Dietary extra virgin olive oil polyphenols supplementation modulates DSS-induced chronic colitis in mice

Journal of Nutritional Biochemistry

Volumn 24, Issue 7, 2013, Pages 1401-1413

  Sánchez Fidalgo, Susana ^a   Cárdeno, Ana ^a   Sánchez Hidalgo, Marina ^a   Aparicio Soto, Marina ^a   De la Lastra, Catalina Alarcón ^a  

^a UNIVERSITY OF SEVILLE   (Spain)

Author keywords

Extra virgin olive oil; I B ; Polyphenol extract; PPAR ; Ulcerative colitis

Indexed keywords

CINNAMIC ACID; CYCLOOXYGENASE 2; DECARBOXYMETHYL LIGSTROSIDE AGLYCONE; DECARBOXYMETHYL OLEUROPEIN AGLYCONE; DOCUSATE SODIUM; DRINKING WATER; EXTRA VIRGIN OLIVE OIL; HYDROXYTYROSOL; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; LIGSTROSIDE AGLYCONE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; OLEUROPEIN AGLYCONE; PARA COUMARIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PHENOL DERIVATIVE; PINORESINOL; PLANT EXTRACT; POLYPHENOL DERIVATIVE; POLYPHENOL EXTRACT; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA; TYROSOL; TYROSYL ACETATE; UNCLASSIFIED DRUG; UNINDEXED DRUG; VANILLIC ACID; DEXTRAN SULFATE; OLIVE OIL; POLYPHENOL; PRIMER DNA; VEGETABLE OIL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL PROLIFERATION; CHEMICAL COMPOSITION; CHRONIC COLITIS; COLITIS; COLON; CONTROLLED STUDY; DIET SUPPLEMENTATION; DIETARY INTAKE; DISEASE ACTIVITY; DISEASE ACTIVITY INDEX; DRUG EFFICACY; FEMALE; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MOUSE; NONHUMAN; PROTEIN BLOOD LEVEL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; CHEMISTRY; CHRONIC DISEASE; NUCLEOTIDE SEQUENCE;

ANIMALIA; MUS;

ANIMALS; BASE SEQUENCE; CHRONIC DISEASE; COLITIS; DEXTRAN SULFATE; DNA PRIMERS; FEMALE; MICE; MICE, INBRED C57BL; PLANT OILS; POLYPHENOLS; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84879297592     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2012.11.008     Document Type: Article

References (79)

1. Molodecky N.A., Soon I.S., Rabi D.M., Ghali W.A., Ferris M., Chernoff G., et al. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology 2012, 142:46-54.
2. Kolios G., Valatas V., Ward S.G. Nitric oxide in inflammatory bowel disease: a universal messenger in an unsolved puzzle. Immunology 2004, 113:427-437.
3. Braus N.A., Elliott D.E. Advances in the pathogenesis and treatment of IBD. Clin Immunol 2009, 132:1-9.
4. Coskun M., Troelsen J.T., Nielsen O.H. The role of CDX2 in intestinal homeostasis and inflammation. Biochim Biophys Acta 2011, 1812:283-289.
5. Wei J., Feng J. Signaling pathways associated with inflammatory bowel disease. Recent Pat Inflamm Allergy Drug Discov 2010, 4:105-117.
6. Dubuquoy L., Rousseaux C., Thuru X., Peyrin-Biroulet L., Romano O., Chavatte P., et al. PPARgamma as a new therapeutic target in inflammatory bowel diseases. Gut 2006, 55:1341-1349.
7. Atreya I., Atreya R., Neurath M.F. NF-kappaB in inflammatory bowel disease. J Intern Med 2008, 263:591-596.
8. Bento A.F., Marcon R., Dutra R.C., Claudino R.F., Cola M., Leite D.F., et al. β-Caryophyllene inhibits dextran sulfate sodium-induced colitis in mice through CB2 receptor activation and PPARγ pathway. Am J Pathol 2011, 178:1153-1166.
9. Wahli W. A gut feeling of the PXR, PPAR and NF-kappaB connection. J Intern Med 2008, 263:613-619.
10. Bédard A., Riverin M., Dodin S., Corneau L., Lemieux S. Sex differences in the impact of the Mediterranean diet on cardiovascular risk profile. Br J Nutr 2012, 6:1-7.
11. Sofi F., Abbate R., Gensini G.F., Casini A. Accruing evidence on benefits of adherence to the Mediterranean diet on health: an updated systematic review and meta-analysis. Am J Clin Nutr 2010, 92:1189-1196.
12. Farr S.A., Price T.O., Dominguez L.J., Motisi A., Saiano F., Niehoff M.L., et al. Extra virgin olive oil improves learning and memory in SAMP8 mice. J Alzheimers Dis 2012, 28:81-92.
13. Bulló M., Lamuela-Raventós R., Salas-Salvadó J. Mediterranean diet and oxidation: nuts and olive oil as important sources of fat and antioxidants. Curr Top Med Chem 2011, 11:1797-1810.
14. Servili M., Esposto S., Fabiani R., Urbani S., Taticchi A., Mariucci F., et al. Phenolic compounds in olive oil: antioxidant, health and organoleptic activities according to their chemical structure. Inflammopharmacology 2009, 17:76-84.
15. Alarcón de la Lastra C., Sánchez-Fidalgo S., Villegas I., Motilva V. New pharmacological perspectives and therapeutic potential of PPAR-gamma agonists. Curr Pharm Des 2004, 10:3505-3524.
16. Sánchez-Fidalgo S., Villegas I., Ca'rdeno A., Talero E., Sánchez-Hidalgo M., Motilva V., et al. Extravirgin olive oil-enriched diet modulates DSS-colitis-associated colon carcinogenesis in mice. Clin Nutr 2010, 29:663-673.
17. Oliveras-Ferraros C., Fernández-Arroyo S., Vázquez-Martin A., Lozano-Sánchez J., Cufí S., Joven J., et al. Crude phenolic extracts from extra virgin olive oil circumvent de novo breast cancer resistance to HER1/HER2-targeting drugs by inducing GADD45-sensed cellular stress, G2/M arrest and hyperacetylation of Histone H3. Int J Oncol 2011, 38:1533-1547.
18. Escrich E., Moral R., Solanas M. Olive oil, an essential component of the Mediterranean diet, and breast cancer. Public Health Nutr 2011, 14:2323-2332.
19. Bermudez B., Lopez S., Ortega A., Varela L.M., Pacheco Y.M., Abia R., et al. Oleic acid in olive oil: from a metabolic framework toward a clinical perspective. Curr Pharm Des 2011, 17:831-843.
20. Escrich E., Solanas M., Moral R., Escrich R. Modulatory effects and molecular mechanisms of olive oil and other dietary lipids in breast cancer. Curr Pharm Des 2011, 17:813-830.
21. Visioli F., De La Lastra C.A., Andres-Lacueva C., Aviram M., Calhau C., Cassano A., et al. Polyphenols and human health: a prospectus. Crit Rev Food Sci Nutr 2011, 51:524-546.
22. Corona G., Spencer J.P., Dessì M.A. Extra virgin olive oil phenolics: absorption, metabolism, and biological activities in the GI tract. Toxicol Ind Health 2009, 25:285-293.
23. Frontela C., Canali R., Virgili F. Use of dietary phenols to modulate inflammatory bowel response. Gastroenterol Hepatol 2010, 33:307-312.
24. Sánchez-Fidalgo S., Cárdeno A., Villegas I., Talero E., de la Lastra C.A. Dietary supplementation of resveratrol attenuates chronic colonic inflammation in mice. Eur J Pharmacol 2010, 633:78-84.
25. Rosillo M.A., Sanchez-Hidalgo M., Cárdeno A., de la Lastra C.A. Protective effect of ellagic acid, a natural polyphenolic compound, in a murine model of Crohn's disease. Biochem Pharmacol 2011, 82:737-745.
26. Romano M., Vitaglione P., Sellitto S., D'Argenio G. Nutraceuticals for protection and healing of gastrointestinal mucosa. Curr Med Chem 2012, 19:109-117.
27. Sumbul S., Ahmad M.A., Mohd A., Mohd A. Role of phenolic compounds in peptic ulcer: an overview. J Pharm Bioallied Sci. 2011, 3:361-367.
28. Alvarez-Suarez J.M., Dekanski D., Ristić S., Radonjić N.V., Petronijević N.D., Giampieri F., et al. Strawberry polyphenols attenuate ethanol-induced gastric lesions in rats by activation of antioxidant enzymes and attenuation of MDA increase. PLoS One 2011, 6:e25878.
29. Villegas I., Sánchez-Fidalgo S., de la Lastra C.A. Chemopreventive effect of dietary curcumin on inflammation-induced colorectal carcinogenesis in mice. MolNutr Food Res 2011, 55:259-267.
30. Fini L., Piazzi G., Daoud Y., Selgrad M., Maegawa S., Garcia M., et al. Chemoprevention of intestinal polyps in ApcMin/+ mice fed with western or balanced diets by drinking annurca apple polyphenol extract. Cancer Prev Res (Phila) 2011, 4:907-915.
31. Xiao H., Hao X., Simi B., Ju J., Jiang H., Reddy B.S., et al. Green tea polyphenols inhibit colorectal aberrant crypt foci (ACF) formation and prevent oncogenic changes in dysplastic ACF in azoxymethane-treated F344 rats. Carcinogenesis 2008, 29:113-119.
32. Sánchez-Fidalgo S., Sánchez de Ibargüen L., Cárdeno A., Alarcón de la Lastra C. Influence of extra virgin olive oil diet enriched with hydroxytyrosol in a chronic DSS colitis model. Eur J Nutr 2012, 51:497-506.
33. Vazquez Roncero A., Janet del Valle M., Janet del Valle L. Componentes fenolicos de la aceituna. III. Polifenoles del aceite. Grasas aceites (B. Aires) 1976, 27:185-191.
34. Montedoro G., Servili M., Baldioli M., Miniati E. Simple and hydrolyzable phenolic compounds in virgin olive oil. 1. Their extraction, separation, and quantitative and semi quantitative evaluation by HPLC. J Agric Food Chem 1992, 40:1571-1576.
35. Allouche Y., Jiménez A., Gaforio J.J., Uceda M., Beltrán G. How heating affects extra virgin olive oil quality indexes and chemical composition. J Agric Food Chem 2007, 55:9646-9654.
36. Hrncirik K., Fritsche S. Comparability and reliability of different techniques for the determination of phenolic compounds in virgin olive oil. Eur J Lipid Sci Technol 2004, 106:540-549.
37. Melgar S., Karlsson A., Michaëlsson E. Acute colitis induced by dextran sulfate sodium progresses to chronicity in C57BL/6 but not in BALB/c mice: correlation between symptoms and inflammation. Am J Physiol Gastrointest Liver Physiol 2005, 288:G1328-G1338.
38. Dieleman L.A., Palmen M.J., Akol H., Bloemena E., Peña A.S., Meuwissen S.G., et al. Chronic experimental colitis induced by dextran sulphate sodium (DSS) is characterized by Th1 and Th2 cytokines. Clin Exp Immunol. 1998, 114:385-391.
39. Sánchez-Fidalgo S., Martín-Lacave I., Illanes M., Bruseghini L., Esteras A., Motilva V. Administration of l-arginine reduces the delay of the healing process caused by ibuprofen. Implication of COX and growth factors expression. Histol Histopathol 2005, 20:437-447.
40. Sánchez-Fidalgo S., Martín-Lacave I., Illanes M., Motilva V. Angiogenesis, cell proliferation and apoptosis in gastric ulcer healing. Effect of a selective cox-2 inhibitor. Eur J Pharmacol 2004, 505:187-194.
41. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
42. Okayasu I., Hatakeyama S., Yamada M., Ohkusa T., Inagaki Y., Nakaya R. A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology 1990, 98:694-702.
43. Kubben F.J., Peeters-Haesevoets A., Engels L.G., Baeten C.G., Schutte B., Arends J.W., et al. Proliferating cell nuclear antigen (PCNA): a new marker to study human colonic cell proliferation. Gut 1994, 35:530-535.
44. Boskou D. Olive oil. World Rev Nutr Diet 2000, 87:56-77.
45. Visioli F., Bernardini E. Extra virgin olive oil's polyphenols: biological activities. Curr Pharm Des 2011, 17:786-804.
46. Lopez-Miranda J., Perez-Jimenez F., Ros E., De Caterina R., Badimón L., Covas M.I., et al. Olive oil and health: summary of the II international conference on olive oil and health consensus report, Jaen and Cordoba (Spain) 2008. Nutr Metab Cardiovasc Dis 2010, 20:284-294.
47. Nieto N., Torres M.I., Ríos A., Gil A. Dietary polyunsaturated fatty acids improve histological and biochemical alterations in rats with experimental ulcerative colitis. J Nutr 2002, 132:11-19.
48. Camuesco D., Gálvez J., Nieto A., Comalada M., Rodri{dotless}'guez-Cabezas M.E., Concha A., et al. Dietary olive oil supplemented with fish oil, rich in EPA and DHA (n-3) polyunsaturated fatty acids, attenuates colonic inflammation in rats with DSS-induced colitis. J Nutr 2005, 135:687-694.
49. Hegazi R.A., Saad R.S., Mady H., Matarese L.E., O'Keefe S., Kandil H.M. Dietary fatty acids modulate chronic colitis, colitis associated colon neoplasia and COX-2 expression in IL-10 knockout mice. Nutrition 2006, 22:275-282.
50. Kontou N., Psaltopoulou T., Panagiotakos D., Dimopoulos M.A., Linos A. The Mediterranean diet in cancer prevention: a review. J Med Food 2011, 14:1065-1078.
51. Sandborn W.J., Targan S.R. Biologic therapy of inflammatory bowel disease. Gastroenterology 2002, 122:1592-1608.
52. MacDermott R.P. Chemokines in the inflammatory bowel diseases. J Clin Immunol. 1999, 19:266-272.
53. McGuckin M.A., Eri R., Simms L.A., Florin T.H., Radford-Smith G. Intestinal barrier dysfunction in inflammatory bowel diseases. Inflamm Bowel Dis 2009, 15:100-113.
54. Bento A.F., Leite D.F., Claudino R.F., Hara D.B., Leal P.C., Calixto J.B. he selective nonpeptide CXCR2 antagonist SB225002 ameliorates acute experimental colitis in mice. J Leukoc Biol 2008, 84:1213-1221.
55. Mukai Y., Sato S. Polyphenol-containing azuki bean (Vigna angularis) seed coats attenuate vascular oxidative stress and inflammation in spontaneously hypertensive rats. J Nutr Biochem 2011, 22:16-21.
56. Daleprane J.B., da Silva Freitas V., Pacheco A., Rudnicki M., Faine L.A., Dörr F.A., et al. Anti-atherogenic and anti-angiogenic activities of polyphenols from propolis. J Nutr Biochem 2012, 23:557-566.
57. Ikarashi N., Toda T., Okaniwa T., Ito K., Ochiai W., Sugiyama K. Anti-obesity and anti-diabetic effects of acacia polyphenol in obese diabetic KKAy mice fed high-fat diet. Evid Based Complement Alternat Med. 2011, 2011:952031-952041.
58. Vetuschi A., Latella G., Sferra R., Caprilli R., Gaudio E. Increased proliferation and apoptosis of colonic epithelial cells in dextran sulfate sodium induced colitis in rats. Dig Dis Sci 2002, 47:1447-1457.
59. D'Argenio G., Mazzone G., Tuccillo C., Ribecco M.T., Graziani G., Gravina A.G., et al. Apple polyphenols extract (APE) improves colon damage in a rat model of colitis. Dig Liver Dis 2012, 44:555-562.
60. Rosillo M.A., Sánchez-Hidalgo M., Cárdeno A., Aparicio-Soto M., Sánchez-Fidalgo S., Villegas I., et al. Dietary supplementation of an ellagic acid-enriched pomegranate extract attenuates chronic colonic inflammation in rats. Pharm Res 2012, 66:235-242.
61. Tsatsanis C., Androulidaki A., Venihaki M., Margioris A.N. Signalling networks regulating cyclooxygenase-2. Int J Biochem Cell Biol 2006, 38:1654-1661.
62. Corona G., Deiana M., Incani A., Vauzour D., Dessì M.A., Spencer J.P. Inhibition of p38/CREB phosphorylation and COX-2 expression by olive oil polyphenols underlies their anti-proliferative effects. Biochem Biophys Res Commun 2007, 362:606-611.
63. Hollenbach E., Neumann M., Vieth M., Roessner A., Malfertheiner P., Naumann M. Inhibition of p38 MAP kinase- and RICK/NFkappaB-signaling suppresses inflammatory bowel disease. FASEB J 2004, 18:1550-1552.
64. Assi K., Pillai R., Gomez-Munoz A., Owen D., Salh B. The specific JNK inhibitor SP600125 targets tumour necrosis factor-alpha production and epithelial cell apoptosis in acute murine colitis. Immunology 2006, 118:112-121.
65. Chromik A.M., Müller A.M., Körner J., Belyaev O., Holland-Letz T., Schmitz F., et al. Genetic deletion of JNK1 and JNK2 aggravates the DSS-induced colitis in mice. J Invest Surg 2007, 20:23-33.
66. Palmieri D., Aliakbarian B., Casazza A.A., Ferrari N., Spinella G., Pane B., et al. Effects of polyphenol extract from olive pomace on anoxia-induced endothelial dysfunction. Microvasc Res 2012, 83(3):281-289.
67. Cheung K.L., Kong A.N. Molecular targets of dietary phenethylisothiocyanate and sulforaphane for cancer chemoprevention. AAPS J 2010, 12:87-97.
68. Itzkowitz S.H. Molecular biology of dysplasia and cancer in inflammatory bowel disease. Gastroenterol Clin North Am 2006, 35:553-571.
69. Coskun M., Olsen J., Seidelin J.B., Nielsen O.H. MAP kinases in inflammatory bowel disease. Clin Chim Acta 2011, 412:513-520.
70. Schreiber S., Nikolaus S., Hampe J. Activation of nuclear factor kappa B inflammatory bowel disease. Gut 1998, 42:477-484.
71. Wullaert A., Bonnet M.C., Pasparakis M. NF-kappaB in the regulation of epithelial homeostasis and inflammation. Cell Res 2011, 21:146-158.
72. Sanchez-Hidalgo M., Martin A.R., Villegas I., Alarcon De La Lastra C. Rosiglitazone, an agonist of peroxisome proliferator-activated receptor gamma, reduces chronic colonic inflammation in rats. Biochem Pharmacol 2005, 69:1733-1744.
73. Brunelleschi S., Bardelli C., Amoruso A., Gunella G., Ieri F., Romani A., et al. Minor polar compounds extra-virgin olive oil extract (MPC-OOE) inhibits NF-kappa B translocation in human monocyte/macrophages. Pharmacol Res 2007, 56:542-549.
74. Dubuquoy L., Jansson E.A., Deeb S., Rakotobe S., Karoui M., Colombel J.F., et al. Impaired expression of peroxisome proliferator-activated receptor gamma in ulcerative colitis. Gastroenterology 2003, 124:1265-1276.
75. Buisine M.P., Desreumaux P., Leteurtre E., Copin M.C., Colombel J.F., Porchet N., et al. Mucin gene expression in intestinal epithelial cells in Crohn's disease. Gut 2001, 49:544-551.
76. Annese V., Rogai F., Settesoldi A., Bagnoli S. PPARγ in inflammatory bowel disease. PPAR Res. 2012, 2012:620839.
77. Lewis S.N., Brannan L., Guri A.J., Lu P., Hontecillas R., Bassaganya-Riera J., et al. Dietary α-eleostearic acid ameliorates experimental inflammatory bowel disease in mice by activating peroxisome proliferator-activated receptor-γ. PLoS One 2011, 6:e24031.
78. Caelles C., González-Sancho J.M., Muñoz A. Nuclear hormone receptor antagonism with AP-1 by inhibition of the JNK pathway. Genes Dev 1997, 11:3351-3364.
79. Hsu W.H., Lee B.H., Liao T.H., Hsu Y.W., Pan T.M. Monascus-fermented metabolite monascin suppresses inflammation via PPAR-γ regulation and JNK inactivation in THP-1 monocytes. Food Chem Toxicol 2012, 50:1178-1186.