Abstract
Glioma, as one of the most severe human malignancies, is defined as the Central Nervous System’s (CNS) tumors. Glioblastoma (GBM) in this regard, is the most malignant type of gliomas. There are multiple therapeutic strategies to cure GBM, for which chemotherapy is often the first-line treatment. Still, various cellular processes, such as uncontrolled proliferation, invasion and metastasis, may disturb the treatment efficacy. Drug resistance is another process in this way, which can also cause undesirable effects. Thereupon, identifying the mechanisms, involved in developing drug resistance and the relevant mechanisms can be very helpful in GBM management. The discovery of exosomal non-coding RNAs (ncRNAs), RNA molecules that can be transferred between the cells and different tissues using the exosomes, was a milestone in this regard. It has been revealed that the key exosomal ncRNAs, including circular RNAs, microRNAs, and long ncRNAs, are able to modulate GBM drug resistance through different signaling pathways or by affecting regulatory proteins and their corresponding genes. Nowadays, researchers are trying to overcome the limitations of chemotherapy by targeting these RNA molecules. Accordingly, this review aims to clarify the substantial roles of exosomal ncRNAs in GBM drug resistance and involved mechanisms.
Similar content being viewed by others
Data availability
All related data are deposited in the manuscript.
References
Bark JM, Kulasinghe A, Chua B, Day BW, Punyadeera C (2020) Circulating biomarkers in patients with glioblastoma. Br J Cancer 122(3):295–305
Louis DN, Perry A, Reifenberger G, Von Deimling A, Figarella-Branger D, Cavenee WK et al (2016) The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol 131(6):803–820
Le Rhun E, Preusser M, Roth P, Reardon DA, van den Bent M, Wen P et al (2019) Molecular targeted therapy of glioblastoma. Cancer Treat Rev 80:101896
Alexander BM, Cloughesy TF (2017) Adult glioblastoma. J Clin Oncol 35(21):2402–2409
Ostrom QT, Gittleman H, Fulop J, Liu M, Blanda R, Kromer C et al (2015) CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2008–2012. Neuro Oncol 17(4):iv1–iv62
Jackson CM, Choi J, Lim M (2019) Mechanisms of immunotherapy resistance: lessons from glioblastoma. Nat Immunol 20(9):1100–1109
Davis FG, Smith TR, Gittleman HR, Ostrom QT, Kruchko C, Barnholtz-Sloan JS (2020) Glioblastoma incidence rate trends in Canada and the United States compared with England, 1995–2015. Neuro Oncology 22(2):301–302
Yin Aa, Zhang Lh, Cheng Jx, Dong Y, Liu Bl, Han N et al (2013) Radiotherapy plus concurrent or sequential temozolomide for glioblastoma in the elderly: a meta-analysis. PLoS ONE 8(9):e74242
Stupp R, Taillibert S, Kanner AA, Kesari S, Steinberg DM, Toms SA et al (2015) Maintenance therapy with tumor-treating fields plus temozolomide vs temozolomide alone for glioblastoma: a randomized clinical trial. JAMA 314(23):2535–2543
Perry JR, Laperriere N, O’Callaghan CJ, Brandes AA, Menten J, Phillips C et al (2017) Short-course radiation plus temozolomide in elderly patients with glioblastoma. N Engl J Med 376(11):1027–1037
Vredenburgh JJ, Desjardins A, Reardon DA, Peters KB, Herndon JE, Marcello J et al (2011) The addition of bevacizumab to standard radiation therapy and temozolomide followed by bevacizumab, temozolomide, and irinotecan for newly diagnosed glioblastoma. Clin Cancer Res 17(12):4119–4124
Chamberlain MC, Johnston SK (2010) Salvage therapy with single agent bevacizumab for recurrent glioblastoma. J Neurooncol 96(2):259–269
Kreisl TN, Kim L, Moore K, Duic P, Royce C, Stroud I et al (2009) Phase II trial of single-agent bevacizumab followed by bevacizumab plus irinotecan at tumor progression in recurrent glioblastoma. J Clin Oncol 27(5):740
Eramo A, Ricci-Vitiani L, Zeuner A, Pallini R, Lotti F, Sette G et al (2006) Chemotherapy resistance of glioblastoma stem cells. Cell Death Differ 13(7):1238–1241
Ricci-Vitiani L, Pedini F, Mollinari C, Condorelli G, Bonci D, Bez A et al (2004) Absence of caspase 8 and high expression of PED protect primitive neural cells from cell death. J Exp Med 200(10):1257–1266
Haar CP, Hebbar P, Wallace GC, Das A, Vandergrift WA, Smith JA et al (2012) Drug resistance in glioblastoma: a mini review. Neurochem Res 37(6):1192–1200
Yao RW, Wang Y, Chen LL (2019) Cellular functions of long noncoding RNAs. Nat Cell Biol 21(5):542–551
Cheng J, Meng J, Zhu L, Peng Y (2020) Exosomal noncoding RNAs in glioma: biological functions and potential clinical applications. Mol Cancer 19(1):1–14
Sherafatian M, Mowla SJ (2017) The origins and evolutionary history of human non-coding RNA regulatory networks. J Bioinform Comput Biol 15(02):1750005
Ponting CP, Oliver PL, Reik W (2009) Evolution and functions of long noncoding RNAs. Cell 136(4):629–641
Nie J-H, Li T-X, Zhang X-Q, Liu J (2019) Roles of non-coding RNAs in normal human brain development, brain tumor, and neuropsychiatric disorders. Noncoding RNA 5(2):36
Zhu L, Liu X, Pu W, Peng Y (2018) tRNA-derived small non-coding RNAs in human disease. Cancer Lett 419:1–7
Zhu L, Li J, Gong Y, Wu Q, Tan S, Sun D et al (2019) Exosomal tRNA-derived small RNA as a promising biomarker for cancer diagnosis. Mol Cancer 18(1):74
Li B, Hong J, Hong M, Wang Y, Yu T, Zang S et al (2019) piRNA-823 delivered by multiple myeloma-derived extracellular vesicles promoted tumorigenesis through re-educating endothelial cells in the tumor environment. Oncogene 38(26):5227–5238
Davis ME (2016) Glioblastoma: overview of disease and treatment. Clin J Oncol Nurs 20(5):S2
Thakkar JP, Dolecek TA, Horbinski C, Ostrom QT, Lightner DD, Barnholtz-Sloan JS et al (2014) Epidemiologic and molecular prognostic review of glioblastoma. Cancer Epidemiol Biomarkers Prev 23(10):1985–1996
Lovely MP, Stewart-Amidei C, Arzbaecher J, Bell S, Maher ME, Maida M et al (2014) Care of the adult patient with a brain tumor. J Neurosci Nurs 46(6):367–369
Phillips HS, Kharbanda S, Chen R, Forrest WF, Soriano RH, Wu TD et al (2006) Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 9(3):157–173
Ellor SV, Pagano-Young TA, Avgeropoulos NG (2014) Glioblastoma: background, standard treatment paradigms, and supportive care considerations. SAGE Publications Sage CA, Los Angeles
Alifieris C, Trafalis DT (2015) Glioblastoma multiforme: pathogenesis and treatment. Pharmacol Ther 152:63–82
Young RM, Jamshidi A, Davis G, Sherman JH (2015) Current trends in the surgical management and treatment of adult glioblastoma. Ann Transl Med. https://doi.org/10.3978/j.issn.2305-5839.2015.05.10
Perry J, Zinman L, Chambers A, Spithoff K, Lloyd N, Laperriere N et al (2006) The use of prophylactic anticonvulsants in patients with brain tumours—a systematic review. Curr Opin 13(6):222
Schiff D, Lee EQ, Nayak L, Norden AD, Reardon DA, Wen PY (2015) Medical management of brain tumors and the sequelae of treatment. Neuro Oncol 17(4):488–504
Nabors LB, Portnow J, Ammirati M, Baehring J, Brem H, Brown P et al (2015) Network NCC. Clinical Practice Guidelines in Oncology: Central nervous system cancers, Version 1.2015. J Natl Compr Canc Netw 13(10):1191–1202
Wilson TA, Karajannis MA, Harter DH (2014) Glioblastoma multiforme: state of the art and future therapeutics. Surg Neurol Int 5:64
Ostrom QT, Bauchet L, Davis FG, Deltour I, Fisher JL, Langer CE et al (2014) The epidemiology of glioma in adults: a “state of the science” review. Neuro Oncol 16(7):896–913
Baietti MF, Zhang Z, Mortier E, Melchior A, Degeest G, Geeraerts A et al (2012) Syndecan–syntenin–ALIX regulates the biogenesis of exosomes. Nat Cell Biol 14(7):677–685
McAndrews KM, Kalluri R (2019) Mechanisms associated with biogenesis of exosomes in cancer. Mol Cancer 18(1):52
Zhang Y, Liu Y, Liu H, Tang WH (2019) Exosomes: biogenesis, biologic function and clinical potential. Cell Biosci 9(1):19
Barile L, Vassalli G (2017) Exosomes: therapy delivery tools and biomarkers of diseases. Pharmacol Ther 174:63–78
Kalluri R (2016) The biology and function of exosomes in cancer. J Clin Invest 126(4):1208–1215
Gangoda L, Boukouris S, Liem M, Kalra H, Mathivanan S (2015) Extracellular vesicles including exosomes are mediators of signal transduction: are they protective or pathogenic? Proteomics 15(2–3):260–271
Greening DW, Gopal SK, Xu R, Simpson RJ, Chen W (2015) Exosomes and their roles in immune regulation and cancer. Semin Cell Dev Biol 40:72–81. https://doi.org/10.1016/j.semcdb.2015.02.009
Lässer C, O’Neil SE, Shelke GV, Sihlbom C, Hansson SF, Gho YS et al (2016) Exosomes in the nose induce immune cell trafficking and harbour an altered protein cargo in chronic airway inflammation. J Transl Med 14(1):181
Kishore R, Garikipati VNS, Gumpert A (2016) Tiny shuttles for information transfer: exosomes in cardiac health and disease. J Cardiovasc Transl Res 9(3):169–175
Silva J, Garcia V, Rodriguez M, Compte M, Cisneros E, Veguillas P et al (2012) Analysis of exosome release and its prognostic value in human colorectal cancer. Genes Chromosomes Cancer 51(4):409–418
Mathieu M, Martin-Jaular L, Lavieu G, Thery C (2019) Specificities of secretion and uptake of exosomes and other extracellular vesicles for cell-to-cell communication. Nat Cell Biol 21(1):9–17
Bebelman MP, Smit MJ, Pegtel DM, Baglio SR (2018) Biogenesis and function of extracellular vesicles in cancer. Pharmacol Ther 188:1–11
Kalluri R, LeBleu VS (2020) The biology, function, and biomedical applications of exosomes. Science 367(6478):eaau6977. https://doi.org/10.1126/science.aau6977
Mahboobeh Z, Pegah M, Fatemeh S, Elham K, Hanieh A, Milad R et al (2020) lncRNA ZEB2-AS1: a promising biomarker in human cancers. IUBMB Life 72(9):1891–1899
Liu J, Wu J, Li L, Li T, Wang J (2020) The role of exosomal non-coding RNAs in coronary artery disease. Front Pharmacol. https://doi.org/10.3389/fphar.2020.603104
Jalali S, Bhartiya D, Lalwani MK, Sivasubbu S, Scaria V (2013) Systematic transcriptome wide analysis of lncRNA-miRNA interactions. PLoS ONE 8(2):e53823
Hanna J, Hossain GS, Kocerha J (2019) The potential for microRNA therapeutics and clinical research. Front Genet 10:478
Beermann J, Piccoli M-T, Viereck J, Thum T (2016) Non-coding RNAs in development and disease: background, mechanisms, and therapeutic approaches. Physiol Rev 96(4):1297–1325
Viereck J, Bang C, Foinquinos A, Thum T (2014) Regulatory RNAs and paracrine networks in the heart. Cardiovasc Res 102(2):290–301
Hajjari M, Khoshnevisan A, Shin YK (2014) Molecular function and regulation of long non-coding RNAs: paradigms with potential roles in cancer. Tumor Biol 35(11):10645–10663
Li Q, Shao Y, Zhang X, Zheng T, Miao M, Qin L et al (2015) Plasma long noncoding RNA protected by exosomes as a potential stable biomarker for gastric cancer. Tumor Biol 36(3):2007–2012
Zheng R, Du M, Wang X, Xu W, Liang J, Wang W et al (2018) Exosome–transmitted long non-coding RNA PTENP1 suppresses bladder cancer progression. Mol Cancer 17(1):143
Tang Y, Bao J, Hu J, Liu L, Xu DY (2020) Circular RNA in cardiovascular disease: expression, mechanisms and clinical prospects. J Cell Mol Med 25(4):1817–1824
Xia L, Song M, Sun M, Wang F, Yang C (2018) Circular RNAs as biomarkers for cancer. Circular RNAs: biogenesis and functions. Springer, Singapore, pp 171–187
Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, Rybak A et al (2013) Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495(7441):333–338
Hsiao K-Y, Sun HS, Tsai SJ (2017) Circular RNA–new member of noncoding RNA with novel functions. Exp Biol Med 242(11):1136–1141
Guo JU, Agarwal V, Guo H, Bartel DP (2014) Expanded identification and characterization of mammalian circular RNAs. Genome Biol 15(7):409
Rooj AK, Mineo M, Godlewski J (2016) MicroRNA and extracellular vesicles in glioblastoma: small but powerful. Brain Tumor Pathol 33(2):77–88
Xie Y, Dang W, Zhang S, Yue W, Yang L, Zhai X et al (2019) The role of exosomal noncoding RNAs in cancer. Mol Cancer 18(1):37
Stupp R, Mason WP, Van Den Bent MJ, Weller M, Fisher B, Taphoorn MJ et al (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352(10):987–996
Qazi M, Vora P, Venugopal C, Sidhu S, Moffat J, Swanton C et al (2017) Intratumoral heterogeneity: pathways to treatment resistance and relapse in human glioblastoma. Ann Oncol 28(7):1448–1456
Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB et al (2006) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444(7120):756–760
Yang J-K, Yang J-P, Tong J, Jing S-Y, Fan B, Wang F et al (2017) Exosomal miR-221 targets DNM3 to induce tumor progression and temozolomide resistance in glioma. J Neurooncol 131(2):255–265
Fan Q, Yang L, Zhang X, Peng X, Wei S, Su D et al (2018) The emerging role of exosome-derived non-coding RNAs in cancer biology. Cancer Lett 414:107–115
Yoshimoto K, Mizoguchi M, Hata N, Murata H, Hatae R, Amano T et al (2012) Complex DNA repair pathways as possible therapeutic targets to overcome temozolomide resistance in glioblastoma. Front Oncol 2:186
Zeng A, Wei Z, Yan W, Yin J, Huang X, Zhou X et al (2018) Exosomal transfer of miR-151a enhances chemosensitivity to temozolomide in drug-resistant glioblastoma. Cancer Lett 436:10–21
Zhang Z, Yin J, Lu C, Wei Y, Zeng A, You Y (2019) Exosomal transfer of long non-coding RNA SBF2-AS1 enhances chemoresistance to temozolomide in glioblastoma. J Exp Clin Cancer Res 38(1):1–16
Yue X, Lan F, Xia T (2019) Hypoxic glioma cell-secreted exosomal miR-301a activates Wnt/β-catenin signaling and promotes radiation resistance by targeting TCEAL7. Mol Ther 27(11):1939–1949
Parney IF, Chang SM (2003) Current chemotherapy for glioblastoma. Cancer J 9(3):149–156
Banelli B, Forlani A, Allemanni G, Morabito A, Pistillo MP, Romani M (2017) MicroRNA in glioblastoma: an overview. Int J Genom. https://doi.org/10.1155/2017/7639084
D’Atri S, Graziani G, Lacal PM, Nisticò V, Gilberti S, Faraoni I et al (2000) Attenuation of O 6-methylguanine-DNA methyltransferase activity and mRNA levels by cisplatin and temozolomide in Jurkat cells. J Pharmacol Exp Ther 294(2):664–671
Buckner JC, Ballman KV, Michalak JC, Burton GV, Cascino TL, Schomberg PJ et al (2006) Phase III trial of carmustine and cisplatin compared with carmustine alone and standard radiation therapy or accelerated radiation therapy in patients with glioblastoma multiforme: north central cancer treatment group 93–72-52 and southwest oncology group 9503 Trials. J Clin Oncol 24(24):3871–3879
Shen D-W, Pouliot LM, Hall MD, Gottesman MM (2012) Cisplatin resistance: a cellular self-defense mechanism resulting from multiple epigenetic and genetic changes. Pharmacol Rev 64(3):706–721
Chen X, Zhang Y, Shi Y, Lian H, Tu H, Han S et al (2015) MiR-873 acts as a novel sensitizer of glioma cells to cisplatin by targeting Bcl-2. Int J Oncol 47(4):1603–1611
Wong STS, Zhang XQ, Zhuang JTF, Chan HL, Li CH, Leung GKK (2012) MicroRNA-21 inhibition enhances in vitro chemosensitivity of temozolomide-resistant glioblastoma cells. Anticancer Res 32(7):2835–2841
Shea A, Harish V, Afzal Z, Chijioke J, Kedir H, Dusmatova S et al (2016) MicroRNAs in glioblastoma multiforme pathogenesis and therapeutics. Cancer Med 5(8):1917–1946
Li Y, Li W, Yang Y, Lu Y, He C, Hu G et al (2009) MicroRNA-21 targets LRRFIP1 and contributes to VM-26 resistance in glioblastoma multiforme. Brain Res 1286:13–18
Costa PM, Cardoso AL, Nóbrega C, de Pereira Almeida LF, Bruce JN, Canoll P et al (2013) MicroRNA-21 silencing enhances the cytotoxic effect of the antiangiogenic drug sunitinib in glioblastoma. Hum Mol Genet 22(5):904–918
Zhang S, Han L, Wei J, Shi Z, Pu P, Zhang J et al (2015) Combination treatment with doxorubicin and microRNA-21 inhibitor synergistically augments anticancer activity through upregulation of tumor suppressing genes. Int J Oncol 46(4):1589–1600
Barker CA, Chang M, Chou JF, Zhang Z, Beal K, Gutin PH et al (2012) Radiotherapy and concomitant temozolomide may improve survival of elderly patients with glioblastoma. J Neurooncol 109(2):391–397
Li RY, Chen LC, Zhang HY, Du WZ, Feng Y, Wang HB et al (2013) MiR-139 inhibits Mcl-1 expression and potentiates TMZ-induced apoptosis in glioma. CNS Neurosci Ther 19(7):477–483
Wang L, Shi Zm, Jiang Cf, Liu X, Chen Qd, Qian X et al (2014) MiR-143 acts as a tumor suppressor by targeting N-RAS and enhances temozolomide-induced apoptosis in glioma. Oncotarget 5(14):5416–5427
Ujifuku K, Mitsutake N, Takakura S, Matsuse M, Saenko V, Suzuki K et al (2010) MiR-195, miR-455-3p and miR-10a∗ are implicated in acquired temozolomide resistance in glioblastoma multiforme cells. Cancer Lett 296(2):241–248
Li1ABCDEF W-Q, Li2ABCDEFG Y-M, Tao2BCD B-B, Lu2ABCDEF Y-C, Hu2CDF G-H, Liu1DF H-M, et al. (2010) Downregulation of ABCG2 expression in glioblastoma cancer stem cells with miRNA-328 may decrease their chemoresistance. Med Sci Monit 16(10):30
Xiao S, Yang Z, Qiu X, Lv R, Liu J, Wu M et al (2016) miR-29c contribute to glioma cells temozolomide sensitivity by targeting O6-methylguanine-DNA methyltransferases indirectly. Oncotarget 7(31):50229
Kushwaha D, Ramakrishnan V, Ng K, Steed T, Nguyen T, Futalan D et al (2014) A genome-wide miRNA screen revealed miR-603 as a MGMT-regulating miRNA in glioblastomas. Oncotarget 5(12):4026
Durmus S, Hendrikx JJ, Schinkel AH (2015) Apical ABC transporters and cancer chemotherapeutic drug disposition. ABC transporters and cancer. Elsevier, Amsterdam, pp 1–41
Cunha PP, Costa PM, Morais CM, Lopes IR, Cardoso AM, Cardoso AL et al (2017) High-throughput screening uncovers miRNAs enhancing glioblastoma cell susceptibility to tyrosine kinase inhibitors. Hum Mol Genet 26(22):4375–4387
Garofalo M, Croce CM (2011) microRNAs: Master regulators as potential therapeutics in cancer. Annu Rev Pharmacol Toxicol 51:25–43
Ghaemmaghami AB, Mahjoubin-Tehran M, Movahedpour A, Morshedi K, Sheida A, Taghavi SP et al (2020) Role of exosomes in malignant glioma: microRNAs and proteins in pathogenesis and diagnosis. Cell Commun Signal 18(1):1–19
Yin J, Zeng A, Zhang Z, Shi Z, Yan W, You Y (2019) Exosomal transfer of miR-1238 contributes to temozolomide-resistance in glioblastoma. EBioMedicine 42:238–251
Shi L, Cheng Z, Zhang J, Li R, Zhao P, Fu Z et al (2008) hsa-mir-181a and hsa-mir-181b function as tumor suppressors in human glioma cells. Brain Res 1236:185–193
Li CH, Chen Y (2013) Targeting long non-coding RNAs in cancers: progress and prospects. Int J Biochem Cell Biol 45(8):1895–1910
de los Santos MC, Dragomir MP, Calin GA (2019) The role of exosomal long non-coding RNAs in cancer drug resistance. Cancer Drug Resist (Alhambra, Calif) 2:1178
Chen F, Wang N, Tan HY, Guo W, Zhang C, Feng Y (2019) The functional roles of exosomes-derived long non-coding RNA in human cancer. Cancer Biol Ther 20(5):583–592
Taber A, Christensen E, Lamy P, Nordentoft I, Prip F, Lindskrog SV et al (2020) Molecular correlates of cisplatin-based chemotherapy response in muscle invasive bladder cancer by integrated multi-omics analysis. Nat Commun 11(1):1–15
Xi J, Sun Q, Ma L, Kang J (2018) Long non-coding RNAs in glioma progression. Cancer Lett 419:203–209
Liu Q, Sun S, Yu W, Jiang J, Zhuo F, Qiu G et al (2015) Altered expression of long non-coding RNAs during genotoxic stress-induced cell death in human glioma cells. J Neurooncol 122(2):283–292
Jiang P, Wang P, Sun X, Yuan Z, Zhan R, Ma X et al (2016) Knockdown of long noncoding RNA H19 sensitizes human glioma cells to temozolomide therapy. Onco Targets Ther 9:3501
Liao Y, Shen L, Zhao H, Liu Q, Fu J, Guo Y et al (2017) LncRNA CASC2 interacts with miR-181a to modulate glioma growth and resistance to TMZ through PTEN pathway. J Cell Biochem 118(7):1889–1899
Li H, Yuan X, Yan D, Li D, Guan F, Dong Y et al (2017) Long non-coding RNA MALAT1 decreases the sensitivity of resistant glioblastoma cell lines to temozolomide. Cell Physiol Biochem 42(3):1192–1201
Wang J, Yang S, Ji Q, Li Q, Zhou F, Li Y et al (2020) Long non-coding RNA EPIC1 promotes cell proliferation and motility and drug resistance in glioma. Mol Ther Oncol 17:130–137. https://doi.org/10.1016/j.omto.2020.03.011
Yan Y, Xu Z, Chen X, Wang X, Zeng S, Zhao Z et al (2019) Novel function of lncRNA ADAMTS9-AS2 in promoting temozolomide resistance in glioblastoma via upregulating the FUS/MDM2 ubiquitination axis. Front Cell Dev Biol 7:217
Hu Y, Zhu QN, Deng JL, Li ZX, Wang G, Zhu YS (2018) Emerging role of long non-coding RNAs in cisplatin resistance. Onco Targets Ther 11:3185
Pang JCS, Li KKW, Lau KM, Ng YL, Wong J, Chung NYF et al (2010) KIAA0495/PDAM is frequently downregulated in oligodendroglial tumors and its knockdown by siRNA induces cisplatin resistance in glioma cells. Brain Pathol 20(6):1021–1032
Ma B, Yuan Z, Zhang L, Lv P, Yang T, Gao J et al (1864) 2017 Long non-coding RNA AC023115. 3 suppresses chemoresistance of glioblastoma by reducing autophagy. Biochim Biophys Acta Mol Cell Res 8:1393–1404
García-Claver A, Lorente M, Mur P, Campos-Martín Y, Mollejo M, Velasco G et al (2013) Gene expression changes associated with erlotinib response in glioma cell lines. Eur J Cancer 49(7):1641–1653
Kino T, Hurt DE, Ichijo T, Nader N, Chrousos GP (2010) Noncoding RNA gas5 is a growth arrest–and starvation-associated repressor of the glucocorticoid receptor. Sci Signal 3(107):ra8. https://doi.org/10.1126/scisignal.2000568
Zhang XQ, Sun S, Lam KF, Kiang KMY, Pu JKS, Ho ASW et al (2013) A long non-coding RNA signature in glioblastoma multiforme predicts survival. Neurobiol Dis 58:123–131
Du P, Zhao H, Peng R, Liu Q, Yuan J, Peng G et al (2017) LncRNA-XIST interacts with miR-29c to modulate the chemoresistance of glioma cell to TMZ through DNA mismatch repair pathway. Biosci Rep. https://doi.org/10.1042/BSR20170696
Chen Z, Shi T, Zhang L, Zhu P, Deng M, Huang C et al (2016) Mammalian drug efflux transporters of the ATP binding cassette (ABC) family in multidrug resistance: a review of the past decade. Cancer Lett 370(1):153–164
Liu K, Gao L, Ma X, Huang JJ, Chen J, Zeng L et al (2020) Long non-coding RNAs regulate drug resistance in cancer. Mol Cancer 19(1):1–13
Hua X, Sun Y, Chen J, Wu Y, Sha J, Han S et al (2019) Circular RNAs in drug resistant tumors. Biomed Pharmacother 118:109233
Zaiou M (2019) Circular RNAs in hypertension: challenges and clinical promise. Hypertens Res 42(11):1653–1663
Ding C, Yi X, Wu X, Bu X, Wang D, Wu Z et al (2020) Exosome-mediated transfer of circRNA CircNFIX enhances temozolomide resistance in glioma. Cancer Lett 479:1–12. https://doi.org/10.1016/j.canlet.2020.03.002
Zhao C, Gao Y, Guo R, Li H, Yang B (2019) Microarray expression profiles and bioinformatics analysis of mRNAs, lncRNAs, and circRNAs in the secondary temozolomide-resistant glioblastoma. Invest New Drugs 38(5):1227–1235. https://doi.org/10.1007/s10637-019-00884-3
Ho KH, Cheng CH, Chou CM, Chen PH, Liu AJ, Lin CW et al (2019) miR-140 targeting CTSB signaling suppresses the mesenchymal transition and enhances temozolomide cytotoxicity in glioblastoma multiforme. Pharmacol Res 147:104390
Wei Y, Lu C, Zhou P, Zhao L, Lyu X, Yin J et al (2020) EIF4A3-induced circular RNA ASAP1 (circASAP1) promotes tumorigenesis and temozolomide resistance of glioblastoma via NRAS/MEK1/ERK1/2 signaling. Neuro Oncol 23(4):611–624. https://doi.org/10.1093/neuonc/noaa214
Yin H, Cui X (2020) Knockdown of circHIPK3 facilitates temozolomide sensitivity in glioma by regulating cellular behaviors through miR-524–5p/KIF2A-mediated PI3K/AKT pathway. Cancer Biother Radiopharm. https://doi.org/10.1089/cbr.2020.3575
Hua L, Huang L, Zhang X, Feng H (2020) Downregulation of hsa_circ_0000936 sensitizes resistant glioma cells to temozolomide by sponging miR-1294. J Biosci 45(1):1–11
Barbagallo D, Caponnetto A, Brex D, Mirabella F, Barbagallo C, Lauretta G et al (2019) CircSMARCA5 regulates VEGFA mRNA splicing and angiogenesis in glioblastoma multiforme through the binding of SRSF1. Cancers 11(2):194
Author information
Authors and Affiliations
Contributions
The authors confirm contribution to the paper as follows: study conception and design: AM, AS; data collection: MK, MS; analysis and interpretation of results: SHM, BN, NK, PN; draft manuscript preparation: OV, MT.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that there is no conflict of interests.
Informed consent
This article does not contain any studies with human participants.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Movahedpour, A., Khatami, S.H., Khorsand, M. et al. Exosomal noncoding RNAs: key players in glioblastoma drug resistance. Mol Cell Biochem 476, 4081–4092 (2021). https://doi.org/10.1007/s11010-021-04221-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11010-021-04221-2