399
Views
5
CrossRef citations to date
0
Altmetric
Original Articles

The positive feedback loop between Nrf2 and phosphogluconate dehydrogenase stimulates proliferation and clonogenicity of human hepatoma cells

, , , , , , , , & show all
Pages 906-917 | Received 29 Oct 2019, Accepted 19 Apr 2020, Published online: 27 May 2020

References

  • Motohashi H, Yamamoto M. Nrf2-Keap1 defines a physiologically important stress response mechanism. Trends Mol Med. 2004;10(11):549–557.
  • Nguyen T, Nioi P, Pickett CB. The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress. J Biol Chem. 2009;284(20):13291–13295.
  • Copple IM. The Keap1-Nrf2 cell defense pathway-a promising therapeutic target? Adv Pharmacol. 2012; 63:43–79.
  • Rojo de la Vega M, Chapman E, Zhang DD. NRF2 and the hallmarks of cancer. Cancer Cell. 2018;34(1):21–43.
  • Cloer EW, Goldfarb D, Schrank TP, et al. NRF2 activation in cancer: from DNA to protein. Cancer Res. 2019;79(5):889–898.
  • Taguchi K, Motohashi H, Yamamoto M. Molecular mechanisms of the Keap1-Nrf2 pathway in stress response and cancer evolution. Genes Cells. 2011;16(2):123–140.
  • Yamamoto M, Kensler TW, Motohashi H. The KEAP1-NRF2 system: a thiol-based sensor-effector apparatus for maintaining redox homeostasis. Physiol Rev. 2018;98(3):1169–1203.
  • Otsuki A, Yamamoto M. Cis-element architecture of Nrf2-sMaf heterodimer binding sites and its relation to diseases. Arch Pharm Res. 2020;43(3):275–285.
  • Thimmulappa RK, Mai KH, Srisuma S. Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray identification of Nrf2-regulated genes induced by the chemopreventive agent. Cancer Res. 2002;2002:5196–5203.
  • Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–674.
  • Cairns RA, Harris IS, Mak TW. Regulation of cancer cell metabolism. Nat Rev Cancer. 2011;11(2):85–95.
  • Boroughs LK, Deberardinis RJ. Metabolic pathways promoting cancer cell survival and growth. Nat Cell Biol. 2015;17(4):351–359.
  • Phan LM, Yeung S-C, Lee M-H. Cancer metabolic reprogramming: importance, main features, and potentials for precise targeted anti-cancer therapies. Cancer Biol Med. 2014;11(1):1–19.
  • Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science. 2009;324(5930):1029–1034.
  • Kroemer G, Pouyssegur J. Tumor cell metabolism: cancer’s achilles’ heel. Cancer Cell. 2008;13(6):472–482.
  • Jiang P, Du W, Wu M. Regulation of the pentose phosphate pathway in cancer. Protein Cell. 2014;5(8):592–602.
  • Stincone A, Prigione A, Cramer T, et al. The return of metabolism: biochemistry and physiology of the pentose phosphate pathway. Biol Rev. 2015;90(3):927–963.
  • Chan B, Vanderlaan PA, Sukhatme VP. 6-Phosphogluconate dehydrogenase regulates tumor cell migration in vitro by regulating receptor tyrosine kinase c-Met. Biochem Biophys Res Commun. 2013;439(2):247–251.
  • Sukhatme VP, Chan B. Glycolytic cancer cells lacking 6-phosphogluconate dehydrogenase metabolize glucose to induce senescence. FEBS Lett. 2012;586(16):2389–2395.
  • Giusti L, Iacconi P, Ciregia F, et al. Fine-needle aspiration of thyroid nodules: proteomic analysis to identify cancer biomarkers. J Proteome Res. 2008;7(9):4079–4088.
  • Jonas SK, Benedetto C, Flatman A, et al. Increased activity of 6-phosphogluconate dehydrogenase and glucose-6-phosphate dehydrogenase in purified cell suspensions and single cells from the uterine cervix in cervical intraepithelial neoplasia. Br J Cancer. 1992;66(1):185–191.
  • Lin R, Elf S, Shan C, et al. 6-Phosphogluconate dehydrogenase links oxidative PPP, lipogenesis and tumour growth by inhibiting LKB1-AMPK signalling. Nat Cell Biol. 2015;17(11):1484–1496.
  • Mitsuishi Y, Taguchi K, Kawatani Y, et al. Nrf2 redirects glucose and glutamine into anabolic pathways in metabolic reprogramming. Cancer Cell. 2012;22(1):66–79.
  • Furfaro AL, Traverso N, Domenicotti C, et al. The Nrf2/HO-1 axis in cancer cell growth and chemoresistance. Oxid Med Cell Longev. 2016; 2016:1–14.
  • Itoh K, Chiba T, Takahashi S, et al. An Nrf2/Small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun. 1997;236(2):313–232.
  • Bryan HK, Olayanju A, Goldring CE, et al. The Nrf2 cell defence pathway: Keap1-dependent and -independent mechanisms of regulation. Biochem Pharmacol. 2013;85(6):705–717.
  • Paul MK, Bisht B, Darmawan DO, et al. Dynamic changes in intracellular ROS levels regulate airway basal stem cell homeostasis through Nrf2-dependent Notch signaling. Cell Stem Cell. 2014;15(2):199–214.
  • Jaramillo MC, Zhang DD. The emerging role of the Nrf2–Keap1 signaling pathway in cancer. Genes Dev. 2013;27(20):2179–2191.
  • Heiss EH, Schachner D, Zimmermann K, et al. Glucose availability is a decisive factor for Nrf2-mediated gene expression. Redox Biol. 2013;1(1):359–365.
  • Itoh K, Wakabayashi N, Katoh Y, et al. Keap1 regulates both cytoplasmic-nuclear shuttling and degradation of Nrf2 in response to electrophiles. Genes Cells. 2003;8(4):379–391.
  • Tian W, Rojo de la Vega M, Schmidlin CJ, et al. Kelch-like ECH-associated protein 1 (KEAP1) differentially regulates nuclear factor erythroid-2-related factors 1 and 2 (NRF1 and NRF2. J Biol Chem. 2018;293(6):2029–2040.
  • Taguchi K, Fujikawa N, Komatsu M, et al. Keap1 degradation by autophagy for the maintenance of redox homeostasis. Proc Natl Acad Sci USA. 2012;109(34):13561–13566.
  • Lau A, Wang X-J, Zhao F, et al. A noncanonical mechanism of Nrf2 activation by autophagy deficiency: direct interaction between Keap1 and p62. Mol Cell Biol. 2010;30(13):3275–3285.
  • Hayes JD, Dinkova-Kostova AT. The Nrf2 regulatory network provides an interface between redox and intermediary metabolism. Trends Biochem Sci. 2014;39(4):199–219.
  • Huang Y, Li W, Su Z, et al. The complexity of the Nrf2 pathway: beyond the antioxidant response. J Nutr Biochem. 2015;26(12):1401–1413.
  • Surh YJ, Kundu JK, Na HK, et al. Redox-sensitive transcription factors as prime targets for chemoprevention with anti-inflammatory and antioxidative phytochemicals. J Nutr. 2005;135(12):2993S–3001S.
  • Ramos-Gomez M, Dolan PM, Itoh K, et al. Interactive effects of nrf2 genotype and oltipraz on benzo[a]pyrene-DNA adducts and tumor yield in mice. Carcinogenesis. 2003;24(3):461–467.
  • Khor TO, Huang M-T, Prawan A, et al. Increased susceptibility of Nrf2 knockout mice to colitis-associated colorectal cancer. Cancer Prev Res (Phila). 2008;1(3):187–191.
  • Iida K, Itoh K, Kumagai Y, et al. Nrf2 is essential for the chemopreventive efficacy of oltipraz against urinary bladder carcinogenesis. Cancer Res. 2004;64(18):6424–6431.
  • Ramos-Gomez M, Kwak M-K, Dolan PM, et al. Sensitivity to carcinogenesis is increased and chemoprotective efficacy of enzyme inducers is lost in nrf2 transcription factor-deficient mice. Proc Natl Acad Sci USA. 2001;98(6):3410–3415.
  • Kim YR, Oh JE, Kim MS, et al. Oncogenic NRF2 mutations in squamous cell carcinomas of oesophagus and skin. J Pathol. 2010;220(4):446–451.
  • Ooi A, Dykema K, Ansari A, et al. CUL3 and NRF2 mutations confer an NRF2 activation phenotype in a sporadic form of papillary renal cell carcinoma. Cancer Res. 2013;73(7):2044–2051.
  • Solis LM, Behrens C, Dong W, et al. Nrf2 and Keap1 abnormalities in non–small cell lung carcinoma and association with clinicopathologic features. Clin Cancer Res. 2010;16(14):3743–3753.
  • Yoo NJ, Kim HR, Kim YR, et al. Somatic mutations of the KEAP1 gene in common solid cancers. Histopathology. 2012;60(6):943–952.
  • Inami Y, Waguri S, Sakamoto A, et al. Persistent activation of Nrf2 through p62 in hepatocellular carcinoma cells. J Cell Biol. 2011;193(2):275–284.
  • Na HK, Surh YJ. Oncogenic potential of Nrf2 and its principal target protein heme oxygenase-1. Free Radic Biol Med. 2014; 67:353–365.
  • Zhou T, Zhang M, Zhao L, et al. Activation of Nrf2 contributes to the protective effect of Exendin-4 against angiotensin II-induced vascular smooth muscle cell senescence. Am J Physiol – Cell Physiol. 2016;311(4):C572–C582.
  • Wu T, Li J, Li Y, et al. Antioxidant and hepatoprotective effect of swertiamarin on carbon tetrachloride-induced hepatotoxicity via the Nrf2/HO-1 pathway. Cell Physiol Biochem. 2017;41(6):2242–2254.
  • Guerrero-Hue M, Farré-Alins V, Palomino-Antolin A et al. Targeting Nrf2 in the protection against renal disease. Curr Med Chem. 2017; 24(33):3583–3605.
  • Milkovic L, Zarkovic N, Saso L. Controversy about pharmacological modulation of Nrf2 for cancer therapy. Redox Biol. 2017; 12:727–732.
  • Kawasaki Y, Okumura H, Uchikado Y, et al. Nrf2 is useful for predicting the effect of chemoradiation therapy on esophageal squamous cell carcinoma. Ann Surg Oncol. 2014;21(7):2347–2352.
  • Park SA, Lee MH, Na HK, et al. 4-Hydroxyestradiol induces mammary epithelial cell transformation through Nrf2-mediated heme oxygenase-1 overexpression. Oncotarget. 2019;10(12):164–178.
  • Seyfried TN, Flores RE, Poff AM, et al. Cancer as a metabolic disease: implications for novel therapeutics. Carcinogenesis. 2014;35(3):515–527.
  • DeBerardinis RJ, Lum JJ, Hatzivassiliou G, et al. The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab. 2008;7(1):11–20.
  • Brocklehurst D, Champion AE, Cheek TR, et al. The value of 6-phosphogluconate dehydrogenase (6-PGDH) activity as a marker of tumour cellularity and prognostic indicator in primary breast cancer. Tumour Biol. 1986;7(2-3):99–104.
  • Ngo HKC, Kim DH, Cha YN, et al. Nrf2 mutagenic activation drives hepatocarcinogenesis. Cancer Res. 2017;77(18):4797–4808.
  • Sunamura M, Duda DG, Ghattas MH, et al. Heme oxygenase-1 accelerates tumor angiogenesis of human pancreatic cancer. Angiogenesis. 2003;6(1):15–24.
  • Li Y, Su J, DingZhang X, et al. PTEN deletion and heme oxygenase-1 overexpression cooperate in prostate cancer progression and are associated with adverse clinical outcome. J Pathol. 2011;224(1):90–100.
  • Mayerhofer M, Florian S, Krauth M-T, et al. Identification of heme oxygenase-1 as a novel BCR/ABL-dependent survival factor in chronic myeloid leukemia. Cancer Res. 2004;64(9):3148–3154.
  • Schlager JJ, Powis G. Cytosolic NAD(P)H:(Quinone-acceptor)oxidoreductase in human normal and tumor tissue: effects of cigarette smoking and alcohol. Int J Cancer. 1990;45(3):403–409.
  • Malkinson AM, Siegel D, Forrest GL, et al. Elevated DT-diaphorase activity and messenger RNA content in human non-small cell lung carcinoma: relationship to the response of lung tumor xenografts to mitomycin Cł. Cancer Res. 1992;52(17):4752–4757.
  • Cabello CM, Bair WB, Bause AS, et al. Antimelanoma activity of the redox dye DCPIP (2,6-dichlorophenolindophenol) is antagonized by NQO1. Biochem Pharmacol. 2009;78(4):344–354.
  • Garate M, Wani AA, Li G. The NAD(P)H:Quinone Oxidoreductase 1 induces cell cycle progression and proliferation of melanoma cells. Free Radic Biol Med. 2010;48(12):1601–1609.
  • Jamshidi M, Bartkova J, Greco D, et al. NQO1 expression correlates inversely with NFκB activation in human breast cancer. Breast Cancer Res Treat. 2012;132(3):955–968.
  • Kim A, Zhang R, Han X, et al. Involvement of glutathione and glutathione metabolizing enzymes in human colorectal cancer cell lines and tissues. Mol Med Rep. 2015;12(3):4314–4319.
  • Fiorillo M, Sotgia F, Sisci D, et al. Mitochondrial “power” drives tamoxifen resistance: NQO1 and GCLC are new therapeutic targets in breast cancer. Oncotarget. 2017;8(12):20309–20327.
  • Cullinan SB, Gordan JD, Jin J, et al. The Keap1-BTB protein is an adaptor that bridges Nrf2 to a Cul3-based E3 ligase: oxidative stress sensing by a Cul3-Keap1 ligase. Mol Cell Biol. 2004;24(19):8477–8486.
  • Suzuki T, Muramatsu A, Saito R, et al. Molecular mechanism of cellular oxidative stress sensing by Keap1. Cell Rep. 2019;28(3):746–758.
  • Wishart DS. Emerging applications of metabolomics in drug discovery and precision medicine. Nat Rev Drug Discov. 2016;15(7):473–484.
  • Yang M, Soga T, Pollard PJ, et al. The emerging role of fumarate as an oncometabolite. Front Oncol. 2012;2:85.
  • Jain M, Nilsson R, Sharma S, et al. Oncometabolites: linking altered metabolism with cancer. Science. 2012;336(6084):1040–1044.
  • Zhang J, Fan J, Venneti S, et al. Asparagine plays a critical role in regulating cellular adaptation to glutamine depletion. Mol Cell. 2014;56(2):205–218.

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.