Skip to main content
SpringerLink
Log in

Novel insights into the interaction between long non-coding RNAs and microRNAs in glioma

  • Published:
Molecular and Cellular Biochemistry Aims and scope Submit manuscript

Abstract

Glioma is the most common brain tumor of the central nervous system. Long non-coding RNAs (lncRNAs) and microRNAs (miRNAs) have been identified to play a vital role in the initiation and progression of glioma, including tumor cell proliferation, survival, apoptosis, invasion, and therapy resistance. New documents emerged, which indicated that the interaction between long non-coding RNAs and miRNAs contributes to the tumorigenesis and pathogenesis of glioma. LncRNAs can act as competing for endogenous RNA (ceRNA), and molecular sponge/deregulator in regulating miRNAs. These interactions stimulate different molecular signaling pathways in glioma, including the lncRNAs/miRNAs/Wnt/β-catenin molecular signaling pathway, the lncRNAs/miRNAs/PI3K/AKT/mTOR molecular signaling pathway, the lncRNAs-miRNAs/MAPK kinase molecular signaling pathway, and the lncRNAs/miRNAs/NF-κB molecular signaling pathway. In this paper, the basic roles and molecular interactions of the lncRNAs and miRNAs pathway glioma were summarized to better understand the pathogenesis and tumorigenesis of glioma.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Data availability

The data used to support the findings of this study are included in the article.

References

  1. Goodenberger ML, Jenkins RB (2012) Genetics of adult glioma. Cancer Genet 205(12):613–621

    Article  CAS  PubMed  Google Scholar 

  2. Shi J, Dong B, Cao J, Mao Y, Guan W, Peng Y, Wang S (2017) Long non-coding RNA in glioma: signaling pathways. Oncotarget 8(16):27582

    Article  PubMed  PubMed Central  Google Scholar 

  3. Böttger K, Hatzikirou H, Chauviere A, Deutsch A (2012) Investigation of the migration/proliferation dichotomy and its impact on avascular glioma invasion. Math Model Nat Phenom 7(1):105–135

    Article  Google Scholar 

  4. Lang H, Hu G, Chen Y, Liu Y, Tu W, Lu Y, Wu L, Xu G (2017) Glioma cells promote angiogenesis through the release of exosomes containing long non-coding RNA POU3F3. Eur Rev Med Pharmacol Sci 21(5):959–972

    PubMed  Google Scholar 

  5. Li RY, Chen LC, Zhang HY, Du WZ, Feng Y, Wang HB, Wen JQ, Liu X, Li XF, Sun Y (2013) MiR-139 inhibits Mcl-1 expression and potentiates TMZ-induced apoptosis in glioma. CNS Neurosci Ther 19(7):477–483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Wang P, Liu Y-H, Yao Y-L, Li Z, Li Z-Q, Ma J, Xue Y-X (2015) Long non-coding RNA CASC2 suppresses malignancy in human gliomas by miR-21. Cell Signal 27(2):275–282

    Article  CAS  PubMed  Google Scholar 

  7. Zhao Z, Sun W, Guo Z, Zhang J, Yu H, Liu B (2019) Mechanisms of lncRNA/microRNA interactions in angiogenesis. Life Sci 254:116900

    Article  PubMed  Google Scholar 

  8. Ling H, Fabbri M, Calin GA (2013) MicroRNAs and other non-coding RNAs as targets for anticancer drug development. Nat Rev Drug Discov 12(11):847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Jia P, Cai H, Liu X, Chen J, Ma J, Wang P, Liu Y, Zheng J, Xue Y (2016) Long non-coding RNA H19 regulates glioma angiogenesis and the biological behavior of glioma-associated endothelial cells by inhibiting microRNA-29a. Cancer Lett 381(2):359–369

    Article  CAS  PubMed  Google Scholar 

  10. Maniati MS, Maniati M, Yousefi T, Ahmadi-Ahangar A, Tehrani SS (2019) New insights into the role of microRNAs and long noncoding RNAs in most common neurodegenerative diseases. J Cell Biochem 120(6):8908–8918

    Article  CAS  PubMed  Google Scholar 

  11. Tehrani SS, Karimian A, Parsian H, Majidinia M, Yousefi B (2018) Multiple functions of long non-coding RNAs in oxidative stress, DNA damage response and cancer progression. J Cell Biochem 119(1):223–236

    Article  CAS  PubMed  Google Scholar 

  12. Rönnau C, Verhaegh G, Luna-Velez M, Schalken J (2014) Noncoding RNAs as novel biomarkers in prostate cancer. BioMed Res Int 2014:591703

    Article  PubMed  PubMed Central  Google Scholar 

  13. Zhou K, Zhang C, Yao H, Zhang X, Zhou Y, Che Y, Huang Y (2018) Knockdown of long non-coding RNA NEAT1 inhibits glioma cell migration and invasion via modulation of SOX2 targeted by miR-132. Mol Cancer 17(1):105

    Article  PubMed  PubMed Central  Google Scholar 

  14. Cheng Z, Li Z, Ma K, Li X, Tian N, Duan J, Xiao X, Wang Y (2017) Long non-coding RNA XIST promotes glioma tumorigenicity and angiogenesis by acting as a molecular sponge of miR-429. J Cancer 8(19):4106

    Article  PubMed  PubMed Central  Google Scholar 

  15. Guo J, Cai H, Zheng J, Liu X, Liu Y, Ma J, Que Z, Gong W, Gao Y, Tao W (2017) Long non-coding RNA NEAT1 regulates permeability of the blood-tumor barrier via miR-181d-5p-mediated expression changes in ZO-1, occludin, and claudin-5. Biochim Biophys Acta 1863(9):2240–2254

    Article  CAS  Google Scholar 

  16. Salta E, De Strooper B (2012) Non-coding RNAs with essential roles in neurodegenerative disorders. Lancet Neurol 11(2):189–200

    Article  CAS  PubMed  Google Scholar 

  17. Idda ML, Munk R, Abdelmohsen K, Gorospe M (2018) Noncoding RNAs in Alzheimer’s disease. Interdiscipl Rev 9(2):e1463

    Google Scholar 

  18. Harrow J, Frankish A, Gonzalez JM, Tapanari E, Diekhans M, Kokocinski F, Aken BL, Barrell D, Zadissa A, Searle S (2012) GENCODE: the reference human genome annotation for The ENCODE project. Genome Res 22(9):1760–1774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Mirhosseini SA, Sarfi M, Samavarchi Tehrani S, Mirazakhani M, Maniati M, Amani J (2019) Modulation of cancer cell signaling by long noncoding RNAs. J Cell Biochem 120(8):12224–12246

    Article  CAS  PubMed  Google Scholar 

  20. Kim E-D, Sung S (2012) Long non-coding RNA: unveiling hidden layer of gene regulatory networks. Trends Plant Sci 17(1):16–21

    Article  CAS  PubMed  Google Scholar 

  21. Sarfi M, Abbastabar M, Khalili E (2019) Long noncoding RNAs biomarker-based cancer assessment. J Cell Physiol 234(10):16971–16986

    Article  CAS  PubMed  Google Scholar 

  22. Faghihi MA, Wahlestedt C (2009) Regulatory roles of natural antisense transcripts. Nat Rev Mol Cell Biol 10(9):637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Bracken AP, Helin K (2009) Polycomb group proteins: navigators of lineage pathways led astray in cancer. Nat Rev Cancer 9(11):773–784

    Article  CAS  PubMed  Google Scholar 

  24. Abolghasemi M, Tehrani SS, Yousefi T, Karimian A, Mahmoodpoor A, Ghamari A, Jadidi-Niaragh F, Yousefi M, Kafil HS, Bastami M (2020) Critical roles of long noncoding RNAs in breast cancer. J Cell Physiol 235(6):5059–5071

    Article  CAS  PubMed  Google Scholar 

  25. Bernstein E, Allis CD (2005) RNA meets chromatin. Genes Dev 19(14):1635–1655

    Article  CAS  PubMed  Google Scholar 

  26. Whitehead J, Pandey GK, Kanduri C (2009) Regulation of the mammalian epigenome by long non-coding RNAs. Biochim Biophys Acta 1790(9):936–947

    Article  CAS  PubMed  Google Scholar 

  27. Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H, Guernec G, Martin D, Merkel A, Knowles DG (2012) The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res 22(9):1775–1789

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Brown CJ, Hendrich BD, Rupert JL, Lafrenière RG, Xing Y, Lawrence J, Willard HF (1992) The human XIST gene: analysis of a 17 kb inactive X-specific RNA that contains conserved repeats and is highly localized within the nucleus. Cell 71(3):527–542

    Article  CAS  PubMed  Google Scholar 

  29. Bunch H (2017) Gene regulation of mammalian long non-coding RNA. Mol Genet Genom 293:1–15

    Article  Google Scholar 

  30. Long Y, Wang X, Youmans DT, Cech TR (2017) How do lncRNAs regulate transcription? Sci Adv 3(9):eaao2110

    Article  PubMed  PubMed Central  Google Scholar 

  31. Wang P, Xu J, Wang Y, Cao X (2017) An interferon-independent lncRNA promotes viral replication by modulating cellular metabolism. Science 358(6366):1051–1055

    Article  CAS  PubMed  Google Scholar 

  32. Liu X, Xiao Z-D, Gan B (2016) An lncRNA switch for AMPK activation. Cell Cycle 15(15):1948

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Luo M, Jeong M, Sun D, Park HJ, Rodriguez BA, Xia Z, Yang L, Zhang X, Sheng K, Darlington GJ (2015) Long non-coding RNAs control hematopoietic stem cell function. Cell Stem Cell 16(4):426–438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Geisler S, Coller J (2013) RNA in unexpected places: long non-coding RNA functions in diverse cellular contexts. Nat Rev Mol Cell Biol 14(11):699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Abbastabar M, Kheyrollah M, Azizian K, Bagherlou N, Tehrani SS, Maniati M, Karimian A (2018) Multiple functions of p27 in cell cycle, apoptosis, epigenetic modification and transcriptional regulation for the control of cell growth: a double-edged sword protein. DNA Repair 69:63–72

    Article  CAS  PubMed  Google Scholar 

  36. Wang KC, Chang HY (2011) Molecular mechanisms of long noncoding RNAs. Mol Cell 43(6):904–914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Peng Y, Croce CM (2016) The role of MicroRNAs in human cancer. Signal Trans Target Ther 1:15004

    Article  Google Scholar 

  38. Denli AM, Tops BB, Plasterk RH, Ketting RF, Hannon GJ (2004) Processing of primary microRNAs by the Microprocessor complex. Nature 432(7014):231

    Article  CAS  PubMed  Google Scholar 

  39. Reddy KB (2015) MicroRNA (miRNA) in cancer. Cancer Cell Int 15(1):38

    Article  PubMed  PubMed Central  Google Scholar 

  40. Abolghasemi M, Tehrani SS, Yousefi T, Karimian A, Mahmoodpoor A, Ghamari A, Jadidi-Niaragh F, Yousefi M, Kafil HS, Bastami M (2020) MicroRNAs in breast cancer: roles, functions, and mechanism of actions. J Cell Physiol 235(6):5008–5029

    Article  CAS  PubMed  Google Scholar 

  41. Ørom UA, Nielsen FC, Lund AH (2008) MicroRNA-10a binds the 5′ UTR of ribosomal protein mRNAs and enhances their translation. Mol Cell 30(4):460–471

    Article  PubMed  Google Scholar 

  42. Calin GA, Sevignani C, Dumitru CD, Hyslop T, Noch E, Yendamuri S, Shimizu M, Rattan S, Bullrich F, Negrini M (2004) Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc Natl Acad Sci USA 101(9):2999–3004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Mendell JT (2005) MicroRNAs: critical regulators of development, cellular physiology and malignancy. Cell Cycle 4(9):1179–1184

    Article  CAS  PubMed  Google Scholar 

  44. Je Wu, Ding J, Yang J, Guo X, Zheng Y (2018) MicroRNA roles in the nuclear factor kappa B signaling pathway in cancer. Front Immunol 9:546

    Article  Google Scholar 

  45. Di Leva G, Garofalo M, Croce CM (2014) MicroRNAs in cancer. Annu Rev Pathol 9:287–314

    Article  PubMed  Google Scholar 

  46. Dews M, Homayouni A, Yu D, Murphy D, Sevignani C, Wentzel E, Furth EE, Lee WM, Enders GH, Mendell JT (2006) Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster. Nat Genet 38(9):1060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Lee J, Hong BS, Ryu HS, Lee H-B, Lee M, Park IA, Kim J, Han W, Noh D-Y, Moon H-G (2017) Transition into inflammatory cancer-associated adipocytes in breast cancer microenvironment requires microRNA regulatory mechanism. PLoS ONE 12(3):e0174126

    Article  PubMed  PubMed Central  Google Scholar 

  48. Yang F, Ning Z, Ma L, Liu W, Shao C, Shu Y, Shen H (2017) Exosomal miRNAs and miRNA dysregulation in cancer-associated fibroblasts. Mol Cancer 16(1):148

    Article  PubMed  PubMed Central  Google Scholar 

  49. Rupaimoole R, Calin GA, Lopez-Berestein G, Sood AK (2016) miRNA deregulation in cancer cells and the tumor microenvironment. Cancer Discov 6(3):235–246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Salmena L, Poliseno L, Tay Y, Kats L, Pandolfi PP (2011) A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell 146(3):353–358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Cesana M, Cacchiarelli D, Legnini I, Santini T, Sthandier O, Chinappi M, Tramontano A, Bozzoni I (2011) A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell 147(2):358–369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, Rybak A, Maier L, Mackowiak SD, Gregersen LH, Munschauer M (2013) Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495(7441):333–338

    Article  CAS  PubMed  Google Scholar 

  53. Peng J, Hou F, Feng J, Xu SX, Meng XY (2018) Long non-coding RNA BCYRN1 promotes the proliferation and metastasis of cervical cancer via targeting microRNA-138 in vitro and in vivo. Oncol Lett 15(4):5809–5818

    PubMed  PubMed Central  Google Scholar 

  54. Guil S, Esteller M (2015) RNA–RNA interactions in gene regulation: the coding and noncoding players. Trends Biochem Sci 40(5):248–256

    Article  CAS  PubMed  Google Scholar 

  55. Pandey RR, Mondal T, Mohammad F, Enroth S, Redrup L, Komorowski J, Nagano T, Mancini-DiNardo D, Kanduri C (2008) Kcnq1ot1 antisense noncoding RNA mediates lineage-specific transcriptional silencing through chromatin-level regulation. Mol Cell 32(2):232–246

    Article  CAS  PubMed  Google Scholar 

  56. Sanyal A, Lajoie BR, Jain G, Dekker J (2012) The long-range interaction landscape of gene promoters. Nature 489(7414):109–113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Li G, Ruan X, Auerbach RK, Sandhu KS, Zheng M, Wang P, Poh HM, Goh Y, Lim J, Zhang J (2012) Extensive promoter-centered chromatin interactions provide a topological basis for transcription regulation. Cell 148(1–2):84–98

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Karreth FA, Tay Y, Perna D, Ala U, Tan SM, Rust AG, DeNicola G, Webster KA, Weiss D, Perez-Mancera PA (2011) In vivo identification of tumor-suppressive PTEN ceRNAs in an oncogenic BRAF-induced mouse model of melanoma. Cell 147(2):382–395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Tehrani SS, Ebrahimi R, Atiyeh A-E, Panahi G, Meshkani R, Younesi S, Saadat P, Parsian H (2020) Competing endogenous RNAs (CeRNAs): novel network in neurological disorders. Curr Med Chem. https://doi.org/10.2174/0929867328666201217141837

    Article  Google Scholar 

  60. Beiter T, Reich E, Williams R, Simon P (2009) Antisense transcription: a critical look in both directions. Cell Mol Life Sci 66(1):94

    Article  CAS  PubMed  Google Scholar 

  61. Katayama S, Tomaru Y, Kasukawa T, Waki K, Nakanishi M, Nakamura M, Nishida H, Yap C, Suzuki M, Kawai J (2005) Antisense transcription in the mammalian transcriptome. Science 309(5740):1564–1566

    Article  PubMed  Google Scholar 

  62. Jeffery L, Nakielny S (2004) Components of the DNA methylation system of chromatin control are RNA-binding proteins. J Biol Chem 279(47):49479–49487

    Article  CAS  PubMed  Google Scholar 

  63. Nair L, Chung H, Basu U (2020) Regulation of long non-coding RNAs and genome dynamics by the RNA surveillance machinery. Nat Rev Mol Cell Biol 21:1–14

    Article  Google Scholar 

  64. Barrandon C, Spiluttini B, Bensaude O (2008) Non-coding RNAs regulating the transcriptional machinery. Biol Cell 100(2):83–95

    Article  CAS  PubMed  Google Scholar 

  65. Änkö M-L, Neugebauer KM (2012) RNA–protein interactions in vivo: global gets specific. Trends Biochem Sci 37(7):255–262

    Article  PubMed  Google Scholar 

  66. Cai B, Song X, Cai J, Zhang S (2014) HOTAIR: a cancer-related long non-coding RNA. Neoplasma 61(4):379–391

    Article  CAS  PubMed  Google Scholar 

  67. Chen Y, Zhao F, Cui D, Jiang R, Chen J, Huang Q, Shi J (2018) HOXD-AS1/miR-130a sponge regulates glioma development by targeting E2F8. Int J Cancer 142(11):2313–2322. https://doi.org/10.1002/ijc.31262

    Article  CAS  PubMed  Google Scholar 

  68. Jain RK, Koenig GC, Dellian M, Fukumura D, Munn LL, Melder RJ (1996) Leukocyte-endothelial adhesion and angiogenesis in tumors. Cancer Metast Rev 15(2):195–204. https://doi.org/10.1007/bf00437472

    Article  CAS  Google Scholar 

  69. Zhang J, Cui Q, Zhao Y, Guo R, Zhan C, Jiang P, Luan P, Zhang P, Wang F, Yang L, Yang X, Xu Y (2020) Mechanism of angiogenesis promotion with Shexiang Baoxin Pills by regulating function and signaling pathway of endothelial cells through macrophages. Atherosclerosis 292:99–111. https://doi.org/10.1016/j.atherosclerosis.2019.11.005

    Article  CAS  PubMed  Google Scholar 

  70. Mashreghi M, Azarpara H, Bazaz MR, Jafari A, Masoudifar A, Mirzaei H, Jaafari MR (2018) Angiogenesis biomarkers and their targeting ligands as potential targets for tumor angiogenesis. J Cell Physiol 233(4):2949–2965. https://doi.org/10.1002/jcp.26049

    Article  CAS  PubMed  Google Scholar 

  71. Onishi M, Ichikawa T, Kurozumi K, Date I (2011) Angiogenesis and invasion in glioma. Brain Tumor Pathol 28(1):13–24. https://doi.org/10.1007/s10014-010-0007-z

    Article  CAS  PubMed  Google Scholar 

  72. Yuan X, Han L, Fu P, Zeng H, Lv C, Chang W, Runyon RS, Ishii M, Han L, Liu K, Fan T, Zhang W, Liu R (2018) Cinnamaldehyde accelerates wound healing by promoting angiogenesis via up-regulation of PI3K and MAPK signaling pathways. Lab Investig 98(6):783–798. https://doi.org/10.1038/s41374-018-0025-8

    Article  CAS  PubMed  Google Scholar 

  73. Yamada K, Miyamoto Y, Tsujii A, Moriyama T, Ikuno Y, Shiromizu T, Serada S, Fujimoto M, Tomonaga T, Naka T, Yoneda Y, Oka M (2016) Cell surface localization of importin alpha1/KPNA2 affects cancer cell proliferation by regulating FGF1 signalling. Sci Rep 6:21410. https://doi.org/10.1038/srep21410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Hori Y, Ito K, Hamamichi S, Ozawa Y, Matsui J, Umeda IO, Fujii H (2017) Functional characterization of VEGF- and FGF-induced tumor blood vessel models in human cancer xenografts. Anticancer Res 37(12):6629–6638. https://doi.org/10.21873/anticanres.12120

    Article  CAS  PubMed  Google Scholar 

  75. Sparacia G, Sparacia B, Robusto V, Gadde J, Iaia A (2013) High-grade gliomas and solitary metastases: differentiation by using peritumoral perfusion and proton spectroscopic MR imaging. American Society of Neuroradiology, Oak Brook, p 305

    Google Scholar 

  76. Grosu A-L, Astner ST, Riedel E, Nieder C, Wiedenmann N, Heinemann F, Schwaiger M, Molls M, Wester H-J, Weber WA (2011) An interindividual comparison of O-(2-[18F] fluoroethyl)-l-tyrosine (FET)–and l-[methyl-11C] methionine (MET)–PET in patients with brain gliomas and metastases. Int J Rad Oncol 81(4):1049–1058

    Article  CAS  Google Scholar 

  77. Li J, Li Q, Lin L, Wang R, Chen L, Du W, Jiang C, Li R (2018) Targeting the Notch1 oncogene by miR-139-5p inhibits glioma metastasis and epithelial-mesenchymal transition (EMT). BMC Neurol 18(1):133

    Article  PubMed  PubMed Central  Google Scholar 

  78. Tune L, Coyle JT (1981) Acute extrapyramidal side effects: serum levels of neuroleptics and anticholinergics. Psychopharmacology 75(1):9–15

    Article  CAS  PubMed  Google Scholar 

  79. Beauchesne P (2011) Extra-neural metastases of malignant gliomas: myth or reality? Cancers 3(1):461–477

    Article  PubMed  PubMed Central  Google Scholar 

  80. Schreiber S, Gross S, Brandis A, Harmelin A, Rosenbach-Belkin V, Scherz A, Salomon Y (2002) Local photodynamic therapy (PDT) of rat C6 glioma xenografts with Pd-bacteriopheophorbide leads to decreased metastases and increase of animal cure compared with surgery. Int J Cancer 99(2):279–285

    Article  CAS  PubMed  Google Scholar 

  81. Amaral PP, Dinger ME, Mercer TR, Mattick JS (2008) The eukaryotic genome as an RNA machine. Science 319(5871):1787–1789. https://doi.org/10.1126/science.1155472

    Article  CAS  PubMed  Google Scholar 

  82. Nakada M, Kita D, Teng L, Pyko IV, Watanabe T, Hayashi Y, Hamada JI (2020) Receptor tyrosine kinases: principles and functions in glioma invasion. Adv Exp Med Biol 1202:151–178. https://doi.org/10.1007/978-3-030-30651-9_8

    Article  CAS  PubMed  Google Scholar 

  83. Lai Z, Markovets A, Ahdesmaki M, Chapman B, Hofmann O, McEwen R, Johnson J, Dougherty B, Barrett JC, Dry JR (2016) VarDict: a novel and versatile variant caller for next-generation sequencing in cancer research. Nucleic Acids Res 44(11):e108. https://doi.org/10.1093/nar/gkw227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Yu H, Li Z, Wang M (2020) Expression and prognostic role of E2F transcription factors in high-grade glioma. CNS Neurosci Ther. https://doi.org/10.1111/cns.13295

    Article  PubMed  PubMed Central  Google Scholar 

  85. Jin DH, Kim Y, Lee BB, Han J, Kim HK, Shim YM, Kim DH (2017) Metformin induces cell cycle arrest at the G1 phase through E2F8 suppression in lung cancer cells. Oncotarget 8(60):101509–101519. https://doi.org/10.18632/oncotarget.21552

    Article  PubMed  PubMed Central  Google Scholar 

  86. Qin J, Liu Y, Lu Y, Liu M, Li M, Li J, Wu L (2017) Hypoxia-inducible factor 1 alpha promotes cancer stem cells-like properties in human ovarian cancer cells by upregulating SIRT1 expression. Sci Rep 7(1):10592. https://doi.org/10.1038/s41598-017-09244-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Eales KL, Hollinshead KE, Tennant DA (2016) Hypoxia and metabolic adaptation of cancer cells. Oncogenesis 5:e190. https://doi.org/10.1038/oncsis.2015.50

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Samanta D (1870) Semenza GL (2018) Metabolic adaptation of cancer and immune cells mediated by hypoxia-inducible factors. Biochim Biophys Acta 1:15–22. https://doi.org/10.1016/j.bbcan.2018.07.002

    Article  CAS  Google Scholar 

  89. Ros S, Schulze A (2013) Balancing glycolytic flux: the role of 6-phosphofructo-2-kinase/fructose 2,6-bisphosphatases in cancer metabolism. Cancer Metabol 1(1):8. https://doi.org/10.1186/2049-3002-1-8

    Article  Google Scholar 

  90. Sreedhar A, Petruska P, Miriyala S, Panchatcharam M, Zhao Y (2017) UCP2 overexpression enhanced glycolysis via activation of PFKFB2 during skin cell transformation. Oncotarget 8(56):95504–95515. https://doi.org/10.18632/oncotarget.20762

    Article  PubMed  PubMed Central  Google Scholar 

  91. Mehta A, Awah CU, Sonabend AM (2018) Topoisomerase II poisons for glioblastoma; existing challenges and opportunities to personalize therapy. Front Neurol 9:459. https://doi.org/10.3389/fneur.2018.00459

    Article  PubMed  PubMed Central  Google Scholar 

  92. Kirk JS, Schaarschuch K, Dalimov Z, Lasorsa E, Ku S, Ramakrishnan S, Hu Q, Azabdaftari G, Wang J, Pili R, Ellis L (2015) Top2a identifies and provides epigenetic rationale for novel combination therapeutic strategies for aggressive prostate cancer. Oncotarget 6(5):3136–3146. https://doi.org/10.18632/oncotarget.3077

    Article  PubMed  Google Scholar 

  93. Wang Q, Seki E (2018) Astrocyte elevated gene-1 (AEG-1): a new potential therapeutic target for the treatment of nonalcoholic steatohepatitis (NASH). Hepatobil Surg Nutr 7(1):44–47. https://doi.org/10.21037/hbsn.2017.11.04

    Article  Google Scholar 

  94. Feng S, Yao J, Zhang Z, Zhang Y, Zhang Z, Liu J, Tan W, Sun C, Chen L, Yu X (2018) miR96 inhibits EMT by targeting AEG1 in glioblastoma cancer cells. Mol Med Rep 17(2):2964–2972. https://doi.org/10.3892/mmr.2017.8227

    Article  CAS  PubMed  Google Scholar 

  95. Ying Z, Li J, Li M (2011) Astrocyte elevated gene 1: biological functions and molecular mechanism in cancer and beyond. Cell Biosci 1(1):36. https://doi.org/10.1186/2045-3701-1-36

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Jin Z, Piao L, Sun G, Lv C, Jing Y, Jin R (2020) Long non-coding RNA PART1 exerts tumor suppressive functions in glioma via sponging miR-190a-3p and inactivation of PTEN/AKT pathway. Onco Targets Ther 13:1073–1086. https://doi.org/10.2147/ott.s232848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Kouchi M, Shibayama Y, Ogawa D, Miyake K, Nishiyama A, Tamiya T (2017) (Pro)renin receptor is crucial for glioma development via the Wnt/beta-catenin signaling pathway. J Neurosurg 127(4):819–828. https://doi.org/10.3171/2016.9.jns16431

    Article  CAS  PubMed  Google Scholar 

  98. Rivero O, Sich S, Popp S, Schmitt A, Franke B, Lesch KP (2013) Impact of the ADHD-susceptibility gene CDH13 on development and function of brain networks. Eur Neuropsychopharmacol 23(6):492–507. https://doi.org/10.1016/j.euroneuro.2012.06.009

    Article  CAS  PubMed  Google Scholar 

  99. Andreeva AV, Kutuzov MA (2010) Cadherin 13 in cancer. Genes Chromosom Cancer 49(9):775–790. https://doi.org/10.1002/gcc.20787

    Article  CAS  PubMed  Google Scholar 

  100. Li Y, Li A, Glas M, Lal B, Ying M, Sang Y, Xia S, Trageser D, Guerrero-Cazares H, Eberhart CG, Quinones-Hinojosa A, Scheffler B, Laterra J (2011) c-Met signaling induces a reprogramming network and supports the glioblastoma stem-like phenotype. Proc Natl Acad Sci USA 108(24):9951–9956. https://doi.org/10.1073/pnas.1016912108

    Article  PubMed  PubMed Central  Google Scholar 

  101. Lesko E, Majka M (2008) The biological role of HGF-MET axis in tumor growth and development of metastasis. Front Biosci 13:1271–1280. https://doi.org/10.2741/2760

    Article  CAS  PubMed  Google Scholar 

  102. Caramel J, Ligier M, Puisieux A (2018) Pleiotropic roles for ZEB1 in cancer. Can Res 78(1):30–35. https://doi.org/10.1158/0008-5472.can-17-2476

    Article  CAS  Google Scholar 

  103. Spaderna S, Schmalhofer O, Wahlbuhl M, Dimmler A, Bauer K, Sultan A, Hlubek F, Jung A, Strand D, Eger A, Kirchner T, Behrens J, Brabletz T (2008) The transcriptional repressor ZEB1 promotes metastasis and loss of cell polarity in cancer. Can Res 68(2):537–544. https://doi.org/10.1158/0008-5472.can-07-5682

    Article  CAS  Google Scholar 

  104. Edwards LA, Li A, Berel D, Madany M, Kim NH, Liu M, Hymowitz M, Uy B, Jung R, Xu M, Black KL, Rentsendorj A, Fan X, Zhang W, Yu JS (2017) ZEB1 regulates glioma stemness through LIF repression. Sci Rep 7(1):69. https://doi.org/10.1038/s41598-017-00106-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Zhang L, Zhang W, Li Y, Alvarez A, Li Z, Wang Y, Song L, Lv D, Nakano I, Hu B, Cheng SY, Feng H (2016) SHP-2-upregulated ZEB1 is important for PDGFRalpha-driven glioma epithelial-mesenchymal transition and invasion in mice and humans. Oncogene 35(43):5641–5652. https://doi.org/10.1038/onc.2016.100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. van Bragt MP, Hu X, Xie Y, Li Z (2014) RUNX1, a transcription factor mutated in breast cancer, controls the fate of ER-positive mammary luminal cells. eLife 3:e03881. https://doi.org/10.7554/eLife.03881

    Article  PubMed  PubMed Central  Google Scholar 

  107. Sangpairoj K, Vivithanaporn P, Apisawetakan S, Chongthammakun S, Sobhon P, Chaithirayanon K (2017) RUNX1 regulates migration, invasion, and angiogenesis via p38 MAPK pathway in human glioblastoma. Cell Mol Neurobiol 37(7):1243–1255. https://doi.org/10.1007/s10571-016-0456-y

    Article  CAS  PubMed  Google Scholar 

  108. Zhang CZ, Cao Y, Fu J, Yun JP, Zhang MF (2016) miR-634 exhibits anti-tumor activities toward hepatocellular carcinoma via Rab1A and DHX33. Mol Oncol 10(10):1532–1541. https://doi.org/10.1016/j.molonc.2016.09.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Wang X, Liu F, Qin X, Huang T, Huang B, Zhang Y, Jiang B (2016) Expression of Rab1A is upregulated in human lung cancer and associated with tumor size and T stage. Aging 8(11):2790–2798. https://doi.org/10.18632/aging.101087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Yang XZ, Li XX, Zhang YJ, Rodriguez-Rodriguez L, Xiang MQ, Wang HY, Zheng XF (2016) Rab1 in cell signaling, cancer and other diseases. Oncogene 35(44):5699–5704. https://doi.org/10.1038/onc.2016.81

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Bian EB, Ma CC, He XJ, Wang C, Zong G, Wang HL, Zhao B (2016) Epigenetic modification of miR-141 regulates SKA2 by an endogenous ‘sponge’ HOTAIR in glioma. Oncotarget 7(21):30610–30625. https://doi.org/10.18632/oncotarget.8895

    Article  PubMed  PubMed Central  Google Scholar 

  112. Sadeh N, Spielberg JM, Logue MW, Wolf EJ, Smith AK, Lusk J, Hayes JP, Sperbeck E, Milberg WP, McGlinchey RE, Salat DH, Carter WC, Stone A, Schichman SA, Humphries DE, Miller MW (2016) SKA2 methylation is associated with decreased prefrontal cortical thickness and greater PTSD severity among trauma-exposed veterans. Mol Psychiatry 21(3):357–363. https://doi.org/10.1038/mp.2015.134

    Article  CAS  PubMed  Google Scholar 

  113. Liu K, Zhao H, Yao H, Lei S, Lei Z, Li T, Qi H (2013) MicroRNA-124 regulates the proliferation of colorectal cancer cells by targeting iASPP. Biomed Res Int 2013:867537. https://doi.org/10.1155/2013/867537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Lei R, Xue M, Zhang L, Lin Z (2017) Long noncoding RNA MALAT1-regulated microRNA 506 modulates ovarian cancer growth by targeting iASPP. Onco Targets Ther 10:35–46. https://doi.org/10.2147/ott.s112686

    Article  CAS  PubMed  Google Scholar 

  115. Esencay M, Sarfraz Y, Zagzag D (2013) CXCR7 is induced by hypoxia and mediates glioma cell migration towards SDF-1alpha. BMC Cancer 13:347. https://doi.org/10.1186/1471-2407-13-347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Calatozzolo C, Canazza A, Pollo B, Di Pierro E, Ciusani E, Maderna E, Salce E, Sponza V, Frigerio S, Di Meco F, Schinelli S, Salmaggi A (2011) Expression of the new CXCL12 receptor, CXCR7, in gliomas. Cancer Biol Ther 11(2):242–253. https://doi.org/10.4161/cbt.11.2.13951

    Article  CAS  PubMed  Google Scholar 

  117. Odemis V, Lipfert J, Kraft R, Hajek P, Abraham G, Hattermann K, Mentlein R, Engele J (2012) The presumed atypical chemokine receptor CXCR7 signals through G(i/o) proteins in primary rodent astrocytes and human glioma cells. Glia 60(3):372–381. https://doi.org/10.1002/glia.22271

    Article  PubMed  Google Scholar 

  118. Wurth R, Bajetto A, Harrison JK, Barbieri F, Florio T (2014) CXCL12 modulation of CXCR4 and CXCR7 activity in human glioblastoma stem-like cells and regulation of the tumor microenvironment. Front Cell Neurosci 8:144. https://doi.org/10.3389/fncel.2014.00144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Deng K, Wang H, Guo X, Xia J (2016) The cross talk between long, non-coding RNAs and microRNAs in gastric cancer. Acta Biochim Biophys Sin 48(2):111–116. https://doi.org/10.1093/abbs/gmv120

    Article  CAS  PubMed  Google Scholar 

  120. Zhao H, Peng R, Liu Q, Liu D, Du P, Yuan J, Peng G, Liao Y (2016) The lncRNA H19 interacts with miR-140 to modulate glioma growth by targeting iASPP. Arch Biochem Biophys 610:1–7. https://doi.org/10.1016/j.abb.2016.09.014

    Article  CAS  PubMed  Google Scholar 

  121. Liu B, Cao W, Ma H (2019) Knockdown of lncRNA LSINCT5 suppresses growth and metastasis of human glioma cells via up-regulating miR-451. Artif Cells Nanomed Biotechnol 47(1):2507–2515. https://doi.org/10.1080/21691401.2019.1626404

    Article  CAS  PubMed  Google Scholar 

  122. Sun G, Wang Y, Zhang J, Lin N, You Y (2018) MiR-15b/HOTAIR/p53 form a regulatory loop that affects the growth of glioma cells. J Cell Biochem 119(6):4540–4547. https://doi.org/10.1002/jcb.26591

    Article  CAS  PubMed  Google Scholar 

  123. Zhao G, Huang Q, Wang F, Zhang X, Hu J, Tan Y, Huang N, Wang Z, Wang Z, Cheng Y (2018) Targeted shRNA-loaded liposome complex combined with focused ultrasound for blood brain barrier disruption and suppressing glioma growth. Cancer Lett 418:147–158. https://doi.org/10.1016/j.canlet.2018.01.035

    Article  CAS  PubMed  Google Scholar 

  124. Bhowmik A, Chakravarti S, Ghosh A, Shaw R, Bhandary S, Bhattacharyya S, Sen PC, Ghosh MK (2017) Anti-SSTR2 peptide based targeted delivery of potent PLGA encapsulated 3,3′-diindolylmethane nanoparticles through blood brain barrier prevents glioma progression. Oncotarget 8(39):65339–65358. https://doi.org/10.18632/oncotarget.18689

    Article  PubMed  PubMed Central  Google Scholar 

  125. van Tellingen O, Yetkin-Arik B, de Gooijer MC, Wesseling P, Wurdinger T, de Vries HE (2015) Overcoming the blood-brain tumor barrier for effective glioblastoma treatment. Drug Resist Updates 19:1–12. https://doi.org/10.1016/j.drup.2015.02.002

    Article  Google Scholar 

  126. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144(5):646–674. https://doi.org/10.1016/j.cell.2011.02.013

    Article  CAS  PubMed  Google Scholar 

  127. Steinbach JP, Weller M (2004) Apoptosis in gliomas: molecular mechanisms and therapeutic implications. J Neurooncol 70(2):247–256. https://doi.org/10.1007/s11060-004-2753-4

    Article  PubMed  Google Scholar 

  128. Shang C, Guo Y, Hong Y, Xue YX (2016) Long non-coding RNA TUSC7, a target of miR-23b, Plays tumor-suppressing roles in human gliomas. Front Cell Neurosci 10:235. https://doi.org/10.3389/fncel.2016.00235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Canobbio I, Trionfini P, Guidetti GF, Balduini C, Torti M (2008) Targeting of the small GTPase Rap2b, but not Rap1b, to lipid rafts is promoted by palmitoylation at Cys176 and Cys177 and is required for efficient protein activation in human platelets. Cell Signal 20(9):1662–1670. https://doi.org/10.1016/j.cellsig.2008.05.016

    Article  CAS  PubMed  Google Scholar 

  130. Paganini S, Guidetti GF, Catricala S, Trionfini P, Panelli S, Balduini C, Torti M (2006) Identification and biochemical characterization of Rap2C, a new member of the Rap family of small GTP-binding proteins. Biochimie 88(3–4):285–295. https://doi.org/10.1016/j.biochi.2005.08.007

    Article  CAS  PubMed  Google Scholar 

  131. Li Z, Xu C, Ding B, Gao M, Wei X, Ji N (2017) Long non-coding RNA MALAT1 promotes proliferation and suppresses apoptosis of glioma cells through derepressing Rap1B by sponging miR-101. J Neurooncol 134(1):19–28. https://doi.org/10.1007/s11060-017-2498-5

    Article  CAS  PubMed  Google Scholar 

  132. Boehm EM, Gildenberg MS, Washington MT (2016) The many roles of PCNA in eukaryotic DNA replication. Enzymes 39:231–254. https://doi.org/10.1016/bs.enz.2016.03.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Yao Q, An Y, Hou W, Cao Y-N, Yao M-F, Ma N-N, Hou L, Zhang H, Liu H-J, Zhang B (2017) LRP6 promotes invasion and metastasis of colorectal cancer through cytoskeleton dynamics. Oncotarget 8(65):109632

    Article  PubMed  PubMed Central  Google Scholar 

  134. Zhang L, Liang X, Li Y (2017) Long non-coding RNA MEG3 inhibits cell growth of gliomas by targeting miR-93 and inactivating PI3K/AKT pathway. Oncol Rep 38(4):2408–2416. https://doi.org/10.3892/or.2017.5871

    Article  CAS  PubMed  Google Scholar 

  135. Dong X, Jin Z, Chen Y, Xu H, Ma C, Hong X, Li Y, Zhao G (2018) Knockdown of long non-coding RNA ANRIL inhibits proliferation, migration, and invasion but promotes apoptosis of human glioma cells by upregulation of miR-34a. J Cell Biochem 119(3):2708–2718. https://doi.org/10.1002/jcb.26437

    Article  CAS  PubMed  Google Scholar 

  136. Wang Q, Teng Y, Wang R, Deng D, You Y, Peng Y, Shao N, Zhi F (2018) The long non-coding RNA SNHG14 inhibits cell proliferation and invasion and promotes apoptosis by sponging miR-92a-3p in glioma. Oncotarget 9(15):12112–12124. https://doi.org/10.18632/oncotarget.23960

    Article  PubMed  PubMed Central  Google Scholar 

  137. Niu H, Wang K, Zhang A, Yang S, Song Z, Wang W, Qian C, Li X, Zhu Y, Wang Y (2012) miR-92a is a critical regulator of the apoptosis pathway in glioblastoma with inverse expression of BCL2L11. Oncol Rep 28(5):1771–1777. https://doi.org/10.3892/or.2012.1970

    Article  CAS  PubMed  Google Scholar 

  138. Yao J, Zhou B, Zhang J, Geng P, Liu K, Zhu Y, Zhu W (2014) A new tumor suppressor LncRNA ADAMTS9-AS2 is regulated by DNMT1 and inhibits migration of glioma cells. Tumor Biol 35(8):7935–7944

    Article  CAS  Google Scholar 

  139. Liao Y, Shen L, Zhao H, Liu Q, Fu J, Guo Y, Peng R, Cheng L (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

    Article  CAS  PubMed  Google Scholar 

  140. Li J, Zhang M, An G, Ma Q (2016) LncRNA TUG1 acts as a tumor suppressor in human glioma by promoting cell apoptosis. Exp Biol Med 241(6):644–649

    Article  CAS  Google Scholar 

  141. Roberts TC, Wood MJ (2013) Therapeutic targeting of non-coding RNAs. Essays Biochem 54:127–145

    Article  CAS  PubMed  Google Scholar 

  142. Rynkeviciene R, Simiene J, Strainiene E, Stankevicius V, Usinskiene J, Miseikyte Kaubriene E, Meskinyte I, Cicenas J, Suziedelis K (2019) Non-coding RNAs in glioma. Cancers 11(1):17

    Article  CAS  Google Scholar 

  143. Ke J, Yao Y-l, Zheng J, Wang P, Liu Y-h, Ma J, Li Z, Liu X-b, Li Z-q, Wang Z-h (2015) Knockdown of long non-coding RNA HOTAIR inhibits malignant biological behaviors of human glioma cells via modulation of miR-326. Oncotarget 6(26):21934

    Article  PubMed  PubMed Central  Google Scholar 

  144. Wang Q, Zhang J, Liu Y, Zhang W, Zhou J, Duan R, Pu P, Kang C, Han L (2016) A novel cell cycle-associated lncRNA, HOXA11-AS, is transcribed from the 5-prime end of the HOXA transcript and is a biomarker of progression in glioma. Cancer Lett 373(2):251–259

    Article  CAS  PubMed  Google Scholar 

  145. Latowska J, Grabowska A, Zarębska Ż, Kuczyński K, Kuczyńska B, Rolle K (2020) Non-coding RNAs in brain tumors, the contribution of lncRNAs, circRNAs, and snoRNAs to cancer development: their diagnostic and therapeutic potential. Int J Mol Sci 21(19):7001

    Article  CAS  PubMed Central  Google Scholar 

  146. Min W, Dai D, Wang J, Zhang D, Zhang Y, Han G, Zhang L, Chen C, Li X, Li Y (2016) Long noncoding RNA miR210HG as a potential biomarker for the diagnosis of glioma. PLoS ONE 11(9):e0160451

    Article  PubMed  PubMed Central  Google Scholar 

  147. Wang K, Huang R, Li G, Zeng F, Zhao Z, Liu Y, Hu H, Jiang T (2018) CKAP2 expression is associated with glioma tumor growth and acts as a prognostic factor in high-grade glioma. Oncol Rep 40(4):2036–2046

    CAS  PubMed  PubMed Central  Google Scholar 

  148. Yang A, Wang H, Yang X (2017) Long non-coding RNA PVT1 indicates a poor prognosis of glioma and promotes cell proliferation and invasion via target EZH2. Biosci Rep 37(6):BSR20170871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Duan R, Han L, Wang Q, Wei J, Chen L, Zhang J, Kang C, Wang L (2015) HOXA13 is a potential GBM diagnostic marker and promotes glioma invasion by activating the Wnt and TGF-β pathways. Oncotarget 6(29):27778

    Article  PubMed  PubMed Central  Google Scholar 

  150. Xiao Y, Zhang L, Song Z, Guo C, Zhu J, Li Z, Zhu S (2016) Potential diagnostic and prognostic value of plasma circulating MicroRNA-182 in human glioma. Med Sci Monit 22:855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Shi Y, Wang Y, Luan W, Wang P, Tao T, Zhang J, Qian J, Liu N, You Y (2014) Long non-coding RNA H19 promotes glioma cell invasion by deriving miR-675. PLoS ONE 9(1):e86295

    Article  PubMed  PubMed Central  Google Scholar 

  152. Yao Y, Ma J, Xue Y, Wang P, Li Z, Liu J, Chen L, Xi Z, Teng H, Wang Z (2015) Knockdown of long non-coding RNA XIST exerts tumor-suppressive functions in human glioblastoma stem cells by up-regulating miR-152. Cancer Lett 359(1):75–86

    Article  CAS  PubMed  Google Scholar 

  153. Ma C-C, Xiong Z, Zhu G-N, Wang C, Zong G, Wang H-L, Bian E-B, Zhao B (2016) Long non-coding RNA ATB promotes glioma malignancy by negatively regulating miR-200a. J Exp Clin Cancer Res 35(1):90

    Article  PubMed  PubMed Central  Google Scholar 

  154. Zhen L, Yun-hui L, Hong-yu D, Jun M, Yi-long Y (2016) Long noncoding RNA NEAT1 promotes glioma pathogenesis by regulating miR-449b-5p/c-Met axis. Tumor Biol 37(1):673–683

    Article  Google Scholar 

  155. Zheng J, Liu X, Wang P, Xue Y, Ma J, Qu C, Liu Y (2016) CRNDE promotes malignant progression of glioma by attenuating miR-384/PIWIL4/STAT3 axis. Mol Ther 24(7):1199–1215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Cao S, Wang Y, Li J, Lv M, Niu H, Tian Y (2016) Tumor-suppressive function of long noncoding RNA MALAT1 in glioma cells by suppressing miR-155 expression and activating FBXW7 function. Am J Cancer Res 6(11):2561

    CAS  PubMed  PubMed Central  Google Scholar 

  157. Cui B, Li B, Liu Q, Cui Y (2017) lncRNA CCAT1 promotes glioma tumorigenesis by sponging miR-181b. J Cell Biochem 118(12):4548–4557

    Article  CAS  PubMed  Google Scholar 

  158. Zhang S, Wang W, Liu G, Xie S, Li Q, Li Y, Lin Z (2017) Long non-coding RNA HOTTIP promotes hypoxia-induced epithelial-mesenchymal transition of malignant glioma by regulating the miR-101/ZEB1 axis. Biomed Pharmacother 95:711–720

    Article  CAS  PubMed  Google Scholar 

  159. Zhao X, Liu Y, Zheng J, Liu X, Chen J, Liu L, Wang P, Xue Y (2017) GAS5 suppresses malignancy of human glioma stem cells via a miR-196a-5p/FOXO1 feedback loop. Biochim Biophys Acta 1864:1605–1617

    Article  CAS  Google Scholar 

  160. Zhang W, Bi Y, Li J, Peng F, Li H, Li C, Wang L, Ren F, Xie C, Wang P (2017) Long noncoding RNA FTX is upregulated in gliomas and promotes proliferation and invasion of glioma cells by negatively regulating miR-342-3p. Lab Invest 97(4):447

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Tehran University of Medical Sciences and Babol University of Medical Sciences for kind supports.

Author information

Author notes

  1. Anahita Ebrahimpour and Mohammad Sarfi have been contributed equally to this work as first authors.

Authors and Affiliations

  1. Student Research Committee, Babol University of Medical Sciences, Babol, Iran

    Anahita Ebrahimpour & Setareh Rezatabar

  2. Department of Clinical Biochemistry, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran

    Mohammad Sarfi & Sadra Samavarchi Tehrani

  3. Student Scientific Research Center, Tehran University of Medical Sciences, Tehran, Iran

    Mohammad Sarfi & Sadra Samavarchi Tehrani

Authors
  1. Anahita Ebrahimpour
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mohammad Sarfi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Setareh Rezatabar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sadra Samavarchi Tehrani
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sadra Samavarchi Tehrani.

Ethics declarations

Conflict of interest

The authors declare that there are no conflict of interests.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

All of the authors consent for publication.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ebrahimpour, A., Sarfi, M., Rezatabar, S. et al. Novel insights into the interaction between long non-coding RNAs and microRNAs in glioma. Mol Cell Biochem 476, 2317–2335 (2021). https://doi.org/10.1007/s11010-021-04080-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11010-021-04080-x

Keywords

Search

Navigation