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Research Paper

Luteolin inhibits Musashi1 binding to RNA and disrupts cancer phenotypes in glioblastoma cells

, , , , , , , , ORCID Icon, , , & show all
Pages 1420-1432 | Received 03 Jul 2018, Accepted 16 Oct 2018, Published online: 18 Nov 2018

References

  • Ostrom QT, Gittleman H, Liao P, et al. CBTRUS statistical report: primary brain and other central nervous system tumors diagnosed in the United States in 2010–2014. Neuro Oncol. 2017 Nov 6;19(suppl_5):v1–v88. PubMed PMID: 29117289; PubMed Central PMCID: PMCPmc5693142. eng.
  • Weller M, Cloughesy T, Perry JR, et al. Standards of care for treatment of recurrent glioblastoma–are we there yet? Neuro Oncol. 2013 Jan;15(1):4–27. PubMed PMID: 23136223; PubMed Central PMCID: PMCPmc3534423. eng.
  • Stupp R, Mason WP, van Den Bent MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005 Mar 10;352(10):987–996. PubMed PMID: 15758009; eng.
  • Nam JY, de Groot JF. Treatment of Glioblastoma. J Oncol Pract. 2017 Oct;13(10):629–638. PubMed PMID: 29020535; eng.
  • Chinot OL, Wick W, Mason W, et al. Bevacizumab plus radiotherapy-temozolomide for newly diagnosed glioblastoma. N Engl J Med. 2014 Feb 20;370(8):709–722. PubMed PMID: 24552318; eng.
  • Gerstberger S, Hafner M, Tuschl T. A census of human RNA-binding proteins. Nat Reviews Genet. 2014 Dec;15(12):829–845. PubMed PMID: 25365966; eng.
  • Lennox AL, Mao H, Silver DL. RNA on the brain: emerging layers of post-transcriptional regulation in cerebral cortex development. Wiley Interdiscip Rev Dev Biol. 2018 Jan;7(1):e290. PubMed PMID: 28837264; PubMed Central PMCID: PMCPmc5746464. eng.
  • Brinegar AE, Cooper TA. Roles for RNA-binding proteins in development and disease. Brain Res. 2016 Sep 15;1647:1–8. PubMed PMID: 26972534; PubMed Central PMCID: PMCPmc5003702. eng.
  • Pereira B, Billaud M, Almeida R. RNA-binding proteins in cancer: old players and new actors. Trends Cancer. 2017 Jul;3(7):506–528. PubMed PMID: 28718405; eng.
  • Hong S. RNA binding protein as an emerging therapeutic target for cancer prevention and treatment. J Cancer Prev. 2017 Dec;22(4):203–210. PubMed PMID: 29302577; PubMed Central PMCID: PMCPmc5751837. eng.
  • Kaneko Y, Sakakibara S, Imai T, et al. Musashi1: an evolutionally conserved marker for CNS progenitor cells including neural stem cells. Dev Neurosci. 2000;22(1–2):139–153. PubMed PMID: 10657706; eng.
  • MacNicol AM, Hardy LL, Spencer HJ, et al. Neural stem and progenitor cell fate transition requires regulation of Musashi1 function. BMC Dev Biol. 2015 Mar 18;15:15. PubMed PMID: 25888190; PubMed Central PMCID: PMCPmc4369890. eng.
  • Kudinov AE, Karanicolas J, Golemis EA, et al. Musashi RNA-binding proteins as cancer drivers and novel therapeutic targets. Clin Cancer Res. 2017 May 1;23(9):2143–2153. PubMed PMID: 28143872; PubMed Central PMCID: PMCPmc5413399. eng.
  • Vo DT, Subramaniam D, Remke M, et al. The RNA-binding protein Musashi1 affects medulloblastoma growth via a network of cancer-related genes and is an indicator of poor prognosis. Am J Pathol. 2012 Nov;181(5):1762–1772. PubMed PMID: 22985791; PubMed Central PMCID: PMCPmc3761132. eng.
  • Kanemura Y, Mori K, Sakakibara S, et al. Musashi1, an evolutionarily conserved neural RNA-binding protein, is a versatile marker of human glioma cells in determining their cellular origin, malignancy, and proliferative activity. Differentiation. 2001 Sep;68(2–3):141–152. PubMed PMID: 11686236; eng.
  • de Araujo PR, Gorthi A, Da Silva AE, et al. Musashi1 impacts radio-resistance in glioblastoma by controlling DNA-protein kinase catalytic subunit. Am J Pathol. 2016 Sep;186(9):2271–2278. PubMed PMID: 27470713; PubMed Central PMCID: PMCPmc5012509. eng.
  • Uren PJ, Vo DT, de Araujo PR, et al. RNA-binding protein musashi1 is a central regulator of adhesion pathways in glioblastoma. Mol Cell Biol. 2015 Sep 1;35(17):2965–2978. PubMed PMID: 26100017; PubMed Central PMCID: PMCPmc4525321. eng.
  • Cambuli FM, Correa BR, Rezza A, et al. A mouse model of targeted musashi1 expression in whole intestinal epithelium suggests regulatory roles in cell cycle and stemness. Stem Cells (Dayton, Ohio). 2015 Dec;33(12):3621–3634. PubMed PMID: 26303183; PubMed Central PMCID: PMCPmc4713339. eng.
  • Sakakibara S, Nakamura Y, Yoshida T, et al. RNA-binding protein Musashi family: roles for CNS stem cells and a subpopulation of ependymal cells revealed by targeted disruption and antisense ablation. Proc Natl Acad Sci USA. 2002 Nov 12;99(23):15194–15199. PubMed PMID: 12407178; PubMed Central PMCID: PMCPmc137566. eng.
  • Plateroti M, de Araujo PR, Da Silva AE, et al. The RNA-binding protein Musashi1: a major player in intestinal epithelium renewal and colon cancer development. Curr Colorectal Cancer Rep. 2012;8(4):290–297. PubMed PMID: 23914149; PubMed Central PMCID: PMCPmc3728701. eng.
  • Lagadec C, Vlashi E, Frohnen P, et al. The RNA-binding protein Musashi-1 regulates proteasome subunit expression in breast cancer- and glioma-initiating cells. Stem Cells (Dayton, Ohio). 2014 Jan;32(1):135–144. PubMed PMID: 24022895; PubMed Central PMCID: PMCPmc3968686. eng.
  • Wang XY, Yu H, Linnoila RI, et al. Musashi1 as a potential therapeutic target and diagnostic marker for lung cancer. Oncotarget. 2013 May;4(5):739–750. PubMed PMID: 23715514; PubMed Central PMCID: PMCPmc3742834. eng.
  • Lathia JD, Mack SC, Mulkearns-Hubert EE, et al. Cancer stem cells in glioblastoma. Genes Dev. 2015 Jun 15;29(12):1203–1217. PubMed PMID: 26109046; PubMed Central PMCID: PMCPmc4495393. eng.
  • Mao P, Joshi K, Li J, et al. Mesenchymal glioma stem cells are maintained by activated glycolytic metabolism involving aldehyde dehydrogenase 1A3. Proc Natl Acad Sci USA. 2013 May 21;110(21):8644–8649. PubMed PMID: 23650391; PubMed Central PMCID: PMCPmc3666732. eng.
  • Hubert CG, Rivera M, Spangler LC, et al. A three-dimensional organoid culture system derived from human glioblastomas recapitulates the hypoxic gradients and cancer stem cell heterogeneity of tumors found in vivo. Cancer Res. 2016 Apr 15;76(8):2465–2477. PubMed PMID: 26896279; PubMed Central PMCID: PMCPmc4873351. eng.
  • Chou TC. Drug combination studies and their synergy quantification using the Chou-Talalay method. Cancer Res. 2010 Jan 15;70(2):440–446. PubMed PMID: 20068163; eng.
  • Deeks ED. Olaparib: first global approval. Drugs. 2015 Feb;75(2):231–240. PubMed PMID: 25616434; eng.
  • Rasmussen RD, Gajjar MK, Jensen KE, et al. Enhanced efficacy of combined HDAC and PARP targeting in glioblastoma. Mol Oncol. 2016 May;10(5):751–763. PubMed PMID: 26794465; PubMed Central PMCID: PMCPmc5423160. eng.
  • Gupta SK, Mladek AC, Carlson BL, et al. Discordant in vitro and in vivo chemo-potentiating effects of the PARP inhibitor veliparib in temozolomide-sensitive versus -resistant glioblastoma multiforme xenografts. Clin Cancer Res. 2014 May 16;20(14):3730–3741. PubMed PMID: PMC4111895.
  • Rasmussen RD, Gajjar MK, Tuckova L, et al. BRCA1-regulated RRM2 expression protects glioblastoma cells from endogenous replication stress and promotes tumorigenicity. Nat Commun. 2016 Nov 15;7:13398. PubMed PMID: 27845331; PubMed Central PMCID: PMCPmc5116074. eng.
  • Kechavarzi B, Janga SC. Dissecting the expression landscape of RNA-binding proteins in human cancers. Genome Biol. 2014 Jan 10;15(1):R14. PubMed PMID: 24410894; PubMed Central PMCID: PMCPmc4053825. eng.
  • Wang J, Liu Q, Shyr Y. Dysregulated transcription across diverse cancer types reveals the importance of RNA-binding protein in carcinogenesis. BMC Genomics. 2015;16 Suppl 7:S5. PubMed PMID: 26100984; PubMed Central PMCID: PMCPmc4474540. eng.
  • Choiniere M, Watt-Watson J, Victor JC, et al. Prevalence of and risk factors for persistent postoperative nonanginal pain after cardiac surgery: a 2-year prospective multicentre study. Cmaj. 2014 Apr 15;186(7):E213–23. PubMed PMID: 24566643; PubMed Central PMCID: PMCPmc3986330. eng.
  • Wang Z, Bhattacharya A, Ivanov DN. Identification of small-molecule inhibitors of the HuR/RNA interaction using a fluorescence polarization screening assay followed by NMR validation. PLoS One. 2015;10(9):e0138780. PubMed PMID: 26390015; PubMed Central PMCID: PMCPmc4577092. eng.
  • Duffy AG, Makarova-Rusher OV, Ulahannan SV, et al. Modulation of tumor eIF4E by antisense inhibition: A phase I/II translational clinical trial of ISIS 183750-an antisense oligonucleotide against eIF4E-in combination with irinotecan in solid tumors and irinotecan-refractory colorectal cancer. Int J Cancer. 2016 Oct 1;139(7):1648–1657. PubMed PMID: 27194579; eng.
  • Sanchez-Diaz PC, Burton TL, Burns SC, et al. Musashi1 modulates cell proliferation genes in the medulloblastoma cell line Daoy. BMC Cancer. 2008 Sep 30;8:280. PubMed PMID: 18826648; PubMed Central PMCID: PMCPmc2572071. eng.
  • Sureban SM, May R, George RJ, et al. Knockdown of RNA binding protein musashi-1 leads to tumor regression in vivo. Gastroenterology. 2008 May;134(5):1448–1458. PubMed PMID: 18471519; eng.
  • Li N, Yousefi M, Nakauka-Ddamba A, et al. The Msi family of RNA-binding proteins function redundantly as intestinal oncoproteins. Cell Rep. 2015 Dec 22;13(11):2440–2455. PubMed PMID: 26673327; PubMed Central PMCID: PMCPmc4894540. eng.
  • Kharas MG, Lengner CJ. Stem cells, cancer, and MUSASHI in blood and guts. Trends Cancer. 2017 May;3(5):347–356. PubMed PMID: 28718412; PubMed Central PMCID: PMCPmc5546142. eng.
  • Shou Z, Jin X, He X, et al. Overexpression of Musashi-1 protein is associated with progression and poor prognosis of gastric cancer. Oncol Lett. 2017 May;13(5):3556–3566. PubMed PMID: 28521458; PubMed Central PMCID: PMCPmc5431268. eng.
  • Chen K, Gao Q, Zhang W, et al. Musashi1 regulates survival of hepatoma cell lines by activation of Wnt signalling pathway. Liver Int. 2015 Mar;35(3):986–998. PubMed PMID: 24444033; eng.
  • Gong P, Wang Y, Gao Y, et al. Msi1 promotes tumor progression by epithelial-to-mesenchymal transition in cervical cancer. Hum Pathol. 2017 Jul;65:53–61. PubMed PMID: 28088346; eng.
  • Wang XY, Penalva LO, Yuan H, et al. Musashi1 regulates breast tumor cell proliferation and is a prognostic indicator of poor survival. Mol Cancer. 2010 Aug 21;9:221. PubMed PMID: 20727204; PubMed Central PMCID: PMCPmc2939568. eng.
  • Luo Y, Shang P, Li D. Luteolin: a flavonoid that has multiple cardio-protective effects and its molecular mechanisms. Front Pharmacol. 2017;8:692. PubMed PMID: 29056912; PubMed Central PMCID: PMCPmc5635727. eng.
  • Jeon IH, Kim HS, Kang HJ, et al. Anti-inflammatory and antipruritic effects of luteolin from Perilla (P. frutescens L.) leaves. Molecules. 2014 May 27;19(6):6941–6951. PubMed PMID: 24871572; eng.
  • Lin Y, Shi R, Wang X, et al. Luteolin, a flavonoid with potential for cancer prevention and therapy. Curr Cancer Drug Targets. 2008 Nov;8(7):634–646. PubMed PMID: 18991571; PubMed Central PMCID: PMCPmc2615542. eng.
  • Kang KA, Piao MJ, Ryu YS, et al. Luteolin induces apoptotic cell death via antioxidant activity in human colon cancer cells. Int J Oncol. 2017 Oct;51(4):1169–1178. PubMed PMID: 28791416; eng.
  • Liu Y, Lang T, Jin B, et al. Luteolin inhibits colorectal cancer cell epithelial-to-mesenchymal transition by suppressing CREB1 expression revealed by comparative proteomics study. J Proteomics. 2017 May 24;161:1–10. PubMed PMID: 28391045; eng.
  • Zang M, Hu L, Zhang B, et al. Luteolin suppresses angiogenesis and vasculogenic mimicry formation through inhibiting Notch1-VEGF signaling in gastric cancer. Biochem Biophys Res Commun. 2017 Aug 26;490(3):913–919. PubMed PMID: 28655612; eng.
  • Zang MD, Hu L, Fan ZY, et al. Luteolin suppresses gastric cancer progression by reversing epithelial-mesenchymal transition via suppression of the Notch signaling pathway. J Transl Med. 2017 Feb 27;15(1):52. PubMed PMID: 28241766; PubMed Central PMCID: PMCPmc5327575. eng.
  • Cook MT, Liang Y, Besch-Williford C, et al. Luteolin inhibits lung metastasis, cell migration, and viability of triple-negative breast cancer cells. Breast Cancer (Dove Medical Press). 2017;9:9–19. PubMed PMID: 28096694; PubMed Central PMCID: PMCPmc5207335. eng.
  • Seo Y, Ryu K, Park J, et al. Inhibition of ANO1 by luteolin and its cytotoxicity in human prostate cancer PC-3 cells. PLoS One. 2017;12(3):e0174935. PubMed PMID: 28362855; PubMed Central PMCID: PMCPmc5376326. eng.
  • Anson DM, Wilcox RM, Huseman ED, et al. Luteolin decreases epidermal growth factor receptor-mediated cell proliferation and induces apoptosis in glioblastoma cell lines. Basic Clin Pharmacol Toxicol. 2018 Jun 23. PubMed PMID: 29935053; eng. DOI:10.1111/bcpt.13077
  • Wang Q, Wang H, Jia Y, et al. Luteolin induces apoptosis by ROS/ER stress and mitochondrial dysfunction in gliomablastoma. Cancer Chemother Pharmacol. 2017 May;79(5):1031–1041. PubMed PMID: 28393257; eng.
  • Wang Q, Wang H, Jia Y, et al. Luteolin reduces migration of human glioblastoma cell lines via inhibition of the p-IGF-1R/PI3K/AKT/mTOR signaling pathway. Oncol Lett. 2017 Sep;14(3):3545–3551. PubMed PMID: 28927111; PubMed Central PMCID: PMCPmc5588063. eng.
  • Cheng WY, Chiao MT, Liang YJ, et al. Luteolin inhibits migration of human glioblastoma U-87 MG and T98G cells through downregulation of Cdc42 expression and PI3K/AKT activity. Mol Biol Rep. 2013 Sep;40(9):5315–5326. PubMed PMID: 23677714; PubMed Central PMCID: PMCPmc3751389. eng.
  • Chakrabarti M, Ray SK. Synergistic anti-tumor actions of luteolin and silibinin prevented cell migration and invasion and induced apoptosis in glioblastoma SNB19 cells and glioblastoma stem cells. Brain Res. 2015 Dec 10;1629:85–93. PubMed PMID: 26471408; eng.
  • Chakrabarti M, Ray SK. Anti-tumor activities of luteolin and silibinin in glioblastoma cells: overexpression of miR-7-1-3p augmented luteolin and silibinin to inhibit autophagy and induce apoptosis in glioblastoma in vivo. Apoptosis. 2016 Mar;21(3):312–328. PubMed PMID: 26573275; eng.
  • Sonoki H, Tanimae A, Endo S, et al. Kaempherol and luteolin decrease claudin-2 expression mediated by inhibition of STAT3 in lung adenocarcinoma A549 cells. Nutrients. 2017 Jun 13;9(6):597. PubMed PMID: 28608828; PubMed Central PMCID: PMCPmc5490576. eng.
  • Xu H, Yang T, Liu X, et al. Luteolin synergizes the antitumor effects of 5-fluorouracil against human hepatocellular carcinoma cells through apoptosis induction and metabolism. Life Sci. 2016 Jan 1;144:138–147. PubMed PMID: 26656468; eng.
  • Tu DG, Lin WT, Yu CC, et al. Chemotherapeutic effects of luteolin on radio-sensitivity enhancement and interleukin-6/signal transducer and activator of transcription 3 signaling repression of oral cancer stem cells. J Formos Med Assoc. 2016 Dec;115(12):1032–1038. PubMed PMID: 27742160; eng.
  • Ohyama T, Nagata T, Tsuda K, et al. Structure of Musashi1 in a complex with target RNA: the role of aromatic stacking interactions. Nucleic Acids Res. 2012 Apr;40(7):3218–3231. PubMed PMID: 22140116; PubMed Central PMCID: PMCPmc3326303. eng.
  • Sayre NL, Sifuentes M, Holstein D, et al. Stimulation of astrocyte fatty acid oxidation by thyroid hormone is protective against ischemic stroke-induced damage. J Cereb Blood Flow Metab. 2017 Feb;37(2):514–527. PubMed PMID: 26873887; PubMed Central PMCID: PMCPmc5381439. eng.

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