The molecular mechanisms of drug resistance of glioblastoma. Part 3. Differentiation and apoptosis of glioblastoma cells

Abstract

Glioblastomas are one of the most malignant and frequent human tumors, characterized by rapid growth, metastasis, resistance to therapy and the formation of relapses. The formation of multidrug resistance mechanisms in glioblastomas cells is often combined with inhibition of cell death and differentiation pathways and prevents an increase in the effectiveness of therapy in this group of patients. The review examines the relationship of molecular mechanisms of multidrug resistance with differentiation and apoptosis of glioblastomas with an emphasis on identifying new targets among proteins, microRNAs, suppressor genes, and oncogenes.

Keywords

glioblastoma / multidrug resistance / chemotherapy drugs / differentiation / apoptosis / growth factors / their receptors / signal transduction kinases / microRNAs / transcription factors / oncogenes and tumor suppressor genes

References

[1] Chen C-H, Chen P-Y, Lin Y-Y, et al. Suppression of tumor growth via IGFBP3 depletion as a potential treatment in glioma. J Neurosurg. 2019;132(1):168–179. DOI: 10.3171/2018.8.JNS181217

[2] Chen C.-H., Chen P.-Y., Lin Y.-Y. et al. Suppression of tumor growth via IGFBP3 depletion as a potential treatment in glioma // J. Neurosurg. 2019. Vol. 132, No. 1. P. 168–179. DOI: 10.3171/2018.8.JNS181217

[3] Auffinger B, Spencer D, Pytel P, et al. The role of glioma stem cells in chemotherapy resistance and glioblastoma multiforme recurrence. Expert Rev Neurother. 2015;15(7):741–752. DOI: 10.1586/14737175.2015.1051968

[4] Auffinger B., Spencer D., Pytel P. et al. The role of glioma stem cells in chemotherapy resistance and glioblastoma multiforme recurrence // Expert Rev. Neurother. 2015. Vol. 15, No. 7. P. 741–752. DOI: 10.1586/14737175.2015.1051968

[5] Tang X, Zuo C, Fang P, et al. Targeting glioblastoma stem cells: a review on biomarkers, signal pathways and targeted therapy. Front Oncol. 2021;11:701291. DOI: 10.3389/fonc.2021.701291

[6] Tang X., Zuo C., Fang P. et al. Targeting glioblastoma stem cells: a review on biomarkers, signal pathways and targeted therapy // Front. Oncol. 2021. Vol. 11. P. 701291. DOI: 10.3389/fonc.2021.701291

[7] Ducassou A, Uro-Coste E, Verrelle P, et al. αvβ3 Integrin and Fibroblast growth factor receptor 1 (FGFR1): Prognostic factors in a phase I–II clinical trial associating continuous administration of Tipifarnib with radiotherapy for patients with newly diagnosed glioblastoma. Eur J Cancer. 2013;49(9):2161–2169. DOI: 10.1016/j.ejca.2013.02.033

[8] Ducassou A., Uro-Coste E., Verrelle P. et al. αvβ3 Integrin and Fibroblast growth factor receptor 1 (FGFR1): Prognostic factors in a phase I–II clinical trial associating continuous administration of Tipifarnib with radiotherapy for patients with newly diagnosed glioblastoma // Eur. J. Cancer. 2013. Vol. 49, No. 9. P. 2161–2169. DOI: 10.1016/j.ejca.2013.02.033

[9] Gouazé-Andersson V, Delmas C, Taurand M, et al. FGFR1 induces glioblastoma radioresistance through the PLCγ/Hif1α pathway. Cancer Res. 2016;76(10):3036–3044. DOI: 10.1158/0008-5472.CAN-15-2058

[10] Gouazé-Andersson V., Delmas C., Taurand M. et al. FGFR1 Induces glioblastoma radioresistance through the PLCγ/Hif1α pathway // Cancer Res. 2016. Vol. 76, No. 10. P. 3036–3044. DOI: 10.1158/0008-5472.CAN-15-2058

[11] Ciechomska IA, Gielniewski B, Wojtas B, et al. EGFR/FOXO3a/BIM signaling pathway determines chemosensitivity of BMP4-differentiated glioma stem cells to temozolomide. Exp Mol Med. 2020;52:1326–1340. DOI: 10.1038/s12276-020-0479-9

[12] Ciechomska I.A., Gielniewski B., Wojtas B. et al. EGFR/FOXO3a/BIM signaling pathway determines chemosensitivity of BMP4-differentiated glioma stem cells to temozolomide // Exp. Mol. Med. 2020. Vol. 52. P. 1326–1340. DOI: 10.1038/s12276-020-0479-9

[13] Kim E-J, Kim S-O, Jin X, et al. Epidermal growth factor receptor variant III renders glioma cancer cells less differentiated by JAGGED1. Tumour Biol. 2015;36(4):2921–2928. DOI: 10.1007/s13277-014-2922-9

[14] Kim E.-J., Kim S.-O., Jin X. et al. Epidermal growth factor receptor variant III renders glioma cancer cells less differentiated by JAGGED1 // Tumour Biol. 2015. Vol. 36, No. 4. P. 2921–2928. DOI: 10.1007/s13277-014-2922-9

[15] Yuan J, Xiao G, Peng G, et al. MiRNA-125a-5p inhibits glioblastoma cell proliferation and promotes cell differentiation by targeting TAZ. Biochem Biophys Res Commun. 2015;457(2):171–176. DOI: 10.1016/j.bbrc.2014.12.078

[16] Yuan J., Xiao G., Peng G. et al. MiRNA-125a-5p inhibits glioblastoma cell proliferation and promotes cell differentiation by targeting TAZ // Biochem. Biophys. Res. Commun. 2015. Vol. 457, No. 2. P. 171–176. DOI: 10.1016/j.bbrc.2014.12.078

[17] Yin D, Chen W, O’Kelly J, et al. Connective tissue growth factor associated with oncogenic activities and drug resistance in glioblastoma multiforme. Int J Cancer. 2010;127(10):2257–2267. DOI: 10.1002/ijc.25257

[18] Yin D., Chen W., O’Kelly J. et al. Connective tissue growth factor associated with oncogenic activities and drug resistance in glioblastoma multiforme // Int. J. Cancer. 2010. Vol. 127, No. 10. P. 2257–2267. DOI: 10.1002/ijc.25257

[19] Silber J, Lim DA, Petritsch C, et al. miR-124 and miR-137 inhibit proliferation of glioblastoma multiforme cells and induce differentiation of brain tumor stem cells. BMC Med. 2008;24(6):14. DOI: 10.1186/1741-7015-6-14

[20] Silber J., Lim D.A., Petritsch C. et al. miR-124 and miR-137 inhibit proliferation of glioblastoma multiforme cells and induce differentiation of brain tumor stem cells // BMC Med. 2008. Vol. 24, No. 6. P. 14. DOI: 10.1186/1741-7015-6-14

[21] Sana J, Busek P, Fadrus P, et al. Identification of microRNAs differentially expressed in glioblastoma stem-like cells and their association with patient survival. Sci Rep. 2018;8:2836. DOI: 10.1038/s41598-018-20929-6

[22] Sana J., Busek P., Fadrus P. et al. Identification of microRNAs differentially expressed in glioblastoma stem-like cells and their association with patient survival // Sci. Rep. 2018. Vol. 8. P. 2836. DOI: 10.1038/s41598-018-20929-6

[23] Tomei S, Volontè A, Ravindran S, et al. MicroRNA expression profile distinguishes glioblastoma stem cells from differentiated tumor cells. J Pers Med. 2021;11(4):264. DOI: 10.3390/jpm11040264

[24] Tomei S., Volontè A., Ravindran S. et al. MicroRNA expression profile distinguishes glioblastoma stem cells from differentiated tumor cells // J. Pers. Med. 2021. Vol. 11, No. 4. P. 264. DOI: 10.3390/jpm11040264

[25] Cardoso AM, Morais CM, Pena F, et al. Differentiation of glioblastoma stem cells promoted by miR-128 or miR-302a overexpression enhances senescence-associated cytotoxicity of axitinib. Hum Mol Genet. 2021;30(3-4):160–171. DOI: 10.1093/hmg/ddab011

[26] Cardoso A.M., Morais C.M., Pena F. et al. Differentiation of glioblastoma stem cells promoted by miR-128 or miR-302a overexpression enhances senescence-associated cytotoxicity of axitinib // Hum. Mol. Genet. 2021. Vol. 30, No. 3-4. P. 160–171. DOI: 10.1093/hmg/ddab011

[27] Safa AR, Saadatzadeh MR, Cohen-Gadol AA, et al. Glioblastoma stem cells (GSCs) epigenetic plasticity and interconversion between differentiated non-GSCs and GSCs. Genes Dis. 2015;2(2):152–163. DOI: 10.1016/j.gendis.2015.02.001

[28] Safa A.R., Saadatzadeh M.R., Cohen-Gadol A.A. et al. Glioblastoma stem cells (GSCs) epigenetic plasticity and interconversion between differentiated non-GSCs and GSCs // Genes Dis. 2015. Vol. 2, No. 2. P. 152–163. DOI: 10.1016/j.gendis.2015.02.001

[29] Zhu J, Wang H, Fan Y, et al. Targeting the NF-E2-related factor 2 pathway: A novel strategy for glioblastoma. Oncol Rep. 2014;32(2):443–450. DOI: 10.3892/or.2014.3259

[30] Zhu J., Wang H., Fan Y. et al. Targeting the NF-E2-related factor 2 pathway: A novel strategy for glioblastoma // Oncol. Rep. 2014. Vol. 32, No. 2. P. 443–450. DOI: 10.3892/or.2014.3259

[31] Gouazé-Andersson V, Ghérardi MJ, Lemarié A, et al. FGFR1/FOXM1 pathway: a key regulator of glioblastoma stem cells radioresistance and a prognosis biomarker. Oncotarget. 2018;9(60):31637–31649. DOI: 10.18632/oncotarget.25827

[32] Gouazé-Andersson V., Ghérardi M.J., Lemarié A. et al. FGFR1/FOXM1 pathway: a key regulator of glioblastoma stem cells radioresistance and a prognosis biomarker // Oncotarget. 2018. Vol. 9, No. 60. P. 31637–31649. DOI: 10.18632/oncotarget.25827

[33] Korkolopoulou P, Levidou G, El-Habr EA, et al. Sox11 expression in astrocytic gliomas: Correlation with nestin/c-Met/IDH1-R132H expression phenotypes, p-Stat-3 and survival. Br J Cancer. 2013;108(10):2142–2152. DOI: 10.1038/bjc.2013.176

[34] Korkolopoulou P., Levidou G., El-Habr E.A. et al. Sox11 expression in astrocytic gliomas: Correlation with nestin/c-Met/IDH1-R132H expression phenotypes, p-Stat-3 and survival // Br. J. Cancer. 2013. Vol. 108, No. 10. P. 2142–2152. DOI: 10.1038/bjc.2013.176

[35] Calvert AE, Chalastanis A, Wu Y, et al. Cancer-associated IDH1 promotes growth and resistance to targeted therapies in the absence of mutation. Cell Rep. 2017;19(9):1858–1873. DOI: 10.1016/j.celrep.2017.05.014

[36] Calvert A.E., Chalastanis A., Wu Y. et al. Cancer-associated IDH1 promotes growth and resistance to targeted therapies in the absence of mutation // Cell Rep. 2017. Vol. 19, No. 9. P. 1858–1873. DOI: 10.1016/j.celrep.2017.05.014

[37] Bai Y, Lathia JD, Zhang P, et al. Molecular targeting of TRF2 suppresses the growth and tumorigenesis of glioblastoma stem cells. Glia. 2014;62(10):1687–1698. DOI: 10.1002/glia.22708

[38] Bai Y., Lathia J.D., Zhang P. et al. Molecular targeting of TRF2 suppresses the growth and tumorigenesis of glioblastoma stem cells // Glia. 2014. Vol. 62, No. 10. P. 1687–1698. DOI: 10.1002/glia.22708

[39] Chudnovsky Y, Kim D, Zheng S. ZFHX4 interacts with the NuRD core memberCHD4 and regulates the glioblastoma tumor-initiating cell state. Cell Rep. 2014;6:313–324. DOI: 10.1016/j.celrep.2013.12.032

[40] Chudnovsky Y., Kim D., Zheng S. ZFHX4 interacts with the NuRD core memberCHD4 and regulates the glioblastoma tumor-initiating cell state // Cell Rep. 2014. Vol. 6. P. 313–324. DOI: 10.1016/j.celrep.2013.12.032

[41] Zhou D, Alver BM, Li S, et al. Distinctive epigenomes characterize glioma stem cells and their response to differentiation cues. Genome Biol. 2018;19(1):43. DOI: 10.1186/s13059-018-1420-6

[42] Zhou D., Alver B.M., Li S. et al. Distinctive epigenomes characterize glioma stem cells and their response to differentiation cues // Genome Biol. 2018. Vol. 19, No. 1. P. 43. DOI: 10.1186/s13059-018-1420-6

[43] MacLeod G, Bozek DA, Rajakulendran N, et al. The functional genomic circuitry of human glioblastoma stem cells. BioRxiv. 2018. DOI: 10.1101/358432

[44] MacLeod G., Bozek D.A., Rajakulendran N. et al. The functional genomic circuitry of human glioblastoma stem cells // BioRxiv. 2018. DOI: 10.1101/358432

[45] Zhang J, Chen L, Han L, et al. EZH2 is a negative prognostic factor and exhibits pro-oncogenic activity in glioblastoma. Cancer Lett. 2015;356(2 Pt B):929–936. DOI: 10.1016/j.canlet.2014.11.003

[46] Zhang J., Chen L., Han L. et al. EZH2 is a negative prognostic factor and exhibits pro-oncogenic activity in glioblastoma // Cancer Lett. 2015. Vol. 356, No. 2 Pt B. P. 929–936. DOI: 10.1016/j.canlet.2014.11.003

[47] Huang M, Zhang D, Wu JY, et al. Wnt-mediated endothelial transformation into mesenchymal stem cell-like cells induces chemoresistance in glioblastoma. Sci Transl Med. 2020;12(532):eaay7522. DOI: 10.1126/scitranslmed.aay7522

[48] Huang M., Zhang D., Wu J.Y. et al. Wnt-mediated endothelial transformation into mesenchymal stem cell-like cells induces chemoresistance in glioblastoma // Sci. Transl. Med. 2020. Vol. 12, No. 532. P. eaay7522. DOI: 10.1126/scitranslmed.aay7522

[49] Fiscon G, Conte F, Licursi V, et al. Computational identification of specific genes for glioblastoma stem-like cells identity. Sci Rep. 2018;8:7769. DOI: 10.1038/s41598-018-26081-5

[50] Fiscon G., Conte F., Licursi V. et al. Computational identification of specific genes for glioblastoma stem-like cells identity // Sci. Rep. 2018. Vol. 8. P. 7769. DOI: 10.1038/s41598-018-26081-5

[51] Suva ML, Rheinbay E, Gillespie SM, et al. Reconstructing and reprogramming the tumor-propagating potential of glioblastoma stem-like cells. Cell. 2014;157(3):580–594. DOI: 10.1016/j.cell.2014.02.030

[52] Suva M.L., Rheinbay E., Gillespie S.M. et al. Reconstructing and reprogramming the tumor-propagating potential of glioblastoma stem-like cells // Cell. 2014. Vol. 157, No. 3. P. 580–594. DOI: 10.1016/j.cell.2014.02.030

[53] Rheinbay E, Suvà ML, Gillespiet SM, et al. An aberrant transcription factor network essential for Wnt signaling and stem cell maintenance in glioblastoma. Cell Rep. 2013;3(5):1567–1579. DOI: 10.1016/j.celrep.2013.04.021

[54] Rheinbay E., Suvà M.L., Gillespiet S.M. et al. An aberrant transcription factor network essential for Wnt signaling and stem cell maintenance in glioblastoma // Cell Rep. 2013. Vol. 3, No. 5. P. 1567–1579. DOI: 10.1016/j.celrep.2013.04.021

[55] Kärrlander M, Lindberg N, Olofsson T, et al. Histidine-rich glycoprotein can prevent development of mouse experimental glioblastoma. PLoS One. 2009;4(12):e8536. DOI: 10.1371/journal.pone.0008536

[56] Kärrlander M., Lindberg N., Olofsson T. et al. Histidine-rich glycoprotein can prevent development of mouse experimental glioblastoma // PLoS One. 2009. Vol. 4, No. 12. P. e8536. DOI: 10.1371/journal.pone.0008536

[57] González-Gómez P, Crecente-Campo J, Zahonero C, et al. Controlled release microspheres loaded with BMP7 suppress primary tumors from human glioblastoma. Oncotarget. 2015;6(13):10950–1063. DOI: 10.18632/oncotarget.3459

[58] González-Gómez P., Crecente-Campo J., Zahonero C. et al. Controlled release microspheres loaded with BMP7 suppress primary tumors from human glioblastoma // Oncotarget. 2015. Vol. 6, No. 13. P. 10950–1063. DOI: 10.18632/oncotarget.3459

[59] Rodriguez V, Bailey R, Larion M, et al. Retinoid receptor turnover mediated by sumoylation, ubiquitination and the valosin-containing protein is disrupted in glioblastoma. Sci Rep. 2019;9(1):16250. DOI: 10.1038/s41598-019-52696-3

[60] Rodriguez V., Bailey R., Larion M. et al. Retinoid receptor turnover mediated by sumoylation, ubiquitination and the valosin-containing protein is disrupted in glioblastoma // Sci. Rep. 2019. Vol. 9, No. 1. P. 16250. DOI: 10.1038/s41598-019-52696-3

[61] Zeng H, Yang Z, Xu N, et al. Connective tissue growth factor promotes temozolomide resistance in glioblastoma through TGF-β1-dependent activation of Smad/ERK signaling. Cell Death Dis. 2017;8(6):e2885. DOI: 10.1038/cddis.2017.248

[62] Zeng H., Yang Z., Xu N. et al. Connective tissue growth factor promotes temozolomide resistance in glioblastoma through TGF-β1-dependent activation of Smad/ERK signaling // Cell Death Dis. 2017. Vol. 8, No. 6. P. e2885. DOI: 10.1038/cddis.2017.248

[63] Clark PA, Iida M, Treisman DM, et al. Activation of multiple ERBB family receptors mediates glioblastoma cancer stem-like cell resistance to EGFR-targeted inhibition. Neoplasia. 2012;14(5):420–428. DOI: 10.1596/neo.12432

[64] Clark P.A., Iida M., Treisman D.M. et al. Activation of multiple ERBB family receptors mediates glioblastoma cancer stem-like cell resistance to EGFR-targeted inhibition // Neoplasia. 2012. Vol. 14, No. 5. P. 420–428. DOI: 10.1596/neo.12432

[65] Maris C, D’Haene N, Trépant A-L, et al. IGF-IR: a new prognostic biomarker for human glioblastoma. Br J Cancer. 2015;113(5):729–737. DOI: 10.1038/bjc.2015.242

[66] Maris C., D’Haene N., Trépant A.-L. et al. IGF-IR: a new prognostic biomarker for human glioblastoma // Br. J. Cancer. 2015. Vol. 113, No. 5. P. 729–737. DOI: 10.1038/bjc.2015.242

[67] Tirrò E, Massimino M, Romano C, et al. Prognostic and therapeutic roles of the insulin growth factor system in glioblastoma. Front Oncol. 2021;10:612385. DOI: 10.3389/fonc.2020.612385

[68] Tirrò E., Massimino M., Romano C. et al. Prognostic and therapeutic roles of the insulin growth factor system in glioblastoma // Front. Oncol. 2021. Vol. 10. P. 612385. DOI: 10.3389/fonc.2020.612385

[69] Schreck KC, Taylor P, Marchionni L, et al. The Notch target Hes1 directly modulates Gli1 expression and hedgehog signaling: a potential mechanism of therapeutic resistance. Clin Cancer Res. 2016;22(14):3700–3701. DOI: 10.1158/1078-0432.CCR-16-1194

[70] Schreck K.C., Taylor P., Marchionni L. et al. The Notch target Hes1 directly modulates Gli1 expression and hedgehog signaling: a potential mechanism of therapeutic resistance // Clin. Cancer Res. 2016. Vol. 22, No. 14. P. 3700–3701. DOI: 10.1158/1078-0432.CCR-16-1194

[71] Yang F, Nam S, Brown CE, et al. A novel berbamine derivative inhibits cell viability and induces apoptosis in cancer stem-like cells of human glioblastoma, via up-regulation of miRNA-4284 and JNK/AP-1 signaling. PLoS One. 2014;9(4):e94443. DOI: 10.1371/journal.pone.0094443

[72] Yang F., Nam S., Brown C.E. et al. A novel berbamine derivative inhibits cell viability and induces apoptosis in cancer stem-like cells of human glioblastoma, via up-regulation of miRNA-4284 and JNK/AP-1 signaling // PLoS One. 2014. Vol. 9, No. 4. P. e94443. DOI: 10.1371/journal.pone.0094443

[73] Liu Z-H, Dai X-M, Du B. Hes1: a key role in stemness, metastasis and multidrug resistance. Cancer Biol Ther. 2015;16(3):353–359. DOI: 10.1080/15384047.2015.1016662

[74] Liu Z.-H., Dai X.-M., Du B. Hes1: a key role in stemness, metastasis and multidrug resistance // Cancer Biol. Ther. 2015. Vol. 16, No. 3. P. 353–359. DOI: 10.1080/15384047.2015.1016662

[75] Popescu AM, Alexandru O, Brindusa C, et al. Targeting the VEGF and PDGF signaling pathway in glioblastoma treatment. Int J Clin Exp Pathol. 2015;8(7):7825–7837.

[76] Popescu A.M., Alexandru O., Brindusa C. et al. Targeting the VEGF and PDGF signaling pathway in glioblastoma treatment // Int. J. Clin. Exp. Pathol. 2015. Vol. 8, No. 7. P. 7825–7837.

[77] Gouazé-Andersson V, Ghérardi M-J, Lemarié A, et al. FGFR1/FOXM1 pathway: a key regulator of glioblastoma stem cells radioresistance and a prognosis biomarker. Oncotarget. 2018;9:31637–31649. DOI: 10.18632/oncotarget.25827

[78] Gouazé-Andersson V., Ghérardi M.-J., Lemarié A. et al. FGFR1/FOXM1 pathway: a key regulator of glioblastoma stem cells radioresistance and a prognosis biomarker // Oncotarget. 2018. Vol. 9. P. 31637–31649. DOI: 10.18632/oncotarget.25827

[79] Fan TY, Wang H, Xiang P, et al. Inhibition of EZH2 reverses chemotherapeutic drug TMZ chemosensitivity in glioblastoma. Int J Clin Exp Pathol. 2014;7(10):6662–6670.

[80] Fan T.Y., Wang H., Xiang P. et al. Inhibition of EZH2 reverses chemotherapeutic drug TMZ chemosensitivity in glioblastoma // Int. J. Clin. Exp. Pathol. 2014. Vol. 7, No. 10. 6662–6670.

[81] Zhang L, Wang H. FTY720 inhibits the Nrf2/ARE pathway in human glioblastoma cell lines and sensitizes glioblastoma cells to temozolomide. Pharmacol Rep. 2017;69(6):1186–1193. DOI: 10.1016/j.pharep.2017.07.003

[82] Zhang L., Wang H. FTY720 inhibits the Nrf2/ARE pathway in human glioblastoma cell lines and sensitizes glioblastoma cells to temozolomide // Pharmacol. Rep. 2017. Vol. 69, No. 6. P. 1186–1193. DOI: 10.1016/j.pharep.2017.07.003

[83] Zhou Y, Wang H-D, Zhu L. Knockdown of Nrf2 enhances autophagy induced by temozolomide in U251 human glioma cell line. Oncol Rep. 2013;29(1):394–400. DOI: 10.3892/or.2012.2115

[84] Zhou Y., Wang H.-D., Zhu L. Knockdown of Nrf2 enhances autophagy induced by temozolomide in U251 human glioma cell line // Oncol. Rep. 2013. Vol. 29, No. 1. P. 394–400. DOI: 10.3892/or.2012.2115

[85] Ji X, Wang H, Zhu J, et al. Correlation of Nrf2 and HIF-1α in glioblastoma and their relationships to clinicopathologic features and survival. Neurol Res. 2013;35(10):1044–1050. DOI: 10.1179/1743132813Y.0000000251

[86] Ji X., Wang H., Zhu J. et al. Correlation of Nrf2 and HIF-1α in glioblastoma and their relationships to clinicopathologic features and survival // Neurol. Res. 2013. Vol. 35, No. 10. P. 1044–1050. DOI: 10.1179/1743132813Y.0000000251

[87] Rocha CR, Kajitani GS, Quinet A, et al. NRF2 and glutathione are key resistance mediators to temozolomide in glioma and melanoma cells. Oncotarget. 2016;7(30):48081–48092. DOI: 10.18632/oncotarget.10129

[88] Rocha C.R., Kajitani G.S., Quinet A. et al. NRF2 and glutathione are key resistance mediators to temozolomide in glioma and melanoma cells // Oncotarget. 2016. Vol. 7, No. 30. P. 48081–48092. DOI: 10.18632/oncotarget.10129

[89] García-Gómez P, Dadras M, Bellomo C, et al. NOX4 regulates TGFβ-induced proliferation and self-renewal in glioblastoma stem cells. BioRxiv. 2019. DOI: 10.1101/804013

[90] García-Gómez P., Dadras M., Bellomo C. et al. NOX4 regulates TGFβ-induced proliferation and self-renewal in glioblastoma stem cells // BioRxiv. 2019. DOI: 10.1101/804013

[91] Agnihotri S, Wolf A, Picard D, et al. GATA4 is a regulator of astrocyte cell proliferation and apoptosis in the human and murine central nervous system. Oncogene. 2009;28(34):3033–3046. DOI: 10.1038/onc.2009.159

[92] Agnihotri S., Wolf A., Picard D. et al. GATA4 is a regulator of astrocyte cell proliferation and apoptosis in the human and murine central nervous system // Oncogene. 2009. Vol. 28, No. 34. P. 3033–3046. DOI: 10.1038/onc.2009.159

[93] Lan J, Xue Y, Chen H, et al. Hypoxia-induced miR-497 decreases glioma cell sensitivity to TMZ by inhibiting apoptosis. FEBS Lett. 2014;588(8):3333–3339. DOI: 10.1016/j.febslet.2014.07.021

[94] Lan J., Xue Y., Chen H. et al. Hypoxia-induced miR-497 decreases glioma cell sensitivity to TMZ by inhibiting apoptosis // FEBS Lett. 2014. Vol. 588, No. 8. P. 3333–3339. DOI: 10.1016/j.febslet.2014.07.021

[95] Zhang JM, Sun CY, Yu SZ, et al. Relationship between miR-218 and CDK6 expression and their biological impact on glioma cell proliferation and apoptosis. Zhonghua Bing Li Xue Za Zhi. 2011;40(7):454–459. (In Chinese)

[96] Zhang J.M., Sun C.Y., Yu S.Z. et al. Relationship between miR-218 and CDK6 expression and their biological impact on glioma cell proliferation and apoptosis // Zhonghua Bing Li Xue Za Zhi. 2011. Vol. 40, No. 7. P. 454–459. (In Chinese)

[97] Xia H, Yan Y, Hu M, et al. MiR-218 sensitizes glioma cells to apoptosis and inhibits tumorigenicity by regulating ECOP-mediated suppression of NF-κB activity. Neuro Oncol. 2013;15:413–422. DOI: 10.1093/neuonc/nos296

[98] Xia H., Yan Y., Hu M. et al. MiR-218 sensitizes glioma cells to apoptosis and inhibits tumorigenicity by regulating ECOP-mediated suppression of NF-κB activity // Neuro Oncol. 2013. Vol. 15. P. 413–422. DOI: 10.1093/neuonc/nos296

[99] Ahmed SP, Castresana JS, Shahi MH. Glioblastoma and MiRNAs. Cancers (Basel). 2021;13(7):1581. DOI: 10.3390/cancers13071581

[100] Ahmed S.P., Castresana J.S., Shahi M.H. Glioblastoma and MiRNAs // Cancers (Basel). 2021. Vol. 13, No. 7. P. 1581. DOI: 10.3390/cancers13071581

[101] Li L, Gao R, Yu Y, et al. Tumor suppressor activity of miR-451: Identification of CARF as a new target. Sci Rep. 2018;8:375. DOI: 10.1038/s41598-017-18559-5

[102] Li L., Gao R., Yu Y. et al. Tumor suppressor activity of miR-451: Identification of CARF as a new target // Sci. Rep. 2018. Vol. 8. P. 375. DOI: 10.1038/s41598-017-18559-5

[103] Korać P, Antica M, Matulić M. MiR-7 in cancer development. Biomedicines. 2021;9(3):325. DOI: 10.3390/biomedicines9030325

[104] Korać P., Antica M., Matulić M. MiR-7 in cancer development // Biomedicines. 2021. Vol. 9, No. 3. P. 325. DOI: 10.3390/biomedicines9030325

[105] Duan J, Zhou K, Tang X, et al. MicroRNA-34a inhibits cell proliferation and induces cell apoptosis of glioma cells via targeting of Bcl-2. Mol Med Rep. 2016;14:432–438. DOI: 10.3892/mmr.2016.5255

[106] Duan J., Zhou K., Tang X. et al. MicroRNA-34a inhibits cell proliferation and induces cell apoptosis of glioma cells via targeting of Bcl-2 // Mol. Med. Rep. 2016. Vol. 14. P. 432–438. DOI: 10.3892/mmr.2016.5255

[107] Shan ZN, Tian R, Zhang M, et al. miR128-1 inhibits the growth of glioblastoma multiforme and glioma stem-like cells via targeting BMI1 and E2F3. Oncotarget. 2016;7:78813–78826. DOI: 10.18632/oncotarget.12385

[108] Shan Z.N., Tian R., Zhang M. et al. miR128-1 inhibits the growth of glioblastoma multiforme and glioma stem-like cells via targeting BMI1 and E2F3 // Oncotarget. 2016. Vol. 7. P. 78813–78826. DOI: 10.18632/oncotarget.12385

[109] Chen M, Medarova Z, Moore А. Role of microRNAs in glioblastoma. Oncotarget. 2021;12:1707–1723. DOI: 10.18632/oncotarget.28039

[110] Chen M., Medarova Z., Moore А. Role of microRNAs in glioblastoma // Oncotarget. 2021. Vol. 12. P. 1707–1723. DOI: 10.18632/oncotarget.28039

[111] Anthiya S, Griveau A, Loussouarn C, et al. MicroRNA-based drugs for brain tumours. Trends Cancer. 2018;4(3):222–238. DOI: 10.1016/j.trecan.2017.12.008

[112] Anthiya S., Griveau A., Loussouarn C. et al. MicroRNA-based drugs for brain tumours // Trends Cancer. 2018. Vol. 4, No. 3. P. 222–238. DOI: 10.1016/j.trecan.2017.12.008

[113] Banelli B, Forlani A, Allemanni G, et al. MicroRNA in glioblastoma: an overview. Int J Genomics. 2017;2017:7639084. DOI: 10.1155/2017/7639084

[114] Banelli B., Forlani A., Allemanni G. et al. MicroRNA in glioblastoma: an overview // Int. J. Genomics. 2017. Vol. 2017. P. 7639084. DOI: 10.1155/2017/7639084

[115] Tang H, Bian Y, Tu C, et al. The miR-183/96/182 cluster regulates oxidative apoptosis and sensitizes cells to chemotherapy in gliomas. Curr Cancer Drug Targets. 2013;13(2):221–231. DOI: 10.2174/1568009611313020010

[116] Tang H., Bian Y., Tu C. et al. The miR-183/96/182 cluster regulates oxidative apoptosis and sensitizes cells to chemotherapy in gliomas // Curr. Cancer Drug Targets. 2013. Vol. 13, No. 2. P. 221–231. DOI: 10.2174/1568009611313020010

[117] Chen Y-Y, Ho H-L, Lin S-C, et al. Upregulation of miR-125b, miR-181d, and miR-221 predicts poor prognosis in MGMT promoter-unmethylated glioblastoma patients. Am J Clin Pathol. 2018;149(5):412–417. DOI: 10.1093/ajcp/aqy008

[118] Chen Y.-Y., Ho H.-L., Lin S.-C. et al. Upregulation of miR-125b, miR-181d, and miR-221 predicts poor prognosis in MGMT promoter-unmethylated glioblastoma patients // Am. J. Clin. Pathol. 2018. Vol. 149, No. 5. P. 412–417. DOI: 10.1093/ajcp/aqy008

[119] Song J, Ouyang Y, Che J, et al. Potential value of miR-221/222 as diagnostic, prognostic, and therapeutic biomarkers for diseases. Front Immunol. 2017;8:56. DOI: 10.3389/fimmu.2017.00056

[120] Song J., Ouyang Y., Che J. et al. Potential value of miR-221/222 as diagnostic, prognostic, and therapeutic biomarkers for diseases // Front. Immunol. 2017. Vol. 8. P. 56. DOI: 10.3389/fimmu.2017.00056

[121] Chen L, Zhang J, Han L, et al. Downregulation of miR-221/222 sensitizes glioma cells to temozolomide by regulating apoptosis independently of p53 status. Oncol Rep. 2012;27:854–860. DOI: 10.3892/or.2011.1535

[122] Chen L., Zhang J., Han L. et al. Downregulation of miR-221/222 sensitizes glioma cells to temozolomide by regulating apoptosis independently of p53 status // Oncol. Rep. 2012. Vol. 27. P. 854–860. DOI: 10.3892/or.2011.1535

[123] Li W, Guo F, Wang P, et al. miR-221/222 confers radioresistance in glioblastoma cells through activating Akt independent of PTEN status. Curr Mol Med. 2014;14:185–195. DOI: 10.2174/1566524013666131203103147

[124] Li W., Guo F., Wang P. et al. miR-221/222 confers radioresistance in glioblastoma cells through activating Akt independent of PTEN status // Curr. Mol. Med. 2014. Vol. 14. P. 185–195. DOI: 10.2174/1566524013666131203103147

[125] Shu M, Zheng X, Wu S, et al. Targeting oncogenic miR-335 inhibits growth and invasion of malignant astrocytoma cells. Mol Cancer. 2011;10:59. DOI: 10.1186/1476-4598-10-59

[126] Shu M., Zheng X., Wu S. et al. Targeting oncogenic miR-335 inhibits growth and invasion of malignant astrocytoma cells // Mol. Cancer. 2011. Vol. 10. P. 59. DOI: 10.1186/1476-4598-10-59

[127] Scarola M, Schoeftner S, Schneider C, et al. miR-335 directly targets Rb1 (pRb/p105) in a proximal connection to p53-dependent stress response. Cancer Res. 2010;70(17):6925–6933. DOI: 10.1158/0008-5472.CAN-10-0141

[128] Scarola M., Schoeftner S., Schneider C. et al. miR-335 directly targets Rb1 (pRb/p105) in a proximal connection to p53-dependent stress response // Cancer Res. 2010. Vol. 70, No. 17. P. 6925–6933. DOI: 10.1158/0008-5472.CAN-10-0141

[129] Yang F, Nam S, Brown CE, et al. A novel berbamine derivative inhibits cell viability and induces apoptosis in cancer stem-like cells of human glioblastoma, via up-regulation of miRNA-4284 and JNK/AP-1 signaling. PLoS One. 2014;9(4):e94443. DOI: 10.1371/journal.pone.0094443

[130] Yang F., Nam S., Brown C.E. et al. A novel berbamine derivative inhibits cell viability and induces apoptosis in cancer stem-like cells of human glioblastoma, via up-regulation of miRNA-4284 and JNK/AP-1 signaling // PLoS One. 2014. Vol. 9, No. 4. P. e94443. DOI: 10.1371/journal.pone.0094443

[131] Izquierdo-Garcia JL, Viswanath P, Eriksson P, et al. Metabolic reprogramming in mutant IDH1 glioma cells. PLoS One. 2015;10(2):e0118781. DOI: 10.1371/journal.pone.0118781

[132] Izquierdo-Garcia J.L., Viswanath P., Eriksson P. et al. Metabolic reprogramming in mutant IDH1 glioma cells // PLoS One. 2015. Vol. 10, No. 2. P. e0118781. DOI: 10.1371/journal.pone.0118781

[133] Valdés-Rives SA, Casique-Aguirre D, Germán-Castelán L, et al. Apoptotic signaling pathways in glioblastoma and therapeutic implications. Biomed Res Int. 2017;2017:7403747. DOI: 10.1155/2017/7403747

[134] Valdés-Rives S.A., Casique-Aguirre D., Germán-Castelán L. et al. Apoptotic signaling pathways in glioblastoma and therapeutic implications // Biomed. Res. Int. 2017. Vol. 2017. P. 7403747. DOI: 10.1155/2017/7403747

[135] Verhaak RGW, Hoadley KA, Purdom E, et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell. 2010;17:98–110. DOI: 10.1016/j.ccr.2009.12.020

[136] Verhaak R.G.W., Hoadley K.A., Purdom E. et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1 // Cancer Cell. 2010. Vol. 17. P. 98–110. DOI: 10.1016/j.ccr.2009.12.020

[137] Miller CR, Perry A. Glioblastoma. Arch Pathol Lab Med. 2007;131(3):397–406. DOI: 10.5858/2007-131-397-G

[138] Miller C.R., Perry A. Glioblastoma // Arch. Pathol. Lab. Med. 2007. Vol. 131, No. 3. P. 397–406. DOI: 10.5858/2007-131-397-G

[139] Mellai M, Piazzi A, Caldera V, et al. Promoter hypermethylation of the EMP3 gene in a series of 229 human gliomas. Biomed Res Int. 2013;2013:756302. DOI: 10.1155/2013/756302

[140] Mellai M., Piazzi A., Caldera V. et al. Promoter hypermethylation of the EMP3 gene in a series of 229 human gliomas // Biomed. Res. Int. 2013. Vol. 2013. P. 756302. DOI: 10.1155/2013/756302

[141] Li K, Ouyang L, He M, et al. IDH1 R132H mutation regulates glioma chemosensitivity through Nrf2 pathway. Oncotarget. 2017;8(17):28865–28879. DOI: 10.18632/oncotarget.15868

[142] Li K., Ouyang L., He M. et al. IDH1 R132H mutation regulates glioma chemosensitivity through Nrf2 pathway // Oncotarget. 2017. Vol. 8, No. 17. P. 28865–28879. DOI: 10.18632/oncotarget.15868

[143] Colardo M, Segatto M, Di Bartolomeo S. Targeting RTK-PI3K-mTOR axis in gliomas: an update. Int J Mol Sci. 2021;22:4899. DOI: 10.3390/ijms22094899

[144] Colardo M., Segatto M., Di Bartolomeo S. Targeting RTK-PI3K-mTOR axis in gliomas: an update // Int. J. Mol. Sci. 2021. Vol. 22. P. 4899. DOI: 10.3390/ijms22094899

[145] Duzgun Z, Eroglu Z, Biray Avci C. Role of mTOR in glioblastoma. Gene. 2016;575(2 Pt 1):187–190. DOI: 10.1016/j.gene.2015.08.060

[146] Duzgun Z., Eroglu Z., Biray Avci C. Role of mTOR in glioblastoma // Gene. 2016. Vol. 575, No. 2 Pt 1. P. 187–190. DOI: 10.1016/j.gene.2015.08.060

[147] Zając A, Sumorek-Wiadro J, Langner E, et al. Involvement of PI3K pathway in glioma cell resistance to temozolomide treatment. Int J Mol Sci. 2021;22(10):5155. DOI: 10.3390/ijms22105155

[148] Zając A., Sumorek-Wiadro J., Langner E. et al. Involvement of PI3K pathway in glioma cell resistance to temozolomide treatment // Int. J. Mol. Sci. 2021. Vol. 22, No. 10. P. 5155. DOI: 10.3390/ijms22105155

[149] Zhou W, Liu L, Xue Y, et al. Combination of endothelial-monocyte-activating polypeptide-II with temozolomide suppress malignant biological behaviors of human glioblastoma stem cells via miR-590-3p/MACC1 inhibiting PI3K/AKT/mTOR signal pathway. Front Mol Neurosci. 2017;10:68. DOI: 10.3389/fnmol.2017.00068

[150] Zhou W., Liu L., Xue Y. et al. Combination of endothelial-monocyte-activating polypeptide-II with temozolomide suppress malignant biological behaviors of human glioblastoma stem cells via miR-590-3p/MACC1 inhibiting PI3K/AKT/mTOR signal pathway // Front. Mol. Neurosci. 2017. Vol. 10. P. 68. DOI: 10.3389/fnmol.2017.00068

[151] Shang C, Hong Y, Guo Y, et al. Influence of the MACC1 gene on sensitivity to chemotherapy in human U251 glioblastoma cells. Asian Pac J Cancer Prev. 2015;16(1):195–199. DOI: 10.7314/apjcp.2015.16.1.195

[152] Shang C., Hong Y., Guo Y. et al. Influence of the MACC1 gene on sensitivity to chemotherapy in human U251 glioblastoma cells // Asian Pac. J. Cancer Prev. 2015. Vol. 16, No. 1. P. 195–199. DOI: 10.7314/apjcp.2015.16.1.195

[153] Pojo M, Gonçalves CS, Xavier-Magalhães A, et al. A transcriptomic signature mediated by HOXA9 promotes human glioblastoma initiation, aggressiveness and resistance to temozolomide. Oncotarget. 2015;6(10):7657–7674. DOI: 10.18632/oncotarget.3150

[154] Pojo M., Gonçalves C.S., Xavier-Magalhães A. et al. A transcriptomic signature mediated by HOXA9 promotes human glioblastoma initiation, aggressiveness and resistance to temozolomide // Oncotarget. 2015. Vol. 6, No. 10. P. 7657–7674. DOI: 10.18632/oncotarget.3150

[155] Le Mercier M, Lefranc F, Mijatovic T, et al. Evidence of galectin-1 involvement in glioma chemoresistance. Toxicol Appl Pharmacol. 2008;229(2):172–183. DOI: 10.1016/j.taap.2008.01.009

[156] Le Mercier M., Lefranc F., Mijatovic T. et al. Evidence of galectin-1 involvement in glioma chemoresistance // Toxicol. Appl. Pharmacol. 2008. Vol. 229, No. 2. P. 172–183. DOI: 10.1016/j.taap.2008.01.009

[157] Sasaki A, Udaka Y, Tsunoda Y, et al. Analysis of p53 and miRNA expressions after irradiation in glioblastoma cell lines. Anticancer Res. 2012;32(11):4709–4713.

[158] Sasaki A., Udaka Y., Tsunoda Y. et al. Analysis of p53 and miRNA expressions after irradiation in glioblastoma cell lines // Anticancer Res. 2012. Vol. 32, No. 11. P. 4709–4713.

[159] Jesionek-Kupnicka D, Braun M, Trąbska-Kluch B, et al. MiR-21, miR-34a, miR-125b, miR-181d and miR-648 levels inversely correlate with MGMT and TP53 expression in primary glioblastoma patients. Arch Med Sci. 2019;15(2):504–512. DOI: 10.5114/aoms.2017.69374

[160] Jesionek-Kupnicka D., Braun M., Trąbska-Kluch B. et al. MiR-21, miR-34a, miR-125b, miR-181d and miR-648 levels inversely correlate with MGMT and TP53 expression in primary glioblastoma patients // Arch. Med. Sci. 2019. Vol. 15, No. 2. P. 504–512. DOI: 10.5114/aoms.2017.69374

[161] Giacomelli C, Natali L, Trincavelli ML, et al. New insights into the anticancer activity of carnosol: p53 reactivation in the U87MG human glioblastoma cell line. Int J Biochem Cell Biol. 2016;74:95–108. DOI: 10.1016/j.biocel.2016.02.019

[162] Giacomelli C., Natali L., Trincavelli M.L. et al. New insights into the anticancer activity of carnosol: p53 reactivation in the U87MG human glioblastoma cell line // Int. J. Biochem. Cell Biol. 2016. Vol. 74. P. 95–108. DOI: 10.1016/j.biocel.2016.02.019

[163] Vadysirisack DD, Baenke F, Ory B, et al. Feedback control of p53 translation by REDD1 and mTORC1 limits the p53-dependent DNA damage response. Mol Cell Biol. 2011;31(21):4356–4365. DOI: 10.1128/MCB.05541-11

[164] Vadysirisack D.D., Baenke F., Ory B. et al. Feedback control of p53 translation by REDD1 and mTORC1 limits the p53-dependent DNA damage response // Mol. Cell Biol. 2011. Vol. 31, No. 21. P. 4356–4365. DOI: 10.1128/MCB.05541-11

[165] George J, Gondi CS, Dinh DH, et al. Restoration of tissue factor pathway inhibitor-2 in a human glioblastoma cell line triggers caspase-mediated pathway and apoptosis. Clin Cancer Res. 2007;13(12):3507–3517. DOI: 10.1158/1078-0432.CCR-06-3023

[166] George J., Gondi C.S., Dinh D.H. et al. Restoration of tissue factor pathway inhibitor-2 in a human glioblastoma cell line triggers caspase-mediated pathway and apoptosis // Clin. Cancer Res. 2007. Vol. 13, No. 12. P. 3507–3517. DOI: 10.1158/1078-0432.CCR-06-3023

[167] Wagner L, Marschall V, Karl S, et al. Smac mimetic sensitizes glioblastoma cells to Temozolomide-induced apoptosis in a RIP1- and NF-κB-dependent manner. Oncogene. 2013;32(8):988–997. DOI: 10.1038/onc.2012.108

[168] Wagner L., Marschall V., Karl S. et al. Smac mimetic sensitizes glioblastoma cells to Temozolomide-induced apoptosis in a RIP1- and NF-κB-dependent manner // Oncogene. 2013. Vol. 32, No. 8. P. 988–997. DOI: 10.1038/onc.2012.108

[169] Gondi CS, Talluri L, Dinh DH, et al. RNAi-mediated downregulation of MMP-2 activates the extrinsic apoptotic pathway in human glioma xenograft cells. Int J Oncol. 2009;35(4):851–859. DOI: 10.3892/ijo_00000399

[170] Gondi C.S, Talluri L., Dinh D.H. et al. RNAi-mediated downregulation of MMP-2 activates the extrinsic apoptotic pathway in human glioma xenograft cells // Int. J. Oncol. 2009. Vol. 35, No. 4. P. 851–859. DOI: 10.3892/ijo_00000399

[171] Mohanty S, Chen Z, Li K, et al. A novel theranostic strategy for MMP-14-expressing glioblastomas impacts survival. Mol Cancer Ther. 2017;16(9):1909–1921. DOI: 10.1158/1535-7163.MCT-17-0022

[172] Mohanty S., Chen Z., Li K. et al. A novel theranostic strategy for MMP-14-expressing glioblastomas impacts survival // Mol. Cancer Ther. 2017. Vol. 16, No. 9. P. 1909–1921. DOI: 10.1158/1535-7163.MCT-17-0022

[173] Tamannai M, Farhangi S, Truss M, et al. The inhibitor of growth 1 (ING1) is involved in trichostatin A-induced apoptosis and caspase 3 signaling in p53-deficient glioblastoma cells. Oncol Res. 2010;18(10):469–480. DOI: 10.3727/096504010x12704916124828

[174] Tamannai M., Farhangi S., Truss M. et al. The inhibitor of growth 1 (ING1) is involved in trichostatin A-induced apoptosis and caspase 3 signaling in p53-deficient glioblastoma cells // Oncol. Res. 2010;18(10):469–480. DOI: 10.3727/096504010x12704916124828

[175] Kouri FM, Jensen SA, Stegh AH. The role of Bcl-2 family proteins in therapy responses of malignant astrocytic gliomas: Bcl2L12 and beyond. Scientific World J. 2012;2012:838916. DOI: 10.1100/2012/838916

[176] Kouri F.M., Jensen S.A., Stegh A.H. The role of Bcl-2 family proteins in therapy responses of malignant astrocytic gliomas: Bcl2L12 and beyond // Scientific World J. 2012. Vol. 2012. P. 838916. DOI: 10.1100/2012/838916

[177] Burton TR, Henson ES, Azad MB, et al. BNIP3 acts as transcriptional repressor of death receptor-5 expression and prevents TRAIL-induced cell death in gliomas. Cell Death Dis. 2013;4(4):e587. DOI: 10.1038/cddis.2013.100

[178] Burton T.R., Henson E.S., Azad M.B. et al. BNIP3 acts as transcriptional repressor of death receptor-5 expression and prevents TRAIL-induced cell death in gliomas // Cell Death Dis. 2013. Vol. 4, No. 4. P. e587. DOI: 10.1038/cddis.2013.100

[179] Lin S-P, Lee Y-T, Wang J-Y, et al. Survival of cancer stem cells under hypoxia and serum depletion via decrease in PP2A activity and activation of p38-MAPKAPK2-Hsp27. PLoS One. 2012;7(11):e49605. DOI: 10.1371/journal.pone.0049605

[180] Lin S.-P., Lee Y.-T., Wang J.-Y. et al. Survival of cancer stem cells under hypoxia and serum depletion via decrease in PP2A activity and activation of p38-MAPKAPK2-Hsp27 // PLoS One. 2012. Vol. 7, No. 11. P. e49605. DOI: 10.1371/journal.pone.0049605

[181] Markouli M, Strepkos D, Papavassiliou AG, Piperi C. Targeting of endoplasmic reticulum (ER) stress in gliomas. Pharmacol Res. 2020;157:104823. DOI: 10.1016/j.phrs.2020.104823

[182] Markouli M., Strepkos D., Papavassiliou A.G., Piperi C. Targeting of endoplasmic reticulum (ER) stress in gliomas // Pharmacol. Res. 2020. Vol. 157. P. 104823. DOI: 10.1016/j.phrs.2020.104823

[183] 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. DOI: 10.1016/j.pharep.2017.03.008

[184] Jakubowicz-Gil J., Bądziul D., Langner E. et al. Temozolomide and sorafenib as programmed cell death inducers of human glioma cells // Pharmacol. Rep. 2017. Vol. 69, No. 4. P. 779–787. DOI: 10.1016/j.pharep.2017.03.008

[185] Jin F, Zhao L, Guo Y-J, et al. Influence of Etoposide on anti-apoptotic and multidrug resistance-associated protein genes in CD133 positive U251 glioblastoma stem-like cells. Brain Res. 2010;1336:103–111. DOI: 10.1016/j.brainres.2010.04.005

[186] Jin F., Zhao L., Guo Y.-J. et al. Influence of Etoposide on anti-apoptotic and multidrug resistance-associated protein genes in CD133 positive U251 glioblastoma stem-like cells // Brain Res. 2010. Vol. 1336. P. 103–111. DOI: 10.1016/j.brainres.2010.04.005

[187] Zheng LT, Lee S, Yin GN, et al. Down-regulation of lipocalin 2 contributes to chemoresistance in glioblastoma cells. J Neurochem. 2009;111(5):1238–1251. DOI: 10.1111/j.1471-4159.2009.06410.x

[188] Zheng L.T., Lee S., Yin G.N. et al. Down-regulation of lipocalin 2 contributes to chemoresistance in glioblastoma cells // J. Neurochem. 2009. Vol. 111, No. 5. P. 1238–1251. DOI: 10.1111/j.1471-4159.2009.06410.x

[189] Zeng L, Kang C, Di C, et al. The adherens junction-associated protein 1 is a negative transcriptional regulator of MAGEA2, which potentiates temozolomide-induced apoptosis in GBM. Int J Oncol. 2014;44(4):1243–1251. DOI: 10.3892/ijo.2014.2277

[190] Zeng L., Kang C., Di C. et al. The adherens junction-associated protein 1 is a negative transcriptional regulator of MAGEA2, which potentiates temozolomide-induced apoptosis in GBM // Int. J. Oncol. 2014. Vol. 44, No. 4. P. 1243–1251. DOI: 10.3892/ijo.2014.2277

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