Effects of methanolic extract form Fuzhuan brick-tea on hydrogen peroxide-induced oxidative stress in human intestinal epithelial adenocarcinoma Caco-2 cells

Song,Jia-Le; Gao,Yang

doi:10.3892/mmr.2014.1884

Effects of methanolic extract form Fuzhuan brick-tea on hydrogen peroxide-induced oxidative stress in human intestinal epithelial adenocarcinoma Caco-2 cells

Authors:
- Jia-Le Song
- Yang Gao
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Affiliations: Department of Food Science and Nutrition, Pusan National University, Busan 609-735, Republic of Korea, Department of Pharmacy, Northern Jiangsu People's Hospital Affiliated to Yangzhou University (Clinical Medical College of Yangzhou University), Yangzhou, Jiangsu 225001, P.R. China
Published online on: January 7, 2014 https://doi.org/10.3892/mmr.2014.1884
Pages: 1061-1067

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Abstract

The present study investigated the protective effect of methanolic extract from Fuzhuan brick‑tea (FME) on hydrogen peroxide (H2O2)‑induced oxidative stress in the human intestinal epithelial adenocarcinoma cell line Caco‑2. Caco‑2 cells were pretreated with different concentrations (50, 100 and 200 µg/ml) of FME for 2 h and then exposed to H2O2 (1 mM) for 6 h. FME did not exhibit a significant cytotoxic effect and increased the cell viability following H2O2 treatment by decreasing lipid peroxidation in Caco‑2 cells. To investigate the protective effect of FME on H2O2‑induced oxidative stress in Caco‑2 cells, the levels of intracellular glutathione (GSH) and the activity of the endogenous antioxidant enzymes catalase (CAT), superoxide dismutase (SOD), glutathione peroxidase (GSH‑px) and glutathione S‑transferase (GST), were determined. FME significantly increased the level of GSH and the activity of antioxidant enzymes. The results from the present study demonstrated that FME has a protective effect on H2O2‑induced oxidative damage in Caco‑2 cells through the inhibition of lipid peroxidation and the increase in the activity of antioxidant enzymes. In addition, FME reduced the H2O2‑induced expression of interleukin‑8 at both the mRNA and protein levels in Caco‑2 cells.

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1	Rezaie A, Parker RD and Abdollahi M: Oxidative stress and pathogenesis of inflammatory bowel disease: an epiphenomenon or the cause? Dig Dis Sci. 52:2015–2021. 2007. View Article : Google Scholar : PubMed/NCBI
2	Brieger K, Schiavone S, Miller FJ Jr and Krause KH: Reactive oxygen species: from health to disease. Swiss Med Wkly. 142:w136592012.PubMed/NCBI
3	Halliwell B: Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol. 141:312–322. 2006. View Article : Google Scholar : PubMed/NCBI
4	Bourlioux P, Koletzko B, Guarner F and Braesco V: The intestine and its microflora are partners for the protection of the host: report on the Danone Symposium ‘The Intelligent Intestine’, held in Paris, June 14, 2002. Am J Clin Nutr. 78:675–683. 2003.PubMed/NCBI
5	Oz HS, Chen TS, McClain CJ and de Villiers WJ: Antioxidants as novel therapy in a murine model of colitis. J Nutr Biochem. 16:297–304. 2005. View Article : Google Scholar : PubMed/NCBI
6	Mazzon E, Muià C, Paola RD, et al: Green tea polyphenol extract attenuates colon injury induced by experimental colitis. Free Radic Res. 39:1017–1025. 2005. View Article : Google Scholar : PubMed/NCBI
7	Song YA, Park YL, Kim KY, et al: Black tea extract prevents lipopolysaccharide-induced NF-κB signaling and attenuates dextran sulfate sodium-induced experimental colitis. BMC Complement Altern Med. 11:912011.PubMed/NCBI
8	Brückner M, Westphal S, Domschke W, Kucharzik T and Lügering A: Green tea polyphenol epigallocatechin-3-gallate shows therapeutic antioxidative effects in a murine model of colitis. J Crohns Colitis. 6:226–235. 2012.PubMed/NCBI
9	Eckmann L, Kagnoff M and Fierer J: Epithelial cells secrete the chemokine interleukin-8 in response to bacterial entry. Infect Immun. 61:4569–4574. 1993.PubMed/NCBI
10	Verhasselt V, Goldman M and Willems F: Oxidative stress up-regulates IL-8 and TNF-alpha synthesis by human dendritic cells. Eur J Immunol. 28:3886–3890. 1998. View Article : Google Scholar : PubMed/NCBI
11	Yamamoto K, Kushima R, Kisaki O, Fujiyama Y and Okabe H: Combined effect of hydrogen peroxide induced oxidative stress and IL-1alpha on IL-8 production in CaCo-2 cells (a human colon carcinoma cell line) and normal intestinal epithelial cells. Inflammation. 27:123–128. 2003. View Article : Google Scholar
12	Nielsen O, Rüdiger N, Gaustadnes M and Horn T: Intestinal interleukin-8 concentration and gene expression in inflammatory bowel disease. Scand J Gastroenterol. 32:1028–1034. 1997. View Article : Google Scholar : PubMed/NCBI
13	Strober W, Fuss I and Mannon P: The fundamental basis of inflammatory bowel disease. J Clin Invest. 117:514–521. 2007. View Article : Google Scholar : PubMed/NCBI
14	Ling TJ, Wan XC, Ling WW, et al: New triterpenoids and other constituents from a special microbial-fermented tea-Fuzhuan brick tea. J Agric Food Chem. 58:4945–4950. 2010. View Article : Google Scholar : PubMed/NCBI
15	Mo H, Zhu Y and Chen Z: Microbial fermented tea: a potential source of natural food preservatives. Trends Food Sci Tech. 19:124–130. 2008.
16	Luo Z-M, Ling TJ, Li LX, et al: A new norisoprenoid and other compounds from Fuzhuan brick tea. Molecules. 17:3539–3546. 2012. View Article : Google Scholar : PubMed/NCBI
17	Li Q, Liu Z, Huang J, et al: Anti-obesity and hypolipidemic effects of Fuzhuan brick tea water extract in high-fat diet-induced obese rats. J Sci Food Agric. 93:1310–1316. 2013. View Article : Google Scholar : PubMed/NCBI
18	Pinto M, Robine-Leon S, Appay MD, et al: Enterocyte-like differentiation and polarization of the human colon carcinoma cell line Caco-2 in culture. Biol Cell. 47:323–330. 1983.
19	Fraga CG, Leibovitz BE and Tappel AL: Lipid peroxidation measured as thiobarbituric acid-reactive substances in tissue slices: characterization and comparison with homogenates and microsomes. Free Radic Biol Med. 4:155–161. 1988. View Article : Google Scholar : PubMed/NCBI
20	Ellman GL: Tissue sulfhydryl groups. Arch Biochem Biophys. 82:70–77. 1959. View Article : Google Scholar
21	Nelson D and Kiesow L: Enthalpy of decomposition of hydrogen peroxide by catalase at 25 degrees C (with molar extinction coefficients of H₂O₂ solutions in the UV). Anal Biochem. 49:474–478. 1972. View Article : Google Scholar : PubMed/NCBI
22	Marklund S and Marklund G: Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem. 47:469–474. 1974. View Article : Google Scholar : PubMed/NCBI
23	Hafeman D, Sunde R and Hoekstra W: Effect of dietary selenium on erythrocyte and liver glutathione peroxidase in the rat. J Nutr. 104:580–587. 1974.PubMed/NCBI
24	Habig WH, Pabst MJ and Jakoby WB: Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem. 249:7130–7139. 1974.PubMed/NCBI
25	Bai B, Yamamoto K, Sato H, Sugiura H and Tanaka T: Combined effect of 25-hydroxycholesterol and IL-1β on IL-8 production in human colon carcinoma cell line (Caco-2). Inflammation. 29:141–146. 2005.PubMed/NCBI
26	Gutteridge J: Lipid peroxidation and antioxidants as biomarkers of tissue damage. Clin Chem. 41:1819–1828. 1995.PubMed/NCBI
27	Masella R, Di Benedetto R, Varì R, Filesi C and Giovannini C: Novel mechanisms of natural antioxidant compounds in biological systems: involvement of glutathione and glutathione-related enzymes. J Nutr Biochem. 16:577–586. 2005. View Article : Google Scholar : PubMed/NCBI
28	Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M and Telser J: Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol. 39:44–84. 2007. View Article : Google Scholar : PubMed/NCBI
29	Zhu H and Li YR: Oxidative stress and redox signaling mechanisms of inflammatory bowel disease: updated experimental and clinical evidence. Exp Biol Med (Maywood). 237:474–480. 2012. View Article : Google Scholar : PubMed/NCBI
30	Goto Y and Ivanov II: Intestinal epithelial cells as mediators of the commensal-host immune crosstalk. Immunol Cell Biol. 91:204–214. 2013. View Article : Google Scholar : PubMed/NCBI
31	Eckburg PB, Bik EM, Bernstein CN, et al: Diversity of the human intestinal microbial flora. Science. 308:1635–1638. 2005. View Article : Google Scholar : PubMed/NCBI
32	Qin J, Li R, Raes J, et al: A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 464:59–65. 2010. View Article : Google Scholar : PubMed/NCBI
33	Macfarlane S, Steed H and Macfarlane GT: Intestinal bacteria and inflammatory bowel disease. Crit Rev Clin Lab Sci. 46:25–54. 2009. View Article : Google Scholar : PubMed/NCBI
34	Huycke MM, Abrams V and Moore DR: Enterococcus faecalis produces extracellular superoxide and hydrogen peroxide that damages colonic epithelial cell DNA. Carcinogenesis. 23:529–536. 2002. View Article : Google Scholar
35	Halliwell B: Antioxidants in human health and disease. Annu Rev Nutr. 16:33–50. 1996. View Article : Google Scholar
36	Wijeratne SS, Cuppett SL and Schlegel V: Hydrogen peroxide induced oxidative stress damage and antioxidant enzyme response in Caco-2 human colon cells. J Agric Food Chem. 53:8768–8774. 2005. View Article : Google Scholar : PubMed/NCBI
37	Ji C, Rouzer CA, Marnett LJ and Pietenpol JA: Induction of cell cycle arrest by the endogenous product of lipid peroxidation, malondialdehyde. Carcinogenesis. 19:1275–1283. 1998. View Article : Google Scholar : PubMed/NCBI
38	Nair U, Bartsch H and Nair J: Lipid peroxidation-induced DNA damage in cancer-prone inflammatory diseases: a review of published adduct types and levels in humans. Free Radic Biol Med. 43:1109–1120. 2007. View Article : Google Scholar : PubMed/NCBI
39	Manna C, Galletti P, Cucciolla V, Moltedo O, Leone A and Zappia V: The protective effect of the olive oil polyphenol (3,4-dihydroxyphenyl)-ethanol counteracts reactive oxygen metabolite-induced cytotoxicity in Caco-2 cells. J Nutr. 127:286–292. 1997.
40	Aherne S and O’Brien N: Protection by the flavonoids myricetin, quercetin, and rutin against hydrogen peroxide-induced DNA damage in Caco-2 and HepG2 cells. Nutr Cancer. 34:160–166. 1999. View Article : Google Scholar : PubMed/NCBI
41	Aherne S and O’Brien N: Lack of Effect of the flavonoids, myricetin, quercetin, and rutin, on repair of H₂O₂-induced DNA single-strand breaks in Caco-2, HepG2, and V79 Cells. Nutr Cancer. 38:106–115. 2000. View Article : Google Scholar : PubMed/NCBI
42	Peng IW and Kuo SM: Flavonoid structure affects the inhibition of lipid peroxidation in Caco-2 intestinal cells at physiological concentrations. J Nutr. 133:2184–2187. 2003.PubMed/NCBI
43	Intra J and Kuo SM: Physiological levels of tea catechins increase cellular lipid antioxidant activity of vitamin C and vitamin E in human intestinal caco-2 cells. Chem Biol Interact. 169:91–99. 2007. View Article : Google Scholar : PubMed/NCBI
44	Katayama S, Ishikawa S, Fan MZ and Mine Y: Oligophosphopeptides derived from egg yolk phosvitin up-regulate gamma-glutamylcysteine synthetase and antioxidant enzymes against oxidative stress in Caco-2 cells. J Agric Food Chem. 55:2829–2835. 2007. View Article : Google Scholar
45	Aherne SA, Kerry JP and O’Brien NM: Effects of plant extracts on antioxidant status and oxidant-induced stress in Caco-2 cells. Br J Nutr. 97:321–328. 2007. View Article : Google Scholar : PubMed/NCBI
46	Kameoka S, Leavitt P, Chang C and Kuo SM: Expression of antioxidant proteins in human intestinal Caco-2 cells treated with dietary flavonoids. Cancer Lett. 146:161–167. 1999. View Article : Google Scholar : PubMed/NCBI
47	Wijeratne SS and Cuppett SL: Potential of rosemary (Rosemarinus officinalis L.) diterpenes in preventing lipid hydroperoxide-mediated oxidative stress in Caco-2 cells. J Agric Food Chem. 55:1193–1199. 2007.
48	Aw TY: Determinants of intestinal detoxication of lipid hydroperoxides. Free Radic Res. 28:637–646. 1998. View Article : Google Scholar : PubMed/NCBI
49	Wingler K, Müller C, Schmehl K, Florian S and Brigelius-Flohé R: Gastrointestinal glutathione peroxidase prevents transport of lipid hydroperoxides in CaCo-2 cells. Gastroenterology. 119:420–430. 2000. View Article : Google Scholar : PubMed/NCBI
50	Carrasco-Pozo C, Gotteland M and Speisky H: Protection by apple peel polyphenols against indometacin-induced oxidative stress, mitochondrial damage and cytotoxicity in Caco-2 cells. J Pharm Pharmacol. 62:943–950. 2010.PubMed/NCBI
51	Martín S, González-Burgos E, Carretero ME and Gómez- Serranillos MP: Neuroprotective properties of Spanish red wine and its isolated polyphenols on astrocytes. Food Chemistry. 128:40–48. 2011.PubMed/NCBI
52	Sharma R, Yang Y, Sharma A, Awasthi S and Awasthi YC: Antioxidant role of glutathione S-transferases: protection against oxidant toxicity and regulation of stress-mediated apoptosis. Antioxid Redox Signal. 6:289–300. 2004. View Article : Google Scholar : PubMed/NCBI
53	Yu MU, Yoo JM, Lee YS, et al: Altered de novo sphingolipid biosynthesis is involved in the serum deprivation-induced cell death in LLC-PK1 cells. J Toxicol Environ Health A. 67:2085–2094. 2004. View Article : Google Scholar : PubMed/NCBI
54	Katayama S and Mine Y: Antioxidative activity of amino acids on tissue oxidative stress in human intestinal epithelial cell model. J Agric Food Chem. 55:8458–8464. 2007. View Article : Google Scholar : PubMed/NCBI
55	Ina K, Kusugami K, Yamaguchi T, et al: Mucosal interleukin-8 is involved in neutrophil migration and binding to extracellular matrix in inflammatory bowel disease. Am J Gastroenterol. 92:1342–1346. 1997.PubMed/NCBI
56	Sanchez-Muñoz F, Dominguez-Lopez A and Yamamoto-Furusho JK: Role of cytokines in inflammatory bowel disease. World J Gastroenterol. 14:4280–4288. 2008.PubMed/NCBI
57	Zhao Z, Shin HS, Satsu H, Totsuka M and Shimizu M: 5-caffeoylquinic acid and caffeic acid down-regulate the oxidative stress- and TNF-alpha-induced secretion of interleukin-8 from Caco-2 cells. J Agric Food Chem. 56:3863–3868. 2008. View Article : Google Scholar : PubMed/NCBI
58	Satsu H, Hyun JS, Shin HS and Shimizu M: Suppressive effect of an isoflavone fraction on tumor necrosis factor-alpha-induced interleukin-8 production in human intestinal epithelial Caco-2 cells. J Nutr Sci Vitaminol (Tokyo). 55:442–446. 2009. View Article : Google Scholar
59	Netsch M, Gutmann H, Aydogan C and 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. 72:697–702. 2006. View Article : Google Scholar : PubMed/NCBI