Green tea polyphenol (-)-epigallocatechin-3-gallate triggered hepatotoxicity in mice: Responses of major antioxidant enzymes and the Nrf2 rescue pathway

Toxicology and Applied Pharmacology

Volumn 283, Issue 1, 2015, Pages 65-74

  Wang, Dongxu ^a   Wang, Yijun ^a   Wan, Xiaochun ^a   Yang, Chung S ^b   Zhang, Jinsong ^a  

^a ANHUI AGRICULTURAL UNIVERSITY   (China)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

( ) Epigallocatechin 3 gallate; Antioxidant enzymes; Dose response; Hepatotoxicity; Nrf2; Selenoprotein

Indexed keywords

ANTIOXIDANT; CATALASE; DJ 1 PROTEIN; EPIGALLOCATECHIN GALLATE; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GLUTATHIONE SYNTHASE; GLUTATHIONE TRANSFERASE; HEME OXYGENASE 1; POLYPHENOL; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); SUPEROXIDE DISMUTASE; THIOREDOXIN; THIOREDOXIN REDUCTASE 1; TRANSCRIPTION FACTOR NRF2; 4-HYDROXY-2-NONENAL; ALANINE AMINOTRANSFERASE; ALDEHYDE; ASPARTATE AMINOTRANSFERASE; CATECHIN; GAMMA-H2AX PROTEIN, MOUSE; HISTONE; INTERLEUKIN 6; TEA; TXN1 PROTEIN, MOUSE; TXNRD1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; LETHAL DOSE; LIVER CYTOSOL; LIVER HOMOGENATE; LIVER TOXICITY; MALE; MAXIMUM TOLERATED DOSE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; TEA; ANALOGS AND DERIVATIVES; ANIMAL; BLOOD; CHEMISTRY; DRUG EFFECTS; DRUG-INDUCED LIVER INJURY; GENETICS; LIVER; METABOLISM; TOXICITY;

MUS;

ALANINE TRANSAMINASE; ALDEHYDES; ANIMALS; ASPARTATE AMINOTRANSFERASES; CATALASE; CATECHIN; DRUG-INDUCED LIVER INJURY; GLUTATHIONE PEROXIDASE; HISTONES; INTERLEUKIN-6; LIVER; MALE; MAXIMUM TOLERATED DOSE; MICE; NF-E2-RELATED FACTOR 2; SUPEROXIDE DISMUTASE; TEA; THIOREDOXIN REDUCTASE 1; THIOREDOXINS;

EID: 84921473737     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2014.12.018     Document Type: Article

References (41)

1. Bonnefont-Rousselot D., Collin F. Melatonin: action as antioxidant and potential applications in human disease and aging. Toxicology 2010, 278:55-67.
2. Brigelius-Flohé R., Flohé L. Basic principles and emerging concepts in the redox control of transcription factors. Antioxid. Redox Signal. 2011, 15:2335-2381.
3. Brigelius-Flohé R., Maiorino M. Glutathione peroxidases. Biochim. Biophys. Acta 2013, 1830:3289-3303.
4. Claiborne A. Catalase activity. CRC Handbook of Methods for Oxygen Radical Research: Greenwald RA 1985.
5. Copeland P.R., Driscoll D.M. Purification, redox sensitivity, and RNA binding properties of SECIS-binding protein 2, a protein involved in selenoprotein biosynthesis. J. Biol. Chem. 1999, 274:25447-25454.
6. Crew K.D., Brown P., Greenlee H., Bevers T.B., Arun B., Hudis C., McArthur H.L., Chang J., Rimawi M., Vornik L., Cornelison T.L., Wang A., Hibshoosh H., Ahmed A., Terry M.B., Santella R.M., Lippman S.M., Hershman D.L. Phase IB randomized, double-blinded, placebo-controlled, dose escalation study of polyphenon E in women with hormone receptor-negative breast cancer. Cancer Prev. Res. (Phila.) 2012, 5:1144-1154.
7. Galati G., Lin A., Sultan A.M., O'Brien P.J. Cellular and in vivo hepatotoxicity caused by green tea phenolic acids and catechins. Free Radic. Biol. Med. 2006, 40:570-580.
8. Goodin M.G., Rosengren R.J. Epigallocatechin gallate modulates CYP450 isoforms in the female Swiss-Webster mouse. Toxicol. Sci. 2003, 76:262-270.
9. Goodin M.G., Bray B.J., Rosengren R.J. Sex- and strain-dependent effects of epigallocatechin gallate (EGCG) and epicatechin gallate (ECG) in the mouse. Food Chem. Toxicol. 2006, 44:1496-1504.
10. Habig W.H., Pabst M.J., Jakoby W.B. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J. Biol. Chem. 1974, 249:7130-7139.
11. Hawkes H.J., Karlenius T.C., Tonissen K.F. Regulation of the human thioredoxin gene promoter and its key substrates: a study of functional and putative regulatory elements. Biochim. Biophys. Acta 2014, 1840:303-314.
12. Holmgren A., Björnstedt M. Thioredoxin and thioredoxin reductase. Methods Enzymol. 1995, 252:199-208.
13. Hong J., Lu H., Meng X., Ryu J.H., Hara Y., Yang C.S. Stability, cellular uptake, biotransformation, and efflux of tea polyphenol (-)-epigallocatechin-3-gallate in HT-29 human colon adenocarcinoma cells. Cancer Res. 2002, 62:7241-7246.
14. Hou Z., Sang S., You H., Lee M.J., Hong J., Chin K.V., Yang C.S. Mechanism of action of (-)-epigallocatechin-3-gallate: auto-oxidation-dependent inactivation of epidermal growth factor receptor and direct effects on growth inhibition in human esophageal cancer KYSE 150 cells. Cancer Res. 2005, 65:8049-8056.
15. Isbrucker R.A., Edwards J.A., Wolz E., Davidovich A., Bausch J. Safety studies on epigallocatechin gallate (EGCG) preparations. Part 3: teratogenicity and reproductive toxicity studies in rats. Food Chem. Toxicol. 2006, 44:651-661.
16. Lambert J.D., Elias R.J. The antioxidant and pro-oxidant activities of green tea polyphenols: a role in cancer prevention. Arch. Biochem. Biophys. 2010, 501:65-72.
17. Lambert J.D., Kennett M.J., Sang S., Reuhl K.R., Ju J., Yang C.S. Hepatotoxicity of high oral dose (-)-epigallocatechin-3-gallate in mice. Food Chem. Toxicol. 2010, 48:409-416.
18. Li G.X., Chen Y.K., Hou Z., Xiao H., Jin H., Lu G., Lee M.J., Liu B., Guan F., Yang Z., Yu A., Yang C.S. Pro-oxidative activities and dose-response relationship of (-)-epigallocatechin-3-gallate in the inhibition of lung cancer cell growth: a comparative study in vivo and in vitro. Carcinogenesis 2010, 31:902-910.
19. Lu J., Holmgren A. The thioredoxin antioxidant system. Free Radic. Biol. Med. 2014, 66:75-87.
20. Ma Q. Role of nrf2 in oxidative stress and toxicity. Annu. Rev. Pharmacol. Toxicol. 2013, 53:401-426.
21. Malhotra D., Thimmulappa R., Navas-Acien A., Sandford A., Elliott M., Singh A., Chen L., Zhuang X., Hogg J., Pare P., Tuder R.M., Biswal S. Decline in NRF2-regulated antioxidants in chronic obstructive pulmonary disease lungs due to loss of its positive regulator, DJ-1. Am. J. Respir. Crit. Care Med. 2008, 178:592-604.
22. Mazzanti G., Menniti-Ippolito F., Moro P.A., Cassetti F., Raschetti R., Santuccio C., Mastrangelo S. Hepatotoxicity from green tea: a review of the literature and two unpublished cases. Eur. J. Clin. Pharmacol. 2009, 65:331-341.
23. Murray J.I., Whitfield M.L., Trinklein N.D., Myers R.M., Brown P.O., Botstein D. Diverse and specific gene expression responses to stresses in cultured human cells. Mol. Biol. Cell 2004, 15:2361-2374.
24. Osborne S.A., Hawkes H.J., Baldwin B.L., Alexander K.A., Svingen T., Clarke F.M., Tonissen K.F. The tert-butylhydroquinone-mediated activation of the human thioredoxin gene reveals a novel promoter structure. Biochem. J. 2006, 398:269-277.
25. Pae M., Ren Z., Meydani M., Shang F., Smith D., Meydani S.N., Wu D. Dietary supplementation with high dose of epigallocatechin-3-gallate promotes inflammatory response in mice. J. Nutr. Biochem. 2012, 23:526-531.
26. Papp L.V., Lu J., Holmgren A., Khanna K.K. From selenium to selenoproteins: synthesis, identity, and their role in human health. Antioxid. Redox Signal. 2007, 9:775-806.
27. Reiners J.J., Kessel D. Susceptibility of myelomonocytic leukemia U937 cells to the induction of apoptosis by the non-peptidic Bcl-2 ligand HA14-1 is cell cycle phase-dependent. Cancer Lett. 2005, 221:153-163.
28. Reiter R.J., Tan D.X., Rosales-Corral S., Manchester L.C. The universal nature, unequal distribution and antioxidant functions of melatonin and its derivatives. Mini Rev. Med. Chem. 2013, 13:373-384.
29. Rundlöf A.K., Carlsten M., Arnér E.S. The core promoter of human thioredoxin reductase 1: cloning, transcriptional activity, and Oct-1, Sp1, and Sp3 binding reveal a housekeeping-type promoter for the AU-rich element-regulated gene. J. Biol. Chem. 2001, 276:30542-30551.
30. Schönthal A.H. Adverse effects of concentrated green tea extracts. Mol. Nutr. Food Res. 2011, 55:874-885.
31. Shanafelt T.D., Call T.G., Zent C.S., LaPlant B., Bowen D.A., Roos M., Secreto C.R., Ghosh A.K., Kabat B.F., Lee M.J., Yang C.S., Jelinek D.F., Erlichman C., Kay N.E. Phase I trial of daily oral polyphenon E in patients with asymptomatic Rai stage 0 to II chronic lymphocytic leukemia. J. Clin. Oncol. 2009, 27:3808-3814.
32. Shanafelt T.D., Call T.G., Zent C.S., Leis J.F., LaPlant B., Bowen D.A., Roos M., Laumann K., Ghosh A.K., Lesnick C., Lee M.J., Yang C.S., Jelinek D.F., Erlichman C., Kay N.E. Phase 2 trial of daily, oral Polyphenon E in patients with asymptomatic, Rai stage 0 to II chronic lymphocytic leukemia. Cancer 2013, 119:363-370.
33. Shen G., Xu C., Hu R., Jain M.R., Nair S., Lin W., Yang C.S., Chan J.Y., Kong A.N. Comparison of (-)-epigallocatechin-3-gallate elicited liver and small intestine gene expression profiles between C57BL/6J mice and C57BL/6J/Nrf2 (-/-) mice. Pharm. Res. 2005, 22:1805-1820.
34. Smith A.D., Levander O.A. High-throughput 96-well microplate assays for determining specific activities of glutathione peroxidase and thioredoxin reductase. Methods Enzymol. 2002, 347:113-121.
35. Sun Y., Oberley L.W., Li Y. A simple method for clinical assay of superoxide dismutase. Clin. Chem. 1988, 34:497-500.
36. Tao L., Forester S.C., Lambert J.D. The role of the mitochondrial oxidative stress in the cytotoxic effects of the green tea catechin, (-)-epigallocatechin-3-gallate, in oral cells. Mol. Nutr. Food Res. 2014, 58:665-676.
37. Tsai P.Y., Ka S.M., Chang J.M., Chen H.C., Shui H.A., Li C.Y., Hua K.F., Chang W.L., Huang J.J., Yang S.S., Chen A. Epigallocatechin-3-gallate prevents lupus nephritis development in mice via enhancing the Nrf2 antioxidant pathway and inhibiting NLRP3 inflammasome activation. Free Radic. Biol. Med. 2011, 51:744-754.
38. Wang Y., Lu H., Wang D., Li S., Sun K., Wan X., Taylor E.W., Zhang J. Inhibition of glutathione synthesis eliminates the adaptive response of ascitic hepatoma 22 cells to nedaplatin that targets thioredoxin reductase. Toxicol. Appl. Pharmacol. 2012, 265:342-350.
39. Xu X.M., Carlson B.A., Irons R., Mix H., Zhong N., Gladyshev V.N., Hatfield D.L. Selenophosphate synthetase 2 is essential for selenoprotein biosynthesis. Biochem. J. 2007, 404:115-120.
40. Yang C.S., Hong J. Prevention of chronic diseases by tea: possible mechanisms and human relevance. Annu. Rev. Nutr. 2013, 33:161-181.
41. Zhang J., Wang H., Yu H. Thioacetamide-induced cirrhosis in selenium-adequate mice displays rapid and persistent abnormity of hepatic selenoenzymes which are mute to selenium supplementation. Toxicol. Appl. Pharmacol. 2007, 224:81-88.