Anti-cancer effects of the HuR inhibitor, MS-444, in malignant glioma cells

References

• van Den Bent MJ, Klein M, Smits M, Reijneveld JC, French PJ, Clement P, Fyf DV, Wick A, Mulholland PJ, Taphoorn MJB, et al. 2018. Bevacizumab and temozolomide in patients with first recurrence of WHO grade II and III glioma, without 1p/19q co-deletion (TAVAREC): a randomised controlled phase 2 EORTC trial. Lancet Oncol. 19:1170–1179. doi:10.1016/S1470-2045(18)30362-0.
   PubMed Web of Science ®Google Scholar
• Desjardins A, Gromeier M, Herndon JE, Beaubier N, Bolognesi DP, Friedman AH, Friedman HS, McSherry F, Muscat AM, Nair S, et al. 2018. Recurrent glioblastoma treated with recombinant poliovirus. N Engl J Med. 379:150–161. doi:10.1056/NEJMoa1716435.
   PubMed Web of Science ®Google Scholar
• Lathia JD, Mack SC, Mulkearns-Hubert EE, Valentim CL, Rich JN. 2015. Cancer stem cells in glioblastoma. Genes Dev. 29:1203–1217. doi:10.1101/gad.261982.115.
   PubMed Web of Science ®Google Scholar
• Cai X, Sughrue ME. 2018. Glioblastoma: new therapeutic strategies to address cellular and genomic complexity. Oncotarget. 9:9540–9554. doi:10.18632/oncotarget.23476.
   PubMedGoogle Scholar
• Maeda H, Kuwahara H, Ichimura Y, Ohtsuki M, Kurakata S, Shiraishi A. TGF-beta enhances macrophage ability to produce IL-10 in normal and tumor-bearing mice. J Immunol. 1995;155:4926–4932.
   PubMed Web of Science ®Google Scholar
• Markovic DS, Vinnakota K, Chirasani S, Synowitz M, Raguet H, Stock K, Sliwa M, Lehmann S, Kälin R, van Rooijen N, et al. 2009. Gliomas induce and exploit microglial MT1-MMP expression for tumor expansion. Proc Natl Acad Sci USA. 106:12530–12535. doi:10.1073/pnas.0804273106.
   PubMed Web of Science ®Google Scholar
• Abdelmohsen K, Gorospe M. 2010. Posttranscriptional regulation of cancer traits by HuR. Wiley Interdiscip Rev RNA. 1:214–229. doi:10.1002/wrna.4.
   PubMed Web of Science ®Google Scholar
• Dixon DA, Tolley ND, King PH, Nabors LB, McIntyre TM, Zimmerman GA, Prescott SM. 2001. Altered expression of the mRNA stability factor HuR promotes cyclooxygenase-2 expression in colon cancer cells. J Clin Invest. 108:1657–1665. doi:10.1172/JCI12973.
   PubMed Web of Science ®Google Scholar
• Filippova N, Yang X, Wang Y, Gillespie GY, Langford C, King PH, Wheeler C, Nabors LB. 2011. The RNA-binding protein HuR promotes glioma growth and treatment resistance. Mol Cancer Res. 9:648–659. doi:10.1158/1541-7786.MCR-10-0325.
   PubMed Web of Science ®Google Scholar
• Nabors LB, Suswam E, Huang Y, Yang X, Johnson MJ, King PH. Tumor necrosis factor alpha induces angiogenic factor up-regulation in malignant glioma cells: a role for RNA stabilization and HuR. Cancer Res. 2003;63:4181–4187.
   PubMed Web of Science ®Google Scholar
• Nabors LB, Gillespie GY, Harkins L, King PH. HuR, an RNA stability factor, is expressed in malignant brain tumors and binds to adenine and uridine-rich elements within the 3ʹ untranslated regions of cytokine and angiogenic factor mRNAs. Cancer Res. 2001;61:2154–2161.
   PubMed Web of Science ®Google Scholar
• Meisner N-C, Hintersteiner M, Mueller K, Bauer R, Seifert J-M, Naegeli H-U, Ottl J, Oberer L, Guenat C, Moss S, et al. Identification and mechanistic characterization of low-molecular-weight inhibitors for HuR. Nat Chem Biol. 2007;3:508–515. doi:10.1038/nchembio.2007.14.
   PubMed Web of Science ®Google Scholar
• Blanco FF, Preet R, Aguado A, Vishwakarma V, Stevens LE, Vyas A, Padhye S, Xu L, Weir SJ, Anant S, et al. 2016. Impact of HuR inhibition by the small molecule MS-444 on colorectal cancer cell tumorigenesis. Oncotarget. 7:74043–74058. doi:10.18632/oncotarget.12189.
   PubMedGoogle Scholar
• Romeo C, Weber MC, Zarei M, DeCicco D, Chand SN, Lobo AD, Winter JM, Sawicki JA, Sachs JN, Meisner-Kober N, et al. 2016. HuR contributes to TRAIL resistance by restricting death receptor 4 expression in pancreatic cancer cells. Mol Cancer Res. 14:599–611. doi:10.1158/1541-7786.mcr-15-0448.
   PubMed Web of Science ®Google Scholar
• Hu Y, Smyth GK. 2009. ELDA: extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays. J Immunol Methods. 347:70–78. doi:10.1016/j.jim.2009.06.008.
   PubMed Web of Science ®Google Scholar
• Bellail AC, Tse MC, Song JH, Phuphanich S, Olson JJ, Sun SY, Hao C. 2010. DR5-mediated DISC controls caspase-8 cleavage and initiation of apoptosis in human glioblastomas. J Cell Mol Med. 14:1303–1317. doi:10.1111/j.1582-4934.2009.00777.x.
   PubMed Web of Science ®Google Scholar
• Song JH, Song DK, Pyrzynska B, Petruk KC, Van Meir EG, Hao C. TRAIL triggers apoptosis in human malignant glioma cells through extrinsic and intrinsic pathways. Brain Pathol. 2003;13:539–553. doi:10.1111/j.1750-3639.2003.tb00484.x.
   PubMed Web of Science ®Google Scholar
• Roth W, Isenmann S, Nakamura M, Platten M, Wick W, Kleihues P, Bahr M, Ohgaki H, Ashkenazi A, Weller M. Soluble decoy receptor 3 is expressed by malignant gliomas and suppresses CD95 ligand-induced apoptosis and chemotaxis. Cancer Res. 2001;61:2759–2765.
   PubMed Web of Science ®Google Scholar
• Srikantan S, Gorospe M. HuR function in disease. Front Biosci (Landmark Ed). 2012;17:189–205. doi:10.2741/3921.
   PubMed Web of Science ®Google Scholar
• Galban S, Kuwano Y, Pullmann R Jr., Martindale JL, Kim HH, Lal A, Abdelmohsen K, Yang X, Dang Y, Liu JO, et al. 2008. RNA-binding proteins HuR and PTB promote the translation of hypoxia-inducible factor-1α. Mol Cell Biol. 28:93–107. doi:10.1128/mcb.00973-07.
   PubMed Web of Science ®Google Scholar
• Rodriguez-Pascual F, Hausding M, Ihrig-Biedert I, Furneaux H, Levy AP, Forstermann U, Kleinert H. Complex contribution of the 3ʹ-untranslated region to the expressional regulation of the human inducible nitric-oxide synthase gene. Involvement of the RNA-binding protein HuR. J Biol Chem. 2000;275:26040–26049. doi:10.1074/jbc.M910460199.
   PubMed Web of Science ®Google Scholar
• Levy NS, Chung S, Furneaux H, Levy AP. Hypoxic stabilization of vascular endothelial growth factor mRNA by the RNA-binding protein HuR. J Biol Chem. 1998;273:6417–6423. doi:10.1074/jbc.273.11.6417.
   PubMed Web of Science ®Google Scholar
• Pineda DM, Rittenhouse DW, Valley CC, Cozzitorto JA, Burkhart RA, Leiby B, Winter JM, Weber MC, Londin ER, Rigoutsos I, et al. HuR’s post-transcriptional regulation of death receptor 5 in pancreatic cancer cells. Cancer Biol Ther. 2012;13:1–10.
   Web of Science ®Google Scholar
• Kwan T, Floyd CL, Kim S, King PH. 2017. RNA binding protein human antigen R is translocated in astrocytes following spinal cord injury and promotes the inflammatory response. J Neurotrauma. 34:1249–1259. doi:10.1089/neu.2016.4757.
   PubMed Web of Science ®Google Scholar
• Matsye P, Zheng L, Si Y, Kim S, Luo W, Crossman DK, Bratcher PE, King PH. 2017. HuR promotes the molecular signature and phenotype of activated microglia: implications for amyotrophic lateral sclerosis and other neurodegenerative diseases. Glia. 65:945–963. doi:10.1002/glia.23137.
   PubMed Web of Science ®Google Scholar
• Filippova N, Yang X, Ananthan S, Sorochinsky A, Hackney JR, Gentry Z, Bae S, King P, Nabors LB. 2017. Hu antigen R (HuR) multimerization contributes to glioma disease progression. J Biol Chem. 292:16999–17010. doi:10.1074/jbc.M117.797878.
   PubMed Web of Science ®Google Scholar
• Filippova N, Yang X, King P, Nabors LB. 2012. Phosphoregulation of the RNA-binding protein Hu antigen R (HuR) by Cdk5 affects centrosome function. J Biol Chem. 287:32277–32287. doi:10.1074/jbc.M112.353912.
   PubMed Web of Science ®Google Scholar
• Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN. 2006. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 444:756–760. doi:10.1038/nature05236.
   PubMed Web of Science ®Google Scholar
• Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR, Lu L, Irvin D, Black KL, Yu JS. 2006. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer. 5:67. doi:10.1186/1476-4598-5-67.
   PubMed Web of Science ®Google Scholar
• Chen J, Li Y, Yu T-S, McKay RM, Burns DK, Kernie SG, Parada LF. 2012. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature. 488:522. doi:10.1038/nature11287.
   PubMed Web of Science ®Google Scholar
• Herrmann A, Cherryholmes G, Schroeder A, Phallen J, Alizadeh D, Xin H, Wang T, Lee H, Lahtz C, Swiderski P, et al. 2014. TLR9 is critical for glioma stem cell maintenance and targeting. Cancer Res. 74:5218–5228. doi:10.1158/0008-5472.can-14-1151.
   PubMed Web of Science ®Google Scholar
• Grivennikov S, Karin M. 2008. Autocrine IL-6 signaling: a key event in tumorigenesis?. Cancer Cell. 13:7–9. doi:10.1016/j.ccr.2007.12.020.
   PubMed Web of Science ®Google Scholar
• Wang H, Lathia JD, Wu Q, Wang J, Li Z, Heddleston JM, Eyler CE, Elderbroom J, Gallagher J, Schuschu J, et al. 2009. Targeting interleukin 6 signaling suppresses glioma stem cell survival and tumor growth. Stem Cells. 27:2393–2404. doi:10.1002/stem.188.
   PubMed Web of Science ®Google Scholar
• Gurgis FM, Yeung YT, Tang MX, Heng B, Buckland M, Ammit AJ, Haapasalo J, Haapasalo H, Guillemin GJ, Grewal T, et al. 2015. The p38-MK2-HuR pathway potentiates EGFRvIII-IL-1beta-driven IL-6 secretion in glioblastoma cells. Oncogene. 34:2934–2942. doi:10.1038/onc.2014.225.
   PubMed Web of Science ®Google Scholar
• Tran AN, Boyd NH, Walker K, Hjelmeland AB. 2017. NOS expression and NO function in glioma and implications for patient therapies. Antioxid Redox Signal. 26:986–999. doi:10.1089/ars.2016.6820.
   PubMed Web of Science ®Google Scholar
• Han J, Alvarez-Breckenridge CA, Wang Q-E YJ. TGF-β signaling and its targeting for glioma treatment. Am J Cancer Res. 2015;5:945–955.
   PubMed Web of Science ®Google Scholar
• Heddleston JM, Hitomi M, Venere M, Flavahan WA, Yang K, Kim Y, Minhas S, Rich JN, Hjelmeland AB. Glioma stem cell maintenance: the role of the microenvironment. Curr Pharm Des. 2011;17:2386–2401. doi:10.2174/138161211797249260.
   PubMed Web of Science ®Google Scholar
• Li W, Graeber MB. 2012. The molecular profile of microglia under the influence of glioma. Neuro-Oncology. 14:958–978. doi:10.1093/neuonc/nos116.
   PubMed Web of Science ®Google Scholar
• Tummers B, Green DR. 2017. Caspase-8: regulating life and death. Immunol Rev. 277:76–89. doi:10.1111/imr.12541.
   PubMed Web of Science ®Google Scholar
• Arakawa Y, Tachibana O, Hasegawa M, Miyamori T, Yamashita J, Hayashi Y. 2005. Frequent gene amplification and overexpression of decoy receptor 3 in glioblastoma. Acta Neuropathol. 109:294–298. doi:10.1007/s00401-004-0956-6.
   PubMed Web of Science ®Google Scholar
• Koff JL, Ramachandiran S, Bernal-Mizrachi L. 2015. A time to kill: targeting apoptosis in cancer. Int J Mol Sci. 16:2942–2955. doi:10.3390/ijms16022942.
   PubMed Web of Science ®Google Scholar
• Zhao X, Laver T, Hong SW, Twitty GB Jr., Devos A, Devos M, Benveniste EN, Nozell SE, An N. 2011. F-kappaB p65-cIAP2 link is necessary for mediating resistance to TNF-alpha induced cell death in gliomas. J Neurooncol. 102:367–381. doi:10.1007/s11060-010-0346-y.
   PubMed Web of Science ®Google Scholar
• LaCasse EC, Mahoney DJ, Cheung HH, Plenchette S, Baird S, Korneluk RG. IAP-targeted therapies for cancer. Oncogene. 2008;27:6252–6275. doi:10.1038/onc.2008.302.
   PubMed Web of Science ®Google Scholar
• Tan AC, Heimberger AB, Khasraw M. 2017. Immune checkpoint inhibitors in gliomas. Curr Oncol Rep. 19:23. doi:10.1007/s11912-017-0586-5.
   PubMed Web of Science ®Google Scholar
• Coelho MA, de Carne Trecesson S, Rana S, Zecchin D, Moore C, Molina-Arcas M, East P, Spencer-Dene B, Nye E, Barnouin K, et al. 2017. Oncogenic RAS signaling promotes tumor immunoresistance by stabilizing PD-L1 mRNA. Immunity. 47:1083–99 e6. doi:10.1016/j.immuni.2017.11.016.
   PubMed Web of Science ®Google Scholar
• Marín-Ramos NI, Thein TZ, Cho H-Y, Swenson SD, Wang W, Schönthal AH, Chen TC, Hofman FM. 2018. NEO212 inhibits migration and invasion of glioma stem cells. Mol Cancer Ther. 17:625–637. doi:10.1158/1535-7163.mct-17-0591.
   PubMed Web of Science ®Google Scholar
• D’Agostino VG, Lal P, Mantelli B, Tiedje C, Zucal C, Thongon N, Gaestel M, Latorre E, Marinelli L, Seneci P, et al. 2015. Dihydrotanshinone-I interferes with the RNA-binding activity of HuR affecting its post-transcriptional function. Sci Rep. 5:16478. doi:10.1038/srep16478.
   PubMed Web of Science ®Google Scholar
• Moradi F, Berglund P, Linnskog R, Leandersson K, Andersson T, Prasad CP. 2016. Dual mechanisms of action of the RNA-binding protein human antigen R explains its regulatory effect on melanoma cell migration. Transl Res. 172:45–60. doi:10.1016/j.trsl.2016.02.007.
   PubMed Web of Science ®Google Scholar
• Muralidharan R, Panneerselvam J, Chen A, Zhao YD, Munshi A, Ramesh R Hu R-targeted nanotherapy in combination with AMD3100 suppresses CXCR4 expression, cell growth, migration and invasion in lung cancer. Cancer Gene Ther 2015. doi:10.1038/cgt.2015.55.
   PubMed Web of Science ®Google Scholar
• Zhu VF, Yang J, LeBrun DG, Li M. Understanding the role of cytokines in Glioblastoma multiforme pathogenesis. Cancer Lett. 2012;316:139–150. doi:10.1016/j.canlet.2011.11.001.
   PubMed Web of Science ®Google Scholar
• Choi C, Kutsch O, Park J, Zhou T, Seol DW, Benveniste EN. Tumor necrosis factor-related apoptosis-inducing ligand induces caspase-dependent interleukin-8 expression and apoptosis in human astroglioma cells. Mol Cell Biol. 2002;22:724–736.
   PubMed Web of Science ®Google Scholar
• Zhang W, Vreeland AC, Noy N. 2016. RNA-binding protein HuR regulates nuclear import of protein. J Cell Sci. 129:4025–4033. doi:10.1242/jcs.192096.
   PubMed Web of Science ®Google Scholar
• Fang Y, Fullwood MJ. 2016. Roles, functions, and mechanisms of long non-coding RNAs in cancer. Genomics Proteomics Bioinformatics. 14:42–54. doi:10.1016/j.gpb.2015.09.006.
   PubMed Web of Science ®Google Scholar
• Qazi MA, Vora P, Venugopal C, Sidhu SS, Moffat J, Swanton C, Singh SK. 2017. Intratumoral heterogeneity: pathways to treatment resistance and relapse in human glioblastoma. Ann Oncol. 28:1448–1456. doi:10.1093/annonc/mdx169.
   PubMed Web of Science ®Google Scholar
• Lopez de Silanes I, Lal A, Gorospe M. HuR: post-transcriptional paths to malignancy. RNA Biol. 2005;2:11–13. doi:10.4161/rna.2.1.1552.
   PubMedGoogle Scholar
• Friedman GK, Langford CP, Coleman JM, Cassady KA, Parker JN, Markert JM, Yancey Gillespie G. 2009. Engineered herpes simplex viruses efficiently infect and kill CD133+ human glioma xenograft cells that express CD111. J Neurooncol. 95:199–209. doi:10.1007/s11060-009-9926-0.
   PubMed Web of Science ®Google Scholar
• Qin H, Niyongere SA, Lee SJ, Baker BJ, Benveniste EN. Expression and functional significance of SOCS-1 and SOCS-3 in astrocytes. J Immunol. 2008;181:3167–3176.
   PubMed Web of Science ®Google Scholar