314
Views
32
CrossRef citations to date
0
Altmetric
Research Article

Wogonin-enhanced reactive oxygen species-induced apoptosis and potentiated cytotoxic effects of chemotherapeutic agents by suppression Nrf2-mediated signaling in HepG2 cells

, , , , , , & show all
Pages 607-621 | Received 13 Dec 2013, Accepted 18 Feb 2014, Published online: 25 Mar 2014

References

  • Forman HJ, Maiorino M, Ursini F. Signaling functions of reactive oxygen species. Biochemistry 2010;49:835–842.
  • Hileman EO, Liu J, Albitar M, Keating MJ, Huang P. Intrinsic oxidative stress in cancer cells: a biochemical basis for therapeutic selectivity. Cancer Chemother Pharmacol 2004;53:209–219.
  • Pelicano H, Carney D, Huang P. ROS stress in cancer cells and therapeutic implications. Drug Resist Updat 2004;7: 97–110.
  • Droge W. Free radicals in the physiological control of cell function. Physiol Rev 2002;82:47–95.
  • Evans JL, Goldfine ID, Maddux BA, Grodsky GM. Are oxidative stress-activated signaling pathways mediators of insulin resistance and beta-cell dysfunction?. Diabetes 2003;52:1–8.
  • Wasserman WW, Fahl WE. Functional antioxidant responsive elements. Proc Natl Acad Sci U S A 1997;94:5361–5366.
  • Nguyen T, Sherratt PJ, Pickett CB. Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. Annu Rev Pharmacol Toxicol 2003;43: 233–260.
  • Itoh K, Tong KI, Yamamoto M. Molecular mechanism activating Nrf2-Keap1 pathway in regulation of adaptive response to electrophiles. Free Radic Biol Med 2004;36: 1208–1213.
  • Chan K, Han XD, Kan YW. An important function of Nrf2 in combating oxidative stress: detoxification of acetaminophen. Proc Natl Acad Sci U S A 2001;98:4611–4616.
  • Cullinan SB, Diehl JA. PERK-dependent activation of Nrf2 contributes to redox homeostasis and cell survival following endoplasmic reticulum stress. J Biol Chem 2004; 279:20108–20117.
  • Niture SK, Kaspar JW, Shen J, Jaiswal AK. Nrf2 signaling and cell survival. Toxicol Appl Pharmacol 2010;244:37–42.
  • Wang XJ, Sun Z, Villeneuve NF, Zhang S, Zhao F, Li Y, et al. Nrf2 enhances resistance of cancer cells to chemotherapeutic drugs, the dark side of Nrf2. Carcinogenesis 2008;29: 1235–1243.
  • Zhang P, Singh A, Yegnasubramanian S, Esopi D, Kombairaju P, Bodas M, et al. Loss of Kelch-like ECH- associated protein 1 function in prostate cancer cells causes chemoresistance and radioresistance and promotes tumor growth. Mol Cancer Ther 2010;9:336–346.
  • Kim HR, Kim S, Kim EJ, Park JH, Yang SH, Jeong ET, et al. Suppression of Nrf2-driven heme oxygenase-1 enhances the chemosensitivity of lung cancer A549 cells toward cisplatin. Lung Cancer 2008;60:47–56.
  • Shaw AT, Winslow MM, Magendantz M, Ouyang C, Dowdle J, Subramanian A, et al. Selective killing of K-ras mutant cancer cells by small molecule inducers of oxidative stress. Proc Natl Acad Sci U S A 2011;108:8773–8778.
  • Maher JM, Dieter MZ, Aleksunes LM, Slitt AL, Guo G, Tanaka Y, et al. Oxidative and electrophilic stress induces multidrug resistance-associated protein transporters via the nuclear factor-E2-related factor-2 transcriptional pathway. Hepatology 2007;46:1597–1610.
  • Konstantinopoulos PA, Spentzos D, Fountzilas E, Francoeur N, Sanisetty S, Grammatikos AP, et al. Keap1 mutations and Nrf2 pathway activation in epithelial ovarian cancer. Cancer Res 2011;71:5081–5089.
  • Kubo M, Asano T, Shiomoto H, Matsuda H. Studies on rehmanniae radix. I. Effect of 50% ethanolic extract from steamed and dried rehmanniae radix on hemorheology in arthritic and thrombosic rats. Biol Pharm Bull 1994;17: 1282–1286.
  • Wang W, Guo Q, You Q, Zhang K, Yang Y, Yu J, et al. Involvement of bax/bcl-2 in wogonin-induced apoptosis of human hepatoma cell line SMMC-7721. Anticancer Drugs 2006;17:797–805.
  • Fresco P, Borges F, Diniz C, Marques MP. New insights on the anticancer properties of dietary polyphenols. Med Res Rev 2006;26:747–766.
  • Li DR, Hou HX, Zhang W, Li L. [Effects of wogonin on inducing apoptosis of human ovarian cancer A2780 cells and telomerase activity]. Ai Zheng 2003;22:801–805.
  • Lee WR, Shen SC, Lin HY, Hou WC, Yang LL, Chen YC. Wogonin and fisetin induce apoptosis in human promyeloleukemic cells, accompanied by a decrease of reactive oxygen species, and activation of caspase 3 and Ca(2+)-dependent endonuclease. Biochem Pharmacol 2002;63:225–236.
  • Wei L, Lu N, Dai Q, Rong J, Chen Y, Li Z, et al. Different apoptotic effects of wogonin via induction of H(2)O(2) generation and Ca(2+) overload in malignant hepatoma and normal hepatic cells. J Cell Biochem 2010;111: 1629–1641.
  • Zhong Y, Zhang F, Sun Z, Zhou W, Li ZY, You QD, et al. Drug resistance associates with activation of Nrf2 in MCF-7/DOX cells, and wogonin reverses it by down-regulating Nrf2-mediated cellular defense response. Mol Carcinog 2012.
  • Hui KM, Huen MS, Wang HY, Zheng H, Sigel E, Baur R, et al. Anxiolytic effect of wogonin, a benzodiazepine receptor ligand isolated from Scutellaria baicalensis Georgi. Biochem Pharmacol 2002;64:1415–1424.
  • Saw CL, Cintron M, Wu TY, Guo Y, Huang Y, Jeong WS, Kong AN. Pharmacodynamics of dietary phytochemical indoles I3C and DIM: induction of Nrf2-mediated phase II drug metabolizing and antioxidant genes and synergism with isothiocyanates. Biopharm Drug Dispos 2011;32:289–300.
  • Ohnuma T, Matsumoto T, Itoi A, Kawana A, Nishiyama T, Ogura K, Hiratsuka A. Enhanced sensitivity of A549 cells to the cytotoxic action of anticancer drugs via suppression of Nrf2 by procyanidins from Cinnamomi Cortex extract. Biochem Biophys Res Commun 2011;413:623–629.
  • Trachootham D, Alexandre J, Huang P. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach?Nat Rev Drug Discov 2009;8:579–591.
  • Young LC, Campling BG, Cole SP, Deeley RG, Gerlach JH. Multidrug resistance proteins MRP3, MRP1, and MRP2 in lung cancer: correlation of protein levels with drug response and messenger RNA levels. Clin Cancer Res 2001;7:1798–1804.
  • Sachdeva M, Mo YY. p53 and c-myc: how does the cell balance “yin” and “yang”?Cell Cycle 2009;8:1303.
  • DeNicola GM, Karreth FA, Humpton TJ, Gopinathan A, Wei C, Frese K, et al. Oncogene-induced Nrf2 transcription promotes ROS detoxification and tumorigenesis. Nature 2011;475:106–109.
  • Tsai CF, Yeh WL, Huang SM, Tan TW, Lu DY. Wogonin induces reactive oxygen species production and cell apoptosis in human glioma cancer cells. Int J Mol Sci 2012;13:9877–9892.
  • Wang CZ, Calway TD, Wen XD, Smith J, Yu C, Wang Y, et al. Hydrophobic flavonoids from Scutellaria baicalensis induce colorectal cancer cell apoptosis through a mitochondrial- mediated pathway. Int J Oncol 2013;42:1018–1026.
  • Lee DH, Lee TH, Jung CH, Kim YH. Wogonin induces apoptosis by activating the AMPK and p53 signaling pathways in human glioblastoma cells. Cell Signal 2012;24:2216–2225.
  • Moi P, Chan K, Asunis I, Cao A, Kan YW. Isolation of NF-E2-related factor 2 (Nrf2), a NF-E2-like basic leucine zipper transcriptional activator that binds to the tandem NF-E2/AP1 repeat of the beta-globin locus control region. Proc Natl Acad Sci U S A 1994;91:9926–9930.
  • Dhakshinamoorthy S, Porter AG. Nitric oxide-induced transcriptional up-regulation of protective genes by Nrf2 via the antioxidant response element counteracts apoptosis of neuroblastoma cells. J Biol Chem 2004;279:20096–20107.
  • Li J, Johnson D, Calkins M, Wright L, Svendsen C, Johnson J. Stabilization of Nrf2 by tBHQ confers protection against oxidative stress-induced cell death in human neural stem cells. Toxicol Sci 2005;83:313–328.
  • Nguyen T, Huang HC, Pickett CB. Transcriptional regulation of the antioxidant response element. Activation by Nrf2 and repression by MafK. J Biol Chem 2000;275: 15466–15473.
  • Yu JQ, Liu HB, Tian DZ, Liu YW, Lei JC, Zou GL. Changes in mitochondrial membrane potential and reactive oxygen species during wogonin-induced cell death in human hepatoma cells. Hepatol Res 2007;37:68–76.
  • Ding XW, Wu JH, Jiang CP. ABCG2: a potential marker of stem cells and novel target in stem cell and cancer therapy. Life Sci 2010;86:631–637.
  • Pelengaris S, Khan M, Evan G. c-MYC: more than just a matter of life and death. Nat Rev Cancer 2002;2:764–776.
  • Ho JS, Ma W, Mao DY, Benchimol S. p53-Dependent transcriptional repression of c-myc is required for G1 cell cycle arrest. Mol Cell Biol 2005;25:7423–7431.
  • Levy S, Forman HJ. C-Myc is a Nrf2-interacting protein that negatively regulates phase II genes through their electrophile responsive elements. IUBMB Life 2010;62:237–246.
  • Huang ST, Wang CY, Yang RC, Chu CJ, Wu HT, Pang JH. Wogonin, an active compound in Scutellaria baicalensis, induces apoptosis and reduces telomerase activity in the HL-60 leukemia cells. Phytomedicine 2010;17:47–54.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.