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Circ_0001588 Upregulates ERBB4 to Promote Glioma Malignant Progression Through Sponging miR-1281

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Abstract

Circular RNA (circRNA) plays a crucial part in glioma progression. However, the function of circ_0001588 in glioma development is still unknown. The study aims to reveal the role of circ_0001588 in glioma malignant progression and the inner molecular mechanism. The RNA expressions of circ_0001588, microRNA-1281 (miR-1281), and erb-b2 receptor tyrosine kinase 4 (ERBB4) were detected by qRT-PCR. Protein expression was checked by western blot analysis or immunohistochemistry assay. Cell proliferation was investigated by cell counting kit-8 and colony formation assays. Flow cytometry, transwell, and tube formation assays were used to detect cell apoptosis, cell migration, and invasion as well as angiogenesis, respectively. The binding relationship between miR-1281 and circ_0001588 or ERBB4 was identified by dual-luciferase reporter and RNA immunoprecipitation assays. Mouse model assay was performed to confirm the effect of circ_0001588 knockdown on tumor formation in vivo. Circ_0001588 and ERBB4 expressions were significantly upregulated, while miR-1281 was downregulated in glioma tissues and cells compared with control groups. Circ_0001588 expression was closely related to tumor size and WHO grade of glioma. Decreased expression of circ_0001588 in glioma cells led to significant decreases of cell proliferation, migration, invasion, and tube formation and an increase of cell apoptosis. Additionally, downregulation of miR-1281, a target miRNA of circ_0001588, rescued circ_0001588 knockdown-mediated effects. MiR-1281 also inhibited glioma malignant progression by targeting ERBB4. Importantly, circ_0001588 regulated ERBB4 expression by interacting with miR-1281. Furthermore, circ_0001588 depletion suppressed tumor formation in vivo. Circ_0001588 acted as an oncogene in glioma malignant progression by miR-1281/ERBB4 pathway, suggesting the potential of circ_0001588 as a therapeutic target for glioma.

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References

  • Alamdari-Palangi V, Karami Z, Karami H, Baazm M (2020) MiRNA-7 Replacement effect on proliferation and tarceva-sensitivity in U373-MG cell line. Asian Pac J Cancer Prev 21(6):1747–1753

    Article  Google Scholar 

  • Bush NA, Chang SM, Berger MS (2017) Current and future strategies for treatment of glioma. Neurosurg Rev 40(1):1–14

    Article  Google Scholar 

  • Chen M, Liu X, Xie P, Wang P, Liu M, Zhan Y et al (2020) Circular RNA circ_0074026 indicates unfavorable prognosis for patients with glioma and facilitates oncogenesis of tumor cells by targeting miR-1304 to modulate ERBB4 expression. J Cell Physiol 235(5):4688–4697

    Article  CAS  Google Scholar 

  • Fan LY, Shi KY, Xu D, Ren LP, Yang P, Zhang L et al (2019) LncRNA GIHCG regulates microRNA-1281 and promotes malignant progression of breast cancer. Eur Rev Med Pharmacol Sci 23(24):10842–10850

    PubMed  Google Scholar 

  • Fang Z, Rajewsky N (2011) The impact of miRNA target sites in coding sequences and in 3’UTRs. PLoS One 6(3):e18067

    Article  CAS  Google Scholar 

  • Fornasari BE, El Soury M, De Marchis S, Perroteau I, Geuna S, Gambarotta G (2016) Neuregulin1 alpha activates migration of neuronal progenitors expressing ErbB4. Mol Cell Neurosci 77:87–94

    Article  CAS  Google Scholar 

  • Gao C, Shen J, Meng ZX, He XF (2020) Sevoflurane inhibits glioma cells proliferation and metastasis through miRNA-124-3p/ROCK1 axis. Pathol Oncol Res 26(2):947–954

    Article  CAS  Google Scholar 

  • He Z, Ruan X, Liu X, Zheng J, Liu Y, Liu L et al (2019) FUS/circ_002136/miR-138-5p/SOX13 feedback loop regulates angiogenesis in Glioma. J Exp Clin Cancer Res 38(1):65

    Article  Google Scholar 

  • Hu G, Liu N, Wang H, Wang Y, Guo Z (2019) LncRNA LINC01857 promotes growth, migration, and invasion of glioma by modulating miR-1281/TRIM65 axis. J Cell Physiol 234(12):22009–22016

    Article  CAS  Google Scholar 

  • Huang D-W, Huang M, Lin X-S, Huang Q (2017) CD155 expression and its correlation with clinicopathologic characteristics, angiogenesis, and prognosis in human cholangiocarcinoma. Onco Targets Ther 10:3817–3825

    Article  Google Scholar 

  • Jeck WR, Sorrentino JA, Wang K, Slevin MK, Burd CE, Liu J et al (2013) Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA (new York, NY) 19(2):141–157

    Article  CAS  Google Scholar 

  • Jiang J, Ma B, Li X, Jin W, Han C, Wang L et al (2018) MiR-1281, a p53-responsive microRNA, impairs the survival of human osteosarcoma cells upon ER stress via targeting USP39. Am J Cancer Res 8(9):1764–1774

    PubMed  PubMed Central  CAS  Google Scholar 

  • Jiang Y, Zhou J, Zhao J, Zhang H, Li L, Li H et al (2020) The U2AF2 /circRNA ARF1/miR-342-3p/ISL2 feedback loop regulates angiogenesis in glioma stem cells. J Exp Clin Cancer Res 39(1):182

    Article  CAS  Google Scholar 

  • Jin T, Liu M, Liu Y, Li Y, Xu Z, He H et al (2020) Lcn2-derived Circular RNA (hsa_circ_0088732) Inhibits cell apoptosis and promotes EMT in glioma via the miR-661/RAB3D Axis. Front Oncol 10:170

    Article  Google Scholar 

  • Kristensen LS, Andersen MS, Stagsted LVW, Ebbesen KK, Hansen TB, Kjems J (2019) The biogenesis, biology and characterization of circular RNAs. Nat Rev Genet 20(11):675–691

    Article  CAS  Google Scholar 

  • Li R, Jiang J, Shi H, Qian H, Zhang X, Xu W (2020a) CircRNA: a rising star in gastric cancer. Cell Mol Life Sci 77(9):1661–1680

    Article  CAS  Google Scholar 

  • Li S, Li W, Chen G, Huang J, Li W (2020b) MiRNA-27a-3p induces temozolomide resistance in glioma by inhibiting NF1 level. Am J Transl Res 12(8):4749–4756

    PubMed  PubMed Central  CAS  Google Scholar 

  • Liang H, Liu M, Yan X, Zhou Y, Wang W, Wang X et al (2015) miR-193a-3p functions as a tumor suppressor in lung cancer by down-regulating ERBB4. J Biol Chem 290(2):926–940

    Article  CAS  Google Scholar 

  • Liu G, Jiang Z, Qiao M, Wang F (2019) Lnc-GIHCG promotes cell proliferation and migration in gastric cancer through miR- 1281 adsorption. Mol Genet Genomic Med 7(6):e711

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Song L, Ni H, Sun L, Jiao W, Chen L et al (2017) ERBB4 acts as a suppressor in the development of hepatocellular carcinoma. Carcinogenesis 38(4):465–473

    Article  CAS  Google Scholar 

  • Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, Rybak A et al (2013) Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495(7441):333–338

    Article  CAS  Google Scholar 

  • Omuro A, DeAngelis LM (2013) Glioblastoma and other malignant gliomas: a clinical review. JAMA 310(17):1842–1850

    Article  CAS  Google Scholar 

  • Paez JG, Jänne PA, Lee JC, Tracy S, Greulich H, Gabriel S et al (2004) EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 304(5676):1497–1500

    Article  CAS  Google Scholar 

  • Rolle K (2015) miRNA Multiplayers in glioma. From bench to bedside. Acta Biochim Pol 62(3):353–365

    Article  CAS  Google Scholar 

  • Segers VFM, Dugaucquier L, Feyen E, Shakeri H, De Keulenaer GW (2020) The role of ErbB4 in cancer. Cell Oncol (Dordr) 43(3):335–352

    Article  Google Scholar 

  • Shi F, Shi Z, Zhao Y, Tian J (2019) CircRNA hsa-circ-0014359 promotes glioma progression by regulating miR-153/PI3K signaling. Biochem Biophys Res Commun 510(4):614–620

    Article  CAS  Google Scholar 

  • Sun Z (2020) Circular RNA hsa_circ_0001588 promotes the malignant progression of lung adenocarcinoma by modulating miR-524–3p/NACC1 signaling. Life Sci 259:118157

    Article  CAS  Google Scholar 

  • Verduci L, Strano S, Yarden Y, Blandino G (2019) The circRNA-microRNA code: emerging implications for cancer diagnosis and treatment. Mol Oncol 13(4):669–680

    Article  Google Scholar 

  • Xu J, Gong L, Qian Z, Song G, Liu J (2018) ERBB4 promotes the proliferation of gastric cancer cells via the PI3K/Akt signaling pathway. Oncol Rep 39(6):2892–2898

    PubMed  CAS  Google Scholar 

  • Wang X, Feng H, Dong W, Wang F, Zhang G, Wu J (2020) Hsa_circ_0008225 inhibits tumorigenesis of glioma via sponging miR-890 and promoting ZMYND11 expression. J Pharmacol Sci 143(2):74–82

    Article  CAS  Google Scholar 

  • Wang Z (2017) ErbB receptors and cancer. Methods Mol Biol 1652:3–35

    Article  CAS  Google Scholar 

  • Woolf EC, Scheck AC (2015) The ketogenic diet for the treatment of malignant glioma. J Lipid Res 56(1):5–10

    Article  CAS  Google Scholar 

  • Zhang HD, Jiang LH, Sun DW, Hou JC, Ji ZL (2018) CircRNA: a novel type of biomarker for cancer. Breast Cancer 25(1):1–7

    Article  Google Scholar 

  • Zhang L, Bu Z, Shen J, Shang L, Chen Y, Wang Y (2020) A novel circular RNA (hsa_circ_0000370) increases cell viability and inhibits apoptosis of FLT3-ITD-positive acute myeloid leukemia cells by regulating miR-1299 and S100A7A. Biomed Pharmacother 122:109619

    Article  CAS  Google Scholar 

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Funding

This work was supported by National Natural Science Foundation of China (No. 81901567).

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Author notes

  1. Jun Wang and Juan Li contributed equally to this paper.

Authors and Affiliations

  1. Department of Neurosurgery, Fancheng District, Xiangyang No.1 People’s Hospital, Hubei University of Medicine, No. 6 Chaoyang Road, Xiangyang City, Hubei Province, 441000, China

    Jun Wang, Juan Li & Yanwei Dang

  2. Department of Obstetrics and Gynaecology, Xiangyang No.1 People’s Hospital, Hubei University of Medicine, Xiangyang City, Hubei Province, China

    Peng Duan

  3. Department of Urology, Xiangyang No.1 People’s Hospital, Hubei University of Medicine, Xiangyang City, Hubei Province, China

    Tao Shi

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  1. Jun Wang
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  2. Juan Li
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  3. Peng Duan
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  4. Yanwei Dang
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  5. Tao Shi
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Contributions

Jun Wang was responsible for drafting the manuscript. Jun Wang and Juan Li contributed to the analysis and interpretation of data. Jun Wang, Yanwei Dang, and Tao Shi contributed in the data collection. All authors read and approved the final manuscript.

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Correspondence to Yanwei Dang or Tao Shi.

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Wang, J., Li, J., Duan, P. et al. Circ_0001588 Upregulates ERBB4 to Promote Glioma Malignant Progression Through Sponging miR-1281. Neurotox Res 40, 89–102 (2022). https://doi.org/10.1007/s12640-021-00464-5

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  • DOI: https://doi.org/10.1007/s12640-021-00464-5

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