Modulation of colonic inflammation in Mdr1a-/- mice by green tea polyphenols and their effects on the colon transcriptome and proteome

Journal of Nutritional Biochemistry

Volumn 24, Issue 10, 2013, Pages 1678-1690

  Barnett, Matthew P G ^a   Cooney, Janine M ^b   Dommels, Yvonne E M ^b   Nones, Katia ^b,e   Brewster, Diane T ^b   Park, Zaneta ^c   Butts, Christine A ^b   McNabb, Warren C ^c,d   Laing, William A ^b   Roy, Nicole C ^a,d  

^a Food Nutrition and Health Team   (New Zealand)

^b THE NEW ZEALAND INSTITUTE FOR PLANT AND FOOD RESEARCH LIMITED   (New Zealand)

^c AGRESEARCH GRASSLANDS   (New Zealand)

^d MASSEY UNIVERSITY   (New Zealand)

^e UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Epigallocatechin gallate (EGCG); Gene expression; Inflammatory bowel diseases; Protein expression

Indexed keywords

GREEN TEA EXTRACT; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; POLYPHENOL; PROTEOME; STAT1 PROTEIN; TRANSCRIPTOME;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; COLITIS; CONTROLLED STUDY; DIETARY INTAKE; ENTERITIS; HISTOPATHOLOGY; LIQUID CHROMATOGRAPHY; MALE; MASS SPECTROMETRY; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; RNA TRANSCRIPTION; TEA; TWO DIMENSIONAL GEL ELECTROPHORESIS; XENOBIOTIC METABOLISM;

ANIMALIA; MUS;

EPIGALLOCATECHIN GALLATE (EGCG); GENE EXPRESSION; INFLAMMATORY BOWEL DISEASES; PROTEIN EXPRESSION;

ANIMALS; COLITIS; COLON; INFLAMMATORY BOWEL DISEASES; MALE; MICE; MODELS, ANIMAL; P-GLYCOPROTEINS; POLYPHENOLS; PPAR ALPHA; PROTEOME; STAT1 TRANSCRIPTION FACTOR; TEA; TRANSCRIPTOME;

EID: 84883771484     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2013.02.007     Document Type: Article

References (55)

1. Panwala C.M., Jones J.C., Viney J.L. A novel model of inflammatory bowel disease: mice deficient for the multiple drug resistance gene, mdr1a, spontaneously develop colitis. J Immunol 1998, 161:5733-5744.
2. Banner K.H., Cattaneo C., Le Net J.L., et al. Macroscopic, microscopic and biochemical characterisation of spontaneous colitis in a transgenic mouse, deficient in the multiple drug resistance 1a gene. Br J Pharmacol 2004, 143:590-598.
3. Dommels Y.E.M., Butts C., Zhu S.T., et al. Characterization of inflammation in mdr1a-/- mice and identification of related gene expression changes in colonic epithelial cells. Genes Nutr 2007, 2:209-223.
4. Puleston J., Cooper M., Murch S., et al. A distinct subset of chemokines dominates the mucosal chemokine response in inflammatory bowel disease. Aliment Pharmacol Ther 2005, 21:109-120.
5. Langmann T., Moehle C., Mauerer R., et al. Loss of detoxification in inflammatory bowel disease: dysregulation of pregnane X receptor target genes. Gastroenterology 2004, 127:26-40.
6. Potter J.D., Steinmetz K. Vegetables, fruit and phytoestrogens as preventive agents. IARC Sci Publ 1996, 61-90.
7. Darvesh A.S., Carroll R.T., Bishayee A., et al. Oxidative stress and Alzheimer's disease: dietary polyphenols as potential therapeutic agents. Expert Rev Neurother 2010, 10:729-745.
8. Crozier A., Jaganath I.B., Clifford M.N. Dietary phenolics: chemistry, bioavailability and effects on health. Nat Prod Rep 2009, 26:1001-1043.
9. Varilek G.W., Yang F., Lee E.Y., et al. Green tea polyphenol extract attenuates inflammation in interleukin-2-deficient mice, a model of autoimmunity. J Nutr 2001, 131:2034-2039.
10. Oz H.S., Chen T.S., McClain C.J., de Villiers W.J. Antioxidants as novel therapy in a murine model of colitis. J Nutr Biochem 2005, 16:297-304.
11. Kim M., Murakami A., Miyamoto S., et al. The modifying effects of green tea polyphenols on acute colitis and inflammation-associated colon carcinogenesis in male ICR mice. Biofactors 2010, 36:43-51.
12. Henning S.M., Aronson W., Niu Y., et al. Tea polyphenols and theaflavins are present in prostate tissue of humans and mice after green and black tea consumption. J Nutr 2006, 136:1839-1843.
13. Townsend P.A., Scarabelli T.M., Pasini E., et al. Epigallocatechin-3-gallate inhibits STAT-1 activation and protects cardiac myocytes from ischemia/reperfusion-induced apoptosis. FASEB J 2004, 18:1621-1623.
14. 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.
15. Park E.I., Paisley E.A., Mangian H.J., et al. Lipid level and type alter stearoyl CoA desaturase mRNA abundance differently in mice with distinct susceptibilities to diet-influenced diseases. J Nutr 1997, 127:566-573.
16. Roy N.C., Barnett M.P.G., Knoch B., et al. Nutrigenomics applied to an animal model of inflammatory bowel diseases: transcriptomic analysis of the effects of eicosapentaenoic acid- and arachidonic acid-enriched diets. Mutat Res 2007, 622:103-116.
17. Smyth G.K. Limma: linear models for microarray data. Bioinformatics and computational biology solutions using R and bioconductor 2005, 397-420. Springer, New York. R. Gentleman, V. Carey, S. Dudoit (Eds.).
18. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Stat Soc Series B (Methodological) 1995, 57:289-300.
19. Edgar R., Domrachev M., Lash A.E. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 2002, 30:207-210.
20. Knoch B., Barnett M.P., Cooney J., et al. Molecular characterization of the onset and progression of colitis in inoculated interleukin-10 gene-deficient mice: a role for PPARalpha. PPAR Res 2010, 2010:621069.
21. Eng J.K., McCormack A.L., Yates Iii J.R. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J Am Soc Mass Spectrom 1994, 5:976-989.
22. Yates J.R., Eng J.K., McCormack A.L., Schieltz D. Method to correlate tandem mass spectra of modified peptides to amino acid sequences in the protein database. Anal Chem 1995, 67:1426-1436.
23. Abboud P.A., Hake P.W., Burroughs T.J., et al. Therapeutic effect of epigallocatechin-3-gallate in a mouse model of colitis. Eur J Pharmacol 2008, 579:411-417.
24. Autschbach F., Giese T., Gassler N., et al. Cytokine/chemokine messenger-RNA expression profiles in ulcerative colitis and Crohn's disease. Virchows Arch 2002, 441:500-513.
25. Frolova L., Drastich P., Rossmann P., et al. Expression of Toll-like receptor 2 (TLR2), TLR4, and CD14 in biopsy samples of patients with inflammatory bowel diseases: upregulated expression of TLR2 in terminal ileum of patients with ulcerative colitis. J Histochem Cytochem 2008, 56:267-274.
26. de Prati A.C., Ciampa A.R., Cavalieri E., et al. STAT1 as a new molecular target of anti-inflammatory treatment. Curr Med Chem 2005, 12:1819-1828.
27. Tedeschi E., Suzuki H., Menegazzi M. Antiinflammatory action of EGCG, the main component of green tea, through STAT-1 inhibition. Ann N Y Acad Sci 2002, 973:435-437.
28. Watson J.L., Ansari S., Cameron H., et al. Green tea polyphenol (-)-epigallocatechin gallate blocks epithelial barrier dysfunction provoked by IFN-gamma but not by IL-4. Am J Physiol Gastrointest Liver Physiol 2004, 287:G954-G961.
29. Darra E., Shoji K., Mariotto S., Suzuki H. Protective effect of epigallocatechin-3-gallate on ischemia/reperfusion-induced injuries in the heart: STAT1 silencing flavonoid. Genes Nutr 2007, 2:307-310.
30. Cheng C.W., Shieh P.C., Lin Y.C., et al. Indoleamine 2,3-dioxygenase, an immunomodulatory protein, is suppressed by (-)-epigallocatechin-3-gallate via blocking of gamma-interferon-induced JAK-PKC-delta-STAT1 signaling in human oral cancer cells. J Agric Food Chem 2010, 58:887-894.
31. Wang J., Ren Z., Xu Y., et al. Epigallocatechin-3-gallate ameliorates experimental autoimmune encephalomyelitis by altering balance among CD4+ T-cell subsets. Am J Pathol 2012, 180:221-234.
32. Delerive P., De Bosscher K., Besnard S., et al. Peroxisome proliferator-activated receptor alpha negatively regulates the vascular inflammatory gene response by negative cross-talk with transcription factors NF-kappaB and AP-1. J Biol Chem 1999, 274:32048-32054.
33. Zhao W., Wang L., Zhang M., et al. Peroxisome proliferator-activated receptor gamma negatively regulates IFN-beta production in Toll-like receptor (TLR) 3- and TLR4-stimulated macrophages by preventing interferon regulatory factor 3 binding to the IFN-beta promoter. J Biol Chem 2011, 286:5519-5528.
34. Mazzei J.C., Zhou H., Brayfield B.P., et al. Suppression of intestinal inflammation and inflammation-driven colon cancer in mice by dietary sphingomyelin: importance of peroxisome proliferator-activated receptor gamma expression. J Nutr Biochem 2011, 22:1160-1171.
35. Tian C., Ye X., Zhang R., et al. Green tea polyphenols reduced fat deposits in high fat-fed rats via erk1/2-PPARgamma-adiponectin pathway. PLoS One 2013, 8:e53796.
36. Zhang K. Integration of ER stress, oxidative stress and the inflammatory response in health and disease. Int J Clin Exp Med 2010, 3:33-40.
37. Zhang L., Pang E., Loo R.R., et al. Concomitant inhibition of HSP90, its mitochondrial localized homologue TRAP1 and HSP27 by green tea in pancreatic cancer HPAF-II cells. Proteomics 2011, 11:4638-4647.
38. Yin Z., Henry E.C., Gasiewicz T.A. (-)-Epigallocatechin-3-gallate is a novel Hsp90 inhibitor. Biochemistry 2009, 48:336-345.
39. Iwakoshi N.N., Lee A.H., Vallabhajosyula P., et al. Plasma cell differentiation and the unfolded protein response intersect at the transcription factor XBP-1. Nat Immunol 2003, 4:321-329.
40. Na H.K., Surh Y.J. Modulation of Nrf2-mediated antioxidant and detoxifying enzyme induction by the green tea polyphenol EGCG. Food Chem Toxicol 2008, 46:1271-1278.
41. Aitken A.E., Richardson T.A., Morgan E.T. Regulation of drug-metabolizing enzymes and transporters in inflammation. Annu Rev Pharmacol Toxicol 2006, 46:123-149.
42. Waxman D.J. P450 gene induction by structurally diverse xenochemicals: central role of nuclear receptors CAR, PXR, and PPAR. Arch Biochem Biophys 1999, 369:11-23.
43. Bonfield T.L., Thomassen M.J., Farver C.F., et al. Peroxisome proliferator-activated receptor-gamma regulates the expression of alveolar macrophage macrophage colony-stimulating factor. J Immunol 2008, 181:235-242.
44. Nakken B., Varga T., Szatmari I., et al. Peroxisome proliferator-activated receptor gamma-regulated cathepsin D is required for lipid antigen presentation by dendritic cells. J Immunol 2011, 187:240-247.
45. Sumanasekera W.K., Tien E.S., Davis J.W., et al. Heat shock protein-90 (Hsp90) acts as a repressor of peroxisome proliferator-activated receptor-alpha (PPARalpha) and PPARbeta activity. Biochemistry 2003, 42:10726-10735.
46. Chen N., Bezzina R., Hinch E., et al. Green tea, black tea, and epigallocatechin modify body composition, improve glucose tolerance, and differentially alter metabolic gene expression in rats fed a high-fat diet. Nutr Res 2009, 29:784-793.
47. Cooney J.M., Barnett M.P., Brewster D., et al. Proteomic analysis of colon tissue from interleukin-10 gene-deficient mice fed polyunsaturated Fatty acids with comparison to transcriptomic analysis. J Proteome Res 2012, 11:1065-1077.
48. Burke J.P., Mulsow J.J., O'Keane C., et al. Fibrogenesis in Crohn's disease. Am J Gastroenterol 2007, 102:439-448.
49. Young M.R., Nair R., Bucheimer N., et al. Transactivation of Fra-1 and consequent activation of AP-1 occur extracellular signal-regulated kinase dependently. Mol Cell Biol 2002, 22:587-598.
50. Dong Z., Ma W., Huang C., Yang C.S. Inhibition of tumor promoter-induced activator protein 1 activation and cell transformation by tea polyphenols, (-)-epigallocatechin gallate, and theaflavins. Cancer Res 1997, 57:4414-4419.
51. Park A.M., Dong Z. Signal transduction pathways: targets for green and black tea polyphenols. J Biochem Mol Biol 2003, 36:66-77.
52. Avouac J., Palumbo K., Tomcik M., et al. Inhibition of activator protein 1 signaling abrogates transforming growth factor beta-mediated activation of fibroblasts and prevents experimental fibrosis. Arthritis Rheum 2012, 64:1642-1652.
53. Sakata R., Ueno T., Nakamura T., et al. Green tea polyphenol epigallocatechin-3-gallate inhibits platelet-derived growth factor-induced proliferation of human hepatic stellate cell line LI90. J Hepatol 2004, 40:52-59.
54. Dona M., Dell'Aica I., Calabrese F., et al. Neutrophil restraint by green tea: inhibition of inflammation, associated angiogenesis, and pulmonary fibrosis. J Immunol 2003, 170:4335-4341.
55. Hoensch H.P., Oertel R. Emerging role of bioflavonoids in gastroenterology: especially their effects on intestinal neoplasia. World J Gastrointest Oncol 2011, 3:71-74.