Oral administration of the flavonoid myricitrin prevents dextran sulfate sodium-induced experimental colitis in mice through modulation of PI3K/Akt signaling pathway

Molecular Nutrition and Food Research

Volumn 57, Issue 11, 2013, Pages 1938-1949

  Schwanke, Raquel Cristina ^a   Marcon, Rodrigo ^a   Meotti, Flavia Carla ^a,b   Bento, Allisson Freire ^a   Dutra, Rafael Cypriano ^a   Pizzollatti, Moacir Geraldo ^a   Calixto, João B ^a  

^a FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

DSS induced colitis; MAPK; Myricitrin; NF B; PI3K Akt pathway

Indexed keywords

ANTIINFLAMMATORY AGENT; CXCL1 CHEMOKINE; CXCL1 PROTEIN, MOUSE; CYCLOOXYGENASE 2; DEXTRAN SULFATE; FLAVONOID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE P38; MYRICETIN 3 RHAMNOSIDE; NOS2 PROTEIN, MOUSE; PHOSPHATIDYLINOSITOL 3 KINASE; PRKCE PROTEIN, MOUSE; PROTEIN KINASE B; PROTEIN KINASE C EPSILON; PTGS2 PROTEIN, MOUSE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL; ARTICLE; BODY WEIGHT; CHEMICALLY INDUCED DISORDER; COLITIS; COLON; DOSE RESPONSE; DRUG EFFECT; DSS-INDUCED COLITIS; GENETICS; MALE; MAPK; METABOLISM; MOUSE; NF-ΚB; ORAL DRUG ADMINISTRATION; PHOSPHORYLATION; PI3K/AKT PATHWAY; SIGNAL TRANSDUCTION;

DSS-INDUCED COLITIS; MAPK; MYRICITRIN; NF-ΚB; PI3K/AKT PATHWAY;

ADMINISTRATION, ORAL; ANIMALS; ANTI-INFLAMMATORY AGENTS; BODY WEIGHT; CHEMOKINE CXCL1; COLITIS; COLON; CYCLOOXYGENASE 2; DEXTRAN SULFATE; DOSE-RESPONSE RELATIONSHIP, DRUG; FLAVONOIDS; INTERLEUKIN-6; MALE; MAP KINASE SIGNALING SYSTEM; MICE; NF-KAPPA B; NITRIC OXIDE SYNTHASE TYPE II; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTEIN KINASE C-EPSILON; PROTO-ONCOGENE PROTEINS C-AKT; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84886802690     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201300134     Document Type: Article

References (63)

1. MacDonald, T. T., Monteleone, I., Fantini, M. C., Monteleone, G., Regulation of homeostasis and inflammation in the intestine. Gastroenterology 2011, 140, 1768-1775.
2. Cadwell, K., Liu, J. Y., Brown, S. L., Miyoshi, H. et al., A key role for autophagy and the autophagy gene Atg16l1 in mouse and human intestinal Paneth cells. Nature 2008, 456, 259-263.
3. Wei, J., Feng, J., Signaling pathways associated with inflammatory bowel disease. Recent Pat. Inflamm. Allergy Drug Discov. 2010, 4, 105-117.
4. Santangelo, C., Vari, R., Scazzocchio, B., Di Benedetto, R. et al., Polyphenols, intracellular signalling and inflammation. Ann. Ist Super Sanita 2007, 43, 394-405.
5. Ruiz, P. A., Haller, D., Functional diversity of flavonoids in the inhibition of the proinflammatory NF-kappaB, IRF, and Akt signaling pathways in murine intestinal epithelial cells. J. Nutr. 2006, 136, 664-671.
6. Ruiz, P. A., Braune, A., Holzlwimmer, G., Quintanilla-Fend, L. et al., Quercetin inhibits TNF-induced NF-kappaB transcription factor recruitment to proinflammatory gene promoters in murine intestinal epithelial cells. J. Nutr. 2007, 137, 1208-1215.
7. Kwon, K. H., Murakami, A., Tanaka, T., Ohigashi, H., Dietary rutin, but not its aglycone quercetin, ameliorates dextran sulfate sodium-induced experimental colitis in mice: attenuation of pro-inflammatory gene expression. Biochem. Pharmacol. 2005, 69, 395-406.
8. Ferry, D. R., Smith, A., Malkhandi, J., Fyfe, D. W. et al., Phase I clinical trial of the flavonoid quercetin: pharmacokinetics and evidence for in vivo tyrosine kinase inhibition. Clin. Cancer Res. 1996, 2, 659-668.
9. Schmeda-Hirschmann, G., Theoduloz, C., Franco, L., Ferro, E. et al., Preliminary pharmacological studies on Eugenia uniflora leaves: xanthine oxidase inhibitory activity. J. Ethnopharmacol. 1987, 21, 183-186.
10. Edenharder, R., Grunhage, D., Free radical scavenging abilities of flavonoids as mechanism of protection against mutagenicity induced by tert-butyl hydroperoxide or cumene hydroperoxide in Salmonella typhimurium TA102. Mutat. Res. 2003, 540, 1-18.
11. Fernandez, S. P., Nguyen, M., Yow, T. T., Chu, C. et al., The flavonoid glycosides, myricitrin, gossypin and naringin exert anxiolytic action in mice. Neurochem. Res. 2009, 34, 1867-1875.
12. Pereira, M., Siba, I. P., Chioca, L. R., Correia, D. et al., Myricitrin, a nitric oxide and protein kinase C inhibitor, exerts antipsychotic-like effects in animal models. Prog. Neuropsychopharmacol. Biol. Psychiat. 2011, 35, 1636-1644.
13. Meotti, F. C., Luiz, A. P., Pizzolatti, M. G., Kassuya, C. A. et al., Analysis of the antinociceptive effect of the flavonoid myricitrin: evidence for a role of the L-arginine-nitric oxide and protein kinase C pathways. J. Pharmacol. Exp. Ther. 2006b, 316, 789-796.
14. Meotti, F. C., Missau, F. C., Ferreira, J., Pizzolatti, M. G. et al., Anti-allodynic property of flavonoid myricitrin in models of persistent inflammatory and neuropathic pain in mice. Biochem. Pharmacol. 2006a, 72, 1707-1713.
15. Shimosaki, S., Tsurunaga, Y., Itamura, H., Nakamura, M., Anti-allergic effect of the flavonoid myricitrin from Myrica rubra leaf extracts in vitro and in vivo. Nat. Prod. Res. 2011, 25, 374-380.
16. Meotti, F. C., Posser, T., Missau, F. C., Pizzolatti, M. G. et al., Involvement of p38MAPK on the antinociceptive action of myricitrin in mice. Biochem. Pharmacol. 2007b, 74, 924-931.
17. Chen, Y., Yang, L., Lee, T. J., Oroxylin A inhibition of lipopolysaccharide-induced iNOS and COX-2 gene expression via suppression of nuclear factor-kappaB activation. Biochem. Pharmacol. 2000, 59, 1445-1457.
18. Meotti, F. C., Senthilmohan, R., Harwood, D. T., Missau, F. C. et al., Myricitrin as a substrate and inhibitor of myeloperoxidase: implications for the pharmacological effects of flavonoids. Free Radic Biol. Med. 2008, 44, 109-120.
19. Franco, J. L., Posser, T., Missau, F., Pizzolatti, M. G. et al., Structure-activity relationship of flavonoids derived from medicinal plants in preventing methylmercury-induced mitochondrial dysfunction. Environ. Toxicol. Pharmacol. 2010, 30, 272-278.
20. Agrawal, P. K. (Ed.), Studies in Organic Chemistry 39: Carbon-13 NMR of Flavonoids, Elsevier Science Publishers, New York 1989.
21. Bento, A. F., Marcon, R., Dutra, R. C., Claudino, R. F. et al., beta-Caryophyllene inhibits dextran sulfate sodium-induced colitis in mice through CB2 receptor activation and PPARgamma pathway. Am. J. Pathol. 2011a, 178, 1153-1166.
22. Wirtz, S., Neufert, C., Weigmann, B., Neurath, M. F., Chemically induced mouse models of intestinal inflammation. Nat. Protoc. 2007, 2, 541-546.
23. Cooper, H. S., Murthy, S. N., Shah, R. S., Sedergran, D. J., Clinicopathologic study of dextran sulfate sodium experimental murine colitis. Lab. Invest. 1993, 69, 238-249.
24. Ghia, J. E., Blennerhassett, P., Collins, S. M., Impaired parasympathetic function increases susceptibility to inflammatory bowel disease in a mouse model of depression. J. Clin. Invest. 2008, 118, 2209-2218.
25. Kimball, E. S., Wallace, N. H., Schneider, C. R., D'Andrea, M. R. et al., Vanilloid receptor 1 antagonists attenuate disease severity in dextran sulphate sodium-induced colitis in mice. Neurogastroenterol. Motil. 2004, 16, 811-818.
26. Rath, H. C., Herfarth, H. H., Ikeda, J. S., Grenther, W. B. et al., Normal luminal bacteria, especially Bacteroides species, mediate chronic colitis, gastritis, and arthritis in HLA-B27/human beta2 microglobulin transgenic rats. J. Clin. Invest. 1996, 98, 945-953.
27. Van der Sluis, M., De Koning, B. A., De Bruijn, A. C., Velcich, A. et al., Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology 2006, 131, 117-129.
28. + regulatory T cells. Br. J. Pharmacol. 2011a, 163, 358-374.
29. Lowry, O. H., Rosebrough, N. J., Farr, A. L., Randall, R. J., Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951, 193, 265-275.
30. Lallena, M. J., Diaz-Meco, M. T., Bren, G., Paya, C. V. et al., Activation of IkappaB kinase beta by protein kinase C isoforms. Mol. Cell Biol. 1999, 19, 2180-2188.
31. Toton, E., Ignatowicz, E., Skrzeczkowska, K., Rybczynska, M., Protein kinase C epsilon as a cancer marker and target for anticancer therapy. Pharmacol. Rep. 2011, 63, 19-29.
32. Ferreira, J., Triches, K. M., Medeiros, R., Calixto, J. B., Mechanisms involved in the nociception produced by peripheral protein kinase C activation in mice. Pain 2005, 117, 171-181.
33. Baumgart, D. C., Sandborn, W. J., Inflammatory bowel disease: clinical aspects and established and evolving therapies. Lancet 2007a, 369, 1641-1657.
34. Romier, B., Schneider, Y. J., Larondelle, Y., During, A., Dietary polyphenols can modulate the intestinal inflammatory response. Nutr. Rev. 2009, 67, 363-378.
35. Comalada, M., Camuesco, D., Sierra, S., Ballester, I. et al., In vivo quercitrin anti-inflammatory effect involves release of quercetin, which inhibits inflammation through down-regulation of the NF-kappaB pathway. Eur. J. Immunol. 2005, 35, 584-592.
36. Camuesco, D., Comalada, M., Rodriguez-Cabezas, M. E., Nieto, A. et al., The intestinal anti-inflammatory effect of quercitrin is associated with an inhibition in iNOS expression. Br. J. Pharmacol. 2004, 143, 908-918.
37. Huang, X. L., Xu, J., Zhang, X. H., Qiu, B. Y. et al., PI3K/Akt signaling pathway is involved in the pathogenesis of ulcerative colitis. Inflamm. Res. 2011, 60, 727-734.
38. Burgering, B. M., Coffer, P. J., Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature 1995, 376, 599-602.
39. Franke, T. F., Kaplan, D. R., Cantley, L. C., Toker, A., Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3, 4-bisphosphate. Science 1997, 275, 665-668.
40. Selvaraj, S. K., Giri, R. K., Perelman, N., Johnson, C. et al., Mechanism of monocyte activation and expression of proinflammatory cytochemokines by placenta growth factor. Blood 2003, 102, 1515-1524.
41. Agullo, G., Gamet-Payrastre, L., Manenti, S., Viala, C. et al., Relationship between flavonoid structure and inhibition of phosphatidylinositol 3-kinase: a comparison with tyrosine kinase and protein kinase C inhibition. Biochem. Pharmacol. 1997, 53, 1649-1657.
42. Gamet-Payrastre, L., Manenti, S., Gratacap, M. P., Tulliez, J. et al., Flavonoids and the inhibition of PKC and PI 3-kinase. Gen. Pharmacol. 1999, 32, 279-286.
43. Kyriakis, J. M., Avruch, J., Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol. Rev. 2001, 81, 807-869.
44. Coskun, M., Olsen, J., Seidelin, J. B., Nielsen, O. H., MAP kinases in inflammatory bowel disease. Clin. Chim. Acta 2011, 412, 513-520.
45. Kaminska, B., MAPK signalling pathways as molecular targets for anti-inflammatory therapy-from molecular mechanisms to therapeutic benefits. Biochim. Biophys. Acta 2005, 1754, 253-262.
46. Carter, A. B., Knudtson, K. L., Monick, M. M., Hunninghake, G. W., The p38 mitogen-activated protein kinase is required for NF-kappaB-dependent gene expression. The role of TATA-binding protein (TBP). J. Biol. Chem. 1999, 274, 30858-30863.
47. Carter, A. B., Hunninghake, G. W., A constitutive active MEK → ERK pathway negatively regulates NF-kappa B-dependent gene expression by modulating TATA-binding protein phosphorylation. J. Biol. Chem. 2000, 275, 27858-27864.
48. Spehlmann, M. E., Eckmann, L., Nuclear factor-kappa B in intestinal protection and destruction. Curr. Opin. Gastroenterol. 2009, 25, 92-99.
49. Karin, M., Lin, A., NF-kappaB at the crossroads of life and death. Nat. Immunol. 2002, 3, 221-227.
50. Kimura, H., Hokari, R., Miura, S., Shigematsu, T. et al., Increased expression of an inducible isoform of nitric oxide synthase and the formation of peroxynitrite in colonic mucosa of patients with active ulcerative colitis. Gut 1998, 42, 180-187.
51. Hendel, J., Nielsen, O. H., Expression of cyclooxygenase-2 mRNA in active inflammatory bowel disease. Am. J. Gastroenterol. 1997, 92, 1170-1173.
52. Liang, Y. C., Huang, Y. T., Tsai, S. H., Lin-Shiau, S. Y. et al., Suppression of inducible cyclooxygenase and inducible nitric oxide synthase by apigenin and related flavonoids in mouse macrophages. Carcinogenesis 1999, 20, 1945-1952.
53. Wang, G. J., Chen, Y. M., Wang, T. M., Lee, C. K. et al., Flavonoids with iNOS inhibitory activity from Pogonatherum crinitum. J. Ethnopharmacol. 2008, 118, 71-78.
54. Seibel, J., Molzberger, A. F., Hertrampf, T., Laudenbach-Leschowski, U. et al., Oral treatment with genistein reduces the expression of molecular and biochemical markers of inflammation in a rat model of chronic TNBS-induced colitis. Eur. J. Nutr. 2009, 48, 213-220.
55. Dallegri, F., Ottonello, L., Ballestrero, A., Bogliolo, F. et al., Cytoprotection against neutrophil derived hypochlorous acid: a potential mechanism for the therapeutic action of 5-aminosalicylic acid in ulcerative colitis. Gut 1990, 31, 184-186.
56. Wallace, J. L., McKnight, W., Asfaha, S., Liu, D. Y., Reduction of acute and reactivated colitis in rats by an inhibitor of neutrophil activation. Am. J. Physiol. 1998, 274, G802-G808.
57. Yamada, T., Zimmerman, B. J., Specian, R. D., Grisham, M. B., Role of neutrophils in acetic acid-induced colitis in rats. Inflammation 1991, 15, 399-411.
58. Owczarek, D., Cibor, D., Szczepanek, M., Mach, T., Biological therapy of inflammatory bowel disease. Pol. Arch. Med. Wewn. 2009, 119, 84-88.
59. Mudter, J., Neurath, M. F., IL-6 signaling in inflammatory bowel disease: pathophysiological role and clinical relevance. Inflamm. Bowel Dis. 2007, 13, 1016-1023.
60. Shanahan, F., Inflammatory bowel disease: immunodiagnostics, immunotherapeutics, and ecotherapeutics. Gastroenterology 2001, 120, 622-635.
61. Zhao, J., Hong, T., Dong, M., Meng, Y. et al., Protective effect of myricetin in dextran sulphate sodium-induced murine ulcerative colitis. Mol. Med. Rep. 2013, 7, 565-570.
62. Manach, C., Scalbert, A., Morand, C., Remesy, C. et al., Polyphenols: food sources and bioavailability. Am. J. Clin. Nutr. 2004, 79, 727-747.
63. Manach, C., Williamson, G., Morand, C., Scalbert, A. et al., Bioavailability and bioefficacy of polyphenols in humans. I. Review of 97 bioavailability studies. Am. J. Clin. Nutr. 2005, 81, 230S-242S.