Advertisement

Journal of Molecular Neuroscience

, Volume 67, Issue 1, pp 72–81 | Cite as

Circular RNAs: Functions and Prospects in Glioma

  • Zheng Hao
  • Si Hu
  • Zheng Liu
  • Weixin Song
  • Yeyu Zhao
  • Meihua LiEmail author
Article

Abstract

Improving the survival rate of patients with glioma, a malignant tumor of the human brain has become increasingly important. In recent years, the function of circular RNAs (circRNAs) in different diseases and the pathophysiological mechanisms involved have been elucidated. In the pathophysiological mechanism, the primary function of circRNAs is to act as microRNA sponges. An increasing number of studies have found that circRNAs are differentially expressed in gliomas and regulate the occurrence, proliferation, and invasion of glioma and thus may be potential markers for the diagnosis of gliomas. Additionally, some circRNAs have been associated with glioma staging and may be useful in determining prognosis. Based on the stability and high conservation of circRNAs, we believe that circRNAs may have molecular targets that are useful for the treatment of glioma. In this review, we summarize the current research regarding the role of circRNAs in gliomas, discuss the potential value and role of circRNAs in gliomas, and provide new perspectives for future research.

Keywords

Circular RNA MicroRNA sponge Biomarker Targeted therapy 

Notes

Funding information

This work was supported by the National Natural Science Foundation of China (NSFC): 81860225. And Jiangxi Provincial Postgraduate Innovation Fund Project (No. YC2017-S102).

References

  1. Abdelmohsen K et al (2017) Identification of HuR target circular RNAs uncovers suppression of PABPN1 translation by CircPABPN1. RNA Biol 14:361–369.  https://doi.org/10.1080/15476286.2017.1279788 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Bai QL, Hu CW, Wang XR, Shang JX, Yin GF (2017) MiR-616 promotes proliferation and inhibits apoptosis in glioma cells by suppressing expression of SOX7 via the Wnt signaling pathway. Eur Rev Med Pharmacol Sci 21:5630–5637.  https://doi.org/10.26355/eurrev_201712_14006 CrossRefPubMedGoogle Scholar
  3. Barbagallo D et al (2016) Dysregulated miR-671-5p / CDR1-AS / CDR1 / VSNL1 axis is involved in glioblastoma multiforme. Oncotarget 7:4746–4759.  https://doi.org/10.18632/oncotarget.6621 CrossRefPubMedGoogle Scholar
  4. Barbagallo D et al. (2018) CircSMARCA5 inhibits migration of glioblastoma multiforme cells by regulating a molecular axis involving splicing factors SRSF1/SRSF3/PTB. Int J Mol Sci 19 doi: https://doi.org/10.3390/ijms19020480
  5. Begum S, Yiu A, Stebbing J, Castellano L (2018) Novel tumour suppressive protein encoded by circular RNA, circ-SHPRH, in glioblastomas. Oncogene 37:4055–4057.  https://doi.org/10.1038/s41388-018-0230-3 CrossRefPubMedGoogle Scholar
  6. Berges R, Balzeau J, Peterson AC, Eyer J (2012) A tubulin binding peptide targets glioma cells disrupting their microtubules, blocking migration, and inducing apoptosis. Mol Ther 20:1367–1377.  https://doi.org/10.1038/mt.2012.45 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bian A et al (2018) Circular RNA complement factor H (CFH) promotes glioma progression by sponging miR-149 and regulating AKT1. Med Sci Monit 24:5704–5712.  https://doi.org/10.12659/MSM.910180 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin.  https://doi.org/10.3322/caac.21492
  9. Burd CE, Jeck WR, Liu Y, Sanoff HK, Wang Z, Sharpless NE (2010) Expression of linear and novel circular forms of an INK4/ARF-associated non-coding RNA correlates with atherosclerosis risk. PLoS Genet 6:e1001233.  https://doi.org/10.1371/journal.pgen.1001233 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Chen Z, Duan X (2018) hsa_circ_0000177-miR-638-FZD7-Wnt signaling cascade contributes to the malignant behaviors in glioma. DNA Cell Biol 37:791–797.  https://doi.org/10.1089/dna.2018.4294 CrossRefPubMedGoogle Scholar
  11. Chen W, Schuman E (2016) Circular RNAs in brain and other tissues: a functional enigma. Trends Neurosci 39:597–604.  https://doi.org/10.1016/j.tins.2016.06.006 CrossRefPubMedGoogle Scholar
  12. Chen LL, Yang L (2015) Regulation of circRNA biogenesis. RNA Biol 12:381–388.  https://doi.org/10.1080/15476286.2015.1020271 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Chen J et al (2017) Circular RNA profile identifies circPVT1 as a proliferative factor and prognostic marker in gastric cancer. Cancer Lett 388:208–219.  https://doi.org/10.1016/j.canlet.2016.12.006 CrossRefPubMedGoogle Scholar
  14. Chen B et al (2018a) circEPSTI1 as a prognostic marker and mediator of triple-negative breast cancer progression. Theranostics 8:4003–4015.  https://doi.org/10.7150/thno.24106 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Chen G, Shi Y, Liu M, Sun J (2018b) circHIPK3 regulates cell proliferation and migration by sponging miR-124 and regulating AQP3 expression in hepatocellular carcinoma. Cell Death Dis 9:175.  https://doi.org/10.1038/s41419-017-0204-3 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Cheng J, Zhuo H, Xu M, Wang L, Xu H, Peng J, Hou J, Lin L, Cai J (2018) Regulatory network of circRNA-miRNA-mRNA contributes to the histological classification and disease progression in gastric cancer. J Transl Med 16:216.  https://doi.org/10.1186/s12967-018-1582-8 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Conn Simon J et al (2015) The RNA binding protein quaking regulates formation of circRNAs. Cell 160:1125–1134.  https://doi.org/10.1016/j.cell.2015.02.014 CrossRefPubMedGoogle Scholar
  18. Du WW, Yang W, Liu E, Yang Z, Dhaliwal P, Yang BB (2016) Foxo3 circular RNA retards cell cycle progression via forming ternary complexes with p21 and CDK2. Nucleic Acids Res 44:2846–2858.  https://doi.org/10.1093/nar/gkw027 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Du WW et al (2017) Foxo3 circular RNA promotes cardiac senescence by modulating multiple factors associated with stress and senescence responses. Eur Heart J 38:1402–1412.  https://doi.org/10.1093/eurheartj/ehw001 CrossRefPubMedGoogle Scholar
  20. Eidem TM, Kugel JF, Goodrich JA (2016) Noncoding RNAs: regulators of the mammalian transcription machinery. J Mol Biol 428:2652–2659.  https://doi.org/10.1016/j.jmb.2016.02.019 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Ferguson SD (2011) Malignant gliomas: diagnosis and treatment. Dis Mon 57:558–569.  https://doi.org/10.1016/j.disamonth.2011.08.020 CrossRefPubMedGoogle Scholar
  22. Filippenkov IB, Kalinichenko EO, Limborska SA, Dergunova LV (2017) Circular RNAs-one of the enigmas of the brain. Neurogenetics 18:1–6.  https://doi.org/10.1007/s10048-016-0490-4 CrossRefPubMedGoogle Scholar
  23. Gatson NN, Chiocca EA, Kaur B (2012) Anti-angiogenic gene therapy in the treatment of malignant gliomas. Neurosci Lett 527:62–70.  https://doi.org/10.1016/j.neulet.2012.08.001 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Ghigna C, Giordano S, Shen H, Benvenuto F, Castiglioni F, Comoglio PM, Green MR, Riva S, Biamonti G (2005) Cell motility is controlled by SF2/ASF through alternative splicing of the Ron protooncogene. Mol Cell 20:881–890.  https://doi.org/10.1016/j.molcel.2005.10.026 CrossRefPubMedGoogle Scholar
  25. Gomez GG, Volinia S, Croce CM, Zanca C, Li M, Emnett R, Gutmann DH, Brennan CW, Furnari FB, Cavenee WK (2014) Suppression of microRNA-9 by mutant EGFR signaling upregulates FOXP1 to enhance glioblastoma tumorigenicity. Cancer Res 74:1429–1439.  https://doi.org/10.1158/0008-5472.CAN-13-2117 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Han YN, Xia SQ, Zhang YY, Zheng JH, Li W (2017) Circular RNAs: a novel type of biomarker and genetic tools in cancer. Oncotarget 8:64551–64563.  https://doi.org/10.18632/oncotarget.18350 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Han B, Chao J, Yao H (2018) Circular RNA and its mechanisms in disease: from the bench to the clinic. Pharmacol Ther 187:31–44.  https://doi.org/10.1016/j.pharmthera.2018.01.010 CrossRefPubMedGoogle Scholar
  28. Hansen TB, Wiklund ED, Bramsen JB, Villadsen SB, Statham AL, Clark SJ, Kjems J (2011) miRNA-dependent gene silencing involving Ago2-mediated cleavage of a circular antisense RNA. EMBO J 30:4414–4422.  https://doi.org/10.1038/emboj.2011.359 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK, Kjems J (2013) Natural RNA circles function as efficient microRNA sponges. Nature 495:384–388.  https://doi.org/10.1038/nature11993 CrossRefGoogle Scholar
  30. He Q et al (2018) Circ-SHKBP1 regulates the angiogenesis of U87 glioma-exposed endothelial cells through miR-544a/FOXP1 and miR-379/FOXP2 pathways. Mol Ther Nucleic Acids 10:331–348.  https://doi.org/10.1016/j.omtn.2017.12.014 CrossRefPubMedGoogle Scholar
  31. Hentze MW, Preiss T (2013) Circular RNAs: splicing's enigma variations. EMBO J 32:923–925.  https://doi.org/10.1038/emboj.2013.53 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Huang G, Li S, Yang N, Zou Y, Zheng D, Xiao T (2017) Recent progress in circular RNAs in human cancers. Cancer Lett 404:8–18.  https://doi.org/10.1016/j.canlet.2017.07.002 CrossRefPubMedGoogle Scholar
  33. Ivanov A, Memczak S, Wyler E, Torti F, Porath HT, Orejuela MR, Piechotta M, Levanon EY, Landthaler M, Dieterich C, Rajewsky N (2015) Analysis of intron sequences reveals hallmarks of circular RNA biogenesis in animals. Cell Rep 10:170–177.  https://doi.org/10.1016/j.celrep.2014.12.019 CrossRefPubMedGoogle Scholar
  34. Jain RK, di Tomaso E, Duda DG, Loeffler JS, Sorensen AG, Batchelor TT (2007) Angiogenesis in brain tumours nature reviews. Neuroscience 8:610–622.  https://doi.org/10.1038/nrn2175 CrossRefPubMedGoogle Scholar
  35. Jeck WR et al (2012) Circular RNAs are abundant, conserved, and associated with ALU repeats Rna 19:141-157.  https://doi.org/10.1261/rna.035667.112
  36. Jin P, Huang Y, Zhu P, Zou Y, Shao T, Wang O (2018) CircRNA circHIPK3 serves as a prognostic marker to promote glioma progression by regulating miR-654/IGF2BP3 signaling. Biochem Biophys Res Commun 503:1570–1574.  https://doi.org/10.1016/j.bbrc.2018.07.081 CrossRefPubMedGoogle Scholar
  37. Kim C, Baek SH, Um JY, Shim BS, Ahn KS (2016) Resveratrol attenuates constitutive STAT3 and STAT5 activation through induction of PTPepsilon and SHP-2 tyrosine phosphatases and potentiates sorafenib-induced apoptosis in renal cell carcinoma. BMC Nephrol 17:19.  https://doi.org/10.1186/s12882-016-0233-7 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Lasda E, Parker R (2014) Circular RNAs: diversity of form and function. RNA 20:1829–1842.  https://doi.org/10.1261/rna.047126.114 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Li B, Huang MZ, Wang XQ, Tao BB, Zhong J, Wang XH, Zhang WC, Li ST (2015a) TMEM140 is associated with the prognosis of glioma by promoting cell viability and invasion. J Hematol Oncol 8:89.  https://doi.org/10.1186/s13045-015-0187-4 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Li Z et al (2015b) Exon-intron circular RNAs regulate transcription in the nucleus. Nat Struct Mol Biol 22:256–264.  https://doi.org/10.1038/nsmb.2959 CrossRefPubMedGoogle Scholar
  41. Li F, Ma K, Sun M, Shi S (2018a) Identification of the tumor-suppressive function of circular RNA ITCH in glioma cells through sponging miR-214 and promoting linear ITCH expression. Am J Transl Res 10:1373–1386PubMedPubMedCentralGoogle Scholar
  42. Li G-F, Li L, Yao Z-Q, Zhuang S-J (2018b) Hsa_circ_0007534/miR-761/ZIC5 regulatory loop modulates the proliferation and migration of glioma cells. Biochem Biophys Res Commun 499:765–771.  https://doi.org/10.1016/j.bbrc.2018.03.219 CrossRefPubMedGoogle Scholar
  43. Li G, Yang H, Han K, Zhu D, Lun P, Zhao Y (2018c) A novel circular RNA, hsa_circ_0046701, promotes carcinogenesis by increasing the expression of miR-142-3p target ITGB8 in glioma. Biochem Biophys Res Commun 498:254–261.  https://doi.org/10.1016/j.bbrc.2018.01.076 CrossRefPubMedGoogle Scholar
  44. Li S, Ma Y, Tan Y, Ma X, Zhao M, Chen B, Zhang R, Chen Z, Wang K (2018d) Profiling and functional analysis of circular RNAs in acute promyelocytic leukemia and their dynamic regulation during all-trans retinoic acid treatment. Cell Death Dis 9:651.  https://doi.org/10.1038/s41419-018-0699-2 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Liu F, Tong D, Li H, Liu M, Li J, Wang Z, Cheng X (2016) Bufalin enhances antitumor effect of paclitaxel on cervical tumorigenesis via inhibiting the integrin alpha2/beta5/FAK signaling pathway. Oncotarget 7:8896–8907.  https://doi.org/10.18632/oncotarget.6840 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Louis DN et al (2016) The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol 131:803–820.  https://doi.org/10.1007/s00401-016-1545-1 CrossRefPubMedGoogle Scholar
  47. Memczak S et al (2013) Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495:333–338.  https://doi.org/10.1038/nature11928 CrossRefPubMedGoogle Scholar
  48. Miller JJ, Wen PY (2016) Emerging targeted therapies for glioma. Expert Opin Emerg Drugs 21:441–452.  https://doi.org/10.1080/14728214.2016.1257609 CrossRefPubMedGoogle Scholar
  49. Mokrejs M (2006) IRESite: the database of experimentally verified IRES structures (www.iresite.org). Nucleic Acids Res 34:D125–D130.  https://doi.org/10.1093/nar/gkj081 CrossRefPubMedGoogle Scholar
  50. Petkovic S, Muller S (2015) RNA circularization strategies in vivo and in vitro. Nucleic Acids Res 43:2454–2465.  https://doi.org/10.1093/nar/gkv045 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Potente M, Urbich C, Sasaki KI, Hofmann WK, Heeschen C, Aicher A, Kollipara R, DePinho RA, Zeiher AM, Dimmeler S (2005) Involvement of Foxo transcription factors in angiogenesis and postnatal neovascularization. J Clin Invest 115:2382–2392.  https://doi.org/10.1172/JCI23126 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Qin M et al (2016) Hsa_circ_0001649: a circular RNA and potential novel biomarker for hepatocellular carcinoma. Cancer Biomark 16:161–169.  https://doi.org/10.3233/CBM-150552 CrossRefPubMedGoogle Scholar
  53. Qu S, Yang X, Li X, Wang J, Gao Y, Shang R, Sun W, Dou K, Li H (2015) Circular RNA: a new star of noncoding RNAs. Cancer Lett 365:141–148.  https://doi.org/10.1016/j.canlet.2015.06.003 CrossRefPubMedGoogle Scholar
  54. Salzman J, Gawad C, Wang PL, Lacayo N, Brown PO (2012) Circular RNAs are the predominant transcript isoform from hundreds of human genes in diverse cell types. PLoS One 7:e30733.  https://doi.org/10.1371/journal.pone.0030733 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Salzman J, Chen RE, Olsen MN, Wang PL, Brown PO (2013) Cell-type specific features of circular RNA expression. PLoS Genet 9:e1003777.  https://doi.org/10.1371/journal.pgen.1003777 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Sanger HL, Klotz G, Riesner D, Gross HJ, Kleinschmidt AK (1976) Viroids are single-stranded covalently closed circular RNA molecules existing as highly base-paired rod-like structures. Proc Natl Acad Sci U S A 73:3852–3856CrossRefGoogle Scholar
  57. Schwartzbaum JA, Fisher JL, Aldape KD, Wrensch M (2006) Epidemiology and molecular pathology of glioma nature clinical practice. Neurology 2:494–503; quiz 491 p following 516.  https://doi.org/10.1038/ncpneuro0289 CrossRefPubMedGoogle Scholar
  58. Shehade H, Acolty V, Moser M, Oldenhove G (2015) Cutting edge: hypoxia-inducible factor 1 negatively regulates Th1 function. J Immunol 195:1372–1376.  https://doi.org/10.4049/jimmunol.1402552 CrossRefPubMedGoogle Scholar
  59. Song X, Zhang N, Han P, Moon BS, Lai RK, Wang K, Lu W (2016) Circular RNA profile in gliomas revealed by identification tool UROBORUS. Nucleic Acids Res 44:e87.  https://doi.org/10.1093/nar/gkw075 CrossRefPubMedPubMedCentralGoogle Scholar
  60. Stupp R, Mason WP, van den Bent M, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO, European Organisation for Research and Treatment of Cancer Brain Tumor and Radiotherapy Groups, National Cancer Institute of Canada Clinical Trials Group (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987–996.  https://doi.org/10.1056/NEJMoa043330 CrossRefPubMedGoogle Scholar
  61. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A (2015) Global cancer statistics, 2012. CA Cancer J Clin 65:87–108.  https://doi.org/10.3322/caac.21262 CrossRefGoogle Scholar
  62. Unk I et al (2006) Human SHPRH is a ubiquitin ligase for Mms2-Ubc13-dependent polyubiquitylation of proliferating cell nuclear antigen. Proc Natl Acad Sci U S A 103:18107–18112.  https://doi.org/10.1073/pnas.0608595103 CrossRefPubMedPubMedCentralGoogle Scholar
  63. van Rossum D, Verheijen BM, Pasterkamp RJ (2016) Circular RNAs: novel regulators of neuronal development. Front Mol Neurosci 9:74.  https://doi.org/10.3389/fnmol.2016.00074 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Wan L, Zhang L, Fan K, Cheng ZX, Sun QC, Wang JJ (2016) Circular RNA-ITCH suppresses lung cancer proliferation via inhibiting the Wnt/beta-catenin pathway. Biomed Res Int 2016:1579490–1579411.  https://doi.org/10.1155/2016/1579490 CrossRefPubMedPubMedCentralGoogle Scholar
  65. Wang Z (2015) Not just a sponge: new functions of circular RNAs discovered Sci China. Life Sci 58:407–408.  https://doi.org/10.1007/s11427-015-4826-3 CrossRefGoogle Scholar
  66. Wang Y, Jiang T (2013) Understanding high grade glioma: molecular mechanism, therapy and comprehensive management. Cancer Lett 331:139–146.  https://doi.org/10.1016/j.canlet.2012.12.024 CrossRefPubMedGoogle Scholar
  67. Wang Q et al (2016a) Interleukin-12 inhibits the hepatocellular carcinoma growth by inducing macrophage polarization to the M1-like phenotype through downregulation of Stat-3. Mol Cell Biochem 415:157–168.  https://doi.org/10.1007/s11010-016-2687-0 CrossRefPubMedGoogle Scholar
  68. Wang Z, Guo Q, Wang R, Xu G, Li P, Sun Y, She X, Liu Q, Chen Q, Yu Z, Liu C, Xiong J, Li G, Wu M (2016b) The D domain of LRRC4 anchors ERK1/2 in the cytoplasm and competitively inhibits MEK/ERK activation in glioma cells. J Hematol Oncol 9:130.  https://doi.org/10.1186/s13045-016-0355-1 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Wang Y, Mo Y, Gong Z, Yang X, Yang M, Zhang S, Xiong F, Xiang B, Zhou M, Liao Q, Zhang W, Li X, Li X, Li Y, Li G, Zeng Z, Xiong W (2017) Circular RNAs in human cancer. Mol Cancer 16:25.  https://doi.org/10.1186/s12943-017-0598-7 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Wang HX et al (2018a) Expression profile of circular RNAs in IDH-wild type glioblastoma tissues. Clin Neurol Neurosurg 171:168–173.  https://doi.org/10.1016/j.clineuro.2018.06.020 CrossRefPubMedGoogle Scholar
  71. Wang Q, Qu L, Chen X, Zhao YH, Luo Q (2018b) Progress in understanding the relationship between circular RNAs and neurological disorders. J Mol Neurosci 65:546–556.  https://doi.org/10.1007/s12031-018-1125-z CrossRefPubMedGoogle Scholar
  72. Wang R et al (2018c) CircNT5E acts as a sponge of miR-422a to promote glioblastoma tumorigenesis. Cancer Res 78:4812–4825.  https://doi.org/10.1158/0008-5472.CAN-18-0532 CrossRefPubMedGoogle Scholar
  73. Wang Y et al (2018d) Decreased circular RNA hsa_circ_0001649 predicts unfavorable prognosis in glioma and exerts oncogenic properties in vitro and in vivo. Gene 676:117–122.  https://doi.org/10.1016/j.gene.2018.07.037 CrossRefPubMedGoogle Scholar
  74. Wu W, Dang S, Feng Q, Liang J, Wang Y, Fan N (2017) MicroRNA-542-3p inhibits the growth of hepatocellular carcinoma cells by targeting FZD7/Wnt signaling pathway. Biochem Biophys Res Commun 482:100–105.  https://doi.org/10.1016/j.bbrc.2016.10.136 CrossRefPubMedGoogle Scholar
  75. Wurth L, Gebauer F (2015) RNA-binding proteins, multifaceted translational regulators in cancer. Biochim Biophys Acta 1849:881–886.  https://doi.org/10.1016/j.bbagrm.2014.10.001 CrossRefPubMedGoogle Scholar
  76. Xie G (2018) Circular RNA hsa-circ-0012129 promotes cell proliferation and invasion in 30 cases of human glioma and human glioma cell lines U373, A172, and SHG44, by targeting microRNA-661 (miR-661). Med Sci Monit 24:2497–2507.  https://doi.org/10.12659/msm.909229 CrossRefPubMedPubMedCentralGoogle Scholar
  77. Xu H, Zhang Y, Qi L, Ding L, Jiang H, Yu H (2018) NFIX circular RNA promotes glioma progression by regulating miR-34a-5p via notch signaling pathway. Front Mol Neurosci 11:225.  https://doi.org/10.3389/fnmol.2018.00225 CrossRefPubMedPubMedCentralGoogle Scholar
  78. Yada M, Hatakeyama S, Kamura T, Nishiyama M, Tsunematsu R, Imaki H, Ishida N, Okumura F, Nakayama K, Nakayama KI (2004) Phosphorylation-dependent degradation of c-Myc is mediated by the F-box protein Fbw7. EMBO J 23:2116–2125.  https://doi.org/10.1038/sj.emboj.7600217 CrossRefPubMedPubMedCentralGoogle Scholar
  79. Yang P et al (2016) Silencing of cZNF292 circular RNA suppresses human glioma tube formation via the Wnt/beta-catenin signaling pathway. Oncotarget 7:63449–63455.  https://doi.org/10.18632/oncotarget.11523 CrossRefPubMedPubMedCentralGoogle Scholar
  80. Yang Y, Gao X, Zhang M, Yan S, Sun C, Xiao F, Huang N, Yang X, Zhao K, Zhou H, Huang S, Xie B, Zhang N (2018) Novel role of FBXW7 circular RNA in repressing glioma tumorigenesis. J Natl Cancer Inst 110:304–315.  https://doi.org/10.1093/jnci/djx166 CrossRefGoogle Scholar
  81. Yi YY, Yi J, Zhu X, Zhang J, Zhou J, Tang X, Lin J, Wang P, Deng ZQ (2018) Circular RNA of vimentin expression as a valuable predictor for acute myeloid leukemia development and prognosis. J Cell Physiol.  https://doi.org/10.1002/jcp.27145
  82. Yuan RH, Lai HS, Hsu HC, Lai PL, Jeng YM (2014) Expression of bile duct transcription factor HNF1beta predicts early tumor recurrence and is a stage-independent prognostic factor in hepatocellular carcinoma. J Gastrointest Surg 18:1784–1794.  https://doi.org/10.1007/s11605-014-2596-z CrossRefPubMedGoogle Scholar
  83. Yuan Y, Jiaoming L, Xiang W, Yanhui L, Shu J, Maling G, Qing M (2018) Analyzing the interactions of mRNAs, miRNAs, lncRNAs and circRNAs to predict competing endogenous RNA networks in glioblastoma. J Neuro-Oncol 137:493–502.  https://doi.org/10.1007/s11060-018-2757-0 CrossRefGoogle Scholar
  84. Zeng K et al (2018) CircHIPK3 promotes colorectal cancer growth and metastasis by sponging miR-7. Cell Death Dis 9:417.  https://doi.org/10.1038/s41419-018-0454-8 CrossRefPubMedPubMedCentralGoogle Scholar
  85. Zhang Y et al (2013) Circular intronic long noncoding RNAs molecular. cell 51:792–806.  https://doi.org/10.1016/j.molcel.2013.08.017 CrossRefGoogle Scholar
  86. Zhang XO, Wang HB, Zhang Y, Lu X, Chen LL, Yang L (2014) Complementary sequence-mediated exon circularization. Cell 159:134–147.  https://doi.org/10.1016/j.cell.2014.09.001 CrossRefPubMedGoogle Scholar
  87. Zhang M, Huang N, Yang X, Luo J, Yan S, Xiao F, Chen W, Gao X, Zhao K, Zhou H, Li Z, Ming L, Xie B, Zhang N (2018) A novel protein encoded by the circular form of the SHPRH gene suppresses glioma tumorigenesis. Oncogene 37:1805–1814.  https://doi.org/10.1038/s41388-017-0019-9 CrossRefPubMedPubMedCentralGoogle Scholar
  88. Zhao ZJ, Shen J (2017) Circular RNA participates in the carcinogenesis and the malignant behavior of cancer. RNA Biol 14:514–521.  https://doi.org/10.1080/15476286.2015.1122162 CrossRefPubMedGoogle Scholar
  89. Zheng J, Liu X, Xue Y, Gong W, Ma J, Xi Z, Que Z, Liu Y (2017) TTBK2 circular RNA promotes glioma malignancy by regulating miR-217/HNF1beta/Derlin-1 pathway. J Hematol Oncol 10:52.  https://doi.org/10.1186/s13045-017-0422-2 CrossRefPubMedPubMedCentralGoogle Scholar
  90. Zhou Y, Huang T, Siu HL, Wong CC, Dong Y, Wu F, Zhang B, Wu WKK, Cheng ASL, Yu J, To KF, Kang W (2017) IGF2BP3 functions as a potential oncogene and is a crucial target of miR-34a in gastric carcinogenesis. Mol Cancer 16:77.  https://doi.org/10.1186/s12943-017-0647-2 CrossRefPubMedPubMedCentralGoogle Scholar
  91. Zhou J, Wang H, Chu J, Huang Q, Li G, Yan Y, Xu T, Chen J, Wang Y (2018a) Circular RNA hsa_circ_0008344 regulates glioblastoma cell proliferation, migration, invasion, and apoptosis. J Clin Lab Anal 32:e22454.  https://doi.org/10.1002/jcla.22454 CrossRefPubMedGoogle Scholar
  92. Zhou MY, Yang JM, Xiong XD (2018b) The emerging landscape of circular RNA in cardiovascular diseases. J Mol Cell Cardiol 122:134–139.  https://doi.org/10.1016/j.yjmcc.2018.08.012 CrossRefPubMedGoogle Scholar
  93. Zhu J et al (2017) Differential expression of circular RNAs in glioblastoma multiforme and its correlation with prognosis. Transl Oncol 10:271–279.  https://doi.org/10.1016/j.tranon.2016.12.006 CrossRefPubMedPubMedCentralGoogle Scholar
  94. Zlotorynski E (2015) Non-coding RNA: circular RNAs promote transcription. Nat Rev Mol Cell Biol 16:206.  https://doi.org/10.1038/nrm3967 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of NeurosurgeryThe First Affiliated Hospital of Nanchang UniversityNanchangChina

Personalised recommendations