Molecular mechanisms of gastrointestinal protection by quercetin against indomethacin-induced damage: Role of NF-κB and Nrf2

Journal of Nutritional Biochemistry

Volumn 27, Issue , 2016, Pages 289-298

  Carrasco Pozo, Catalina ^a   Castillo, Rodrigo L ^a   Beltrán, Caroll ^b   Miranda, Alfonso ^b   Fuentes, Jocelyn ^c   Gotteland, Martin ^a,c  

^a UNIVERSITY OF CHILE   (Chile)

^b HOSPITAL CLÍNICO UNIVERSIDAD DE CHILE   (Chile)

^c UNIVERSITY OF CHILE   (Chile)

Author keywords

Indomethacin; Inflammation; NF kB; Nrf2; Oxidative stress; Quercetin

Indexed keywords

FLAVONOL; GLUTATHIONE PEROXIDASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDOMETACIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 8; MYELOPEROXIDASE; PADGEM PROTEIN; PROSTAGLANDIN E2; QUERCETIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR NRF2; XANTHINE OXIDASE; NFE2L2 PROTEIN, RAT; NONSTEROID ANTIINFLAMMATORY AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; CACO 2 CELL LINE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DIGESTIVE SYSTEM INJURY; DRUG MECHANISM; ENZYME ACTIVITY; ENZYME INHIBITION; GASTRIC MUCOSA; ILEUM MUCOSA; NONHUMAN; OXIDATIVE STRESS; PROSTAGLANDIN SYNTHESIS; PROTEIN LOCALIZATION; RAT; SINGLE DRUG DOSE; ANIMAL; CACO-2 CELL LINE; DRUG EFFECTS; GASTROINTESTINAL TRACT; HUMAN; MALE; METABOLISM; SPRAGUE DAWLEY RAT;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; CACO-2 CELLS; GASTROINTESTINAL TRACT; HUMANS; INDOMETHACIN; MALE; NF-E2-RELATED FACTOR 2; NF-KAPPA B; QUERCETIN; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84952861968     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2015.09.016     Document Type: Article

References (56)

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 indometacin-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., 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.
5. Carrasco-Pozo C., Morales P., Gotteland M. Polyphenols protect the epithelial barrier function of Caco-2 cells exposed to indomethacin through the modulation of occludin and zonula occludens-1 expression. J Agric Food Chem 2013, 61:5291-5297.
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, 12:26.
7. 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, 59:6459-6466.
8. Ganguly K., Swarnakar S. Chronic gastric ulceration causes matrix metalloproteinases-9 and -3 augmentation: alleviation by melatonin. Biochimie 2012, 94:2687-2698.
9. Lee H.J., Han Y.M., Kim E.H., Kim Y.J., Hahm K.B. A possible involvement of Nrf2-mediated heme oxygenase-1 up-regulation in protective effect of the proton pump inhibitor pantoprazole against indomethacin-induced gastric damage in rats. BMC Gastroenterol 2012, 12:12-143.
10. Mouzaoui S., Djerdjouri B., Makhezer N., Kroviarski Y., El-Benna J., Dang P.M. Tumor necrosis factor-alpha-induced colitis increases NADPH oxidase 1 expression, oxidative stress, and neutrophil recruitment in the colon: preventive effect of apocynin. Mediators Inflamm 2014, 2014:312484. [Epub 2014 Sep 4]. 10.1155/2014/312484.
11. Futosi K., Fodor S., Mocsai A. Reprint of Neutrophil cell surface receptors and their intracellular signal transduction pathways. Int Immunopharmacol 2013, 17:1185-1197.
12. Morise Z., Granger D.N., Fuseler J.W., Anderson D.C., Grisham M.B. Indomethacin induced gastropathy in CD18, intercellular adhesion molecule 1, or P-selectin deficient mice. Gut 1999, 45:523-528.
13. Chan F.K. Primer: managing NSAID-induced ulcer complications--balancing gastrointestinal and cardiovascular risks. Nat Clin Pract Gastroenterol Hepatol 2006, 3:563-573.
14. Stavric B. Quercetin in our diet: from potent mutagen to probable anticarcinogen. Clin Biochem 1994, 27:245-248.
15. Ovaskainen M.L., Torronen R., Koponen J.M., Sinkko H., Hellstrom J., Reinivuo H., et al. Dietary intake and major food sources of polyphenols in Finnish adults. J Nutr 2008, 138:562-566.
16. Perez-Jimenez J., Fezeu L., Touvier M., Arnault N., Manach C., Hercberg S., et al. Dietary intake of 337 polyphenols in French adults. Am J Clin Nutr 2011, 93:1220-1228.
17. Hertog M.G.L., Hollman P.C.H., Katan M.B. Content of potentially anticarcinogenic flavonoids of 28 vegetables and 9 fruits commonly consumed in the Netherlands. J Agric Food Chem 1992, 40:2379-2383.
18. 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.
19. Tanigawa S., Fujii M., Hou D.X. Action of Nrf2 and Keap1 in ARE-mediated NQO1 expression by quercetin. Free Radic Biol Med 2007, 42:1690-1703.
20. Hur W., Gray N.S. Small molecule modulators of antioxidant response pathway. Curr Opin Chem Biol 2011, 15:162-173.
21. Chirumbolo S. The role of quercetin, flavonols and flavones in modulating inflammatory cell function. Inflamm Allergy Drug Targets 2010, 9:263-285.
22. Bryan H.K., Olayanju A., Goldring C.E., Park B.K. The Nrf2 cell defence pathway: Keap1-dependent and -independent mechanisms of regulation. Biochem Pharmacol 2013, 85:705-717.
23. Jung K.A., Kwak M.K. The Nrf2 system as a potential target for the development of indirect antioxidants. Molecules 2010, 15:7266-7291.
24. Verhelst K., Carpentier I., Beyaert R. Regulation of TNF-induced NF-kappaB activation by different cytoplasmic ubiquitination events. Cytokine Growth Factor Rev 2011, 22:277-286.
25. Ramaswami S., Hayden M.S. Electrophoretic mobility shift assay analysis of NF-kappaB DNA binding. Methods Mol Biol 2015, 1280:3-13.
26. Deryckere F., Gannon F. A one-hour minipreparation technique for extraction of DNA-binding proteins from animal tissues. Biotechniques 1994, 16:405.
27. Castillo R., Rodrigo R., Perez F., Cereceda M., Asenjo R., Zamorano J., et al. Antioxidant therapy reduces oxidative and inflammatory tissue damage in patients subjected to cardiac surgery with extracorporeal circulation. Basic Clin Pharmacol Toxicol 2011, 108:256-262.
28. Zhang L., Li N., Caicedo R., Neu J. Alive and dead Lactobacillus rhamnosus GG decrease tumor necrosis factor-alpha-induced interleukin-8 production in Caco-2 cells. J Nutr 2005, 135:1752-1756.
29. Nebot C., Moutet M., Huet P., Xu J.Z., Yadan J.C., Chaudiere J. Spectrophotometric assay of superoxide dismutase activity based on the activated autoxidation of a tetracyclic catechol. Anal Biochem 1993, 214:442-451.
30. Flohe L., Gunzler W.A. Assays of glutathione peroxidase. Methods Enzymol 1984, 105:114-121.
31. Carrasco-Pozo C., Gotteland M., Castillo R.L., Chen C. 3,4-dihydroxyphenylacetic acid, a microbiota-derived metabolite of quercetin, protects against pancreatic beta-cells dysfunction induced by high cholesterol. Exp Cell Res 2015, 4:115-119.
32. Tammali R., Ramana K.V., Srivastava S.K. Aldose reductase regulates TNF-alpha-induced PGE2 production in human colon cancer cells. Cancer Lett 2007, 252:299-306.
33. Li J.Y., Lai Y.J., Yeh H.I., Chen C.L., Sun S., Wu S.J., et al. Atrial gap junctions, NF-kappaB and fibrosis in patients undergoing coronary artery bypass surgery: the relationship with postoperative atrial fibrillation. Cardiology 2009, 112:81-88.
34. Banerjee A.K. Non-steroidal anti-inflammatory drugs (NSAIDs) and the ileum. J R Soc Med 1990, 83:600-
35. Wallace J.L., McKnight W., Miyasaka M., Tamatani T., Paulson J., Anderson D.C., et al. Role of endothelial adhesion molecules in NSAID-induced gastric mucosal injury. Am J Physiol 1993, 265:G993-G998.
36. Morandini R., Boeynaems J.M., Duhant X., Jacquemotte F., Kinnaert E., Ghanem G. SODs are involved in the regulation of ICAM-1 expression in human melanoma and endothelial cells. Cell Mol Biol 1999, 45:1053-1063.
37. Siomek A. NF-kappaB signaling pathway and free radical impact. Acta Biochim Pol 2012, 59:323-331.
38. DiVietro J.A., Smith M.J., Smith B.R., Petruzzelli L., Larson R.S., Lawrence M.B. Immobilized IL-8 triggers progressive activation of neutrophils rolling in vitro on P-selectin and intercellular adhesion molecule-1. J Immunol 2001, 167:4017-4025.
39. Roebuck K.A. Oxidant stress regulation of IL-8 and ICAM-1 gene expression: differential activation and binding of the transcription factors AP-1 and NF-kappaB (Review). Int J Mol Med 1999, 4:223-230.
40. Lu C.Y., Yang Y.C., Li C.C., Liu K.L., Lii C.K., Chen H.W. Andrographolide inhibits TNFalpha-induced ICAM-1 expression via suppression of NADPH oxidase activation and induction of HO-1 and GCLM expression through the PI3K/Akt/Nrf2 and PI3K/Akt/AP-1 pathways in human endothelial cells. Biochem Pharmacol 2014, 91:40-50.
41. Kobuchi H., Roy S., Sen C.K., Nguyen H.G., Packer L. Quercetin inhibits inducible ICAM-1 expression in human endothelial cells through the JNK pathway 1999.
42. Ying B., Yang T., Song X., Hu X., Fan H., Lu X., et al. Quercetin inhibits IL-1 beta-induced ICAM-1 expression in pulmonary epithelial cell line A549 through the MAPK pathways. Mol Biol Rep 2009, 36:1825-1832.
43. Rogerio A.P., Dora C.L., Andrade E.L., Chaves J.S., Silva L.F., Lemos-Senna E., et al. Anti-inflammatory effect of quercetin-loaded microemulsion in the airways allergic inflammatory model in mice. Pharmacol Res 2010, 61:288-297.
44. Suzuki H., Nishizawa T., Tsugawa H., Mogami S., Hibi T. Roles of oxidative stress in stomach disorders. J Clin Biochem Nutr 2012, 50:35-39.
45. Kanter M., Coskun O., Uysal H. The antioxidative and antihistaminic effect of Nigella sativa and its major constituent, thymoquinone on ethanol-induced gastric mucosal damage. Arch Toxicol 2006, 80:217-224.
46. Pi J., Bai Y., Reece J.M., Williams J., Liu D., Freeman M.L., et al. Molecular mechanism of human Nrf2 activation and degradation: role of sequential phosphorylation by protein kinase CK2. Free Radic Biol Med 2007, 42:1797-1806.
47. Shih P.H., Yen G.C. Differential expressions of antioxidant status in aging rats: the role of transcriptional factor Nrf2 and MAPK signaling pathway. Biogerontology 2007, 8:71-80.
48. Li M.H., Cha Y.N., Surh Y.J. Peroxynitrite induces HO-1 expression via PI3K/Akt-dependent activation of NF-E2-related factor 2 in PC12 cells. Free Radic Biol Med 2006, 41:1079-1091.
49. Granado-Serrano A.B., Martin M.A., Bravo L., Goya L., Ramos S. Quercetin modulates Nrf2 and glutathione-related defenses in HepG2 cells: involvement of p38. Chem Biol Interact 2012, 195:154-164.
50. Yao P., Nussler A., Liu L., Hao L., Song F., Schirmeier A., et al. Quercetin protects human hepatocytes from ethanol-derived oxidative stress by inducing heme oxygenase-1 via the MAPK/Nrf2 pathways. J Hepatol 2007, 47:253-261.
51. Yeh C.T., Chiu H.F., Yen G.C. Protective effect of sulforaphane on indomethacin-induced cytotoxicity via heme oxygenase-1 expression in human intestinal Int 407 cells. Mol Nutr Food Res 2009, 53:1166-1176.
52. Jin W., Wang H., Yan W., Xu L., Wang X., Zhao X., et al. Disruption of Nrf2 enhances upregulation of nuclear factor-kappaB activity, proinflammatory cytokines, and intercellular adhesion molecule-1 in the brain after traumatic brain injury. Mediators Inflamm 2008, 725174:25.
53. Kim J., Cha Y.N., Surh Y.J. A protective role of nuclear factor-erythroid 2-related factor-2 (Nrf2) in inflammatory disorders. Mutat Res 2010, 690:12-23.
54. Price K.R., Rhodes M.J.C. Analysis of the major flavonol glycosides present in four varieties of onion (Allium cepa) and changes in composition resulting from autolysis. J Sci Food Agric 1997, 74:331-339.
55. Boots A.W., Haenen G.R., Bast A. Health effects of quercetin: from antioxidant to nutraceutical. Eur J Pharmacol 2008, 585:325-337.
56. Reagan-Shaw S., Nihal M., Ahmad N. Dose translation from animal to human studies revisited. FASEB J 2008, 22:659-661.