barbara, G.; Aubert, P.; Bruley des Varannes, S.; Dainese, R.; Nano, J. L.; Cremon, C.; Stanghellini, V.; De Giorgio, R.; Galmiche, J. P.; Neunlist, M. Impaired intestinal barrier integrity in the colon of patients with irritable bowel syndrome: Involvement of soluble mediators Gut. 2009, 58, 196-201
31. Chang, S.; Chen, W.; Yang, J. Another formula for calculating the gene change rate in real-time RT-PCR Mol. Biol. Rep. 2009, 36, 2165-2168
32. Bjarnason, I.; Fehilly, B.; Smethurst, P.; Menzies, I. S.; Levi, A. J. Importance of local versus systemic effects of non-steroidal anti-inflammatory drugs in increasing small intestinal permeability in man Gut 1991, 32, 275-277
33. Fasano, A.; Fiorentini, C.; Donelli, G.; Uzzau, S.; Kaper, J. B.; Margaretten, K.; Ding, X.; Guandalini, S.; Comstock, L.; Goldblum, S. E. Zonula occludens toxin modulates tight junctions through protein kinase C-dependent actin reorganization, in vitro J. Clin. Invest. 1995, 96, 710-720
34. Ilbäck, N. G.; Nyblom, M.; Carlfors, J.; Fagerlund-Aspenstrom, B.; Tavelin, S.; Glynn, A. W. Do surface-active lipids in food increase the intestinal permeability to toxic substances and allergenic agents? Med. Hypotheses 2004, 63, 724-730 (Pubitemid 39485847)
35. Fasano, A.; Shea-Donohue, T. Mechanisms of disease: The role of intestinal barrier function in the pathogenesis of gastrointestinal autoimmune diseases Nat. Clin. Pract. Gastroenterol. Hepatol. 2005, 2, 416-422 (Pubitemid 41486094)
36. Hollander, D. Crohn's disease-A permeability disorder of the tight junction? Gut 1988, 29, 1621-1624
37. Ma, T. Y. Intestinal epithelial barrier dysfunction in Crohn's disease Proc. Soc. Exp. Biol. Med. 1997, 214, 318-327
38. Nagano, Y.; Matsui, H.; Muramatsu, M.; Shimokawa, O.; Shibahara, T.; Yanaka, A.; Nakahara, A.; Matsuzaki, Y.; Tanaka, N.; Nakamura, Y. Rebamipide significantly inhibits indomethacin-induced mitochondrial damage, lipid peroxidation, and apoptosis in gastric epithelial RGM-1 cells Dig. Dis. Sci. 2005, 50, S76-S83
39. Kaneko, T.; Matsui, H.; Shimokawa, O.; Nakahara, A.; Hyodo, I. Cellular membrane fluidity measurement by fluorescence polarization in indomethacin-induced gastric cellular injury in vitro J. Gastroenterol. 2007, 42, 939-946
40. Tang, A. S.; Chikhale, P. J.; Shah, P. K.; Borchardt, R. T. Utilization of a human intestinal epithelial cell culture system (Caco-2) for evaluating cytoprotective agents Pharm. Res. 1993, 10, 1620-6 (Pubitemid 23325666)
41. Walsh-Reitz, M. M.; Huang, E. F.; Musch, M. W.; Chang, E. B.; Martin, T. E.; Kartha, S.; Toback, F. G. AMP-18 protects barrier function of colonic epithelial cells: role of tight junction proteins Am. J. Physiol. Gastrointest. Liver. Physiol. 2005, 289, G163-G171
42. Omatsu, T.; Naito, Y.; Handa, O.; Hayashi, N.; Mizushima, K.; Qin, Y.; Hirata, I.; Adachi, S.; Okayama, T.; Kishimoto, E.; Takagi, T.; Kokura, S.; Ichikawa, H.; Yoshikawa, T. Involvement of reactive oxygen species in indomethacin-induced apoptosis of small intestinal epithelial cells J. Gastroenterol. 2009, 19, 30-34
43. 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 Mol. Biol. Cell 2009, 20, 3930-3940
44. Vepa, S.; Scribner, W. M.; Parinandi, N. L.; English, D.; Garcia, J. G.; Natarajan, V. Hydrogen peroxide stimulates tyrosine phosphorylation of focal adhesion kinase in vascular endothelial cells Am. J. Physiol. 1999, 277, L150-L158
45. Sáenz-Morales, D.; Escribese, M. M.; Stamatakis, K.; Garcia-Martos, M.; Alegre, L.; Conde, E.; Perez-Sala, D.; Mampaso, F.; Garcia-Bermejo, M. L. Requirements for proximal tubule epithelial cell detachment in response to ischemia: Role of oxidative stress Exp. Cell. Res. 2006, 312, 3711-3727 (Pubitemid 44637176)
46. Banan, A.; Farhadi, A.; Fields, J. Z.; Zhang, L. J.; Shaikh, M.; Keshavarzian, A. The delta-isoform of protein kinase C causes inducible nitric-oxide synthase and nitric oxide up-regulation: Key mechanism for oxidant-induced carbonylation, nitration, and disassembly of the microtubule cytoskeleton and hyperpermeability of barrier of intestinal epithelia J. Pharmacol. Exp. Ther. 2003, 305, 482-494 (Pubitemid 36459161)
47. Jenner, A. M.; Rafter, J.; Halliwell, B. Human fecal water content of phenolics: The extent of colonic exposure to aromatic compounds Free Radical Biol. Med. 2005, 38, 763-772 (Pubitemid 40249747)
48. Fiorani, M.; Guidarelli, A.; Blasa, M.; Azzolini, C.; Candiracci, M.; Piatti, E.; Cantoni, O. Mitochondria accumulate large amounts of quercetin: Prevention of mitochondrial damage and release upon oxidation of the extramitochondrial fraction of the flavonoid J. Nutr. Biochem. 2010, 21, 397-404
49. Jaganath, I. B.; Mullen, W.; Edwards, C. A.; Crozier, A. The relative contribution of the small and large intestine to the absorption and metabolism of rutin in man Free Radical Res. 2006, 40, 1035-1046 (Pubitemid 44480544)
50. Del Rio, D.; Calani, L.; Cordero, C.; Salvatore, S.; Pellegrini, N.; Brighenti, F. Bioavailability and catabolism of green tea flavan-3-ols in humans Nutrition 2010, 26, 1110-1116
51. Del Rio, D.; Rodriguez-Mateos, A.; Spencer, J. P.; Tognolini, M.; Borges, G.; Crozier, A. Dietary (poly)phenolics in human health: Structures, bioavailability, and evidence of protective effects against chronic diseases Antioxid. Redox Signaling 2013, 18, 1818-1892
52. Chuenkitiyanon, S.; Pengsuparp, T.; Jianmongkol, S. Protective effect of quercetin on hydrogen peroxide-induced tight junction disruption Int. J. Toxicol. 2010, 29, 418-424
53. Amasheh, M.; Schlichter, S.; Amasheh, S.; Mankertz, J.; Zeitz, M.; Fromm, M.; Schulzke, J. D. Quercetin enhances epithelial barrier function and increases claudin-4 expression in Caco-2 cells J. Nutr. 2008, 138, 1067-1073 (Pubitemid 351769130)
54. Amasheh, M.; Luettig, J.; Amasheh, S.; Zeitz, M.; Fromm, M.; Schulzke, J. D. Effects of quercetin studied in colonic HT-29/B6 cells and rat intestine in vitro Ann. N. Y. Acad. Sci. 2012, 1258, 100-107