Green and Black Tea Inhibit Cytokine-Induced Il-8 Production and Secretion in AGS Gastric Cancer Cells via Inhibition of NF-κB Activity

Abstract

Consumption of tea is associated with a reduced risk for several gastrointestinal cancers. Inflammatory processes, such as secretion of IL-8 from the gastric epithelium in response to chronic chemokine or antigen exposure, serve both as a chemoattractant for white blood cells and a prerequisite for gastric carcinogenesis. In this study, the gastric adenocarcinoma cell line AGS was used to investigate the effect of green tea extract, black tea extract, and epigallocatechin gallate (EGCG), the most abundant catechin in tea, on cytokine-induced inflammation. AGS cells were stimulated with interleukin-1β (IL-1β) to initiate inflammation, followed by exposure to either tea extracts or EGCG. We found that both green and black tea extracts at concentrations of 20 and 2 µM total catechins, respectively, significantly (p < 0.05) inhibited IL-1β-induced IL-8 production and secretion to a similar extent. Treatment of AGS cells with EGCG (8 µM) produced similar reductions in IL-1β-induced IL-8 production and secretion. Inhibition of NF-κB activity was found to be responsible, in part, for these observed effects. Our findings demonstrate that both green and black tea extracts with distinctly different catechin profiles, are capable of disrupting the molecular link between inflammation and carcinogenesis via inhibition of NF-κB activity in AGS cells.

black tea - inflammation - gastric cancer - epigallocatechin gallate - green tea

References

• 1 Parkin D M. Global cancer statistics in the year 2000.  Lancet Oncol. 2001;  2 533-543
• 2 Jakszyn P, Gonzalez C A. Nitrosamine and related food intake and gastric and oesophageal cancer risk: a systematic review of the epidemiological evidence.  World J Gastroenterol. 2006;  12 4296-4303
• 3 Tsugane S, Sasazuki S. Diet and the risk of gastric cancer: review of epidemiological evidence.  Gastric Cancer. 2007;  10 75-83
• 4 Sasazuki S, Inoue M, Hanaoka T, Yamamoto S, Sobue T, Tsugane S. Green tea consumption and subsequent risk of gastric cancer by subsite: the JPHC Study.  Cancer Causes Control. 2004;  15 483-491
• 5 Inoue M, Sasazuki S, Wakai K, Suzuki T, Matsuo K, Shimazu T, Tsuji I, Tanaka K, Mizoue T, Nagata C, Tamakoshi A, Sawada N, Tsugane S. Green tea consumption and gastric cancer in Japanese: a pooled analysis of six cohort studies.  Gut. 2009;  58 1323-1332
• 6 van der Woude C J, Kleibeuker J H, Jansen P L, Moshage H. Chronic inflammation, apoptosis and (pre-)malignant lesions in the gastro-intestinal tract.  Apoptosis. 2004;  9 123-130
• 7 Na H K, Kim E H, Jung J H, Lee H H, Hyun J W, Surh Y J. (−)-Epigallocatechin gallate induces Nrf2-mediated antioxidant enzyme expression via activation of PI3K and ERK in human mammary epithelial cells.  Arch Biochem Biophys. 2008;  476 171-177
• 8 Lee K W, Lee H J, Lee C Y. Antioxidant activity of black tea vs. green tea.  J Nutr. 2002;  132 785
• 9 Maeda S, Omata M. Inflammation and cancer: role of nuclear factor-kappaB activation.  Cancer Sci. 2008;  99 836-842
• 10 Pikarsky E, Porat R M, Stein I, Abramovitch R, Amit S, Kasem S, Gutkovich-Pyest E, Urieli-Shoval S, Galun E, Ben-Neriah Y. NF-kappaB functions as a tumour promoter in inflammation-associated cancer.  Nature. 2004;  431 461-466
• 11 Li Q, Yu Y Y, Zhu Z G, Ji Y B, Zhang Y, Liu B Y, Chen X H, Lin Y Z. Effect of NF-kappaB constitutive activation on proliferation and apoptosis of gastric cancer cell lines.  Eur Surg Res. 2005;  37 105-110
• 12 Bartchewsky Jr W, Martini M R, Masiero M, Squassoni A C, Alvarez M C, Ladeira M S, Salvatore D, Trevisan M, Pedrazzoli Jr J, Ribeiro M L. Effect of Helicobacter pylori infection on IL-8, IL-1beta and COX-2 expression in patients with chronic gastritis and gastric cancer.  Scand J Gastroenterol. 2009;  44 153-161
• 13 Kitadai Y, Haruma K, Mukaida N, Ohmoto Y, Matsutani N, Yasui W, Yamamoto S, Sumii K, Kajiyama G, Fidler I J, Tahara E. Regulation of disease-progression genes in human gastric carcinoma cells by interleukin 8.  Clin Cancer Res. 2000;  6 2735-2740
• 14 Graham H N. Green tea composition, consumption, and polyphenol chemistry.  Prev Med. 1992;  21 334-350
• 15 Tanaka T, Mine C, Watarumi S, Fujioka T, Mihashi K, Zhang Y J, Kouno I. Accumulation of epigallocatechin quinone dimers during tea fermentation and formation of theasinensins.  J Nat Prod. 2002;  65 1582-1587
• 16 Lin L Z, Chen P, Harnly J M. New phenolic components and chromatographic profiles of green and fermented teas.  J Agric Food Chem. 2008;  56 8130-8140
• 17 Binns C W, Lee A H, Fraser M L. Tea or coffee? A case study on evidence for dietary advice.  Public Health Nutr. 2008;  11 1132-1141
• 18 Neilson A P, Green R J, Wood K V, Ferruzzi M G. High-throughput analysis of catechins and theaflavins by high performance liquid chromatography with diode array detection.  J Chromatogr. 2006;  1132 132-140
• 19 Hwang Y S, Jeong M, Park J S, Kim M H, Lee D B, Shin B A, Mukaida N, Ellis L M, Kim H R, Ahn B W, Jung Y D. Interleukin-1beta stimulates IL-8 expression through MAP kinase and ROS signaling in human gastric carcinoma cells.  Oncogene. 2004;  23 6603-6611
• 20 Lurje G, Husain H, Power D G, Yang D, Groshen S, Pohl A, Zhang W, Ning Y, Manegold P C, El-Khoueiry A, Iqbal S, Tang L H, Shah M A, Lenz H J. Genetic variations in angiogenesis pathway genes associated with clinical outcome in localized gastric adenocarcinoma.  Ann Oncol. 2009;  21 78-86
• 21 Konno H, Ohta M, Baba M, Suzuki S, Nakamura S. The role of circulating IL-8 and VEGF protein in the progression of gastric cancer.  Cancer Sci. 2003;  94 735-740
• 22 Porath D, Riegger C, Drewe J, Schwager J. Epigallocatechin-3-gallate impairs chemokine production in human colon epithelial cell lines.  J Pharmacol Exp Ther. 2005;  315 1172-1180
• 23 Netsch M I, Gutmann H, Aydogan C, Drewe J. Green tea extract induces interleukin-8 (IL-8) mRNA and protein expression but specifically inhibits IL-8 secretion in caco-2 cells.  Planta Med. 2006;  72 697-702
• 24 Chen P C, Wheeler D S, Malhotra V, Odoms K, Denenberg A G, Wong H R. A green tea-derived polyphenol, epigallocatechin-3-gallate, inhibits IkappaB kinase activation and IL-8 gene expression in respiratory epithelium.  Inflammation. 2002;  26 233-241
• 25 Wheeler D S, Catravas J D, Odoms K, Denenberg A, Malhotra V, Wong H R. Epigallocatechin-3-gallate, a green tea-derived polyphenol, inhibits IL-1 beta-dependent proinflammatory signal transduction in cultured respiratory epithelial cells.  J Nutr. 2004;  134 1039-1044
• 26 Spencer J P. Metabolism of tea flavonoids in the gastrointestinal tract.  J Nutr. 2003;  133 3255S-3261S
• 27 Escarcega R O, Fuentes-Alexandro S, Garcia-Carrasco M, Gatica A, Zamora A. The transcription factor nuclear factor-kappa B and cancer.  Clin Oncol. 2007;  19 154-161
• 28 Gilmore T D, Herscovitch M. Inhibitors of NF-kappaB signaling: 785 and counting.  Oncogene. 2006;  25 6887-6899
• 29 Kopp E, Ghosh S. Inhibition of NF-kappa B by sodium salicylate and aspirin.  Science. 1994;  265 956-959
• 30 Elwood P C, Gallagher A M, Duthie G G, Mur L A, Morgan G. Aspirin, salicylates, and cancer.  Lancet. 2009;  373 1301-1309
• 31 Kim H S, Kim M H, Jeong M, Hwang Y S, Lim S H, Shin B A, Ahn B W, Jung Y D. EGCG blocks tumor promoter-induced MMP-9 expression via suppression of MAPK and AP-1 activation in human gastric AGS cells.  Anticancer Res. 2004;  24 747-753
• 32 Fiore E, Fusco C, Romero P, Stamenkovic I. Matrix metalloproteinase 9 (MMP-9/gelatinase B) proteolytically cleaves ICAM-1 and participates in tumor cell resistance to natural killer cell-mediated cytotoxicity.  Oncogene. 2002;  21 5213-5223
• 33 Nomura Y, Takasaki K, Tada M, Yoshimoto M, Ishida H, Murata N, Kubota S. Pro-MMP-9 is associated with poor prognosis in gastric cancer.  Scand J Gastroenterol. 2007;  42 1070-1072
• 34 Leung L K, Su Y, Chen R, Zhang Z, Huang Y, Chen Z Y. Theaflavins in black tea and catechins in green tea are equally effective antioxidants.  J Nutr. 2001;  131 2248-2251
• 35 Pan M H, Lin-Shiau S Y, Ho C T, Lin J H, Lin J K. Suppression of lipopolysaccharide-induced nuclear factor-kappaB activity by theaflavin-3,3′-digallate from black tea and other polyphenols through down-regulation of IkappaB kinase activity in macrophages.  Biochem Pharmacol. 2000;  59 357-367
• 36 Ukil A, Maity S, Das P K. Protection from experimental colitis by theaflavin-3,3′-digallate correlates with inhibition of IKK and NF-kappaB activation.  Br J Pharmacol. 2006;  149 121-131
• 37 Seo J H, Lim J W, Kim H, Kim K H. Helicobacter pylori in a Korean isolate activates mitogen-activated protein kinases, AP-1, and NF-kappaB and induces chemokine expression in gastric epithelial AGS cells.  Lab Invest. 2004;  84 49-62