Targeting drug resistance in glioblastoma (Review)
- Authors:
- Jonathan H. Sherman
- Adam Bobak
- Tasneem Arsiwala
- Paul Lockman
- Sonikpreet Aulakh
-
Affiliations: Department of Neurosurgery, Rockefeller Neuroscience Institute, West Virginia University, Martinsburg, WV 25401, USA, Department of Biology, Seton Hill University, Greensburg, PA 15601, USA, Department of Basic Pharmaceutical Sciences, School of Pharmacy, West Virginia University, Morgantown, WV 26506, USA, Section of Hematology/Oncology, Department of Internal Medicine, West Virginia University, Morgantown, WV 26506, USA - Published online on: July 9, 2024 https://doi.org/10.3892/ijo.2024.5668
- Article Number: 80
-
Copyright: © Sherman et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Omuro A and DeAngelis LM: Glioblastoma and other malignant gliomas: A clinical review. JAMA. 310:1842–1850. 2013. View Article : Google Scholar : PubMed/NCBI | |
Hale JS, Sinyuk M, Rich JN and Lathia JD: Decoding the cancer stem cell hypothesis in glioblastoma. CNS Oncol. 2:319–330. 2013. View Article : Google Scholar : | |
Thakkar JP, Dolecek TA, Horbinski C, Ostrom QT, Lightner DD, Barnholtz-Sloan JS and Villano JL: Epidemiologic and molecular prognostic review of glioblastoma. Cancer Epidemiol Biomark Amp Prev. 23:1985–1996. 2014. View Article : Google Scholar | |
Hanif F, Muzaffar K, Perveen K, Malhi SM and Simjee ShU: Glioblastoma Multiforme: A review of its epidemiology and pathogenesis through clinical presentation and treatment. Asian Pac J Cancer Prev. 18:3–9. 2017.PubMed/NCBI | |
Alexander BM and Cloughesy TF: Adult Glioblastoma. J Clin Oncol. 35:2402–2409. 2017. View Article : Google Scholar : PubMed/NCBI | |
De Vleeschouwer S: Glioblastoma. Codon Publications; Brisbane, QLD: 2017, View Article : Google Scholar | |
Young RM, Jamshidi A, Davis G and Sherman JH: Current trends in the surgical management and treatment of adult glioblastoma. Ann Transl Med. 3:1212015.PubMed/NCBI | |
Louis DN, Perry A, Wesseling P, Brat DJ, Cree IA, Figarella-Branger D, Hawkins C, Ng HK, Pfister SM, Reifenberger G, et al: The 2021 WHO classification of tumors of the central nervous system: A summary. Neuro Oncol. 23:1231–1251. 2021. View Article : Google Scholar : PubMed/NCBI | |
Ohgaki H and Kleihues P: Genetic pathways to primary and secondary glioblastoma. Am J Pathol. 170:1445–1453. 2007. View Article : Google Scholar : PubMed/NCBI | |
Ohgaki H and Kleihues P: The Definition of primary and secondary glioblastoma. Clin Cancer Res. 19:764–772. 2013. View Article : Google Scholar | |
Valentinis L, Tuniz F, Valent F, Mucchiut M, Little D, Skrap M, Bergonzi P and Zanchin G: Headache attributed to intracranial tumours: A prospective cohort study. Cephalalgia. 30:389–398. 2010. View Article : Google Scholar | |
Chaichana KL, Parker SL, Olivi A and Quiñones-Hinojosa A: Long-term seizure outcomes in adult patients undergoing primary resection of malignant brain astrocytomas: Clinical article. J Neurosurg. 111:282–292. 2009. View Article : Google Scholar : PubMed/NCBI | |
Davis ME: Glioblastoma: Overview of disease and treatment. Clin J Oncol Nurs. 20(5 Suppl): S2–S8. 2016. View Article : Google Scholar : PubMed/NCBI | |
Wen PY, Weller M, Lee EQ, Alexander BM, Barnholtz-Sloan JS, Barthel FP, Batchelor TT, Bindra RS, Chang SM, Chiocca EA, et al: Glioblastoma in adults: A Society for Neuro-Oncology (SNO) and European Society of Neuro-Oncology (EANO) consensus review on current management and future directions. Neuro-Oncol. 22:1073–1113. 2020. View Article : Google Scholar : PubMed/NCBI | |
Wen PY, Macdonald DR, Reardon DA, Cloughesy TF, Sorensen AG, Galanis E, Degroot J, Wick W, Gilbert MR, Lassman AB, et al: Updated response assessment criteria for high-grade gliomas: Response assessment in neuro-oncology working group. J Clin Oncol. 28:1963–1972. 2010. View Article : Google Scholar : PubMed/NCBI | |
Hu LS, Eschbacher JM, Dueck AC, Heiserman JE, Liu S, Karis JP, Smith KA, Shapiro WR, Pinnaduwage DS, Coons SW, et al: Correlations between perfusion MR imaging cerebral blood volume, microvessel quantification, and clinical outcome using stereotactic analysis in recurrent high-grade glioma. Am J Neuroradiol. 33:692012. View Article : Google Scholar | |
Zhang J, Stevens MF and Bradshaw TD: Temozolomide: Mechanisms of action, repair and resistance. Curr Mol Pharmacol. 5:102–114. 2012. View Article : Google Scholar | |
Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, Ludwin SK, Allgeier A, Fisher B, Belanger K, et al: Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 10:459–466. 2009. View Article : Google Scholar : PubMed/NCBI | |
Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, et al: Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 352:987–996. 2005. View Article : Google Scholar : PubMed/NCBI | |
Stupp R, Taillibert S, Kanner A, Read W, Steinberg D, Lhermitte B, Toms S, Idbaih A, Ahluwalia MS, Fink K, et al: Effect of tumor-treating fields plus maintenance temozolomide vs maintenance temozolomide alone on survival in patients with glioblastoma: A randomized clinical trial. JAMA. 318:2306–2316. 2017. View Article : Google Scholar : PubMed/NCBI | |
Perry JR, Rizek P, Cashman R, Morrison M and Morrison T: Temozolomide rechallenge in recurrent malignant glioma by using a continuous temozolomide schedule. Cancer. 113:2152–2157. 2008. View Article : Google Scholar : PubMed/NCBI | |
Brandes AA, Tosoni A, Amistà P, Nicolardi L, Grosso D, Berti F and Ermani M: How effective is BCNU in recurrent glioblastoma in the modern era? Neurology. 63:12812004. View Article : Google Scholar : PubMed/NCBI | |
Reithmeier T, Graf E, Piroth T, Trippel M, Pinsker MO and Nikkhah G: BCNU for recurrent glioblastoma multiforme: Efficacy, toxicity and prognostic factors. BMC Cancer. 10:302010. View Article : Google Scholar : PubMed/NCBI | |
Wick W, Puduvalli VK, Chamberlain MC, van den Bent MJ, Carpentier AF, Cher LM, Mason W, Weller M, Hong S, Musib L, et al: Phase III study of enzastaurin compared with lomustine in the treatment of recurrent intracranial glioblastoma. J Clin Oncol. 28:1168–1174. 2010. View Article : Google Scholar : PubMed/NCBI | |
Taal W, Oosterkamp HM, Walenkamp AM, Dubbink HJ, Beerepoot LV, Hanse MC, Buter J, Honkoop AH, Boerman D, de Vos FY, et al: Single-agent bevacizumab or lomustine versus a combination of bevacizumab plus lomustine in patients with recurrent glioblastoma (BELOB trial): A randomised controlled phase 2 trial. Lancet Oncol. 15:943–953. 2014. View Article : Google Scholar : PubMed/NCBI | |
Glas M, Happold C, Rieger J, Wiewrodt D, Bähr O, Steinbach JP, Wick W, Kortmann RD, Reifenberger G, Weller M and Herrlinger U: Long-term survival of patients with glioblastoma treated with radiotherapy and lomustine plus temozolomide. J Clin Oncol. 27:1257–1261. 2009. View Article : Google Scholar : PubMed/NCBI | |
Herrlinger U, Rieger J, Koch D, Loeser S, Blaschke B, Kortmann RD, Steinbach JP, Hundsberger T, Wick W, Meyermann R, et al: Phase II trial of lomustine plus temozolomide chemotherapy in addition to radiotherapy in newly diagnosed glioblastoma: UKT-03. J Clin Oncol. 24:4412–4417. 2006. View Article : Google Scholar : PubMed/NCBI | |
Brem H, Piantadosi S, Burger PC, Walker M, Selker R, Vick NA, Black K, Sisti M, Brem S, Mohr G, et al: Placebo-controlled trial of safety and efficacy of intraoperative controlled delivery by biodegradable polymers of chemotherapy for recurrent gliomas. Lancet. 345:1008–1012. 1995. View Article : Google Scholar : PubMed/NCBI | |
McGirt MJ and Brem H: Carmustine wafers (Gliadel) plus concomitant temozolomide therapy after resection of malignant astrocytoma: Growing evidence for safety and efficacy. Ann Surg Oncol. 17:1729–1731. 2010. View Article : Google Scholar : PubMed/NCBI | |
Lombardi G, De Salvo GL, Brandes AA, Eoli M, Rudà R, Faedi M, Lolli I, Pace A, Daniele B, Pasqualetti F, et al: Regorafenib compared with lomustine in patients with relapsed glioblastoma (REGOMA): A multicentre, open-label, randomised, controlled, phase 2 trial. Lancet Oncol. 20:110–119. 2019. View Article : Google Scholar | |
Friedman HS, Prados MD, Wen PY, Mikkelsen T, Schiff D, Abrey LE, Yung WKA, Paleologos N, Nicholas MK, Jensen R, et al: Bevacizumab alone and in combination with irinotecan in recurrent glioblastoma. J Clin Oncol. 27:4733–4740. 2009. View Article : Google Scholar : PubMed/NCBI | |
Wick W, Gorlia T, Bendszus M, Taphoorn M, Sahm F, Harting I, Brandes AA, Taal W, Domont J, Idbaih A, et al: Lomustine and bevacizumab in progressive glioblastoma. N Engl J Med. 377:1954–1963. 2017. View Article : Google Scholar : PubMed/NCBI | |
Ameratunga M, Pavlakis N, Wheeler H, Grant R, Simes J and Khasraw M: Anti-angiogenic therapy for high-grade glioma. Cochrane Database Syst Rev. 11:CD0082182018.PubMed/NCBI | |
Kaley T, Nolan C, Carver A and Omuro A: Bevacizumab for acute neurologic deterioration in patients with glioblastoma. CNS Oncol. 2:413–418. 2013. View Article : Google Scholar | |
Wick W, Weller M, van den Bent M and Stupp R: Bevacizumab and recurrent malignant gliomas: A european perspective. J Clin Oncol. 28:e188–e189. 2010. View Article : Google Scholar : PubMed/NCBI | |
Kazmi F, Soon YY, Leong YH, Koh WY and Vellayappan B: Re-irradiation for recurrent glioblastoma (GBM): A systematic review and meta-analysis. J Neurooncol. 142:79–90. 2019. View Article : Google Scholar | |
Stupp R, Wong ET, Kanner AA, Steinberg D, Engelhard H, Heidecke V, Kirson ED, Taillibert S, Liebermann F, Dbalý V, et al: NovoTTF-100A versus physician's choice chemotherapy in recurrent glioblastoma: A randomised phase III trial of a novel treatment modality. Eur J Cancer. 48:2192–2202. 2012. View Article : Google Scholar : PubMed/NCBI | |
Lee SX, Tunkyi A, Wong E and Swanson KD: Mitosis interference of cancer cells during anaphase by electric field from NovoTTF-100A: An update. J Clin Oncol. 30(15_Suppl): e21078. 2012. View Article : Google Scholar | |
Lee E, Yong RL, Paddison P and Zhu J: Comparison of glioblastoma (GBM) molecular classification methods. Semin Cancer Biol. 53:201–211. 2018. View Article : Google Scholar : PubMed/NCBI | |
Snuderl M, Fazlollahi L, Le LP, Nitta M, Zhelyazkova BH, Davidson CJ, Akhavanfard S, Cahill DP, Aldape KD, Betensky RA, et al: Mosaic amplification of multiple receptor tyrosine kinase genes in glioblastoma. Cancer Cell. 20:810–817. 2011. View Article : Google Scholar : PubMed/NCBI | |
Sottoriva A, Spiteri I, Piccirillo SG, Touloumis A, Collins VP, Marioni JC, Curtis C, Watts C and Tavaré S: Intratumor heterogeneity in human glioblastoma reflects cancer evolutionary dynamics. Proc Natl Acad Sci. 110:4009–4014. 2013. View Article : Google Scholar : PubMed/NCBI | |
Aldape K, Zadeh G, Mansouri S, Reifenberger G and von Deimling A: Glioblastoma: Pathology, molecular mechanisms and markers. Acta Neuropathol (Berl). 129:829–848. 2015. View Article : Google Scholar : PubMed/NCBI | |
An Z, Aksoy O, Zheng T, Fan QW and Weiss WA: Epidermal growth factor receptor and EGFRvIII in glioblastoma: Signaling pathways and targeted therapies. Oncogene. 37:1561–1575. 2018. View Article : Google Scholar : PubMed/NCBI | |
Arteaga CL and Engelman JA: ERBB receptors: From oncogene discovery to basic science to mechanism-based cancer therapeutics. Cancer Cell. 25:282–303. 2014. View Article : Google Scholar : PubMed/NCBI | |
Narita Y, Nagane M, Mishima K, Huang HJS, Furnari FB and Cavenee WK: Mutant Epidermal growth factor receptor signaling Down-Regulates p27 through activation of the phosphatidylinositol 3-Kinase/Akt pathway in glioblastomas. Cancer Res. 62:6764–6769. 2002.PubMed/NCBI | |
Huang HJS, Nagane M, Klingbeil CK, Lin H, Nishikawa R, Ji XD, Huang CM, Gill GN, Wiley HS and Cavenee WK: The enhanced tumorigenic activity of a mutant epidermal growth factor receptor common in human cancers is mediated by threshold levels of constitutive tyrosine phosphorylation and unattenuated signaling. J Biol Chem. 272:2927–2935. 1997. View Article : Google Scholar : PubMed/NCBI | |
Nagane M, Levitzki A, Gazit A, Cavenee WK and Huang HJS: Drug resistance of human glioblastoma cells conferred by a tumor-specific mutant epidermal growth factor receptor through modulation of Bcl-XL and caspase-3-like proteases. Proc Natl Acad Sci. 95:5724–5729. 1998. View Article : Google Scholar : PubMed/NCBI | |
Inda M del M, Bonavia R, Mukasa A, Narita Y, Sah DW, Vandenberg S, Brennan C, Johns TG, Bachoo R, Hadwiger P, et al: Tumor heterogeneity is an active process maintained by a mutant EGFR-induced cytokine circuit in glioblastoma. Genes Dev. 24:1731–1745. 2010. View Article : Google Scholar | |
Giacinti C and Giordano A: RB and cell cycle progression. Oncogene. 25:5220–5227. 2006. View Article : Google Scholar : PubMed/NCBI | |
Nakamura M, Yonekawa Y, Kleihues P and Ohgaki H: Promoter Hypermethylation of the RB1 gene in Glioblastomas. Lab Invest. 81:77–82. 2001. View Article : Google Scholar : PubMed/NCBI | |
Cerami E, Demir E, Schultz N, Taylor BS and Sander C: Automated network analysis identifies core pathways in glioblastoma. PLoS One. 5:e89182010. View Article : Google Scholar : PubMed/NCBI | |
Muñoz-Hidalgo L, San-Miguel T, Megías J, Monleón D, Navarro L, Roldán P, Cerdá-Nicolás M and López-Ginés C: Somatic copy number alterations are associated with EGFR amplification and shortened survival in patients with primary glioblastoma. Neoplasia. 22:10–21. 2020. View Article : Google Scholar | |
Aubrey BJ, Strasser A and Kelly GL: Tumor-suppressor functions of the TP53 pathway. Cold Spring Harb Perspect Med. 6:a0260622016. View Article : Google Scholar : PubMed/NCBI | |
Verhaak RGW, Hoadley KA, Purdom E, Wang V, Qi Y, Wilkerson MD, Miller CR, Ding L, Golub T, Mesirov JP, et al: Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell. 17:98–110. 2010. View Article : Google Scholar : PubMed/NCBI | |
Zhang Y, Dube C, Gibert M Jr, Cruickshanks N, Wang B, Coughlan M, Yang Y, Setiady I, Deveau C, Saoud K, et al: The p53 pathway in glioblastoma. Cancers (Basel). 10:2972018. View Article : Google Scholar : PubMed/NCBI | |
Ham SW, Jeon HY, Jin X, Kim EJ, Kim JK, Shin YJ, Lee Y, Kim SH, Lee SY, Seo S, et al: TP53 gain-of-function mutation promotes inflammation in glioblastoma. Cell Death Differ. 26:409–425. 2019. View Article : Google Scholar : | |
Forte IM, Indovina P, Iannuzzi CA, Cirillo D, Di Marzo D, Barone D, Capone F, Pentimalli F and Giordano A: Targeted therapy based on p53 reactivation reduces both glioblastoma cell growth and resistance to temozolomide. Int J Oncol. 54:2189–2199. 2019.PubMed/NCBI | |
Verreault M, Schmitt C, Goldwirt L, Pelton K, Haidar S, Levasseur C, Guehennec J, Knoff D, Labussière M, Marie Y, et al: Preclinical efficacy of the MDM2 inhibitor RG7112 in MDM2-smplified and TP53 Wild-type glioblastomas. Clin Cancer Res. 22:1185–1196. 2016. View Article : Google Scholar | |
Mizoguchi M, Nutt CL, Mohapatra G and Louis DN: Genetic alterations of phosphoinositide 3-kinase subunit genes in human glioblastomas. Brain Pathol. 14:372–377. 2004. View Article : Google Scholar : PubMed/NCBI | |
Papa A and Pandolfi PP: The PTEN-PI3K axis in cancer. Biomolecules. 9:1532019. View Article : Google Scholar | |
Lino MM and Merlo A: PI3Kinase signaling in glioblastoma. J Neurooncol. 103:417–427. 2011. View Article : Google Scholar : | |
Koul D: PTEN signaling pathways in glioblastoma. Cancer Biol Ther. 7:1321–1325. 2008. View Article : Google Scholar : PubMed/NCBI | |
Parsons DW, Jones S, Zhang X, Lin JC, Leary RJ, Angenendt P, Mankoo P, Carter H, Siu IM, Gallia GL, et al: An integrated genomic analysis of human glioblastoma multiforme. Science. 26:3212008. | |
Rao SK, Edwards J, Joshi AD, Siu IM and Riggins GJ: A survey of glioblastoma genomic amplifications and deletions. J Neurooncol. 96:169–179. 2010. View Article : Google Scholar | |
von Achenbach C, Weller M, Kaulich K, Gramatzki D, Zacher A, Fabbro D, Reifenberger G and Szabó E: Synergistic growth inhibition mediated by dual PI3K/mTOR pathway targeting and genetic or direct pharmacological AKT inhibition in human glioblastoma models. J Neurochem. 153:510–524. 2020. View Article : Google Scholar | |
Lin F, de Gooijer MC, Hanekamp D, Chandrasekaran G, Buil LC, Thota N, Sparidans RW, Beijnen JH, Würdinger T and van Tellingen O: PI3K-mTOR Pathway Inhibition exhibits efficacy against high-grade glioma in clinically relevant mouse models. Clin Cancer Res. 23:12862017. View Article : Google Scholar | |
Wen PY, Lee EQ, Reardon DA, Ligon KL and Alfred Yung WK: Current clinical development of PI3K pathway inhibitors in glioblastoma. Neuro Oncol. 14:819–829. 2012. View Article : Google Scholar : PubMed/NCBI | |
Cohen MH, Johnson JR and Pazdur R: Food and drug administration drug approval summary: Temozolomide plus radiation therapy for the treatment of newly diagnosed glioblastoma multiforme. Clin Cancer Res. 11:67672005. View Article : Google Scholar : PubMed/NCBI | |
Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, Kros JM, Hainfellner JA, Mason W, Mariani L, et al: MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med. 352:997–1003. 2005. View Article : Google Scholar : PubMed/NCBI | |
Kitange GJ, Carlson BL, Schroeder MA, Grogan PT, Lamont JD, Decker PA, Wu W, James CD and Sarkaria JN: Induction of MGMT expression is associated with temozolomide resistance in glioblastoma xenografts. Neuro Oncol. 11:281–291. 2009. View Article : Google Scholar : | |
Alnahhas I, Alsawas M, Rayi A, Palmer JD, Raval R, Ong S, Giglio P, Murad MH and Puduvalli V: Characterizing benefit from temozolomide in MGMT promoter unmethylated and methylated glioblastoma: A systematic review and meta-analysis. Neuro Oncol Adv. 2:vdaa0822020. View Article : Google Scholar | |
Luo W, Yan D, Song Z, Zhu X, Liu X, Li X and Zhao S: miR-126-3p sensitizes glioblastoma cells to temozolomide by inactivating Wnt/β-catenin signaling via targeting SOX2. Life Sci. 226:98–106. 2019. View Article : Google Scholar : PubMed/NCBI | |
Garg M: Epithelial-mesenchymal transition-activating transcription factors-multifunctional regulators in cancer. World J Stem Cells. 5:188–195. 2013. View Article : Google Scholar : PubMed/NCBI | |
Diaz RJ, Ali S, Qadir MG, De La Fuente MI, Ivan ME and Komotar RJ: The role of bevacizumab in the treatment of glioblastoma. J Neurooncol. 133:455–467. 2017. View Article : Google Scholar : PubMed/NCBI | |
Gilbert MR, Dignam JJ, Armstrong TS, Wefel JS, Blumenthal DT, Vogelbaum MA, Colman H, Chakravarti A, Pugh S, Won M, et al: A randomized trial of bevacizumab for newly diagnosed glioblastoma. N Engl J Med. 370:699–708. 2014. View Article : Google Scholar : PubMed/NCBI | |
Kreisl TN, Kim L, Moore K, Duic P, Royce C, Stroud I, Garren N, Mackey M, Butman JA, Camphausen K, et al: Phase II Trial of Single-Agent Bevacizumab Followed by Bevacizumab Plus Irinotecan at Tumor Progression in Recurrent Glioblastoma. J Clin Oncol. 5:740–745. 2009. View Article : Google Scholar | |
Bergers G and Hanahan D: Modes of resistance to anti-angiogenic therapy. Nat Rev Cancer. 8:592–603. 2008. View Article : Google Scholar : PubMed/NCBI | |
Haibe Y, Kreidieh M, El Hajj H, Khalifeh I, Mukherji D, Temraz S and Shamseddine A: Resistance mechanisms to Anti-angiogenic therapies in cancer. Front Oncol. 10:2212020. View Article : Google Scholar : PubMed/NCBI | |
Forsythe JA, Jiang BH, Iyer NV, Agani F, Leung SW, Koos RD and Semenza GL: Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol. 16:4604–4613. 1996. View Article : Google Scholar : PubMed/NCBI | |
Trusolino L, Bertotti A and Comoglio PM: MET signalling: Principles and functions in development, organ regeneration and cancer. Nat Rev Mol Cell Biol. 11:834–848. 2010. View Article : Google Scholar : PubMed/NCBI | |
Birchmeier C, Birchmeier W, Gherardi E and Vande Woude GF: Met, metastasis, motility and more. Nat Rev Mol Cell Biol. 4:915–925. 2003. View Article : Google Scholar : PubMed/NCBI | |
Lu KV, Chang JP, Parachoniak CA, Pandika MM, Aghi MK, Meyronet D, Isachenko N, Fouse SD, Phillips JJ, Cheresh DA, et al: VEGF inhibits tumor cell invasion and mesenchymal transition through a MET/VEGFR2 complex. Cancer Cell. 22:21–35. 2012. View Article : Google Scholar : PubMed/NCBI | |
Hande KR: Etoposide: Four decades of development of a topoisomerase II inhibitor. Eur J Cancer. 34:1514–1521. 1998. View Article : Google Scholar | |
Montecucco A, Zanetta F and Biamonti G: Molecular mechanisms of etoposide. EXCLI J. 14:95–108. 2015.PubMed/NCBI | |
Biasoli D, Kahn SA, Cornélio TA, Furtado M, Campanati L, Chneiweiss H, Moura-Neto V and Borges HL: Retinoblastoma protein regulates the crosstalk between autophagy and apoptosis, and favors glioblastoma resistance to etoposide. Cell Death Dis. 4:e767. 2013. View Article : Google Scholar : PubMed/NCBI | |
McLendon R, Friedman A, Bigner D, Van Meir EG, Brat DJ, Marie Mastrogianakis G, Olson JJ, Mikkelsen T, Lehman N, Aldape A, et al: Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature. 455:1061–1068. 2008. View Article : Google Scholar | |
Senturk JC, Bohlman S and Manfredi JJ: Mdm2 selectively suppresses DNA damage arising from inhibition of topoisomerase II independent of p53. Oncogene. 36:6085–6096. 2017. View Article : Google Scholar : PubMed/NCBI | |
Conradt L, Henrich A, Wirth M, Reichert M, Lesina M, Algül H, Schmid RM, Krämer OH, Saur D and Schneider G: Mdm2 inhibitors synergize with topoisomerase II inhibitors to induce p53-independent pancreatic cancer cell death. Int J Cancer. 132:2248–2257. 2013. View Article : Google Scholar | |
Kondo S, Kondo Y, Hara H, Kaakaji R, Peterson JW, Morimura T, Takeuchi J and Barnett GH: mdm2 gene mediates the expression of mdr1 gene and P-glycoprotein in a human glioblastoma cell line. Br J Cancer. 74:1263–1268. 1996. View Article : Google Scholar : PubMed/NCBI | |
Galluzzi L, Senovilla L, Vitale I, Michels J, Martins I, Kepp O, Castedo M and Kroemer G: Molecular mechanisms of cisplatin resistance. Oncogene. 31:1869–1883. 2012. View Article : Google Scholar | |
Pénzváltó Z, Lánczky A, Lénárt J, Meggyesházi N, Krenács T, Szoboszlai N, Denkert C, Pete I and Győrffy B: MEK1 is associated with carboplatin resistance and is a prognostic biomarker in epithelial ovarian cancer. BMC Cancer. 14:8372014. View Article : Google Scholar : PubMed/NCBI | |
Ahmad A, Robinson AR, Duensing A, van Drunen E, Beverloo HB, Weisberg DB, Hasty P, Hoeijmakers JH and Niedernhofer LJ: ERCC1-XPF endonuclease facilitates DNA double-strand break repair. Mol Cell Biol. 28:5082–5092. 2008. View Article : Google Scholar : PubMed/NCBI | |
Walker MD, Alexander E Jr, Hunt WE, MacCarty CS, Mahaley MS Jr, Mealey J Jr, Norrell HA, Owens G, Ransohoff J, Wilson CB, et al: Evaluation of BCNU and/or radiotherapy in the treatment of anaplastic gliomas: A cooperative clinical trial. J Neurosurg. 49:333–343. 1978. View Article : Google Scholar : PubMed/NCBI | |
Walker MD, Strike TA and Sheline GE: An analysis of dose-effect relationship in the radiotherapy of malignant gliomas. Int J Radiat Oncol. 5:1725–1731. 1979. View Article : Google Scholar | |
van Rijn J, Heimans JJ, van den Berg J, van der Valk P and Slotman BJ: Survival of human glioma cells treated with various combination of temozolomide and X-rays. Int J Radiat Oncol. 47:779–784. 2000. View Article : Google Scholar | |
Blumenthal DT, Gorlia T, Gilbert MR, Kim MM, Burt Nabors L, Mason WP, Hegi ME, Zhang P, Golfinopoulos V, Perry JR, et al: Is More better? The impact of extended adjuvant temozolomide in newly diagnosed glioblastoma: A secondary analysis of EORTC and NRG Oncology/RTOG. Neuro Oncol. 19:1119–1126. 2017. View Article : Google Scholar : PubMed/NCBI | |
van Linde ME, Brahm CG, de Witt Hamer PC, Reijneveld JC, Bruynzeel AME, Vandertop WP, van de Ven PM, Wagemakers M, van der Weide HL, Enting RH, et al: Treatment outcome of patients with recurrent glioblastoma multiforme: A retrospective multicenter analysis. J Neurooncol. 135:183–192. 2017. View Article : Google Scholar : PubMed/NCBI | |
Monteiro AR, Hill R, Pilkington GJ and Madureira PA: The role of hypoxia in glioblastoma invasion. Cells. 6:452017. View Article : Google Scholar : PubMed/NCBI | |
Gray LH, Conger AD, Ebert M, Hornsey S and Scott OCA: The concentration of oxygen dissolved in tissues at the time of irradiation as a factor in radiotherapy. Br J Radiol. 26:638–648. 1953. View Article : Google Scholar : PubMed/NCBI | |
Horsman MR, Mortensen LS, Petersen JB, Busk M and Overgaard J: Imaging hypoxia to improve radiotherapy outcome. Nat Rev Clin Oncol. 9:674–687. 2012. View Article : Google Scholar : PubMed/NCBI | |
Ikeda E, Achen MG, Breier G and Risau W: Hypoxia-induced transcriptional activation and increased mRNA stability of vascular endothelial growth factor in C6 glioma cells. J Biol Chem. 270:19761–19766. 1995. View Article : Google Scholar : PubMed/NCBI | |
Chinot OL, Wick W, Mason W, Henriksson R, Saran F, Nishikawa R, Carpentier AF, Hoang-Xuan K, Kavan P, Cernea D, et al: Bevacizumab plus Radiotherapy-Temozolomide for newly diagnosed glioblastoma. N Engl J Med. 370:709–722. 2014. View Article : Google Scholar : PubMed/NCBI | |
Colman H, Zhang L, Sulman EP, McDonald JM, Shooshtari NL, Rivera A, Popoff S, Nutt CL, Louis DN, Cairncross JG, et al: A multigene predictor of outcome in glioblastoma. Neuro Oncol. 12:49–57. 2010. View Article : Google Scholar : PubMed/NCBI | |
Li Z, Bao S, Wu Q, Wang H, Eyler C, Sathornsumetee S, Shi Q, Cao Y, Lathia J, McLendon RE, et al: Hypoxia-Inducible factors regulate tumorigenic capacity of glioma stem cells. Cancer Cell. 15:501–513. 2009. View Article : Google Scholar : PubMed/NCBI | |
Visvader JE and Lindeman GJ: Cancer stem cells in solid tumours: Accumulating evidence and unresolved questions. Nat Rev Cancer. 8:755–768. 2008. View Article : Google Scholar : PubMed/NCBI | |
Prieto-Vila M, Takahashi RU, Usuba W, Kohama I and Ochiya T: Drug resistance driven by cancer stem cells and their niche. Int J Mol Sci. 18:25742017. View Article : Google Scholar : PubMed/NCBI | |
Batlle E and Clevers H: Cancer stem cells revisited. Nat Med. 23:1124–1134. 2017. View Article : Google Scholar : PubMed/NCBI | |
Roninson IB, Broude EV and Chang BD: If not apoptosis, then what? Treatment-induced senescence and mitotic catastrophe in tumor cells. Drug Resist Updat. 4:303–313. 2001. View Article : Google Scholar | |
Chen J, Li Y, Yu TS, McKay RM, Burns DK, Kernie SG and Parada LF: A restricted cell population propagates glioblastoma growth after chemotherapy. Nature. 488:522–526. 2012. View Article : Google Scholar : PubMed/NCBI | |
Peh GSL, Lang RJ, Pera MF and Hawes SM: CD133 expression by neural progenitors derived from human embryonic stem cells and its use for their prospective isolation. Stem Cells Dev. 18:269–282. 2009. View Article : Google Scholar | |
Kim YS, Kaidina AM, Chiang JH, Yarygin KN and Lupatov AY: Cancer stem cell molecular markers verified in vivo. Biochem Mosc Suppl Ser B Biomed Chem. 11:43–54. 2017. View Article : Google Scholar | |
Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD and Rich JN: Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 444:756–760. 2006. View Article : Google Scholar : PubMed/NCBI | |
Kim H, Zheng S, Amini SS, Virk SM, Mikkelsen T, Brat DJ, Grimsby J, Sougnez C, Muller F, Hu J, et al: Whole-genome and multisector exome sequencing of primary and post-treatment glioblastoma reveals patterns of tumor evolution. Genome Res. 25:316–327. 2015. View Article : Google Scholar : PubMed/NCBI | |
Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J and Dirks PB: Identification of a cancer stem cell in human brain tumors. Cancer Res. 63:58212003.PubMed/NCBI | |
Brennan CW, Verhaak RGW, McKenna A, Campos B, Noushmehr H, Salama SR, Zheng S, Chakravarty D, Sanborn JZ, Berman SH, et al: The somatic genomic landscape of glioblastoma. Cell. 155:462–477. 2013. View Article : Google Scholar : PubMed/NCBI | |
Wong AJ, Ruppert JM, Bigner SH, Grzeschik CH, Humphrey PA, Bigner DS and Vogelstein B: Structural alterations of the epidermal growth factor receptor gene in human gliomas. Proc Natl Acad Sci. 89:29651992. View Article : Google Scholar : PubMed/NCBI | |
Lammering G, Hewit TH, Valerie K, Contessa JN, Amorino GP, Dent P and Schmidt-Ullrich RK: EGFRvIII-mediated radioresistance through a strong cytoprotective response. Oncogene. 22:5545–5553. 2003. View Article : Google Scholar : PubMed/NCBI | |
Mukherjee B, McEllin B, Camacho CV, Tomimatsu N, Sirasanagandala S, Nannepaga S, Hatanpaa KJ, Mickey B, Madden C, Maher E, et al: EGFRvIII and DNA double-strand break repair: A molecular mechanism for radioresistance in glioblastoma. Cancer Res. 69:42522009. View Article : Google Scholar : PubMed/NCBI | |
Chakravarti A, Wang M, Robins HI, Lautenschlaeger T, Curran WJ, Brachman DG, Schultz CJ, Choucair A, Dolled-Filhart M, Christiansen J, et al: RTOG 0211: A Phase 1/2 study of radiation therapy with concurrent gefitinib for newly diagnosed glioblastoma patients. Int J Radiat Oncol. 85:1206–1211. 2013. View Article : Google Scholar | |
Kao GD, Jiang Z, Fernandes AM, Gupta AK and Maity A: Inhibition of phosphatidylinositol-3-OH Kinase/Akt signaling impairs DNA repair in glioblastoma cells following ionizing radiation. J Biol Chem. 282:21206–21212. 2007. View Article : Google Scholar : PubMed/NCBI | |
Charles NA, Holland EC, Gilbertson R, Glass R and Kettenmann H: The brain tumor microenvironment. Glia. 60:502–514. 2012. View Article : Google Scholar : PubMed/NCBI | |
Wahl DR, Kim MM, Aryal MP, Hartman H, Lawrence TS, Schipper MJ, Parmar HA and Cao Y: Combining perfusion and High B-value diffusion MRI to inform prognosis and predict failure patterns in glioblastoma. Int J Radiat Oncol Biol Phys. 102:757–764. 2018. View Article : Google Scholar : PubMed/NCBI | |
Gérard M, Corroyer-Dulmont A, Lesueur P, Collet S, Chérel M, Bourgeois M, Stefan D, Limkin EJ, Perrio C, Guillamo JS, et al: Hypoxia imaging and adaptive radiotherapy: A State-of-the-Art approach in the management of glioma. Front Med. 6:1172019. View Article : Google Scholar | |
Drake LR, Hillmer AT and Cai Z: Approaches to PET imaging of glioblastoma. Molecules. 25:5682020. View Article : Google Scholar : PubMed/NCBI | |
Wallner KE, Galicich JH, Krol G, Arbit E and Malkin MG: Patterns of failure following treatment for glioblastoma multiforme and anaplastic astrocytoma. Int J Radiat Oncol. 16:1405–1409. 1989. View Article : Google Scholar | |
Niranjan A, Monaco EAI, Kano H, Flickinger JC and Lunsford LD: Stereotactic radiosurgery in the multimodality management of residual or recurrent glioblastoma multiforme. Prog Neurol Surg. 31:48–61. 2018. View Article : Google Scholar : PubMed/NCBI | |
Shaw E, Scott C, Souhami L, Dinapoli R, Kline R, Loeffler J and Farnan N: Single dose radiosurgical treatment of recurrent previously irradiated primary brain tumors and brain metastases: Final report of RTOG protocol 90-05. Int J Radiat Oncol. 47:291–298. 2000. View Article : Google Scholar | |
Kim Y, Varn FS, Park SH, Yoon BW, Park HR, Lee C, Verhaak RGW and Paek SH: Perspective of mesenchymal transformation in glioblastoma. Acta Neuropathol Commun. 9:502021. View Article : Google Scholar : PubMed/NCBI | |
Wang Z, Hu P, Tang F, Lian H, Chen X, Zhang Y, He X, Liu W and Xie C: HDAC6 promotes cell proliferation and confers resistance to temozolomide in glioblastoma. Cancer Lett. 379:134–142. 2016. View Article : Google Scholar : PubMed/NCBI | |
Yang WB, Hsu CC, Hsu TI, Liou JP, Chang KY, Chen PY, Liu JJ, Yang ST, Wang JY, Yeh SH, et al: Increased activation of HDAC1/2/6 and Sp1 underlies therapeutic resistance and tumor growth in glioblastoma. Neuro Oncol. 22:1439–1451. 2020. View Article : Google Scholar : PubMed/NCBI | |
Liu S, Wang Z, Wang Y, Fan X, Zhang C, Ma W, Qiu X and Jiang T: PD-1 related transcriptome profile and clinical outcome in diffuse gliomas. OncoImmunology. 7:e13827922018. View Article : Google Scholar : PubMed/NCBI | |
Wang Z, Zhang C, Liu X, Wang Z, Sun L, Li G, Liang J, Hu H, Liu Y, Zhang W and Jiang T: Molecular and clinical characterization of PD-L1 expression at transcriptional level via 976 samples of brain glioma. OncoImmunology. 5:e11963102016. View Article : Google Scholar : PubMed/NCBI | |
Li G, Wang Z, Zhang C, Liu X, Cai J, Wang Z, Hu H, Wu F, Bao Z, Liu Y, et al: Molecular and clinical characterization of TIM-3 in glioma through 1,024 samples. OncoImmunology. 6:e13283392017. View Article : Google Scholar : PubMed/NCBI | |
McGranahan T, Therkelsen KE, Ahmad S and Nagpal S: Current state of immunotherapy for treatment of glioblastoma. Curr Treat Options Oncol. 20:242019. View Article : Google Scholar : PubMed/NCBI | |
Tong L, Li J, Li Q, Wang X, Medikonda R, Zhao T, Li T, Ma H, Yi L, Liu P, et al: ACT001 reduces the expression of PD-L1 by inhibiting the phosphorylation of STAT3 in glioblastoma. Theranostics. 10:5943–5956. 2020. View Article : Google Scholar : PubMed/NCBI | |
Scholz A, Harter PN, Cremer S, Yalcin BH, Gurnik S, Yamaji M, Di Tacchio M, Sommer K, Baumgarten P, Bähr O, et al: Endothelial cell-derived angiopoietin-2 is a therapeutic target in treatment-naive and bevacizumab-resistant glioblastoma. EMBO Mol Med. 8:39–57. 2016. View Article : Google Scholar | |
Piao Y, Liang J, Holmes L, Henry V, Sulman E and Groot JF: Acquired resistance to Anti-VEGF therapy in glioblastoma is associated with a mesenchymal transition. Clin Cancer Res. 19:4392–4403. 2013. View Article : Google Scholar : PubMed/NCBI | |
Carbonell WS, DeLay M, Jahangiri A, Park CC and Aghi MK: β1 Integrin targeting potentiates antiangiogenic therapy and inhibits the growth of bevacizumab-resistant glioblastoma. Cancer Res. 73:3145–3154. 2013. View Article : Google Scholar : PubMed/NCBI | |
Zanca C, Villa GR, Benitez JA, Thorne AH, Koga T, D'Antonio M, Ikegami S, Ma J, Boyer AD, Banisadr A, et al: Glioblastoma cellular cross-talk converges on NF-κB to attenuate EGFR inhibitor sensitivity. Genes Dev. 31:1212–1227. 2017. View Article : Google Scholar : PubMed/NCBI | |
Liu X, Chen X, Shi L, Shan Q, Cao Q, Yue C, Li H, Li S, Wang J, Gao S, et al: The third-generation EGFR inhibitor AZD9291 overcomes primary resistance by continuously blocking ERK signaling in glioblastoma. J Exp Clin Cancer Res. 38:2192019. View Article : Google Scholar : PubMed/NCBI | |
Sigova AA, Mullen AC, Molinie B, Gupta S, Orlando DA, Guenther MG, Almada AE, Lin C, Sharp PA, Giallourakis CC and Young RA: Divergent transcription of long noncoding RNA/mRNA gene pairs in embryonic stem cells. Proc Natl Acad Sci. 110:2876–2881. 2013. View Article : Google Scholar : PubMed/NCBI | |
Lu C, Wei Y, Wang X, Zhang Z, Yin J, Li W, Chen L, Lyu X, Shi Z, Yan W and You Y: DNA-methylation-mediated activating of lncRNA SNHG12 promotes temozolomide resistance in glioblastoma. Mol Cancer. 19:282020. View Article : Google Scholar : PubMed/NCBI | |
Mazor G, Levin L, Picard D, Ahmadov U, Carén H, Borkhardt A, Reifenberger G, Leprivier G, Remke M and Rotblat B: The lncRNA TP73-AS1 is linked to aggressiveness in glioblastoma and promotes temozolomide resistance in glioblastoma cancer stem cells. Cell Death Dis. 10:2462019. View Article : Google Scholar : PubMed/NCBI | |
Li Y, Liu Y, Ren J, Deng S, Yi G, Guo M, Shu S, Zhao L, Peng Y and Qi S: miR-1268a regulates ABCC1 expression to mediate temozolomide resistance in glioblastoma. J Neurooncol. 138:499–508. 2018. View Article : Google Scholar : PubMed/NCBI | |
Biamonte F, Sica G, Filippini A and D'Alessio A: Evidence of reelin signaling in GBM and its derived cancer stem cells. Brain Sci. 11:7452021. View Article : Google Scholar : PubMed/NCBI | |
Tulip IJ, Kim SO, Kim EJ, Kim J, Lee JY, Kim H and Kim SC: Combined inhibition of STAT and Notch signalling effectively suppresses tumourigenesis by inducing apoptosis and inhibiting proliferation, migration and invasion in glioblastoma cells. Anim Cells Syst (Seoul). 25:161–170. 2021. View Article : Google Scholar : PubMed/NCBI | |
Lavanya C, Venkataswamy MM, Sibin MK, Srinivas Bharath MM and Chetan GK: Down regulation of human telomerase reverse transcriptase (hTERT) expression by BIBR1532 in human glioblastoma LN18 cells. Cytotechnology. 70:1143–1154. 2018. View Article : Google Scholar : PubMed/NCBI | |
Sibin MK, Bhat DI, Narasingarao KV, Lavanya CH and Chetan GK: CDKN2A (p16) mRNA decreased expression is a marker of poor prognosis in malignant high-grade glioma. Tumour Biol. 36:7607–7614. 2015. View Article : Google Scholar : PubMed/NCBI |