265
Views
13
CrossRef citations to date
0
Altmetric
Original Articles

Inhibition of Nrf2 might enhance the anti-tumor effect of temozolomide in glioma cells via inhibition of Ras/Raf/MEK signaling pathway

, , , &
Pages 975-983 | Received 21 Jul 2019, Accepted 27 Apr 2020, Published online: 26 May 2020

References

  • Fitzmaurice C, Dicker D, Pain A, et al. The Global Burden of cancer 2013. JAMA Oncol. 2015;1(4):505–527.
  • Strobel H, Baisch T, Fitzel R, et al. Temozolomide and other alkylating agents in glioblastoma therapy. Biomedicines. 2019;7(3):69.
  • Stupp R, Mason WP, van den Bent MJ, et al. European organisation for research and treatment of cancer brain tumor and radiotherapy groups, national cancer institute of canada clinical trials group. N Engl J Med. 2005;352(10):987–996.
  • Friedman HS, Kerby T, Calvert H. Temozolomide and treatment of malignant glioma. Clin Cancer Res. 2000;6(7):2585–2597.
  • Brandes AA, Franceschi E, Tosoni A, et al. MGMT promoter methylation status can predict the incidence and outcome of pseudoprogression after concomitant radiochemotherapy in newly diagnosed glioblastoma patients. J Clin Oncol. 2008;26(13):2192–2197.
  • Roy S, Lahiri D, Maji T, et al. Recurrent glioblastoma: where we stand. South Asian J Cancer. 2015;4(4):163–173.
  • Kansanen E, Kuosmanen SM, Leinonen H, et al. The Keap1-Nrf2 pathway: mechanisms of activation and dysregulation in cancer. Redox Biol. 2013;1:45–49.
  • Tebay LE, Robertson H, Durant ST, et al. Mechanisms of activation of the transcription factor Nrf2 by redox stressors, nutrient cues, and energy status and the pathways through which it attenuates degenerative disease. Free Radic Biol Med. 2015;88(Pt B):108–146.
  • Rojo AI, Rada P, Mendiola M, et al. The PTEN/NRF2 axis promotes human carcinogenesis. Antioxid Redox Signal. 2014;21(18):2498–2514.
  • Hamada S, Taguchi K, Masamune A, et al. Nrf2 promotes mutant K-ras/p53-driven pancreatic carcinogenesis. Carcinogenesis. 2017;38(6):661–670.
  • Liu D, Zhang Y, Wei Y, et al. Activation of AKT pathway by Nrf2/PDGFA feedback loop contributes to HCC progression. Oncotarget. 2016;7(40):65389–65402.
  • Wang T, Hu P, Li B, et al. Role of Nrf2 signaling pathway in the radiation tolerance of patients with head and neck squamous cell carcinoma: an in vivo and in vitro study. Onco Targets Ther. 2017;10:1809–1819.
  • Jakubowicz-Gil J, Bądziul D, Langner E, et al. Temozolomide and sorafenib as programmed cell death inducers of human glioma cells. Pharmacol Rep. 2017;69(4):779–787.
  • Jakubowicz-Gil J, Bądziul D, Langner E, et al. RTA 408 Inhibits Interleukin-1β-Induced MMP-9 Expression via Suppressing Protein Kinase-Dependent NF-κB and AP-1 Activation in Rat Brain Astrocytes. Int J Mol Sci. 2019;20:E2826.
  • Singh A, Venkannagari S, Oh KH, et al. Small molecule inhibitor of NRF2 selectively intervenes therapeutic resistance in KEAP1-deficient NSCLC tumors. ACS Chem Biol. 2016;11(11):3214–3225.
  • Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001;25(4):402–408.
  • Chen LM, Song TJ, Xiao JH, et al. Tripchlorolide induces autophagy in lung cancer cells by inhibiting the PI3K/AKT/mTOR pathway and improves cisplatin sensitivity in A549/DDP cells. Oncotarget. 2017;8(38):63911–63922.
  • Le Rhun E, Taillibert S, Chamberlain MC. Anaplastic glioma: current treatment and management. Expert Rev Neurother. 2015;15(6):601–620.
  • Zeng T, Cui D, Gao L. Glioma: an overview of current classifications, characteristics, molecular biology and target therapies. Front Biosci (Landmark Ed)). 2015;20:1104–1115.
  • Hart MG, Garside R, Rogers G, et al. Temozolomide for high grade glioma. Cochrane Database Syst Rev. 2013;4:CD007415.
  • Corcoran RB, André T, Atreya CE, et al. Combined BRAF, EGFR, and MEK inhibition in patients with BRAFV600E-mutant colorectal cancer. Cancer Discov. 2018;8(4):428–443.
  • Yen I, Shanahan F, Merchant M, et al. Pharmacological induction of RAS-GTP confers RAF inhibitor sensitivity in KRAS mutant tumors. Cancer Cell. 2018;34(4):611–625.
  • Hayashi T, Desmeules P, Smith RS, et al. RASA1 and NF1 are preferentially co-mutated and define a distinct genetic subset of smoking-associated non–small cell lung carcinomas sensitive to MEK inhibition. Clin Cancer Res. 2018;24(6):1436–1447.
  • Jaiswal BS, Durinck S, Stawiski EW, et al. ERK mutations and amplification confer resistance to ERK-inhibitor therapy. Clin Cancer Res. 2018;24(16):4044–4055.
  • Chen M, Wan L, Zhang J, et al. Deregulated PP1α phosphatase activity towards MAPK activation is antagonized by a tumor suppressive failsafe mechanism. Nat Commun. 2018;9(1):159.
  • Eblen ST. Extracellular-regulated kinases: signaling from Ras to ERK substrates to control biological outcomes. Adv Cancer Res. 2018;138:99–142.
  • Steelman LS, Pohnert SC, Shelton JG, et al. JAK/STAT, Raf/MEK/ERK, PI3K/Akt and BCR-ABL in cell cycle progression and leukemogenesis. Leukemia. 2004;18(2):189–218.
  • Nakano H, Shindo M, Sakon S, et al. Differential regulation of IkappaB kinase alpha and beta by two upstream kinases, NF-kappaB-inducing kinase and mitogen-activated protein kinase/ERK kinase kinase-1. Proc Natl Acad Sci USA. 1998;95(7):3537–3542.
  • Weinstein-Oppenheimer CR, Henríquez-Roldán CF, Davis J, et al. Role of the Raf signal transduction cascade in the in vitro resistance to the anticancer drug doxorubicin. Clinical Cancer Res. 2001;7:2892–2907.
  • Davis JM, Weinstein-Oppenheimer CR, Steelman LS, et al. Raf-1 and Bcl-2 induce distinct and common pathways which contribute to breast cancer drug resistance. Clinical Cancer Res. 2003;9:1161–1170.
  • Kang MI, Kobayashi A, Wakabayashi N, et al. Scaffolding of Keap1 to the actin cytoskeleton controls the function of Nrf2 as key regulator of cytoprotective phase 2 genes. Proc Natl Acad Sci USA. 2004;101(7):2046–2051.
  • Dinkova-Kostova AT, Holtzclaw WD, Wakabayashi N. Keap1, the sensor for electrophiles and oxidants that regulates the phase 2 response, is a zinc metalloprotein. Biochemistry. 2005;44(18):6889–6899.
  • Bellezza I, Giambanco I, Minelli A, et al. Nrf2-Keap1 signaling in oxidative and reductive stress. Biochim Biophys Acta Mol Cell Res. 2018;1865(5):721–733.
  • Chen W, Sun Z, Wang XJ, et al. Direct interaction between Nrf2 and p21(Cip1/WAF1) upregulates the Nrf2-mediated antioxidant response. Mol Cell. 2009;34(6):663–673.
  • Maines MD. The heme oxygenase system: update 2005. Antioxid Redox Signal. 2005;7(11-12):1761–1766.
  • Kourti M, Jiang WG, Cai J. Aspects of carbon monoxide in form of CO-releasing molecules used in cancer treatment: more light on the way. Oxid Med Cell Longev. 2017;2017:9326454
  • Andres MM, Luszczki JJ. Modified western blot technique in fast detection of heme oxygenase (HO-1/HO-2) in various tissues and organs of experimental animals. Ann Univ Mariae Curie Sklodowska Med. 2004;59(2):298–302.
  • Wei W, Shurui C, Zipeng Z, et al. Aspirin suppresses neuronal apoptosis, reduces tissue inflammation, and restrains astrocyte activation by activating the Nrf2/HO-1 signaling pathway. Neuroreport. 2018;29(7):524–531.
  • Mylroie H, Dumont O, Bauer A, et al. PKCε-CREB-Nrf2 signalling induces HO-1 in the vascular endothelium and enhances resistance to inflammation and apoptosis. Cardiovasc Res. 2015;106(3):509–519.
  • An X, Shang F. RA-XII exerts anti-oxidant and anti-inflammatory activities on lipopolysaccharide-induced acute renal injury by suppressing NF-κB and MAPKs regulated by HO-1/Nrf2 pathway. Biochem Biophys Res Commun. 2018;495(3):2317–2323.
  • Hammond CL, Lee TK, Ballatori N. Novel roles for glutathione in gene expression, cell death, and membrane transport of organic solutes. J Hepatol. 2001;34(6):946–954.
  • Gaucher C, Boudier A, Bonetti J, et al. Glutathione: antioxidant properties dedicated to nanotechnologies. Antioxidants. 2018;7(5):62.
  • Deponte M. The incomplete glutathione puzzle: just guessing at numbers and figures? Antioxid Redox Signal. 2017;27(15):1130–1161.
  • Rhee SG, Kil IS. Multiple functions and regulation of mammalian peroxiredoxins. Annu Rev Biochem. 2016;85:127.
  • Sharapov MG, Novoselov VI. Catalytic and Signaling Role of Peroxiredoxins in Carcinogenesis. Biochemistry Mosc. 2019;84(2):79–100.
  • Jarvis RM, Hughes SM, Ledgerwood EC. Peroxiredoxin 1 functions as a signal peroxidase to receive, transduce, and transmit peroxide signals in mammalian cells. Free Radic Biol Med. 2012;53(7):1522–1530.
  • Laurent TC, Moore EC, Reichard P. Enzymatic synthesis of deoxyribonucleotides. Iv. Isolation and characterization of thioredoxin, the hydrogen donor from Escherichia coli B. J Biol Chem. 1964;239:3436–3444.
  • Zeng XS, Jia JJ, Kwon Y, et al. The role of thioredoxin-1 in suppression of endoplasmic reticulum stress in Parkinson disease. Free Radic Biol Med. 2014;67:10–18.
  • Saggioro D, Rigobello MP, Paloschi L, et al. Gold(III)-dithiocarbamato complexes induce cancer cell death triggered by thioredoxin redox system inhibition and activation of ERK pathway. Chem Biol. 2007;14(10):1128–1139.
  • Cattaruzza L, Fregona D, Mongiat M, et al. Antitumor activity of gold(III)-dithiocarbamato derivatives on prostate cancer cells and xenografts. Int J Cancer. 2011;128(1):206–215.
  • Hwang TS, Choi HK, Han HS. Differential expression of manganese superoxide dismutase, copper/zinc superoxide dismutase, and catalase in gastric adenocarcinoma and normal gastric mucosa. Eur J Surg Oncol. 2007;33(4):474–479.
  • Kalinina EV, Chernov NN, Saprin AN, et al. Changes in expression of genes encoding antioxidant enzymes, heme oxygenase-1, Bcl-2, and Bcl-xl and in level of reactive oxygen species in tumor cells resistant to doxorubicin. Biochemistry Mosc. 2006;71(11):1200–1206.
  • Glorieux C, Sandoval JM, Fattaccioli A, et al. Chromatin remodeling regulates catalase expression during cancer cells adaptation to chronic oxidative stress. Free Radic Biol Med. 2016a;99:436–450.

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.