Tert-butylhydroquinone as a phenolic activator of Nrf2 antagonizes arsenic-induced oxidative cytotoxicity but promotes arsenic methylation and detoxication in human hepatocyte cell line

Biological Trace Element Research

Volumn 160, Issue 2, 2014, Pages 294-302

  Duan, Xiaoxu ^a   Liu, Dan ^a   Xing, Xiaoyue ^a   Li, Jinlong ^a   Zhao, Shuo ^a   Nie, Huifang ^a   Zhang, Yang ^a   Sun, Guifan ^a   Li, Bing ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

Author keywords

Arsenic; Human hepatocytes; Nrf2; Oxidative stress; tBHQ

Indexed keywords

ARSENIC; GLUTATHIONE; HEME OXYGENASE 1; MESSENGER RNA; NADPH:QUININE OXIDOREDUCTASE 1; OXIDOREDUCTASE; REACTIVE OXYGEN METABOLITE; TERT BUTYLHYDROQUINONE; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; 2-TERT-BUTYLHYDROQUINONE; ANTIOXIDANTS; GLUTATHIONE REDUCTASE; HEME OXYGENASE-1; HMOX1 PROTEIN, HUMAN; HYDROQUINONES; MALONDIALDEHYDE; NAD(P)H DEHYDROGENASE (QUINONE); NF-E2-RELATED FACTOR 2; NFE2L2 PROTEIN, HUMAN; NQO1 PROTEIN, HUMAN; PROTECTIVE AGENTS; REACTIVE OXYGEN SPECIES;

ARTICLE; BIOMETHYLATION; CELL LINE; CELL PROLIFERATION; CELL PROTECTION; CONTROLLED STUDY; CYTOTOXICITY; DETOXIFICATION; DRUG ANTAGONISM; GENE EXPRESSION; GLUTATHIONE METABOLISM; HUMAN; HUMAN CELL; LIPID PEROXIDATION; LIVER CELL; METAL METABOLISM; METHYLATION; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; UPREGULATION; CELL LINE, TUMOR; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG EFFECTS; GENETICS; HEPATOCYTES; HUMANS; METABOLISM; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

ANTIOXIDANTS; ARSENIC; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION; GLUTATHIONE; GLUTATHIONE REDUCTASE; HEME OXYGENASE-1; HEPATOCYTES; HUMANS; HYDROQUINONES; MALONDIALDEHYDE; METHYLATION; NAD(P)H DEHYDROGENASE (QUINONE); NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; PROTECTIVE AGENTS; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84904299757     PISSN: 01634984     EISSN: 15590720     Source Type: Journal    
DOI: 10.1007/s12011-014-0042-4     Document Type: Article

References (48)

1. Sun G, Xu Y, Li X, Jin Y, Li B, Sun X (2007) Urinary arsenic metabolites in children and adults exposed to arsenic in drinking water in Inner Mongolia, China. Environ Health Perspect 115: 648-652 (Pubitemid 46585541)
2. Endo H, Sugioka Y, Nakagi Y, Saijo Y, Yoshida T (2008) A novel role of the NRF2 transcription factor in the regulation of arenitemediated keratin 16 gene expression in human keratinocytes. Environ Health Perspect 116:873-879 (Pubitemid 351943893)
3. Manna P, Sinha M, Sil PC (2008) Arsenic-induced oxidative myocardial injury: protective role of arjunolic acid. Arch Toxicol 82:137-149
4. Chowdhury R, Chatterjee R, Giri AK, Mandal C, Chaudhuri K (2010) Arsenic-induced cell proliferation is associated with enhanced ROS generation, ErKsignaling and CyclinA expression. Toxicol Lett 198:263-271
5. Flora SJ (2011) Arsenic-induced oxidative stress and its reversibility. Free Radic Biol Med 51:257-281
6. Jain A, Flora GJ, Bhargava R, Flora SJ (2012) Influence of age on arsenic-induced oxidative stress in rat. Biol Trace Elem Res 149:382-390
7. Naziroglu M, Karaoǧlu A, Aksoy AO (2004) Selenium and high dose vitamin E administration protects cisplatin-induced oxidative damage to renal, liver and lens tissues in rats. Toxicology 195: 221-230 (Pubitemid 38125121)
8. Kockar MC, Naziroǧlu M, Çelik O, Tola HT, Bayram D, Koyu A (2010) N-acetylcysteine modulates doxorubicin-induced oxidative stress and antioxidant vitamin concentrations in liver of rats. Cell Biochem Funct 28:673-677
9. Chen C, Jiang X, Hu Y, Zhang Z (2013) The protective role of resveratrol in the sodium arsenite-induced oxidative damage via modulation of intracellular GSH homeostasis. Biol Trace Elem Res 155:119-131
10. Zhang Q, Pi J, Woods CG, Andersen ME (2010) A systems biology perspective on Nrf2-mediated antioxidant response. Toxicol Appl Pharmacol 244:84-97
11. Blum NM, Mueller K, Lippmann D, Metges CC, Linn T, Pallauf J, Mueller AS (2013) Feeding of selenium alone or in combination with glucoraphanin differentially affects intestinal and hepatic antioxidant and phase II enzymes in growing rats. Biol Trace Elem Res 151:384-399
12. Magesh S, Chen Y, Hu L (2012) Small molecule modulators of Keap1-Nrf2-ARE pathway as potential preventive and therapeutic agents. Med Res Rev 32:687-726
13. Kwak MK, Kensler TW (2010) Targeting NRF2 signaling for cancer chemoprevention. Toxicol Appl Pharmacol 244:66-76
14. Nam KW, Kim YH, Kwon HJ, Rhee SK, Kim WJ, Han MD (2013) Tert-Butylhydroquinone reduces lipid accumulation in C57BL/6 mice with lower body weight gain. Arch Pharm Res 36:897-904
15. Koh K, Cha Y, Kim S, Kim J (2009) tBHQ inhibits LPS-induced microglial activation via Nrf2-mediated suppression of p38 phosphorylation. Biochem Biophys Res Commun 380:449-453
16. Hara H, Ohta M, Ohta K, Kuno S, Adachi T (2003) Increase of antioxidative potential by tert-butylhydroquinone protects against cell death associated with 6-hydroxydopamine-induced oxidative stress in neuroblastoma SH-SY5Y cells. Brain Res Mol Brain Res 119:125-131 (Pubitemid 37415085)
17. Pi J, Zhang Q, Woods CG, Wong V, Collins S, Andersen ME (2008) Activation of Nrf2-mediated oxidative stress response in macrophages by hypochlorous acid. Toxicol Appl Pharmacol 226:236-243 (Pubitemid 351172412)
18. Keum YS, Han YH, Liew C, Kim JH, Xu C, Yuan X, Shakarjian MP, Chong S, Kong AN (2006) Induction of heme oxygenase-1 (HO-1) and NAD[P]H: quinone oxidoreductase 1 (NQO1) by a phenolic antioxidant, butylated hydroxyanisole (BHA) and its metabolite, tertbutylhydroquinone (tBHQ) in primary-cultured human and rat hepatocytes. Pharm Res 23:2586-2594 (Pubitemid 44691605)
19. Kann S, Estes C, Reichard JF, Huang MY, Sartor MA, Schwemberger S, Chen Y, Dalton TP, Shertzer HG, Xia Y, Puga A (2005) Butylhydroquinone protects cells genetically deficient in glutathione biosynthesis from arsenite-induced apoptosis without significantly changing their prooxidant status. Toxicol Sci 87:365-384 (Pubitemid 41300684)
20. Chung JS, Haque R, Guha Mazumder DN, Moore LE, Ghosh N, Samanta S, Mitra S, Hira-Smith MM, von Ehrenstein O, Basu A, Liaw J, Smith AH (2006) Blood concentrations of methionine, selenium, beta-carotene, and other micronutrients in a case-control study of arsenic-induced skin lesions in West Bengal, India. Environ Res 101:230-237
21. Ghatak S, Biswas A, Dhali GK, Chowdhury A, Boyer JL, Santra A (2011) Oxidative stress and hepatic stellate cell activation are key events in arsenic induced liver fibrosis in mice. Toxicol Appl Pharmacol 251:59-69
22. Li B, Li X, Zhu B, Zhang X, Wang Y, Xu Y, Wang H, Hou Y, Zheng Q, Sun G (2013) Sodium arsenite induced reactive oxygen species generation, nuclear factor (erythroid-2-related) factor 2 activation, heme oxygenase-1 expression, and glutathione elevation in Chang human hepatocytes. Environ Toxicol 28:401-410
23. Liu D, Duan X, Dong D, Bai C, Li X, Sun G, Li B (2013) Activation of the Nrf2 Pathway by inorganic arsenic in human hepatocytes and the role of transcriptional repressor bach1. Oxidative Med Cell Longev 2013:1-10
24. Su S, Yang X, Omiecinski CJ (2014) Intronic DNA elements regulate Nrf2 chemical responsiveness of the human microsomal epoxide hydrolase gene (EPHX1) through a far upstream alternative promoter. Biochim Biophys Acta 1839:493-505
25. Alarcón-Aguilar A, Luna-López A, Ventura-Gallegos JL, LazzariniR G-AS, González-Puertos VY, Morán J, Santamaría A, KönigsbergM (2014) Primary cultured astrocytes from old rats are capable to activate the Nrf2 response against MPP+ toxicity after tBHQ pretreatment. Neurobiol Aging 35:1901-1912
26. Ahmed S, Mahabbat-e Khoda S, Rekha RS, Gardner RM, Ameer SS, Moore S, Ekström EC, Vahter M, Raqib R (2011) Arsenicassociated oxidative stress, inflammation, and immune disruption in human placenta and cord blood. Environ Health Perspect 119: 258-264
27. Cheng WW, Lin ZQ, Wei BF, Zeng Q, Han B, Wei CX, Fan XJ, Hu CL, Liu LH, Huang JH, Yang X, Xi ZG (2011) Single-walled carbon nanotube induction of rat aortic endothelial cell apoptosis: reactive oxygen species are involved in the mitochondrial pathway. Int J Biochem Cell Biol 43:564-572
28. Weijl NI, Cleton FJ, Osanto S (1997) Free radicals and antioxidants in chemotherapy-induced toxicity. Cancer Treat Rev 23:209-240 (Pubitemid 27464149)
29. Tietze F (1969) Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal Biochem 27:502 -522
30. Bazzichi L, Ciompi ML, Betti L, Rossi A, Melchiorre D, Fiorini M, Giannaccini G (2002) Lucacchini A impaired glutathione reductase activity and levels of collagenase and elastase in synovial fluid in rheumatoid arthritis. Clin Exp Rheumatol 20:761-766 (Pubitemid 35446965)
31. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
32. Xu Y, Wang Y, Zheng Q, Li X, Li B, Jin Y, Sun X, Sun G (2008) Association of oxidative stress with arsenic methylation in chronic arsenic-exposed children and adults. Toxicol Appl Pharmacol 232: 142-149
33. Gao S, Duan X, Wang X, Dong D, Liu D, Li X, Sun G, Li B (2013) Curcumin attenuates arsenic-induced hepatic injuries and oxidative stress in experimental mice through activation of Nrf2 pathway, promotion of arsenic methylation and urinary excretion. Food Chem Toxicol 59:739-747
34. Thomas DJ, Li J, Waters SB, Xing W, Adair BM, Drobna Z, Devesa V, Styblo M (2007) Arsenic (+3 oxidation state) methyltransferase and the methylation of arsenicals. Exp Biol Med 232:3-13 (Pubitemid 46089936)
35. Murugaiyan J, Rockstroh M, Wagner J, Baumann S, Schorsch K, Trump S, Lehmann I, Bergen MV, Tomm JM(2013) Benzo[a]pyrene affects Jurkat Tcells in the activated state via the antioxidant response element dependent Nrf2 pathway leading to decreased IL-2 secretion and redirecting glutamine metabolism. Toxicol Appl Pharmacol 269: 307-316
36. Hellou J, Ross NW, Moon TW (2012) Glutathione, glutathione Stransferase, and glutathione conjugates, complementary markers of oxidative stress in aquatic biota. Environ Sci Pollut Res Int 19: 2007-2023
37. Wang XJ, Sun Z, Chen W, Eblin KE, Gandolfi JA, Zhang DD (2007) Nrf2 protects human bladder urothelial cells from arsenite and monomethylarsonous acid toxicity. Toxicol Appl Pharmacol 225: 206-213 (Pubitemid 350088062)
38. Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M (2006) Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact 160:1-40 (Pubitemid 43227479)
39. Yan D, Dong J, Sulik KK, Chen SY (2010) Induction of the Nrf2-driven antioxidant response by tert-butylhydroquinone prevents ethanol-induced apoptosis in cranial neural crest cells. Biochem Pharmacol 80:144-14940
40. Khodagholi F, Tusi SK (2011) Stabilization of Nrf2 by tBHQ prevents LPS-induced apoptosis in differentiated PC12 cells. Mol Cell Biochem 354:97-112
41. Kong AN, Owuor E, Yu R, Hebbar V, Chen C, Hu R, Mandlekar S (2001) Induction of xenobiotic enzymes by theMAP kinase pathway and the antioxidant or electrophile response element (ARE/EpRE). Drug Metab Rev 33:255-271 (Pubitemid 33136265)
42. Li S, Li J, Shen C, Zhang X, Sun S, Cho M, Sun C, Song Z (2014) tert-Butylhydroquinone (tBHQ) protects hepatocytes against lipotoxicity via inducing autophagy independently of Nrf2 activation. Biochim Biophys Acta 1841:22-33
43. Arredondo F, Echeverry C, Abin-Carriquiry JA, Blasina F, Antúnez K, Jones DP, Go YM, Liang YL, Dajas F (2010) After cellular internalization, quercetin causes Nrf2 nuclear translocation, increases glutathione levels, and prevents neuronal death against an oxidative insult. Free Radic Biol Med 49:738-747
44. Kuhn AM, Tzieply N, Schmidt MV, von Knethen A, Namgaladze D, Yamamoto M, Brüne B (2011) Antioxidant signaling via Nrf2 counteracts lipopolysaccharide-mediated inflammatory responses in foam cell macrophages. Free Radic Biol Med 50:1382-1391
45. Thomas DJ, Nava GM, Cai SY, Boyer JL, Hernández-Zavala A, Gaskins HR (2010) Arsenic (+3 oxidation state) methyltransferase and the methylation of arsenicals in the invertebrate chordate Ciona intestinalis. Toxicol Sci 113:70-76
46. Marapakala K, Qin J, Rosen BP (2012) Identification of catalytic residues in the As(III) S-adenosylmethionine methyltransferase. Biochemistry 51:944-951
47. Li X, Li B, Xi S, Zheng Q, Wang D, Sun G (2013) Association of urinary monomethylated arsenic concentration and risk of hypertension: a cross-sectional study from arsenic contaminated areas in northwestern China. Environ Health 12:37
48. Wu CC, Chen MC, Huang YK, Huang CY, Lai LA, Chung CJ, Shiue HS, Pu YS, Lin YC, Han BC, Wang YH, Hsueh YM (2013) Environmental tobacco smoke and arsenic methylation capacity are associated with urothelial carcinoma. J Formos Med Assoc 112:554-560