Sulforaphane Regulates NFE2L2/Nrf2-Dependent Xenobiotic Metabolism Phase II and Phase III Enzymes Differently in Human Colorectal Cancer and Untransformed Epithelial Colon Cells

References

• Higdon JV, Delage B, Williams DE, and Dashwood RH: Cruciferous vegetables and human cancer risk: epidemiologic evidence and mechanistic basis. Pharmacol Res 55, 224–236, 2007.
   PubMed Web of Science ®Google Scholar
• Fahey JW, Zalcmann AT, and Talalay P: The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 56, 5–51, 2001.
   PubMed Web of Science ®Google Scholar
• Guerrero-Beltrán CE, Caderón-Olivier M, Pedraza-Chaverri J, and Chirino YI: Protective effect of sulforaphane against oxidative stress: recent advances. Esp Toxicol Pathol 64, 503–508, 2012.
   PubMed Web of Science ®Google Scholar
• Shen G and Kong AN: Nrf2 plays an important role in coordinated regulation of Phase II drug metabolism enzymes and Phase III drug transporters. Biopharm Drug Dispos 30, 345–355, 2009.
   PubMed Web of Science ®Google Scholar
• McWalter GK, Higgins LG, McLellan LI, Henderson CJ, Song L, et al.: Transcription factor Nrf2 is essential for induction of NAD(P)H:quinone oxidoreductase 1, glutathione S-transferases, and glutamate cysteine ligase by broccoli seeds and isothiocyanates. J Nutr 134, 3499S–3506S, 2004.
   PubMed Web of Science ®Google Scholar
• Vollrath V, Wielandt AM, Iruretagoyena M, and Chianale J: Role of Nrf2 in the regulation of the Mrp2 (ABCC2) gene. Biochem J 395, 599–609, 2006.
   PubMed Web of Science ®Google Scholar
• Itoh K, Wakabayashi N, Katoh Y, Ishii T, Igarashi K, et al.: Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev 13, 76–86, 1999.
   PubMed Web of Science ®Google Scholar
• Dhakshinamoorthy S and Jaiswal AK: Functional characterization and role of INrf2 in antioxidant response element-mediated expression and antioxidant induction of NAD(P)H: quinone oxidoreductase1 gene. Oncogene 20, 3906–3917, 2001.
   PubMed Web of Science ®Google Scholar
• Itoh K, Chiba T, Takahashi S, Ishii T, Igarashi K, et al.: An Nrf2Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun 236, 313–322, 1997.
   PubMed Web of Science ®Google Scholar
• Venugopal R and Jaiswal AK: Nrf2 and Nrf1 in association with Jun proteins regulate antioxidant response element-mediated expression and coordinated induction of genes encoding detoxifying enzymes. Oncogene 17, 3145–3156, 1998.
   PubMed Web of Science ®Google Scholar
• Kwak MK, Wakabayashi N, Greenlaw JL, Yamamoto M, and Kensler TW: Antioxidants enhance mammalian proteasome expression through the Keap1-Nrf2 signaling pathway. Mol Cell Biol 23, 8786–8794, 2003.
   PubMed Web of Science ®Google Scholar
• Tripathi DN and Jena GB: Effect of melatonin on the expression of Nrf2 and NF-kappaB during cyclophosphamide induced urinary bladder injury in rat. J Pineal Res 48, 324–331, 2010.
   PubMed Web of Science ®Google Scholar
• Kensler TW, Wakabayashi N, and Biswal S: Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 47, 89–116, 2007.
   PubMed Web of Science ®Google Scholar
• Lau A, Villeneuve NF, Sun Z, Wong PK, and Zhang DD: Dual roles of Nrf2 in cancer. Pharmacol Res 58, 262–270, 2008.
   PubMed Web of Science ®Google Scholar
• Jaramillo MC and Zhang DD: The emerging role of the Nrf2-Keap1 signaling pathway in cancer. Genes Dev 27, 2179–2191, 2013.
   PubMed Web of Science ®Google Scholar
• Wang XJ, Sun Z, Villeneuve NF, Zhang S, Zhao F, et al.: Nrf2 enhances resistance of cancer cells to chemoptherapeutic drugs, the dark side of Nrf2. Carcinogenesis 29 1235–1243, 2008.
   PubMed Web of Science ®Google Scholar
• Moon J and Giaccia A: Dual roles of Nrf2 in tumor prevention and progression: possible implications in cancer treatment. Free Radic Biol Med 79, 292–299, 2015.
   PubMed Web of Science ®Google Scholar
• Ji L, Wei Y, Jiang T, and Wang S: Correlation of Nrf2, NQO1, MRP1, cmyc and p53 in colorectal cancer and their relationships to clinicopathologic features and survival. Int J Clin Exp Pathol 7, 1124–1131, 2014.
   PubMed Web of Science ®Google Scholar
• Ji L, Li H, Gao P, Shang G, Zhang DD, et al.: Nrf2 pathway regulates multidrug-resistance-associated protein 1 in small cell lung cancer. PLoS One 8, e63404, 2013.
   PubMed Web of Science ®Google Scholar
• Dinkova-Kostova AT, Fahey JW, and Talalay P: Chemical structures of inducers of nicotinamide quinone oxidoreductase 1 (NQO1). Methods Enzymol 382, 423–448, 2004.
   PubMed Web of Science ®Google Scholar
• Harris KE and Jeffery EH: Sulforaphane and erucin increase MRP1 and MRP2 in human carcinoma cell lines. J Nutr Biochem 19, 246–254, 2008.
   PubMed Web of Science ®Google Scholar
• De Larco JE, Park CA, Dronava H, and Furcht LT: Paradoxical roles for antioxidants in tumor prevention and eradication. Cancer Biol Ther 9, 362–370, 2010.
   PubMed Web of Science ®Google Scholar
• Tseng E, Kamath A, and Morris ME: Effect of organic isothiocyanates on the P-glycoprotein- and MRP1-mediated transport of daunomycin and vinblastine. Pharm Res 19, 1509–1515, 2002.
   PubMed Web of Science ®Google Scholar
• Qazi A, Pal J, Mait MP, Fulciniti M, Pelluru D, et al.: Anticancer activity of a broccoli derivative, sulforaphane, in barrett adenocarcinoma: potential use in chemoprevention and as adjuvant in chemotherapy. Trans Oncol 3, 389–399, 2010.
   PubMed Web of Science ®Google Scholar
• Misiewicz I, Skupińska K, and Kasprzycka-Guttman T: Differential response of human healthy lymphoblastoid and CCRF-SB leukemia cells to sulforaphane and its two analogues: 2-oxohexyl isothiocyanate and alyssin. Pharmacol Rep 59, 80–87, 2007.
   PubMed Web of Science ®Google Scholar
• Schmid H and Karrer P: Synthese der racemischen und der optischaktivenformen des sulforaphans. Helv Chim Acta 31, 1497–1505, 1948.
   PubMed Web of Science ®Google Scholar
• Prochaska HJ and Santamaria AB: Direct measurement of NAD(P)H:quinone reductase from cells cultured in microtiter: a screening sssay for anticarcinogenic enzyme inducers. Anal Biochem 169, 328–336, 1988.
   PubMed Web of Science ®Google Scholar
• Bradford MM: 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, 1976.
   PubMed Web of Science ®Google Scholar
• Bratosin D, Mitrofan L, Palii C, Estaquier J, and Montreuil J: Novel fluorescence assay using calcein-AM for the determination of human erythrocyte viability and aging. Cytometry A 66, 78–84, 2005.
   PubMed Web of Science ®Google Scholar
• van der Kolk DM, de Vries EG, Noordhoek L, ven den Berg E, van der Pol MA, et al.: Activity and expression of the multidrug resistance proteins P-glycoprotein, MRP1, MRP2, MRP3 and MRP5 in de novo and relapsed acute myeloid leukemia. Leukemia 10, 1544–1553, 2001.
   Web of Science ®Google Scholar
• Bustin SA: Quantification of mRNA using real-time reverse transcription PCR (RT-PCR): trends and problems. J Mol Endocrinol 29, 23–39, 2002.
   PubMed Web of Science ®Google Scholar
• Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C(T)) method. Methods 25, 402–408, 2001.
   PubMed Web of Science ®Google Scholar
• Skupinska K, Misiewicz-Krzeminska I, Stypulkowski R, Lubelska K, and Kasprzycka-Guttman T: Sulforaphane and its analogues inhibit CYP1A1 and CYP1A2 activity induced by benzo(a)pyrene. J Biochem Mol Toxicol 23, 18–28, 2009.
   PubMed Web of Science ®Google Scholar
• Wang M, Zhu JY, Chen S, Qing Y, Wu D, et al.: Effects of co-treatment with sulforaphane and autophagy modulators on uridine 5′-diphospho-glucuronosyltransferase 1A isoforms and cytochrome P450 3A4 expression in Caco-2 human colon cancer cells. Oncol Lett 8, 2407–2416, 2014.
   PubMed Web of Science ®Google Scholar
• Minarini A, Milelli A, Fimognari C, Simoni E, Turrini E, et al.: Exploring the effects of isothiocyanates on chemotherapeutic drugs. Expert Opin Drug Metab Toxicol 10, 25–38, 2014.
   PubMed Web of Science ®Google Scholar
• Yang YM, Noh K, Han CY, and Kim SG: Transactivation of genes encoding for phase II enzymes and phase III transporters by phytochemical antioxidants. Molecules 15, 6332–6348, 2010.
   PubMed Web of Science ®Google Scholar
• Nakata K, Tanaka Y, Nakano T, Adachi T, Tanaka H, et al.: Nuclear receptor-mediated transcriptional regulation in Phase I, II, and III xenobiotic metabolizing systems. Drug Metab Pharmacokinet 6, 437–457, 2006.
   Web of Science ®Google Scholar
• Milczarek M, Misiewicz-Krzemińska I, Lubelska K, and Wiktorska K: Combination treatment with 5-fluorouracil and isothiocyanates shows an antagonistic effect in Chinese hamster fibroblast cells line-V79. Acta Pol Pharm 68, 331–342, 2011.
   PubMed Web of Science ®Google Scholar
• Wang XF, Wu DM, Li BX, Lu YJ, and Yang BF: Synergistic inhibitory effect of sulforaphane and 5-fluorouracil in high and low metastasis cell lines of salivary gland adenoid cystic carcinoma. Phytother Res 23, 303–307, 2009.
   PubMed Web of Science ®Google Scholar
• Kansanen E, Kousmanen SM, Leinonen H, Levonen H, and Levonen AL: The Keap1-Nrf2 pathway: mechanisms of activation and dysregulation in cancer. Redox Biol 1, 45–49, 2013.
   PubMed Web of Science ®Google Scholar
• Johnson DR and Klaassen CD: Regulation of rat multidrug resistance protein 2 by classes of prototypical microsomal enzyme inducers that activate distinct transcription pathways. Toxicol Sci 67, 182–189, 2002.
   PubMed Web of Science ®Google Scholar
• Winski SL, Koutalos Y, Bentley DL, and Ross D: Subcellular localization of NAD(P)H:quinone oxidoreductase 1 in human cancer cells. Cancer Res 62, 1420–1424, 2002.
   PubMed Web of Science ®Google Scholar
• Seow HA, Penketh PG, Belcourt MF, Tomasz M, Rockwell S, et al.: Nuclear overexpression of NAD(P)H:quinone oxidoreductase 1 in Chinese hamster ovary cells increases the cytotoxicity of mitomycin C under aerobic and hypoxic conditions. J Biol Chem 279, 31606–31612, 2004.
   PubMed Web of Science ®Google Scholar
• Fisher S, Loncar J, Zaja R, Schnell S, Schirmer K, et al.: Constitutive mRNA expression and protein activity levels of nine ABC efflux transporters in seven permanent cell lines derived from different tissues of rainbow trout (Oncorhynchusmykiss). Aquat Toxicol 101, 438–446, 2011.
   PubMed Web of Science ®Google Scholar
• Perez MJ, Gonzalez-Sanchez E, Gonzalez-Loyola A, Gonzalez-Buitrago JM, and Marin JJ: Mitochondrial genome depletion dysregulates bile acid- and paracetamol-induced expression of the transporters Mdr1, Mrp1 and Mrp4 in liver cells. Br J Pharmacol 162, 1686–1699, 2011.
   PubMed Web of Science ®Google Scholar
• Siegel D, Anwar A, Winski SL, Kepa JK, Zolman KL, et al.: Rapid polyubiquitination and proteasomal degradation of a mutant form of NAD(P)H:quinoneoxidoreductase 1. Mol Pharmacol 59, 263–268, 2001.
   PubMed Web of Science ®Google Scholar
• Rajagopal A and Simon SM: Subcellular localization and activity of multidrug resistance proteins. Mol Biol Cell 14, 3389–3399, 2003.
   PubMed Web of Science ®Google Scholar
• Li Z, Zhang Y, Jin T, Men J, Lin Z, et al.: NQO1 protein expression predicts poor prognosis of non-small cell lung cancers. BMC Cancer 15, 207, 2015.
   PubMed Web of Science ®Google Scholar
• Cui X, Li L, Yan G, Meng K, Lin Z, et al.: High expression of NQO1 is associated with poor prognosis in serous ovarian carcinoma. BMC Cancer 15, 244, 2015.
   PubMed Web of Science ®Google Scholar
• Siegel D, Yan C, and Ross D: NAD(P)H:quinoneoxidoreductase 1 (NQO1) in the sensitivity and resistance to antitumor quinones. Biochem Pharmacol 83, 1033–1040, 2012.
   PubMed Web of Science ®Google Scholar
• Li LS, Bey EA, Dong Y, Meng J, Patra B, et al.: Modulating endogenous NQO1 levels identifies key regulatory mechanisms of action of β-lapachone for pancreatic cancer therapy. Clin Cancer Res 17, 275–285, 2011.
   PubMed Web of Science ®Google Scholar
• Dinkova-Kostova AT and Talalay P: NAD(P)H:quinone acceptor oxidoreductase 1 (NQO1), a multifunctional antioxidant enzyme and exceptionally versatile cytoprotector. Arch Biochem Biophys 501, 116–123, 2010.
   PubMed Web of Science ®Google Scholar