Abstract
MicroRNAs (miRNAs) are non-coding RNAs with only 20–22 nucleic acids that inhibit gene transcription and translation by binding to mRNA. MiRNAs have a diverse set of target genes and can alter most physiological processes, including cell cycle checkpoints, cell survival, and cell death mechanisms, affecting the growth, development, and invasion of various cancers, including gliomas. So optimum management of miRNA expression is essential for preserving a normal biological environment. Due to their small size, stability, and capability of specifically targeting oncogenes, miRNAs have emerged as a promising marker and new biopharmaceutical targeted therapy for glioma patients. This review focuses on the most common miRNAs associated with gliomagenesis and development by controlling glioma-determining markers such as angiogenesis. We also summarized the recent research about miRNA effects on signaling pathways, their mechanistic role and cellular targets in the development of gliomas angiogenesis. Strategies for miRNA-based therapeutic targets, as well as limitations in clinical applications, are also discussed.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
Not applicable.
Abbreviations
- NcRNAs:
-
Non-coding RNAs
- MiRNAs:
-
MicroRNAs
- VEGF:
-
Vascular endothelial growth factor
- MMPs:
-
Matrix metalloproteinases
- TME:
-
Tumor microenvironment
- EC:
-
Endothelial cell
- CNS:
-
Central nervous system
- HUVECs:
-
Human umbilical vein endothelial cells
- RBPs:
-
RNA-binding proteins
- GBM:
-
Glioblastoma multiforme
- RISC:
-
RNA-induced silencing complex
- ECM:
-
Extracellular matrix components
- FGF:
-
Fibroblast growth factor
- HIF1-α:
-
Hypoxia-inducible factor 1-alpha
- LRIG2:
-
Leucine-rich repeats and immunoglobulin-like domains protein 2
References
Abdellatif M (2012) Differential expression of microRNAs in different disease states. Circ Res 110(4):638–650. https://doi.org/10.1161/CIRCRESAHA.111.247437
Achkar NP, Cambiagno DA, Manavella PA (2016) miRNA biogenesis: a dynamic pathway. Trends Plant Sci 21(12):1034–1044. https://doi.org/10.1016/j.tplants.2016.09.003
Alizadeh-Fanalou S, Hosseinkhani S, Nazarizadeh A, Ezzati-Mobaser S, Hesari Z, Aziminezhadan P, Nourbakhsh M (2021) MiR-613 promotes cell death in breast cancer cells by downregulation of nicotinamide phosphoribosyltransferase and reduction of NAD. DNA Cell Biol 40(7):1026–1036. https://doi.org/10.1089/dna.2021.0330
Alkan AH, Akgül B (2022) Endogenous miRNA sponges. Mirnomics 91:104. https://doi.org/10.1007/978-1-0716-1170-8_5
Alles J, Fehlmann T, Fischer U, Backes C, Galata V, Minet M, Lenhof H-P et al (2019) An estimate of the total number of true human miRNAs. Nucleic Acids Res 47(7):3353–3364. https://doi.org/10.1093/nar/gkz097
Amulya E, Sikder A, Vambhurkar G, Shah S, Khatri DK, Raghuvanshi RS, Srivastava S et al (2023) Nanomedicine based strategies for oligonucleotide traversion across the blood–brain barrier. J Control Release 354:554–571. https://doi.org/10.1016/j.jconrel.2023.01.031
An L, Liu Y, Wu A, Guan Y (2013) microRNA-124 inhibits migration and invasion by down-regulating ROCK1 in glioma. PLoS ONE 8(7):e69478. https://doi.org/10.1371/journal.pone.0069478
Arab S, Ghasemi S, Ghanbari A, Bahraminasab M, Satari A, Mousavi M, Asgharzade S et al (2021) Chemopreventive effect of spirulina microalgae on an animal model of glioblastoma via down-regulation of PI3K/AKT/mTOR and up-regulation of miR-34a/miR-125B expression. Phytotherapy Res 35(11):6452–6461. https://doi.org/10.1002/ptr.7298
Asangani IA, Rasheed SA, Nikolova D, Leupold J, Colburn N, Post S, Allgayer H (2008) MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 27(15):2128–2136. https://doi.org/10.1038/sj.onc.1210856
Balandeh E, Mohammadshafie K, Mahmoudi Y, Hossein Pourhanifeh M, Rajabi A, Bahabadi ZR, Mirzaei H et al (2021) Roles of non-coding RNAs and angiogenesis in glioblastoma. Front Cell Dev Biol 25:43. https://doi.org/10.3389/fcell.2021.716462
Bandres E, Agirre X, Bitarte N, Ramirez N, Zarate R, Roman-Gomez J, Garcia-Foncillas J et al (2009) Epigenetic regulation of microRNA expression in colorectal cancer. Int J Cancer 125(11):2737–2743. https://doi.org/10.1002/ijc.24638
Banelli B, Forlani A, Allemanni G, Morabito A, Pistillo MP, Romani M (2017) MicroRNA in glioblastoma: an overview. Int J Genomics 20:17. https://doi.org/10.1155/2017/7639084
Barata P, Sood AK, Hong DS (2016) RNA-targeted therapeutics in cancer clinical trials: current status and future directions. Cancer Treat Rev 50:35–47. https://doi.org/10.1016/j.ctrv.2016.08.004
Bartel DP (2018) Metazoan micrornas. Cell 173(1):20–51. https://doi.org/10.1016/j.cell.2018.03.006
Bergers G, Brekken R, McMahon G, Vu TH, Itoh T, Tamaki K, Werb Z et al (2000) Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2(10):737–744. https://doi.org/10.1038/35036374
Bertoli G, Cava C, Castiglioni I (2015) MicroRNAs: new biomarkers for diagnosis, prognosis, therapy prediction and therapeutic tools for breast cancer. Theranostics 5(10):1122. https://doi.org/10.7150/thno.11543
Beyer S, Fleming J, Meng W, Singh R, Haque SJ, Chakravarti A (2017) The role of miRNAs in angiogenesis, invasion and metabolism and their therapeutic implications in gliomas. Cancers 9(7):85. https://doi.org/10.3390/cancers9070085
Bhootra S, Jill N, Shanmugam G, Rakshit S, Sarkar K (2023) DNA methylation and cancer: transcriptional regulation, prognostic, and therapeutic perspective. Med Oncol 40(2):1–17. https://doi.org/10.1007/s12032-022-01943-1
Blackledge NP, Klose RJ (2021) The molecular principles of gene regulation by Polycomb repressive complexes. Nat Rev Mol Cell Biol 22(12):815–833. https://doi.org/10.1038/s41580-021-00398-y
Borchert GM, Lanier W, Davidson BL (2006) RNA polymerase III transcribes human microRNAs. Nat Struct Mol Biol 13(12):1097–1101. https://doi.org/10.1038/nsmb1167
Bossone SA, Asselin C, Patel AJ, Marcu KB (1992) MAZ, a zinc finger protein, binds to c-MYC and C2 gene sequences regulating transcriptional initiation and termination. Proc Natl Acad Sci 89(16):7452–7456. https://doi.org/10.1073/pnas.89.16.7452
Bouzari B, Mohammadi S, Bokov DO, Krasnyuk II, Hosseini-Fard SR, Hajibaba M, Karampoor S et al (2022) Angioregulatory role of miRNAs and exosomal miRNAs in glioblastoma pathogenesis. Biomed Pharmacother 148:112760. https://doi.org/10.1016/j.biopha.2022.112760
Buruiană A, Florian ȘI, Florian AI, Timiș T-L, Mihu CM, Miclăuș M, Farcaș M et al (2020) The roles of miRNA in glioblastoma tumor cell communication: diplomatic and aggressive negotiations. Int J Mol Sci 21(6):1950. https://doi.org/10.3390/ijms21061950
Camps C, Buffa FM, Colella S, Moore J, Sotiriou C, Sheldon H, Ragoussis J et al (2008) hsa-miR-210 Is induced by hypoxia and is an independent prognostic factor in breast cancer. Clin Cancer Res 14(5):1340–1348. https://doi.org/10.1158/1078-0432.CCR-07-1755
Cannell IG, Kong YW, Bushell M (2008) How do microRNAs regulate gene expression? Biochem Soc Trans 36(6):1224–1231. https://doi.org/10.1042/BST0361224
Carmeliet P (2005) Angiogenesis in life, disease and medicine. Nature 438(7070):932–936. https://doi.org/10.1038/nature04478
Cha S-T, Chen P-S, Johansson G, Chu C-Y, Wang M-Y, Jeng Y-M, Jee S-H et al (2010) MicroRNA-519c suppresses hypoxia-inducible factor-1α expression and tumor angiogenesis MicroRNA-519c suppresses tumor angiogenesis. Cancer Res 70(7):2675–2685. https://doi.org/10.1158/0008-5472.CAN-09-2448
Cha J, Kang S-G, Kim P (2016) Strategies of mesenchymal invasion of patient-derived brain tumors: microenvironmental adaptation. Sci Rep 6(1):1–12. https://doi.org/10.1038/srep24912
Chai Y, Liu J, Zhang Z, Liu L (2016) HuR-regulated lnc RNA NEAT 1 stability in tumorigenesis and progression of ovarian cancer. Cancer Med 5(7):1588–1598. https://doi.org/10.1002/cam4.710
Chakraborty S, Zawieja DC, Davis MJ, Muthuchamy M (2015) MicroRNA signature of inflamed lymphatic endothelium and role of miR-9 in lymphangiogenesis and inflammation. Am J Physiol Cell Physiol 309(10):C680–C692. https://doi.org/10.1152/ajpcell.00122.2015
Chan JA, Krichevsky AM, Kosik KS (2005) MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res 65(14):6029–6033. https://doi.org/10.1158/0008-5472.CAN-05-0137
Chava S, Reynolds CP, Pathania AS, Gorantla S, Poluektova LY, Coulter DW, Challagundla KB et al (2020) miR-15a-5p, miR-15b-5p, and miR-16-5p inhibit tumor progression by directly targeting MYCN in neuroblastoma. Mol Oncol 14(1):180–196. https://doi.org/10.1002/1878-0261.12588
Chen P-S, Su J-L, Hung M-C (2012) Dysregulation of microRNAs in cancer. J Biomed Sci 19(1):1–8. https://doi.org/10.1186/1423-0127-19-90
Chen L, Miao W, Tang X, Zhang H, Wang S, Luo F, Yan J (2013a) The expression and significance of neuropilin-1 (NRP-1) on glioma cell lines and glioma tissues. J Biomed Nanotechnol 9(4):559–563. https://doi.org/10.1166/jbn.2013.1624
Chen L, Zhang R, Li P, Liu Y, Qin K, Fa Z-Q, Jiang X-D et al (2013b) P53-induced microRNA-107 inhibits proliferation of glioma cells and down-regulates the expression of CDK6 and Notch-2. Neurosci Lett 534:327–332. https://doi.org/10.1016/j.neulet.2012.11.047
Chen L, Zhang K, Shi Z, Zhang A, Jia Z, Wang G, Han L et al (2014a) A lentivirus-mediated miR-23b sponge diminishes the malignant phenotype of glioma cells in vitro and in vivo. Oncol Rep 31(4):1573–1580. https://doi.org/10.3892/or.2014.3012
Chen Z, Li D, Cheng Q, Ma Z, Jiang B, Peng R, Wan X et al (2014b) MicroRNA-203 inhibits the proliferation and invasion of U251 glioblastoma cells by directly targeting PLD2. Mol Med Rep 9(2):503–508. https://doi.org/10.3892/mmr.2013.1814
Chen F, Chen L, He H, Huang W, Zhang R, Li P, Jiang X et al (2016a) Up-regulation of microRNA-16 in glioblastoma inhibits the function of endothelial cells and tumor angiogenesis by targeting Bmi-1. Anti-Cancer Agents Med Chem 16(5):609–620. https://doi.org/10.2174/1871520615666150916092251
Chen L, Li Z-Y, Xu S-Y, Zhang X-J, Zhang Y, Luo K, Li W-P (2016b) Upregulation of miR-107 inhibits glioma angiogenesis and VEGF expression. Cell Mol Neurobiol 36(1):113–120. https://doi.org/10.1007/s10571-015-0225-3
Chen X, Yang F, Zhang T, Wang W, Xi W, Li Y, Yang A et al (2019) MiR-9 promotes tumorigenesis and angiogenesis and is activated by MYC and OCT4 in human glioma. J Exp Clin Cancer Res 38(1):1–16. https://doi.org/10.1186/s13046-019-1078-2
Chen M, Medarova Z, Moore A (2021) Role of microRNAs in glioblastoma. Oncotarget 12(17):1707. https://doi.org/10.18632/oncotarget.28039
Chen B, Dragomir MP, Yang C, Li Q, Horst D, Calin GA (2022) Targeting non-coding RNAs to overcome cancer therapy resistance. Signal Transduct Target Ther 7(1):121. https://doi.org/10.1038/s41392-022-00975-3
Condrat CE, Thompson DC, Barbu MG, Bugnar OL, Boboc A, Cretoiu D, Voinea SC et al (2020) miRNAs as biomarkers in disease: latest findings regarding their role in diagnosis and prognosis. Cells 9(2):276. https://doi.org/10.3390/cells9020276
Costa PM, Cardoso AL, Nobrega C, Pereira de Almeida LF, Bruce JN, Canoll P, Pedroso de Lima MC (2013) MicroRNA-21 silencing enhances the cytotoxic effect of the antiangiogenic drug sunitinib in glioblastoma. Hum Mol Genet 22(5):904–918. https://doi.org/10.1093/hmg/dds496
Dai D, Huang W, Lu Q, Chen H, Liu J, Hong B (2018) miR-24 regulates angiogenesis in gliomas. Mol Med Rep 18(1):358–368. https://doi.org/10.3892/mmr.2018.8978
Dalmay T, Edwards D (2006) MicroRNAs and the hallmarks of cancer. Oncogene 25(46):6170–6175. https://doi.org/10.1038/sj.onc.1209911
De Rie D, Abugessaisa I, Alam T, Arner E, Arner P, Ashoor H, Burroughs AM et al (2017) An integrated expression atlas of miRNAs and their promoters in human and mouse. Nat Biotechnol 35(9):872–878. https://doi.org/10.1038/nbt.3947
Dong L, Han C, Zhang H, Gu X, Li J, Wu Y, Wang X (2012) Construction of a recombinant lentivirus containing human microRNA-7-3 and its inhibitory effects on glioma proliferation. Neural Regen Res 7(27):2144. https://doi.org/10.3969/j.issn.1673-5374.2012.27.009
El Fatimy R, Subramanian S, Uhlmann EJ, Krichevsky AM (2017) Genome editing reveals glioblastoma addiction to microRNA-10b. Mol Ther 25(2):368–378. https://doi.org/10.1016/j.ymthe.2016.11.004
Fan Y-C, Mei P-J, Chen C, Miao F-A, Zhang H, Li Z-L (2013) MiR-29c inhibits glioma cell proliferation, migration, invasion and angiogenesis. J Neurooncol 115(2):179–188. https://doi.org/10.1007/s11060-013-1223-2
Faraz M, Herdenberg C, Holmlund C, Henriksson R, Hedman H (2018) A protein interaction network centered on leucine-rich repeats and immunoglobulin-like domains 1 (LRIG1) regulates growth factor receptors. J Biol Chem 293(9):3421–3435. https://doi.org/10.1074/jbc.M117.807487
Folkman J (2002) Role of angiogenesis in tumor growth and metastasis. Paper presented at the Seminars in oncology
Gabriely G, Yi M, Narayan RS, Niers JM, Wurdinger T, Imitola J, Stephens RM et al (2011) Human glioma growth is controlled by microRNA-10b. Cancer Res 71(10):3563–3572. https://doi.org/10.1158/0008-5472.CAN-10-3568
Gao W, Shen H, Liu L, Xu J, Xu J, Shu Y (2011) MiR-21 overexpression in human primary squamous cell lung carcinoma is associated with poor patient prognosis. J Cancer Res Clin Oncol 137(4):557–566. https://doi.org/10.1007/s00432-010-0918-4
Garofalo M, Quintavalle C, Romano G, Mcroce C, Condorelli G (2012) miR221/222 in cancer: their role in tumor progression and response to therapy. Current Mol Med 12(1):27–33. https://doi.org/10.2174/156652412798376170
Garzon R, Garofalo M, Martelli MP, Briesewitz R, Wang L, Fernandez-Cymering C, Haferlach T et al (2008) Distinctive microRNA signature of acute myeloid leukemia bearing cytoplasmic mutated nucleophosmin. Proc Natl Acad Sci 105(10):3945–3950. https://doi.org/10.1073/pnas.0800135105
Glinka Y, Stoilova S, Mohammed N, Prud’homme GJ (2011) Neuropilin-1 exerts co-receptor function for TGF-beta-1 on the membrane of cancer cells and enhances responses to both latent and active TGF-beta. Carcinogenesis 32(4):613–621. https://doi.org/10.1093/carcin/bgq281
Goenka A, Tiek DM, Song X, Iglesia RP, Lu M, Hu B, Cheng S-Y (2022) The role of non-coding RNAs in glioma. Biomedicines 10(8):2031. https://doi.org/10.3390/biomedicines10082031
Guo D, Nilsson J, Haapasalo H, Raheem O, Bergenheim T, Hedman H, Henriksson R (2006) Perinuclear leucine-rich repeats and immunoglobulin-like domain proteins (LRIG1-3) as prognostic indicators in astrocytic tumors. Acta Neuropathol 111(3):238–246. https://doi.org/10.1007/s00401-006-0032-5
Guo Y, Chen Z, Zhang L, Zhou F, Shi S, Feng X, Luo M et al (2008) Distinctive microRNA profiles relating to patient survival in esophageal squamous cell carcinoma. Cancer Res 68(1):26–33. https://doi.org/10.1158/0008-5472.CAN-06-4418
Guo X, Jiao H, Cao L, Meng F (2022) Biological implications and clinical potential of invasion and migration related miRNAs in glioma. Front Integr Neurosci. https://doi.org/10.3389/fnint.2022.989029
Hamerlik P, Lathia JD, Rasmussen R, Wu Q, Bartkova J, Lee M, Lukas J et al (2012) Autocrine VEGF–VEGFR2–Neuropilin-1 signaling promotes glioma stem-like cell viability and tumor growth. J Exp Med 209(3):507–520. https://doi.org/10.1084/jem.20111424
Han J, Denli AM, Gage FH (2012) The enemy within: intronic miR-26b represses its host gene, ctdsp2, to regulate neurogenesis. Genes Dev 26(1):6–10. https://doi.org/10.1101/gad.184416.111
Hanif F, Muzaffar K, Perveen K, Malhi SM, Simjee SU (2017) Glioblastoma multiforme: a review of its epidemiology and pathogenesis through clinical presentation and treatment. Asian Pac J Cancer Prev 18(1):3. https://doi.org/10.22034/APJCP.2017.18.1.3
Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK, Kjems J (2013) Natural RNA circles function as efficient microRNA sponges. Nature 495(7441):384–388. https://doi.org/10.1038/nature11993
Hayes J, Thygesen H, Tumilson C, Droop A, Boissinot M, Hughes TA, Short SC et al (2015) Prediction of clinical outcome in glioblastoma using a biologically relevant nine-microRNA signature. Mol Oncol 9(3):704–714
Hayes J, Thygesen H, Gregory W, Westhead DR, French PJ, Van Den Bent MJ, Short SC et al (2016) A validated microRNA profile with predictive potential in glioblastoma patients treated with bevacizumab. Mol Oncol 10(8):1296–1304. https://doi.org/10.1016/j.molonc.2016.06.004
Hossian A, Sajib M, Tullar PE, Mikelis CM, Mattheolabakis G (2018) Multipronged activity of combinatorial miR-143 and miR-506 inhibits lung cancer cell cycle progression and angiogenesis in vitro. Sci Rep 8(1):1–14. https://doi.org/10.1038/s41598-018-28872-2
Howe JR, Li ES, Streeter SE, Rahme GJ, Chipumuro E, Russo GB, Skelton PD et al (2017) MiR-338–3p regulates neuronal maturation and suppresses glioblastoma proliferation. PLoS ONE 12(5):e0177661. https://doi.org/10.1371/journal.pone.0177661
Hu Q, Liu F, Yan T, Wu M, Ye M, Shi G, Zhu X et al (2019) MicroRNA-576-3p inhibits the migration and proangiogenic abilities of hypoxia-treated glioma cells through hypoxia-inducible factor-1α. Int J Mol Med 43(6):2387–2397. https://doi.org/10.3892/ijmm.2019.4157
Huang T, Alvarez AA, Pangeni RP, Horbinski C, Lu S, Kim S-H, Brenann CW et al (2016) A regulatory circuit of miR-125b/miR-20b and Wnt signalling controls glioblastoma phenotypes through FZD6-modulated pathways. Nat Commun 7(1):1–16. https://doi.org/10.1038/ncomms12885
Huang Y, Zhang H, Wang L, Liu C, Guo M, Tan H, Liu Z (2021) MiR-613 inhibits the proliferation, migration, and invasion of papillary thyroid carcinoma cells by directly targeting TAGLN2. Cancer Cell Int 21(1):1–13. https://doi.org/10.1186/s12935-021-02083-8
Huse JT, Brennan C, Hambardzumyan D, Wee B, Pena J, Rouhanifard SH, Tuschl T et al (2009) The PTEN-regulating microRNA miR-26a is amplified in high-grade glioma and facilitates gliomagenesis in vivo. Genes Dev 23(11):1327–1337. https://doi.org/10.1101/gad.1777409
Huse JT, Phillips HS, Brennan CW (2011) Molecular subclassification of diffuse gliomas: seeing order in the chaos. Glia 59(8):1190–1199. https://doi.org/10.1002/glia.21165
Iorio MV, Croce CM (2012) Causes and consequences of microRNA dysregulation. Cancer J 18(3):215
Iorio MV, Ferracin M, Liu C-G, Veronese A, Spizzo R, Sabbioni S, Campiglio M et al (2005) MicroRNA gene expression deregulation in human breast cancer. Cancer Res 65(16):7065–7070
Iorio MV, Visone R, Di Leva G, Donati V, Petrocca F, Casalini P, Alder H et al (2007) MicroRNA signatures in human ovarian cancer. Cancer Res 67(18):8699–8707
Jain RK, Tong RT, Munn LL (2007) Effect of vascular normalization by antiangiogenic therapy on interstitial hypertension, peritumor edema, and lymphatic metastasis: insights from a mathematical model. Cancer Res 67(6):2729–2735
Jain R, Narang J, Gutierrez J, Schultz LR, Scarpace L, Rosenblum M, Rock JP et al (2011) Correlation of immunohistologic and perfusion vascular parameters with MR contrast enhancement using image-guided biopsy specimens in gliomas. Acad Radiol 18(8):955–962. https://doi.org/10.1016/j.acra.2011.04.003
Jain R, Griffith B, Alotaibi F, Zagzag D, Fine H, Golfinos J, Schultz L (2015) Glioma angiogenesis and perfusion imaging: understanding the relationship between tumor blood volume and leakiness with increasing glioma grade. Am J Neuroradiol 36(11):2030–2035. https://doi.org/10.3174/ajnr.A4405
Ji J, Shi J, Budhu A, Yu Z, Forgues M, Roessler S, Croce CM et al (2009) MicroRNA expression, survival, and response to interferon in liver cancer. N Engl J Med 361(15):1437–1447
Jiang J, Wang S, Meng Q, Yu R, Wei S, Wang J, Wang C et al (2020) Study on the expression of non-coding microRNA-376b-3p in serum exosomes of patients with malignant glioma and the mechanism of anti-angiogenesis. Zhonghua Yi Xue Za Zhi 100(21):1634–1639
Jie J, Liu D, Wang Y, Wu Q, Wu T, Fang R (2022) Generation of MiRNA sponge constructs targeting multiple MiRNAs. J Clin Lab Anal 36(7):e24527
Jiménez-Morales JM, Hernández-Cuenca YE, Reyes-Abrahantes A, Ruiz-García H, Barajas-Olmos F, García-Ortiz H, del Carmen Abrahantes-Pérez M et al (2022) MicroRNA delivery systems in glioma therapy and perspectives: a systematic review. J Control Release 349:712–730
Jovčevska I, Kočevar N, Komel R (2013) Glioma and glioblastoma-how much do we (not) know? Mol Clin Oncol 1(6):935–941
Kato M, Dang V, Wang M, Park JT, Deshpande S, Kadam S, Putta S et al (2013) TGF-β induces acetylation of chromatin and of Ets-1 to alleviate repression of miR-192 in diabetic nephropathy. Sci Signal 6(278):r43–r43. https://doi.org/10.1126/scisignal.2003389
Kaur B, Khwaja FW, Severson EA, Matheny SL, Brat DJ, Van Meir EG (2005) Hypoxia and the hypoxia-inducible-factor pathway in glioma growth and angiogenesis. Neuro Oncol 7(2):134–153. https://doi.org/10.1215/S1152851704001115
Kennedy GC, Rutter WJ (1992) Pur-1, a zinc-finger protein that binds to purine-rich sequences, transactivates an insulin promoter in heterologous cells. Proc Natl Acad Sci 89(23):11498–11502. https://doi.org/10.1073/pnas.89.23.11498
Kim YK, Kim VN (2007) Processing of intronic microRNAs. EMBO J 26(3):775–783. https://doi.org/10.1038/sj.emboj.7601512
Kim WY, Lee HY (2009) Brain angiogenesis in developmental and pathological processes: mechanism and therapeutic intervention in brain tumors. FEBS J 276(17):4653–4664
Kneitz B, Krebs M, Kalogirou C, Schubert M, Joniau S, van Poppel H, Ströbel P et al (2014) Survival in patients with high-risk prostate cancer is predicted by miR-221, which regulates proliferation, apoptosis, and invasion of prostate cancer cells by inhibiting IRF2 and SOCS3mir-221 Is a biomarker in prostate cancer and inhibits IRF2 and SOCS3. Cancer Res 74(9):2591–2603. https://doi.org/10.1158/0008-5472.CAN-13-1606
Kota J, Chivukula RR, O’Donnell KA, Wentzel EA, Montgomery CL, Hwang H-W, Clark KR et al (2009) Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell 137(6):1005–1017. https://doi.org/10.1016/j.cell.2009.04.021
Kwak PB, Tomari Y (2012) The N domain of Argonaute drives duplex unwinding during RISC assembly. Nat Struct Mol Biol 19(2):145–151. https://doi.org/10.1038/nsmb.2232
Kwon JJ, Factora TD, Dey S, Kota J (2019) A systematic review of miR-29 in cancer. Mol Therapy-Oncolytics 12:173–194. https://doi.org/10.1016/j.omto.2018.12.011
Lei Z, Li B, Yang Z, Fang H, Zhang G-M, Feng Z-H, Huang B (2009) Regulation of HIF-1α and VEGF by miR-20b tunes tumor cells to adapt to the alteration of oxygen concentration. PLoS ONE 4(10):e7629. https://doi.org/10.1371/journal.pone.0007629
Li M, Fu W, Wo L, Shu X, Liu F, Li C (2013a) miR-128 and its target genes in tumorigenesis and metastasis. Exp Cell Res 319(20):3059–3064. https://doi.org/10.1016/j.yexcr.2013.07.031
Li Y, Xu J, Chen H, Bai J, Li S, Zhao Z, Kang C et al (2013b) Comprehensive analysis of the functional microRNA–mRNA regulatory network identifies miRNA signatures associated with glioma malignant progression. Nucleic Acids Res 41(22):e203–e203
Li R, Gao K, Luo H, Wang X, Shi Y, Dong Q, You Y et al (2014) Identification of intrinsic subtype-specific prognostic microRNAs in primary glioblastoma. J Exp Clin Cancer Res 33(1):9. https://doi.org/10.1186/1756-9966-33-9
Li B, Liu L, Li X, Wu L (2015) miR-503 suppresses metastasis of hepatocellular carcinoma cell by targeting PRMT1. Biochem Biophys Res Commun 464(4):982–987. https://doi.org/10.1016/j.bbrc.2015.06.169
Li C-Y, Zhang W-W, Xiang J-L, Wang X-H, Li J, Wang J-L (2019a) Identification of microRNAs as novel biomarkers for esophageal squamous cell carcinoma: a study based on The Cancer Genome Atlas (TCGA) and bioinformatics. Chin Med J 132(18):2213–2222. https://doi.org/10.1097/CM9.0000000000000427
Li W, Li J, Mu H, Guo M, Deng H (2019b) MiR-503 suppresses cell proliferation and invasion of gastric cancer by targeting HMGA2 and inactivating WNT signaling pathway. Cancer Cell Int 19(1):1–12. https://doi.org/10.1186/s12935-019-0875-1
Li J, Yuan H, Xu H, Zhao H, Xiong N (2020) Hypoxic cancer-secreted exosomal miR-182-5p promotes glioblastoma angiogenesis by targeting Kruppel-like factor 2 and 4miR-182-5p promotes glioblastoma angiogenesis. Mol Cancer Res 18(8):1218–1231. https://doi.org/10.1158/1541-7786.MCR-19-0725
Liang Z, Li S, Xu X, Xu X, Wang X, Wu J, Mao Y et al (2015) MicroRNA-576–3p inhibits proliferation in bladder cancer cells by targeting cyclin D1. Mol Cells 38(2):130. https://doi.org/10.14348/molcells.2015.2146
Lin J, Teo S, Lam DH, Jeyaseelan K, Wang S (2012) MicroRNA-10b pleiotropically regulates invasion, angiogenicity and apoptosis of tumor cells resembling mesenchymal subtype of glioblastoma multiforme. Cell Death Dis 3(10):e398–e398. https://doi.org/10.1038/cddis.2012.134
Liu L-Z, Li C, Chen Q, Jing Y, Carpenter R, Jiang Y, Jiang B-H et al (2011) MiR-21 induced angiogenesis through AKT and ERK activation and HIF-1α expression. PLoS ONE 6(4):e19139. https://doi.org/10.1371/journal.pone.0019139
Liu F, Lou Y-L, Wu J, Ruan Q-F, Xie A, Guo F, Wang Y et al (2012) Upregulation of microRNA-210 regulates renal angiogenesis mediated by activation of VEGF signaling pathway under ischemia/perfusion injury in vivo and in vitro. Kidney Blood Pressure Res 35(3):182–191. https://doi.org/10.1159/000331054
Liu S, Yin F, Zhang J, Wicha MS, Chang AE, Fan W, Li Q et al (2014) Regulatory roles of miRNA in the human neural stem cell transformation to glioma stem cells. J Cell Biochem 115(8):1368–1380. https://doi.org/10.1002/jcb.24786
Liu X, Tang H, Chen J, Song C, Yang L, Liu P, Xie X et al (2015) MicroRNA-101 inhibits cell progression and increases paclitaxel sensitivity by suppressing MCL-1 expression in human triple-negative breast cancer. Oncotarget 6(24):20070–20083. https://doi.org/10.18632/oncotarget.4039
Liu X, Li J, Qin F, Dai S (2016) miR-152 as a tumor suppressor microRNA: target recognition and regulation in cancer. Oncol Lett 11(6):3911–3916. https://doi.org/10.3892/ol.2016.4509
Liu Y, Xu C-F, Iqbal S, Yang X-Z, Wang J (2017) Responsive nanocarriers as an emerging platform for cascaded delivery of nucleic acids to cancer. Adv Drug Deliv Rev 115:98–114. https://doi.org/10.1016/j.addr.2017.03.004
Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Kleihues P et al (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114(2):97–109. https://doi.org/10.1007/s00401-007-0243-4
Lu Z, Liu M, Stribinskis V, Klinge C, Ramos K, Colburn N, Li Y (2008) MicroRNA-21 promotes cell transformation by targeting the programmed cell death 4 gene. Oncogene 27(31):4373–4379. https://doi.org/10.1038/onc.2008.72
Lucero R, Zappulli V, Sammarco A, Murillo OD, Cheah PS, Srinivasan S, Roth ME et al (2020) Glioma-derived miRNA-containing extracellular vesicles induce angiogenesis by reprogramming brain endothelial cells. Cell Rep 30(7):2065–2074. https://doi.org/10.1016/j.celrep.2020.01.073
Lui W-O, Pourmand N, Patterson BK, Fire A (2007) Patterns of known and novel small RNAs in human cervical cancer. Cancer Res 67(13):6031–6043. https://doi.org/10.1158/0008-5472.CAN-06-0561
Luo B, Zhang J (2020) MicroRNA-16 inhibits the migration and invasion of glioma cell by targeting Bcl-2 gene. Trop J Pharm Res 19(12):2499–2504. https://doi.org/10.4314/tjpr.v19i12.3
Lv J, Qiu M, Xia W, Liu C, Xu Y, Wang J, Zhao M et al (2016) High expression of long non-coding RNA SBF2-AS1 promotes proliferation in non-small cell lung cancer. J Exp Clin Cancer Res 35(1):1–13. https://doi.org/10.1186/s13046-016-0352-9
Lv T, Liu Y, Li Z, Huang R, Zhang Z, Li J (2018) miR-503 is down-regulated in osteosarcoma and suppressed MG63 proliferation and invasion by targeting VEGFA/Rictor. Cancer Biomark 23(3):315–322. https://doi.org/10.3233/CBM-170906
Ma L, Teruya-Feldstein J, Weinberg RA (2007) Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 449(7163):682–688. https://doi.org/10.1038/nature06174
Ma X, Yoshimoto K, Guan Y, Hata N, Mizoguchi M, Sagata N, Sasaki T et al (2012) Associations between microRNA expression and mesenchymal marker gene expression in glioblastoma. Neuro Oncol 14(9):1153–1162. https://doi.org/10.1093/neuonc/nos145
Mafi A, Rahmati A, Babaei Aghdam Z, Salami R, Salami M, Vakili O, Aghadavod E (2022) Recent insights into the microRNA-dependent modulation of gliomas from pathogenesis to diagnosis and treatment. Cell Mol Biol Lett 27(1):1–32. https://doi.org/10.1186/s11658-022-00354-4
Mahmoudi E, Cairns M (2017) MiR-137: an important player in neural development and neoplastic transformation. Mol Psychiatry 22(1):44–55. https://doi.org/10.1038/mp.2016.150
Makowska M, Smolarz B, Romanowicz H (2023) microRNAs (miRNAs) in glioblastoma multiforme (GBM)—recent literature review. Int J Mol Sci 24(4):3521. https://doi.org/10.3390/ijms24043521
Malhotra M, Sekar TV, Ananta JS, Devulapally R, Afjei R, Babikir HA, Massoud TF et al (2018) Targeted nanoparticle delivery of therapeutic antisense microRNAs presensitizes glioblastoma cells to lower effective doses of temozolomide in vitro and in a mouse model. Oncotarget 9(30):21478. https://doi.org/10.18632/oncotarget.25135
Mancini M, Toker A (2009) NFAT proteins: emerging roles in cancer progression. Nat Rev Cancer 9(11):810–820. https://doi.org/10.1038/nrc2735
Marcuello M, Duran-Sanchon S, Moreno L, Lozano JJ, Bujanda L, Castells A, Gironella M (2019) Analysis of A 6-mirna signature in serum from colorectal cancer screening participants as non-invasive biomarkers for advanced adenoma and colorectal cancer detection. Cancers 11(10):1542. https://doi.org/10.3390/cancers11101542
Matsuo M, Nakada C, Tsukamoto Y, Noguchi T, Uchida T, Hijiya N, Moriyama M et al (2013) MiR-29c is downregulated in gastric carcinomas and regulates cell proliferation by targeting RCC2. Mol Cancer 12(1):1–9. https://doi.org/10.1186/1476-4598-12-15
Meng F, Henson R, Wehbe-Janek H, Ghoshal K, Jacob ST, Patel T (2007) MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology 133(2):647–658. https://doi.org/10.1053/j.gastro.2007.05.022
Menon A, Abd-Aziz N, Khalid K, Poh CL, Naidu R (2022) miRNA: a promising therapeutic target in cancer. Int J Mol Sci 23(19):11502. https://doi.org/10.3390/ijms231911502
Mishra S, Ande SR, Nyomba BG (2010) The role of prohibitin in cell signaling. FEBS J 277(19):3937–3946. https://doi.org/10.1111/j.1742-4658.2010.07809.x
Mukwaya A, Jensen L, Lagali N (2021) Relapse of pathological angiogenesis: functional role of the basement membrane and potential treatment strategies. Exp Mol Med 53(2):189–201. https://doi.org/10.1038/s12276-021-00566-2
Müller J, Hart CM, Francis NJ, Vargas ML, Sengupta A, Wild B, Simon JA et al (2002) Histone methyltransferase activity of a drosophila polycomb group repressor complex. Cell 111(2):197–208. https://doi.org/10.1016/s0092-8674(02)00976-5
Nahand JS, Karimzadeh MR, Nezamnia M, Fatemipour M, Khatami A, Jamshidi S, Shafiee A et al (2020) The role of miR-146a in viral infection. IUBMB Life 72(3):343–360. https://doi.org/10.1002/iub.2222
Nakada M, Niska JA, Tran NL, McDonough WS, Berens ME (2005) EphB2/R-Ras signaling regulates glioma cell adhesion, growth, and invasion. Am J Pathol 167(2):565–576. https://doi.org/10.1016/S0002-9440(10)62998-7
Niccolini B, Palmieri V, De Spirito M, Papi M (2022) Opportunities offered by graphene nanoparticles for micrornas delivery for amyotrophic lateral sclerosis treatment. Materials 15(1):126. https://doi.org/10.3390/ma15010126
Oh B, Song H, Lee D, Oh J, Kim G, Ihm S-H, Lee M (2017) Anti-cancer effect of R3V6 peptide-mediated delivery of an anti-microRNA-21 antisense-oligodeoxynucleotide in a glioblastoma animal model. J Drug Target 25(2):132–139. https://doi.org/10.1080/1061186X.2016.1207648
Ohgaki H, Kleihues P (2005) Epidemiology and etiology of gliomas. Acta Neuropathol 109(1):93–108. https://doi.org/10.1007/s00401-005-0991-y
Oliveto S, Mancino M, Manfrini N, Biffo S (2017) Role of microRNAs in translation regulation and cancer. World J Biol Chem 8(1):45. https://doi.org/10.4331/wjbc.v8.i1.45
Onishi M, Ichikawa T, Kurozumi K (2011) Angiogenesis and invasion in glioma. Brain Tumor Pathol 28(1):13–24. https://doi.org/10.1007/s10014-010-0007-z
Osada H, Tokunaga T, Nishi M, Hatanaka H, Abe Y, Tsugu A, Nakamura M et al (2004) Overexpression of the neuropilin 1 (NRP1) gene correlated with poor prognosis in human glioma. Anticancer Res 24(2B):547–552
Pang C, Guan Y, Zhao K, Chen L, Bao Y, Cui R, Wang Y et al (2015) Up-regulation of microRNA-15b correlates with unfavorable prognosis and malignant progression of human glioma. Int J Clin Exp Pathol 8(5):4943
Papagiannakopoulos T, Friedmann-Morvinski D, Neveu P, Dugas JC, Gill RM, Huillard E, Kosik KS et al (2012) Pro-neural miR-128 is a glioma tumor suppressor that targets mitogenic kinases. Oncogene 31(15):1884–1895. https://doi.org/10.1038/onc.2011.380
Parks CL, Shenk T (1996) The serotonin 1a receptor gene contains a TATA-less promoter that responds to MAZ and Sp1 (∗). J Biol Chem 271(8):4417–4430. https://doi.org/10.1074/jbc.271.8.4417
Peng Y, Croce CM (2016) The role of MicroRNAs in human cancer. Signal Transduct Target Ther 1(1):1–9. https://doi.org/10.1038/sigtrans.2015.4
Peng B, Theng PY, Le MT (2021) Essential functions of miR-125b in cancer. Cell Prolif 54(2):e12913. https://doi.org/10.1111/cpr.12913
Qian X, Zhao P, Li W, Shi ZM, Wang L, Xu Q, Jiang BH et al (2013) Micro RNA-26a promotes tumor growth and angiogenesis in glioma by directly targeting prohibitin. CNS Neurosci Therap 19(10):804–812. https://doi.org/10.1111/cns.12149
Ramalingam P, Palanichamy JK, Singh A, Das P, Bhagat M, Kassab MA, Chattopadhyay P et al (2014) Biogenesis of intronic miRNAs located in clusters by independent transcription and alternative splicing. RNA 20(1):76–87. https://doi.org/10.1261/rna.041814.113
Ratti M, Lampis A, Ghidini M, Salati M, Mirchev MB, Valeri N, Hahne JC (2020) MicroRNAs (miRNAs) and long non-coding RNAs (lncRNAs) as new tools for cancer therapy: first steps from bench to bedside. Target Oncol 15:261–278. https://doi.org/10.1007/s11523-020-00717-x
Ray BK, Shakya A, Ray A (2007) Vascular endothelial growth factor expression in arthritic joint is regulated by SAF-1 transcription factor. J Immunol 178(3):1774–1782. https://doi.org/10.4049/jimmunol.178.3.1774
Ricklefs F, Mineo M, Rooj AK, Nakano I, Charest A, Weissleder R, Bronisz A et al (2016) Extracellular vesicles from high-grade glioma exchange diverse pro-oncogenic signals that maintain intratumoral heterogeneitytumor heterogeneity is enhanced by extracellular vesicles. Cancer Res 76(10):2876–2881. https://doi.org/10.1158/0008-5472.CAN-15-3432
Rupaimoole R, Slack FJ (2017) MicroRNA therapeutics: towards a new era for the management of cancer and other diseases. Nat Rev Drug Discov 16(3):203–222. https://doi.org/10.1038/nrd.2016.246
Salami M, Salami R, Aarabi M-H, Mafi A, Ghorbanhosseini SS, Shafabakhsh R, Asemi Z (2022) Targeting glioma cells with nutraceuticals: therapeutic effects based on molecular mechanisms, new evidence, and perspectives. Mini Rev Med Chem. https://doi.org/10.2174/1389557522666220531151137
Samad AFA, Kamaroddin MF (2023) Innovative approaches in transforming microRNAs into therapeutic tools. Wiley Interdiscip Rev 14(1):e1768. https://doi.org/10.1002/wrna.1768
Seker-Polat F, Pinarbasi Degirmenci N, Solaroglu I, Bagci-Onder T (2022) Tumor cell infiltration into the brain in glioblastoma: from mechanisms to clinical perspectives. Cancers 14(2):443. https://doi.org/10.3390/cancers14020443
Seo D-W, Li H, Guedez L, Wingfield PT, Diaz T, Salloum R, Stetler-Stevenson WG et al (2003) TIMP-2 mediated inhibition of angiogenesis: an MMP-independent mechanism. Cell 114(2):171–180. https://doi.org/10.1016/s0092-8674(03)00551-8
Shang C, Guo Y, Hong Y, Liu Y-H, Xue Y-X (2015) MiR-21 up-regulation mediates glioblastoma cancer stem cells apoptosis and proliferation by targeting FASLG. Mol Biol Rep 42(3):721–727. https://doi.org/10.1007/s11033-014-3820-3
Shang Y, Zang A, Li J, Jia Y, Li X, Zhang L, Ge K et al (2016) MicroRNA-383 is a tumor suppressor and potential prognostic biomarker in human non-small cell lung caner. Biomed Pharmacother 83:1175–1181. https://doi.org/10.1016/j.biopha.2016.08.006
Shea A, Harish V, Afzal Z, Chijioke J, Kedir H, Dusmatova S, Blancato J et al (2016) MicroRNAs in glioblastoma multiforme pathogenesis and therapeutics. Cancer Med 5(8):1917–1946. https://doi.org/10.1002/cam4.775
Shi Z-M, Wang X-F, Qian X, Tao T, Wang L, Chen Q-D, Zhang J-X et al (2013) MiRNA-181b suppresses IGF-1R and functions as a tumor suppressor gene in gliomas. RNA 19(4):552–560. https://doi.org/10.1261/rna.035972.112
Shi Z, Chen Q, Li C, Wang L, Qian X, Jiang C, Kang C et al (2014) MiR-124 governs glioma growth and angiogenesis and enhances chemosensitivity by targeting R-Ras and N-Ras. Neuro Oncol 16(10):1341–1353. https://doi.org/10.1093/neuonc/nou084
Silber J, Lim D, Petritsch C, Persson A, Maunakea A, Yu M, Costello J et al (2008a) miR-124 and miR-137 inhibit proliferation of glioblastoma multiforme cells and induce differentiation of brain tumor stem cells. BMC Med 6:14. https://doi.org/10.1186/1741-7015-6-14
Silber J, Lim DA, Petritsch C, Persson AI, Maunakea AK, Yu M, Costello JF et al (2008b) miR-124 and miR-137 inhibit proliferation of glioblastoma multiforme cells and induce differentiation of brain tumor stem cells. BMC Med 6(1):1–17. https://doi.org/10.1186/1741-7015-6-14
Slaby O, Lakomy R, Fadrus P, Hrstka R, Kren L, Lzicarova E, Nováková J et al (2010) MicroRNA-181 family predicts response to concomitant chemoradiotherapy with temozolomide in glioblastoma patients. Neoplasma 57(3):264
Smits M, Nilsson J, Mir SE, van der Stoop PM, Hulleman E, Niers JM, Krichevsky AM et al (2010) miR-101 is down-regulated in glioblastoma resulting in EZH2-induced proliferation, migration, and angiogenesis. Oncotarget 1(8):710. https://doi.org/10.18632/oncotarget.205
Smits M, Wurdinger T, van het Hof B, Drexhage JA, Geerts D, Wesseling P, Reijerkerk A et al (2012) Myc-associated zinc finger protein (MAZ) is regulated by miR-125b and mediates VEGF-induced angiogenesis in glioblastoma. FASEB J 26(6):2639–2647. https://doi.org/10.1096/fj.11-202820
Song H, Oh B, Choi M, Oh J, Lee M (2015) Delivery of anti-microRNA-21 antisense-oligodeoxynucleotide using amphiphilic peptides for glioblastoma gene therapy. J Drug Target 23(4):360–370. https://doi.org/10.3109/1061186X.2014.1000336
Song Q, An Q, Niu B, Lu X, Zhang N, Cao X (2019) Role of miR-221/222 in tumor development and the underlying mechanism. J Oncol. https://doi.org/10.1155/2019/7252013
Stamatopoulos B, Meuleman N, Haibe-Kains B, Saussoy P, Van Den Neste E, Michaux L, Lagneaux L et al (2009) microRNA-29c and microRNA-223 down-regulation has in vivo significance in chronic lymphocytic leukemia and improves disease risk stratification. Blood 113(21):5237–5245. https://doi.org/10.1182/blood-2008-11-189407
Sun J, Zheng G, Gu Z, Guo Z (2015) MiR-137 inhibits proliferation and angiogenesis of human glioblastoma cells by targeting EZH2. J Neurooncol 122(3):481–489. https://doi.org/10.1007/s11060-015-1753-x
Sun LL, Li WD, Lei FR, Li XQ (2018) The regulatory role of micro RNA s in angiogenesis-related diseases. J Cell Mol Med 22(10):4568–4587. https://doi.org/10.1111/jcmm.13700
Sun S-L, Shu Y-G, Tao M-Y (2019) miR-503 inhibits proliferation, migration, and angiogenesis of glioma by acting on VEGFA through targeting LRIG2. Cancer Manag Res 11:10599. https://doi.org/10.2147/CMAR.S222681
Suzhi Z, Liang T, Yuexia P, Lucy L, Xiaoting H, Yuan Z, Qin W (2015) Gap junctions enhance the antiproliferative effect of microRNA-124-3p in glioblastoma cells. J Cell Physiol 230(10):2476–2488. https://doi.org/10.1002/jcp.24982
Svoronos AA, Engelman DM, Slack FJ (2016) OncomiR or tumor suppressor? The duplicity of microRNAs in cancer. Can Res 76(13):3666–3670. https://doi.org/10.1158/0008-5472.CAN-16-0359
Tanzer A, Stadler PF (2004) Molecular evolution of a microRNA cluster. J Mol Biol 339(2):327–335. https://doi.org/10.1016/j.jmb.2004.03.065
Thomas S, Snowden J, Zeidler M, Danson S (2015) The role of JAK/STAT signalling in the pathogenesis, prognosis and treatment of solid tumours. Br J Cancer 113(3):365–371. https://doi.org/10.1038/bjc.2015.233
Tian Y, Luo A, Cai Y, Su Q, Ding F, Chen H, Liu Z (2010) MicroRNA-10b promotes migration and invasion through KLF4 in human esophageal cancer cell lines. J Biol Chem 285(11):7986–7994. https://doi.org/10.1074/jbc.M109.062877
Ucuzian AA, Gassman AA, East AT, Greisler HP (2010) Molecular mediators of angiogenesis. J Burn Care Res 31(1):158–175. https://doi.org/10.1097/BCR.0b013e3181c7ed82
Vale N, Duarte D, Silva S, Correia AS, Costa B, Gouveia MJ, Ferreira A (2020) Cell-penetrating peptides in oncologic pharmacotherapy: a review. Pharmacol Res 162:105231. https://doi.org/10.1016/j.phrs.2020.105231
Volinia S, Calin GA, Liu C-G, Ambs S, Cimmino A, Petrocca F, Ferracin M et al (2006) A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci 103(7):2257–2261. https://doi.org/10.1073/pnas.0510565103
Waitkus MS, Diplas BH, Yan H (2016) Isocitrate dehydrogenase mutations in gliomas. Neuro Oncol 18(1):16–26. https://doi.org/10.1093/neuonc/nov136
Wang C-Z, Deng F, Li H, Wang D-D, Zhang W, Ding L, Tang J-H (2018) MiR-101: a potential therapeutic target of cancers. Am J Transl Res 10(11):3310
Wang Z-F, Liao F, Wu H, Dai J (2019) Glioma stem cells-derived exosomal miR-26a promotes angiogenesis of microvessel endothelial cells in glioma. J Exp Clin Cancer Res 38(1):1–15. https://doi.org/10.1186/s13046-019-1181-4
Weber SM, Carroll SL (2021) The role of R-Ras proteins in normal and pathologic migration and morphologic change. Am J Pathol 191(9):1499–1510. https://doi.org/10.1016/j.ajpath.2021.05.008
Wei J, Wang F, Kong L-Y, Xu S, Doucette T, Ferguson SD, Gjyshi O et al (2013) miR-124 inhibits STAT3 signaling to enhance T cell-mediated immune clearance of glioma miRNA-mediated glioma immunosuppression. Cancer Res 73(13):3913–3926. https://doi.org/10.1158/0008-5472.CAN-12-4318
Wei Z, Batagov AO, Schinelli S, Wang J, Wang Y, El Fatimy R, Hochberg F et al (2017) Coding and noncoding landscape of extracellular RNA released by human glioma stem cells. Nat Commun 8(1):1–15. https://doi.org/10.1038/s41467-017-01196-x
Woo SK, Lee SD, Na KY, Park WK, Kwon HM (2002) TonEBP/NFAT5 stimulates transcription of HSP70 in response to hypertonicity. Mol Cell Biol 22(16):5753–5760. https://doi.org/10.1128/MCB.22.16.5753-5760.2002
Wu K, Li L, Li S (2015) Circulating microRNA-21 as a biomarker for the detection of various carcinomas: an updated meta-analysis based on 36 studies. Tumor Biol 36(3):1973–1981. https://doi.org/10.1007/s13277-014-2803-2
Würdinger T, Tannous BA (2009) Glioma angiogenesis: towards novel RNA therapeutics. Cell Adh Migr 3(2):230–235. https://doi.org/10.4161/cam.3.2.7910
Xu Z, Zeng X, Tian D, Xu H, Cai Q, Wang J, Chen Q (2014) MicroRNA-383 inhibits anchorage-independent growth and induces cell cycle arrest of glioma cells by targeting CCND1. Biochem Biophys Res Commun 453(4):833–838. https://doi.org/10.1016/j.bbrc.2014.10.047
Xu D, Ma P, Gao G, Gui Y, Niu X, Jin B (2015) MicroRNA-383 expression regulates proliferation, migration, invasion, and apoptosis in human glioma cells. Tumor Biol 36(10):7743–7753. https://doi.org/10.1007/s13277-015-3378-2
Xu CH, Liu Y, Xiao LM, Chen LK, Zheng SY, Zeng EM, Li YP et al (2019) Silencing microRNA-221/222 cluster suppresses glioblastoma angiogenesis by suppressor of cytokine signaling-3-dependent JAK/STAT pathway. J Cell Physiol 234(12):22272–22284. https://doi.org/10.1002/jcp.28794
Yang F, Wang W, Zhou C, Xi W, Yuan L, Chen X, Wang T et al (2015) MiR-221/222 promote human glioma cell invasion and angiogenesis by targeting TIMP2. Tumor Biol 36(5):3763–3773. https://doi.org/10.1007/s13277-014-3017-3
Yang C, Zheng J, Xue Y, Yu H, Liu X, Ma J, Cai H et al (2018a) The effect of MCM3AP-AS1/miR-211/KLF5/AGGF1 axis regulating glioblastoma angiogenesis. Front Mol Neurosci 10:437. https://doi.org/10.3389/fnmol.2017.00437
Yang L, Ma Y, Xin Y, Han R, Li R, Hao X (2018b) Role of the microRNA 181 family in glioma development. Mol Med Rep 17(1):322–329. https://doi.org/10.3390/ijms21062092
Yang W, Ma J, Zhou W, Cao B, Zhou X, Zhang H, Fan D et al (2019) Reciprocal regulations between miRNAs and HIF-1α in human cancers. Cell Mol Life Sci 76(3):453–471. https://doi.org/10.1007/s00018-018-2941-6
Yang M, Ke H, Zhou W (2020) LncRNA RMRP promotes cell proliferation and invasion through miR-613/NFAT5 axis in non-small cell lung cancer. Onco Targets Ther 13:8941. https://doi.org/10.2147/OTT.S255126
Yao Q, Chen Y, Zhou X (2019) The roles of microRNAs in epigenetic regulation. Curr Opin Chem Biol 51:11–17. https://doi.org/10.1016/j.cbpa.2019.01.024
Ye T, Zhong L, Ye X, Liu J, Li L, Yi H (2021) miR-221-3p and miR-222-3p regulate the SOCS3/STAT3 signaling pathway to downregulate the expression of NIS and reduce radiosensitivity in thyroid cancer. Exp Ther Med 21(6):1–9. https://doi.org/10.3892/etm.2021.10084
Ye X, Schreck KC, Ozer BH, Grossman SA (2022) High-grade glioma therapy: adding flexibility in trial design to improve patient outcomes. Expert Rev Anticancer Ther 22(3):275–287
Yi Q, Xie W, Sun W, Sun W, Liao Y (2022) A concise review of MicroRNA-383: exploring the insights of its function in tumorigenesis. J Cancer 13(1):313. https://doi.org/10.7150/jca.64846
Yin H, Shao Y, Chen X (2017) The effects of CD147 on the cell proliferation, apoptosis, invasion, and angiogenesis in glioma. Neurol Sci 38(1):129–136. https://doi.org/10.1007/s10072-016-2727-2
Yu X, Wang W (2017) Tumor suppressor microRNA-613 inhibits glioma cell proliferation, invasion and angiogenesis by targeting vascular endothelial growth factor A. Mol Med Rep 16(5):6729–6735. https://doi.org/10.3892/mmr.2017.7422
Yu H, Zheng J, Liu X, Xue Y, Shen S, Zhao L, Liu Y et al (2017) Transcription factor NFAT5 promotes glioblastoma cell-driven angiogenesis via SBF2-AS1/miR-338–3p-mediated EGFL7 expression change. Front Mol Neurosci 10:301. https://doi.org/10.3389/fnmol.2017.00301
Yuan C, Zhang Y, Tu W, Guo Y (2019) Integrated miRNA profiling and bioinformatics analyses reveal upregulated miRNAs in gastric cancer. Oncol Lett 18(2):1979–1988. https://doi.org/10.3892/ol.2019.10495
Zhang B, Liu X-X, He J-R, Zhou C-X, Guo M, He M, Zhao Q et al (2011a) Pathologically decreased miR-26a antagonizes apoptosis and facilitates carcinogenesis by targeting MTDH and EZH2 in breast cancer. Carcinogenesis 32(1):2–9. https://doi.org/10.1093/carcin/bgq209
Zhang J-G, Guo J-F, Liu D-L, Liu Q, Wang J-J (2011b) MicroRNA-101 exerts tumor-suppressive functions in non-small cell lung cancer through directly targeting enhancer of zeste homolog 2. J Thorac Oncol 6(4):671–678. https://doi.org/10.1097/JTO.0b013e318208eb35
Zhang K, Zhang Y, Ren K, Zhao G, Yan K, Ma B (2014) MicroRNA-101 inhibits the metastasis of osteosarcoma cells by downregulation of EZH2 expression. Oncol Rep 32(5):2143–2149. https://doi.org/10.3892/or.2014.3459
Zhang G, Chen L, Sun K, Khan AA, Yan J, Liu H, Gu N et al (2016) Neuropilin-1 (NRP-1)/GIPC1 pathway mediates glioma progression. Tumor Biol 37(10):13777–13788. https://doi.org/10.1007/s13277-016-5138-3
Zhang G, Chen L, Khan AA, Li B, Gu B, Lin F, Yan J et al (2018) miRNA-124-3p/neuropilin-1 (NRP-1) axis plays an important role in mediating glioblastoma growth and angiogenesis. Int J Cancer 143(3):635–644. https://doi.org/10.1002/ijc.31329
Zhao L-N, Wang P, Liu Y-H, Cai H, Ma J, Liu L-B, Xue Y-X et al (2017) MiR-383 inhibits proliferation, migration and angiogenesis of glioma-exposed endothelial cells in vitro via VEGF-mediated FAK and Src signaling pathways. Cell Signal 30:142–153. https://doi.org/10.1016/j.cellsig.2016.09.007
Zhao M, Wang R, Yang K, Jiang Y, Peng Y, Li Y, Shi S et al (2022) Nucleic acid nanoassembly-enhanced RNA therapeutics and diagnosis. Acta Pharmaceutica Sinica B. https://doi.org/10.1016/j.apsb.2022.10.019
Zheng Q, Hou W (2021) Regulation of angiogenesis by microRNAs in cancer. Mol Med Rep 24(2):1–13. https://doi.org/10.3892/mmr.2021.12222
Zheng X, Chopp M, Lu Y, Buller B, Jiang F (2013) MiR-15b and miR-152 reduce glioma cell invasion and angiogenesis via NRP-2 and MMP-3. Cancer Lett 329(2):146–154. https://doi.org/10.1016/j.canlet.2012.10.026
Zhou Y, Peng Y, Liu M, Jiang Y (2017) MicroRNA-181b inhibits cellular proliferation and invasion of glioma cells via targeting Sal-like protein 4. Oncol Res 25(6):947. https://doi.org/10.3727/096504016X14791732531006
Zhu S, Wu H, Wu F, Nie D, Sheng S, Mo Y-Y (2008) MicroRNA-21 targets tumor suppressor genes in invasion and metastasis. Cell Res 18(3):350–359. https://doi.org/10.1038/cr.2008.24
Acknowledgements
Not applicable.
Funding
Not applicable.
Author information
Authors and Affiliations
Contributions
The authors confirm contributions to this paper as follows; AM: Conceptualization, investigation, database searching, writing and review manuscript. RM and SK: editing, validating and adjusting the overall structure of the manuscript, NH, RS and MR: Writing, and draft preparation. RMD and SSG: Contributed to data collection and draw the figure. MA: Review, editing, validation and project administration. RA-S: Review and editing the manuscript. All authors read and approved the final version of manuscript for submission.
Corresponding author
Ethics declarations
Competing Interests
The authors declare no conflict of interest.
Ethical Approval and Consent to Participate
Not applicable.
Consent for Publication
Not applicable.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Mafi, A., Mannani, R., Khalilollah, S. et al. The Significant Role of microRNAs in Gliomas Angiogenesis: A Particular Focus on Molecular Mechanisms and Opportunities for Clinical Application. Cell Mol Neurobiol 43, 3277–3299 (2023). https://doi.org/10.1007/s10571-023-01385-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10571-023-01385-x