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Circular RNA circMMP1 Contributes to the Progression of Glioma Through Regulating TGIF2 Expression by Sponging miR-195-5p

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Abstract

Glioma is characterized by high morbidity and mortality worldwide. Circular RNA (circRNA) matrix metallopeptidase 1 (circMMP1, hsa_circ_0024108) was reported to be increased in glioma. This study is designed to explore the role and mechanism of circMMP1 in glioma progression. CircMMP1, linear MMP1, microRNA-195-5p (miR-195-5p), and transforming growth factor-beta-induced 2 (TGIF2) level were detected by real-time quantitative polymerase chain reaction (RT-qPCR). The protein levels of TGIF2, Beclin1, and p62 were examined by Western blot assay. Colony number, migration, invasion, and apoptosis were detected by Colony formation, transwell, and flow cytometry assays, severally. The binding relationship between miR-195-5p and circMMP1 or TGIF2 was predicted by starbase or Targetscan and then verified by a dual-luciferase reporter and RNA Immunoprecipitation (RIP) assays. The biological role of circMMP1 on glioma cell growth was examined by the xenograft tumor model in vivo. CircMMP1 and TGIF2 expression were upregulated, and miR-195-5p expression was downregulated in glioma tissues and cells. And the knockdown of circMMP1 could block colony formation, migration, and invasion and expedite apoptosis and autophagy in glioma cells. The mechanical analysis discovered that circMMP1 acted as a sponge of miR-195-5p to regulate TGIF2 expression. CircMMP1 knockdown suppressed cell growth of glioma in vivo. CircMMP1 boosted glioma progression partly by targeting the miR-195-5p/TGIF2 axis, suggesting a promising circRNA-targeted therapy for glioma treatment.

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All data generated or analyzed during this study are included in this article.

Abbreviations

TGIF2:

Transforming growth factor-beta-induced 2

References

  • Chen B, Huang S (2018) Circular RNA: an emerging non-coding RNA as a regulator and biomarker in cancer. Cancer Lett 418:41–50

    Article  CAS  Google Scholar 

  • Diao Y, Jin B, Huang L, Zhou W (2018) MiR-129-5p inhibits glioma cell progression in vitro and in vivo by targeting TGIF2. J Cell Mol Med 22(4):2357–2367

    Article  CAS  Google Scholar 

  • Dou D, Ren X, Han M, Xu X, Ge X, Gu Y, Wang X (2020) CircUBE2D2 (hsa_circ_0005728) promotes cell proliferation, metastasis and chemoresistance in triple-negative breast cancer by regulating miR-512–3p/CDCA3 axis. Cancer Cell Int 20:454. https://doi.org/10.1186/s12935-020-01547-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ebbesen KK, Kjems J, Hansen TB (2016) Circular RNAs: identification, biogenesis and function. Biochim Biophys Acta 1859(1):163–168

    Article  CAS  Google Scholar 

  • Gregory RI, Chendrimada TP, Cooch N, Shiekhattar R (2005) Human RISC couples microRNA biogenesis and posttranscriptional gene silencing. Cell 123(4):631–640

    Article  CAS  Google Scholar 

  • Gui X, Li Y, Zhang X, Su K, Cao W (2020) Circ_LDLR promoted the development of papillary thyroid carcinoma via regulating miR-195-5p/LIPH axis. Cancer Cell Int 20:241

    Article  CAS  Google Scholar 

  • Guo Z, Guozhang H, Wang H, Li Z, Liu N (2019) Ampelopsin inhibits human glioma through inducing apoptosis and autophagy dependent on ROS generation and JNK pathway. Biomed Pharmacother 116:108524

    Article  CAS  Google Scholar 

  • He R, Liu P, Xie X, Zhou Y, Liao Q, Xiong W, Li X, Li G, Zeng Z, Tang H (2017) circGFRA1 and GFRA1 act as ceRNAs in triple negative breast cancer by regulating miR-34a. J Exp Clin Cancer Res 36(1):145

    Article  Google Scholar 

  • Jiang J, Wu RH, Zhou HL, Li ZM, Kou D, Deng Z, Dong M, Chen LH (2020) TGIF2 promotes cervical cancer metastasis by negatively regulating FCMR. Eur Rev Med Pharmacol Sci 24(11):5953–5962

    CAS  PubMed  Google Scholar 

  • Kagami H, Akutsu T, Maegawa S, Hosokawa H, Nacher JC (2015) Determining associations between human diseases and non-coding RNAs with critical roles in network control. Sci Rep 5:14577

    Article  CAS  Google Scholar 

  • Knizhnik AV, Roos WP, Nikolova T, Quiros S, Tomaszowski KH, Christmann M, Kaina B (2013) Survival and death strategies in glioma cells: autophagy, senescence and apoptosis triggered by a single type of temozolomide-induced DNA damage. PLoS ONE 8(1):e55665

    Article  CAS  Google Scholar 

  • Kong L, Zhang C (2020) LncRNA DLX6-AS1 aggravates the development of ovarian cancer via modulating FHL2 by sponging miR-195-5p. Cancer Cell Int 20:370

    Article  CAS  Google Scholar 

  • Lenting K, Verhaak R, Ter Laan M, Wesseling P, Leenders W (2017) Glioma: experimental models and reality. Acta Neuropathol 133(2):263–282

    Article  Google Scholar 

  • Li G, Yang H, Han K, Zhu D, Lun P, Zhao Y (2018) 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(1):254–261

    Article  CAS  Google Scholar 

  • Liu C, Yi X (2020) miR-541 serves as a prognostic biomarker of osteosarcoma and its regulatory effect on tumor cell proliferation, migration and invasion by targeting TGIF2. Diagn Pathol 15(1):96

    Article  CAS  Google Scholar 

  • Liu J, Liang H, Chen C, Wang X, Qu F, Wang H, Yang K, Wang Q, Zhao N, Meng J, Gao A (2019) Ivermectin induces autophagy-mediated cell death through the AKT/mTOR signaling pathway in glioma cells. Biosci Rep. https://doi.org/10.1042/BSR20192489

  • López-Jiménez E, Rojas AM, Andrés-León E (2018) RNA sequencing and prediction tools for circular RNAs analysis. Adv Exp Med Biol 1087:17–33

    Article  Google Scholar 

  • Ma N, Li X, Wei H, Zhang H, Zhang S (2020) Circular RNA circNFATC3 acts as a miR-9–5p sponge to promote cervical cancer development by upregulating SDC2. Cell Oncol. https://doi.org/10.1007/s13402-020-00555-z

    Article  Google Scholar 

  • Meng S, Zhou H, Feng Z, Xu Z, Tang Y, Li P, Wu M (2017) CircRNA: functions and properties of a novel potential biomarker for cancer. Mol Cancer 16(1):94

    Article  Google Scholar 

  • 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(2):141–148

    Article  CAS  Google Scholar 

  • Qu Y, Zhu J, Liu J, Qi L (2019) Circular RNA circ_0079593 indicates a poor prognosis and facilitates cell growth and invasion by sponging miR-182 and miR-433 in glioma. J Cell Biochem 120(10):18005–18013

    Article  CAS  Google Scholar 

  • Rizzo A, Donzelli S, Girgenti V, Sacconi A, Vasco C, Salmaggi A, Blandino G, Maschio M, Ciusani E (2017) In vitro antineoplastic effects of brivaracetam and lacosamide on human glioma cells. J Exp Clin Cancer Res 36(1):76

    Article  Google Scholar 

  • Song YZ, Li JF (2018) Circular RNA hsa_circ_0001564 regulates osteosarcoma proliferation and apoptosis by acting miRNA sponge. Biochem Biophys Res Commun 495(3):2369–2375

    Article  CAS  Google Scholar 

  • Tyler MA, Ulasov IV, Lesniak MS (2009) Cancer cell death by design: apoptosis, autophagy and glioma virotherapy. Autophagy 5(6):856–857

    Article  Google Scholar 

  • Wang J, Qi Q, Zhou W, Feng Z, Huang B, Chen A, Zhang D, Li W, Zhang Q, Jiang Z, Bjerkvig R, Prestegarden L, Thorsen F, Wang X, Li X, Wang J (2018) Inhibition of glioma growth by flavokawain B is mediated through endoplasmic reticulum stress induced autophagy. Autophagy 14(11):2007–2022

    Article  CAS  Google Scholar 

  • Wang Y, Sui X, Zhao H, Cong L, Li Y, Xin T, Guo M, Hao W (2018) Decreased circular RNA hsa_circ_0001649 predicts unfavorable prognosis in glioma and exerts oncogenic properties in vitro and in vivo. Gene 676:117–122

    Article  CAS  Google Scholar 

  • Wang X, Li XD, Fu Z, Zhou Y, Huang X, Jiang X (2020) Long non-coding RNA LINC00473/miR-195-5p promotes glioma progression via YAP1-TEAD1-Hippo signaling. Int J Oncol 56(2):508–521

    CAS  PubMed  Google Scholar 

  • Wang H, Niu X, Jiang H, Mao F, Zhong B, Jiang X, Fu G (2020) Long non-coding RNA DLX6-AS1 facilitates bladder cancer progression through modulating miR-195-5p/VEGFA signaling pathway. Aging 12(16):16021–16034

    Article  CAS  Google Scholar 

  • Weller M, Wick W, Aldape K, Brada M, Berger M, Pfister SM, Nishikawa R, Rosenthal M, Wen PY, Stupp R, Reifenberger G (2015) Glioma. Nat Rev Dis Primers 1:15017

    Article  Google Scholar 

  • Xing Z, Li S, Liu Z, Zhang C, Meng M, Bai Z (2020) The long non-coding RNA LINC00473 contributes to cell proliferation via JAK-STAT3 signaling pathway by regulating miR-195–5p/SEPT2 axis in prostate cancer. Biosci Rep. https://doi.org/10.1042/BSR20191850

  • Xiong S, Li D, Wang D, Huang L, Liang G, Wu Z, Long J, Yang D, Teng Y, Lei S, Li Y (2020) Circular RNA MYLK promotes glycolysis and proliferation of non-small cell lung cancer cells by sponging miR-195–5p and increasing glucose transporter member 3 expression. Cancer Manag Res 12:5469–5478

    Article  CAS  Google Scholar 

  • Xu N, Xu J, Zuo Z, Liu Y, Yan F, Han C (2020) Downregulation of lncRNA SNHG12 reversed IGF1R-induced osteosarcoma metastasis and proliferation by targeting miR-195-5p. Gene 726:144145

    Article  CAS  Google Scholar 

  • Yang M, Li G, Fan L, Zhang G, Xu J, Zhang J (2019) Circular RNA circ_0034642 elevates BATF3 expression and promotes cell proliferation and invasion through miR-1205 in glioma. Biochem Biophys Res Commun 508(3):980–985

    Article  CAS  Google Scholar 

  • Yang Y, Zhang Y, Chen B, Ding L, Mu Z (2019) Elevation of circular RNA circ-POSTN facilitates cell growth and invasion by sponging miR-1205 in glioma. J Cell Biochem 120(10):16567–16574

    Article  CAS  Google Scholar 

  • Yi C, Li H, Li D, Qin X, Wang J, Liu Y, Liu Z, Zhang J (2019) Upregulation of circular RNA circ_0034642 indicates unfavorable prognosis in glioma and facilitates cell proliferation and invasion via the miR-1205/BATF3 axis. J Cell Biochem 120(8):13737–13744

    Article  CAS  Google Scholar 

  • Yin K, Liu X (2020) CircMMP1 promotes the progression of glioma through miR-433/HMGB3 axis in vitro and in vivo. IUBMB Life 72(11):2508–2524

    Article  CAS  Google Scholar 

  • Yin RH, Zhao SJ, Jiao Q, Wang ZY, Bai M, Fan YX, Zhu YB, Bai WL (2020) CircRNA-1926 promotes the differentiation of goat SHF stem cells into hair follicle lineage by miR-148a/b-3p/CDK19 Axis. Anim Open Access J MDPI. https://doi.org/10.3390/ani10091552

    Article  Google Scholar 

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Acknowledgements

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Funding

This study was supported by Key Discipline Construction Project of Pudong Health Bureau of Shanghai (Grant No. PWZxk2017-23, PWYgf2018-05).

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KZ conceived and designed the experiments, performed the experiments, analyzed and interpreted the data, and wrote the paper. QW analyzed and interpreted the data and performed the experiments. DZ performed the experiments and analyzed the data. ZL analyzed and interpreted the data.

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Correspondence to Zhen Liu.

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The research related to human use has been complied with all the relevant national regulations and has been approved by the review board of Shanghai East Hospital.

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Zhang, K., Wang, Q., Zhao, D. et al. Circular RNA circMMP1 Contributes to the Progression of Glioma Through Regulating TGIF2 Expression by Sponging miR-195-5p. Biochem Genet 60, 770–789 (2022). https://doi.org/10.1007/s10528-021-10119-x

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