{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,3]],"date-time":"2026-09-03T21:39:25Z","timestamp":1788471565351,"version":"build-2803163510"},"reference-count":86,"publisher":"MDPI AG","issue":"17","license":[{"start":{"date-parts":[[2025,8,26]],"date-time":"2025-08-26T00:00:00Z","timestamp":1756166400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"University of Catania","award":["326469\/2024"],"award-info":[{"award-number":["326469\/2024"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>In bulk meningioma (MNG) tumors, a biomarker based on the expression of 34 transcripts (34HR-MNG) has recently been described to be able to predict their outcome, including recurrence. To better study the molecular mechanisms regulating the expression of the 34HR-MNG transcripts and predict their functional involvement in MNG recurrence, we built a competitive endogenous RNA (ceRNA) network through an in silico approach. MiRNAs targeting 34HR-MNG transcripts and corresponding sponging circRNAs were retrieved through MiRTarbase and ENCORI databases, respectively. The expression of candidate circRNA host genes belonging to the 34HR-MNG transcripts was correlated with specific molecular and clinical features of 89 and 20 WHO grade 1 and 2 MNGs, respectively, by querying the RNA-seq dataset GSE189672. The expression of candidate circRNAs and their host gene was validated through qRT-PCR. Among the 34HR-MNG transcripts, the Pim-1 proto-oncogene, serine\/threonine kinase (PIM1) was significantly upregulated in (i) WHO grade 2 vs. grade 1 and (ii) recurrent vs. not recurrent WHO grade 2 MNGs. PIM1 expression positively and negatively correlated with that of Ki-67 and NF2, respectively, in recurrent WHO grade 2 MNGs. CircRNAs 0076215 and 0076216, both generated from the PIM1 host gene, were predicted to sponge miRNAs 16-5p and 195-5p, two tumor suppressors in MNG, in turn targeting PIM1. The expression of circRNAs 0076215 and 0076216, validated for the first time in a set of 19 physiological human tissues, positively correlated with that of their host gene (Rho value = 0.579 and 0.681, p-value = 0.026 and 0.013, respectively). Our data suggest that PIM1 is an oncogene involved in the recurrence of WHO grade 2 MNG and that the upstream ceRNA network, comprising circRNAs 0076215 and 0076216 and miRNAs 16-5p and 195-5p, is responsible for its upregulation through a feed-forward loop.<\/jats:p>","DOI":"10.3390\/ijms26178263","type":"journal-article","created":{"date-parts":[[2025,8,26]],"date-time":"2025-08-26T14:43:18Z","timestamp":1756219398000},"page":"8263","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["In Silico Identification of circPIM1\/miR-16-5p\/miR-195-5p\/PIM1 Feed-Forward Loop in Recurrent Grade 2 Meningioma"],"prefix":"10.3390","volume":"26","author":[{"given":"Giuseppe","family":"Sotera","sequence":"first","affiliation":[{"name":"Department of Medical, Surgical Sciences and Advanced Technologies \u201cG.F. Ingrassia\u201d, Neurological Surgery, Policlinico Rodolico-San Marco University Hospital, University of Catania, Via Santa Sofia, 87, 95123 Catania, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carla","family":"Forte","sequence":"additional","affiliation":[{"name":"Department of Biological, Geological and Environmental Sciences, University of Catania, Corso Italia, 57, 95129 Catania, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniele Giuseppe","family":"D\u2019Urso","sequence":"additional","affiliation":[{"name":"Department of Biomedical and Biotechnological Sciences, Section of Biology and Genetics \u201cGiovanni Sichel\u201d, University of Catania, Via Santa Sofia, 97, 95123 Catania, Italy"},{"name":"Department of Biology and Biotechnology \u201cLazzaro Spallanzani\u201d, University of Pavia, Via Adolfo Ferrata, 9, 27100 Pavia, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Domenica","family":"Reina","sequence":"additional","affiliation":[{"name":"Department of Biomedical and Biotechnological Sciences, Section of Biology and Genetics \u201cGiovanni Sichel\u201d, University of Catania, Via Santa Sofia, 97, 95123 Catania, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Noemi","family":"Zuccaro","sequence":"additional","affiliation":[{"name":"Department of Molecular Biotechnology and Health Sciences, Molecular Biotechnology Center \u201cGuido Tarone\u201d, University of Torino, Via Nizza, 52, 10126 Torino, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0006-8029-2534","authenticated-orcid":false,"given":"Andrea Giuseppe","family":"Toscano","sequence":"additional","affiliation":[{"name":"Department of Molecular Biotechnology and Health Sciences, Molecular Biotechnology Center \u201cGuido Tarone\u201d, University of Torino, Via Nizza, 52, 10126 Torino, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Angela","family":"Caponnetto","sequence":"additional","affiliation":[{"name":"Department of Biomedical and Biotechnological Sciences, Section of Biology and Genetics \u201cGiovanni Sichel\u201d, University of Catania, Via Santa Sofia, 97, 95123 Catania, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6769-4516","authenticated-orcid":false,"given":"Cristina","family":"Barbagallo","sequence":"additional","affiliation":[{"name":"Department of Biomedical and Biotechnological Sciences, Section of Biology and Genetics \u201cGiovanni Sichel\u201d, University of Catania, Via Santa Sofia, 97, 95123 Catania, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2576-6523","authenticated-orcid":false,"given":"Giuseppe","family":"Broggi","sequence":"additional","affiliation":[{"name":"Department of Medical, Surgical Sciences and Advanced Technologies \u201cG.F. Ingrassia\u201d, Section of Anatomic Pathology, University of Catania, Via Santa Sofia, 87, 95123 Catania, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6346-2769","authenticated-orcid":false,"given":"Francesco","family":"Certo","sequence":"additional","affiliation":[{"name":"Department of Medical, Surgical Sciences and Advanced Technologies \u201cG.F. Ingrassia\u201d, Neurological Surgery, Policlinico Rodolico-San Marco University Hospital, University of Catania, Via Santa Sofia, 87, 95123 Catania, Italy"},{"name":"Interdisciplinary Research Centre on the Diagnosis and Therapy of Brain Tumors, University of Catania, Via Santa Sofia, 78, 95123 Catania, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4282-920X","authenticated-orcid":false,"given":"Marco","family":"Ragusa","sequence":"additional","affiliation":[{"name":"Department of Biomedical and Biotechnological Sciences, Section of Biology and Genetics \u201cGiovanni Sichel\u201d, University of Catania, Via Santa Sofia, 97, 95123 Catania, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8591-8010","authenticated-orcid":false,"given":"Rosario","family":"Caltabiano","sequence":"additional","affiliation":[{"name":"Department of Medical, Surgical Sciences and Advanced Technologies \u201cG.F. Ingrassia\u201d, Section of Anatomic Pathology, University of Catania, Via Santa Sofia, 87, 95123 Catania, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6036-4469","authenticated-orcid":false,"given":"Cinzia","family":"Di Pietro","sequence":"additional","affiliation":[{"name":"Department of Biomedical and Biotechnological Sciences, Section of Biology and Genetics \u201cGiovanni Sichel\u201d, University of Catania, Via Santa Sofia, 97, 95123 Catania, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Giuseppe Maria Vincenzo","family":"Barbagallo","sequence":"additional","affiliation":[{"name":"Department of Medical, Surgical Sciences and Advanced Technologies \u201cG.F. Ingrassia\u201d, Neurological Surgery, Policlinico Rodolico-San Marco University Hospital, University of Catania, Via Santa Sofia, 87, 95123 Catania, Italy"},{"name":"Interdisciplinary Research Centre on the Diagnosis and Therapy of Brain Tumors, University of Catania, Via Santa Sofia, 78, 95123 Catania, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8873-3660","authenticated-orcid":false,"given":"Michele","family":"Purrello","sequence":"additional","affiliation":[{"name":"Department of Biomedical and Biotechnological Sciences, Section of Biology and Genetics \u201cGiovanni Sichel\u201d, University of Catania, Via Santa Sofia, 97, 95123 Catania, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5331-4554","authenticated-orcid":false,"given":"Davide","family":"Barbagallo","sequence":"additional","affiliation":[{"name":"Department of Biomedical and Biotechnological Sciences, Section of Biology and Genetics \u201cGiovanni Sichel\u201d, University of Catania, Via Santa Sofia, 97, 95123 Catania, Italy"},{"name":"Interdisciplinary Research Centre on the Diagnosis and Therapy of Brain Tumors, University of Catania, Via Santa Sofia, 78, 95123 Catania, Italy"},{"name":"Interdisciplinary Research Centre for the Study of Prevention, Diagnosis and Treatment of Tumors (PreDiCT), University of Catania, Via Santa Sofia, 97, 95123 Catania, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,8,26]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"iv1","DOI":"10.1093\/neuonc\/noad149","article-title":"CBTRUS Statistical Report: Primary Brain and Other Central Nervous System Tumors Diagnosed in the United States in 2016\u20132020","volume":"25","author":"Ostrom","year":"2023","journal-title":"Neuro Oncol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1231","DOI":"10.1093\/neuonc\/noab106","article-title":"The 2021 WHO Classification of Tumors of the Central Nervous System: A Summary","volume":"23","author":"Louis","year":"2021","journal-title":"Neuro Oncol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1345","DOI":"10.3171\/2019.8.JNS191266","article-title":"Correlations between Genomic Subgroup and Clinical Features in a Cohort of More than 3000 Meningiomas","volume":"133","author":"Youngblood","year":"2020","journal-title":"J. Neurosurg."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"641","DOI":"10.1016\/j.ncrna.2024.02.011","article-title":"MicroRNAs in Meningiomas: Potential Biomarkers and Therapeutic Targets","volume":"9","author":"Beylerli","year":"2024","journal-title":"Noncoding RNA Res."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1007\/978-3-031-29750-2_13","article-title":"The Epigenetic Landscape of Meningiomas","volume":"1416","author":"Wang","year":"2023","journal-title":"Adv. Exp. Med. Biol."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Cirnigliaro, M., Barbagallo, C., Gulisano, M., Domini, C.N., Barone, R., Barbagallo, D., Ragusa, M., Di Pietro, C., Rizzo, R., and Purrello, M. (2017). Expression and Regulatory Network Analysis of MiR-140-3p, a New Potential Serum Biomarker for Autism Spectrum Disorder. Front. Mol. Neurosci., 10.","DOI":"10.3389\/fnmol.2017.00250"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1055","DOI":"10.1093\/neuros\/nyaa009","article-title":"Identification of Meningioma Patients at High Risk of Tumor Recurrence Using MicroRNA Profiling","volume":"87","author":"Slavik","year":"2020","journal-title":"Neurosurgery"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"8433","DOI":"10.1002\/cam4.5566","article-title":"MicroRNA 200a as a Histologically Independent Marker for Meningioma Recurrence: Results of a Four MicroRNA Panel Analysis in Meningiomas","volume":"12","author":"Urbschat","year":"2023","journal-title":"Cancer Med."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"354","DOI":"10.1016\/j.bbrc.2015.03.038","article-title":"MicroRNA-224 Targets ERG2 and Contributes to Malignant Progressions of Meningioma","volume":"460","author":"Wang","year":"2015","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Hergalant, S., Casse, J.-M., Oussalah, A., Houlgatte, R., Helle, D., Rech, F., Vallar, L., Gu\u00e9ant, J.-L., Vignaud, J.-M., and Battaglia-Hsu, S.-F. (2023). MicroRNAs MiR-16 and MiR-519 Control Meningioma Cell Proliferation via Overlapping Transcriptomic Programs Shared with the RNA-Binding Protein HuR. Front. Oncol., 13.","DOI":"10.3389\/fonc.2023.1158773"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"384","DOI":"10.1038\/nature11993","article-title":"Natural RNA Circles Function as Efficient MicroRNA Sponges","volume":"495","author":"Hansen","year":"2013","journal-title":"Nature"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1038\/nature11928","article-title":"Circular RNAs Are a Large Class of Animal RNAs with Regulatory Potency","volume":"495","author":"Memczak","year":"2013","journal-title":"Nature"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"185","DOI":"10.2174\/1573409918666220615151614","article-title":"Construction and Investigation of CircRNA-Associated CeRNA Regulatory Network in Molecular Subtypes of Breast Cancer","volume":"18","author":"Zhong","year":"2022","journal-title":"Curr. Comput. Aided Drug Des."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1007\/s00018-021-04119-8","article-title":"Competing Endogenous RNA Network Mediated by Circ_3205 in SARS-CoV-2 Infected Cells","volume":"79","author":"Barbagallo","year":"2022","journal-title":"Cell Mol. Life Sci."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"188","DOI":"10.1038\/s41571-021-00585-y","article-title":"The Emerging Roles of CircRNAs in Cancer and Oncology","volume":"19","author":"Kristensen","year":"2022","journal-title":"Nat. Rev. Clin. Oncol."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Merulla, A.E., Stella, M., Barbagallo, C., Battaglia, R., Caponnetto, A., Broggi, G., Altieri, R., Certo, F., Caltabiano, R., and Ragusa, M. (2022). CircSMARCA5 Is an Upstream Regulator of the Expression of MiR-126-3p, MiR-515-5p, and Their MRNA Targets, Insulin-like Growth Factor Binding Protein 2 (IGFBP2) and NRAS Proto-Oncogene, GTPase (NRAS) in Glioblastoma. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms232213676"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"895","DOI":"10.1007\/s11011-024-01345-4","article-title":"Hsa_circ_0004872 Mitigates Proliferation, Metastasis and Immune Escape of Meningioma Cells by Suppressing PD-L1","volume":"39","author":"Chen","year":"2024","journal-title":"Metab. Brain Dis."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Huang, Y., Wu, Z., Peng, Z., Liu, A., Yuan, W., Han, D., and Peng, J. (2024). Hsa_circ_0004872 Alleviates Meningioma Progression by Sponging MiR-190a-3p\/PTEN Signaling. BMC Cancer, 24.","DOI":"10.1186\/s12885-024-12084-1"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1880","DOI":"10.1002\/jcb.29423","article-title":"SNHG1\/MiR-556-5p\/TCF12 Feedback Loop Enhances the Tumorigenesis of Meningioma through Wnt Signaling Pathway","volume":"121","author":"Zhang","year":"2020","journal-title":"J. Cell Biochem."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"10223","DOI":"10.1111\/jcmm.15637","article-title":"An Allele of Rs619586 Polymorphism in MALAT1 Alters the Invasiveness of Meningioma via Modulating the Expression of Collagen Type V Alpha (COL5A1)","volume":"24","author":"Zheng","year":"2020","journal-title":"J. Cell Mol. Med."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Li, T., Ren, J., Ma, J., Wu, J., Zhang, R., Yuan, H., and Han, X. (2019). LINC00702\/MiR-4652-3p\/ZEB1 Axis Promotes the Progression of Malignant Meningioma through Activating Wnt\/\u03b2-Catenin Pathway. Biomed. Pharmacother., 113.","DOI":"10.1016\/j.biopha.2019.108718"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"388","DOI":"10.14348\/molcells.2022.2232","article-title":"LncRNA-IMAT1 Promotes Invasion of Meningiomas by Suppressing KLF4\/Hsa-MiR22-3p\/Snai1 Pathway","volume":"45","author":"Ding","year":"2022","journal-title":"Mol. Cells"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"677","DOI":"10.1016\/j.biopha.2018.06.005","article-title":"Long Noncoding RNA LINC00460 Targets MiR-539\/MMP-9 to Promote Meningioma Progression and Metastasis","volume":"105","author":"Xing","year":"2018","journal-title":"Biomed. Pharmacother."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Ding, C., Yi, X., Xu, J., Huang, Z., Bu, X., Wang, D., Ge, H., Zhang, G., Gu, J., and Kang, D. (2020). Long Non-Coding RNA MEG3 Modifies Cell-Cycle, Migration, Invasion, and Proliferation Through AKAP12 by Sponging MiR-29c in Meningioma Cells. Front. Oncol., 10.","DOI":"10.3389\/fonc.2020.537763"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1055\/s-0043-1777352","article-title":"The Natural History and Treatment of Meningiomas: An Update","volume":"44","author":"Nyalundja","year":"2024","journal-title":"Semin. Neurol."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Huntoon, K., Toland, A.M.S., and Dahiya, S. (2020). Meningioma: A Review of Clinicopathological and Molecular Aspects. Front. Oncol., 10.","DOI":"10.3389\/fonc.2020.579599"},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Corniola, M.V., Lem\u00e9e, J.-M., and Meling, T.R. (2020). Histological Transformation in Recurrent WHO Grade I Meningiomas. Sci. Rep., 10.","DOI":"10.1038\/s41598-020-68177-x"},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Li, Z., Gao, Y., Zhang, J., Han, L., and Zhao, H. (2023). DNA Methylation Meningioma Biomarkers: Attributes and Limitations. Front. Mol. Neurosci., 16.","DOI":"10.3389\/fnmol.2023.1182759"},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Biswas, D., Halder, A., Barpanda, A., Ghosh, S., Chauhan, A., Bhat, L., Epari, S., Shetty, P., Moiyadi, A., and Ball, G.R. (2023). Integrated Meta-Omics Analysis Unveils the Pathways Modulating Tumorigenesis and Proliferation in High-Grade Meningioma. Cells, 12.","DOI":"10.3390\/cells12202483"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1038\/s41586-021-03850-3","article-title":"A Clinically Applicable Integrative Molecular Classification of Meningiomas","volume":"597","author":"Nassiri","year":"2021","journal-title":"Nature"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"649","DOI":"10.1038\/s41588-022-01061-8","article-title":"Meningioma DNA Methylation Groups Identify Biological Drivers and Therapeutic Vulnerabilities","volume":"54","author":"Choudhury","year":"2022","journal-title":"Nat. Genet."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"100566","DOI":"10.1016\/j.xgen.2024.100566","article-title":"Meningioma Transcriptomic Landscape Demonstrates Novel Subtypes with Regional Associated Biology and Patient Outcome","volume":"4","author":"Thirimanne","year":"2024","journal-title":"Cell Genom."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"eabm6247","DOI":"10.1126\/sciadv.abm6247","article-title":"Multiple Approaches Converge on Three Biological Subtypes of Meningioma and Extract New Insights from Published Studies","volume":"8","author":"Bayley","year":"2022","journal-title":"Sci. Adv."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"26","DOI":"10.21037\/cco-20-226","article-title":"High Risk of Recurrence for Grade II Meningioma: A 10-Year Multicenter Analysis of Prognosis Factors","volume":"10","author":"Bender","year":"2021","journal-title":"Chin. Clin. Oncol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1227\/01.NEU.0000330399.55586.63","article-title":"Long-Term Recurrence Rates of Atypical Meningiomas after Gross Total Resection with or without Postoperative Adjuvant Radiation","volume":"64","author":"Aghi","year":"2009","journal-title":"Neurosurgery"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"3067","DOI":"10.1038\/s41591-023-02586-z","article-title":"Targeted Gene Expression Profiling Predicts Meningioma Outcomes and Radiotherapy Responses","volume":"29","author":"Chen","year":"2023","journal-title":"Nat. Med."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1016\/j.gendis.2022.11.025","article-title":"Cancer Cell Cycle Heterogeneity as a Critical Determinant of Therapeutic Resistance","volume":"11","author":"Maleki","year":"2024","journal-title":"Genes. Dis."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"4858","DOI":"10.7150\/thno.56596","article-title":"In Vivo Fermentation Production of Humanized Noncoding RNAs Carrying Payload MiRNAs for Targeted Anticancer Therapy","volume":"11","author":"Li","year":"2021","journal-title":"Theranostics"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"69","DOI":"10.3892\/ijmm.2021.4902","article-title":"MiR-124-3p Inhibits the Viability and Motility of Glioblastoma Multiforme by Targeting RhoG","volume":"47","author":"Cai","year":"2021","journal-title":"Int. J. Mol. Med."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"345","DOI":"10.3892\/mmr.2013.1561","article-title":"MiR-124 Inhibits the Growth of Glioblastoma through the Downregulation of SOS1","volume":"8","author":"Lv","year":"2013","journal-title":"Mol. Med. Rep."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"101","DOI":"10.3892\/ijmm.2013.1365","article-title":"Downregulation of MiR-124 Promotes the Growth and Invasiveness of Glioblastoma Cells Involving Upregulation of PPP1R13L","volume":"32","author":"Zhao","year":"2013","journal-title":"Int. J. Mol. Med."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1016\/j.bbrc.2017.02.120","article-title":"MiR-124 Suppresses Glioblastoma Growth and Potentiates Chemosensitivity by Inhibiting AURKA","volume":"486","author":"Qiao","year":"2017","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1317","DOI":"10.1166\/jbn.2018.2579","article-title":"MiR-135a-5p and MiR-124-3p Inhibit Malignancy of Glioblastoma by Downregulation of Syndecan Binding Protein","volume":"14","author":"Lin","year":"2018","journal-title":"J. Biomed. Nanotechnol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1016\/j.gene.2018.11.073","article-title":"Circular RNA HIPK3 Promotes Glioma Progression by Binding to MiR-124-3p","volume":"690","author":"Hu","year":"2019","journal-title":"Gene"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"3913","DOI":"10.1158\/0008-5472.CAN-12-4318","article-title":"MiR-124 Inhibits STAT3 Signaling to Enhance T Cell-Mediated Immune Clearance of Glioma","volume":"73","author":"Wei","year":"2013","journal-title":"Cancer Res."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"899","DOI":"10.1111\/cas.12946","article-title":"MicroRNA-124-3p Regulates Cell Proliferation, Invasion, Apoptosis, and Bioenergetics by Targeting PIM1 in Astrocytoma","volume":"107","author":"Deng","year":"2016","journal-title":"Cancer Sci."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"821","DOI":"10.5732\/cjc.011.10289","article-title":"MiR-124 Suppresses Multiple Steps of Breast Cancer Metastasis by Targeting a Cohort of pro-Metastatic Genes in Vitro","volume":"30","author":"Lv","year":"2011","journal-title":"Chin. J. Cancer"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"2367","DOI":"10.1002\/ijc.24219","article-title":"DNA Methylation of MicroRNA Genes in Gastric Mucosae of Gastric Cancer Patients: Its Possible Involvement in the Formation of Epigenetic Field Defect","volume":"124","author":"Ando","year":"2009","journal-title":"Int. J. Cancer"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"4443","DOI":"10.1158\/0008-5472.CAN-08-4025","article-title":"Epigenetic Silencing of the Tumor Suppressor MicroRNA Hsa-MiR-124a Regulates CDK6 Expression and Confers a Poor Prognosis in Acute Lymphoblastic Leukemia","volume":"69","author":"Agirre","year":"2009","journal-title":"Cancer Res."},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"El-Gewely, M.R., Andreassen, M., Walquist, M., Ursvik, A., Knutsen, E., Nystad, M., Coucheron, D.H., Myrmel, K.S., Hennig, R., and Johansen, S.D. (2016). Differentially Expressed MicroRNAs in Meningiomas Grades I and II Suggest Shared Biomarkers with Malignant Tumors. Cancers, 8.","DOI":"10.3390\/cancers8030031"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1250","DOI":"10.1093\/neuonc\/nov014","article-title":"Posttranscriptional Deregulation of Signaling Pathways in Meningioma Subtypes by Differential Expression of MiRNAs","volume":"17","author":"Ludwig","year":"2015","journal-title":"Neuro Oncol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1093\/neuonc\/nou216","article-title":"Pim1 Kinase Is Upregulated in Glioblastoma Multiforme and Mediates Tumor Cell Survival","volume":"17","author":"Herzog","year":"2015","journal-title":"Neuro Oncol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"140","DOI":"10.3892\/br.2015.561","article-title":"Pim-1 Kinase as Cancer Drug Target: An Update","volume":"4","author":"Tursynbay","year":"2016","journal-title":"Biomed. Rep."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"326","DOI":"10.1016\/j.chembiol.2023.10.023","article-title":"PIM1 Targeted Degradation Prevents the Emergence of Chemoresistance in Prostate Cancer","volume":"31","author":"Katerji","year":"2024","journal-title":"Cell Chem. Biol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"E15","DOI":"10.3171\/2013.9.FOCUS13325","article-title":"Atypical Meningiomas: Is Postoperative Radiotherapy Indicated?","volume":"35","author":"Lee","year":"2013","journal-title":"Neurosurg. Focus."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"e58","DOI":"10.1016\/j.wneu.2020.05.145","article-title":"Recurrence Interval Within 1 Year Leads to Death in Patients with Grade 2 Meningioma","volume":"142","author":"Ukai","year":"2020","journal-title":"World Neurosurg."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"783","DOI":"10.1093\/neuonc\/noaa226","article-title":"Associations of Meningioma Molecular Subgroup and Tumor Recurrence","volume":"23","author":"Youngblood","year":"2021","journal-title":"Neuro Oncol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1016\/j.devcel.2020.06.009","article-title":"Single-Cell Transcriptomic Analyses of the Developing Meninges Reveal Meningeal Fibroblast Diversity and Function","volume":"54","author":"DeSisto","year":"2020","journal-title":"Dev. Cell"},{"key":"ref_59","doi-asserted-by":"crossref","unstructured":"Yuan, H., Liao, X., Hu, D., Guan, D., and Tian, M. (2024). Back to the Origin: Mechanisms of CircRNA-Directed Regulation of Host Genes in Human Disease. Noncoding RNA, 10.","DOI":"10.3390\/ncrna10050049"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"885","DOI":"10.1038\/s41419-019-2127-7","article-title":"CircRNA-ENO1 Promoted Glycolysis and Tumor Progression in Lung Adenocarcinoma through Upregulating Its Host Gene ENO1","volume":"10","author":"Zhou","year":"2019","journal-title":"Cell Death Dis."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1016\/j.omtn.2019.09.022","article-title":"CircAMOTL1 Motivates AMOTL1 Expression to Facilitate Cervical Cancer Growth","volume":"19","author":"Ou","year":"2020","journal-title":"Mol. Ther. Nucleic Acids"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"3887","DOI":"10.1002\/jcp.27162","article-title":"Circular RNA Circ-VANGL1 as a Competing Endogenous RNA Contributes to Bladder Cancer Progression by Regulating MiR-605-3p\/VANGL1 Pathway","volume":"234","author":"Zeng","year":"2019","journal-title":"J. Cell Physiol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1186\/s13046-023-02657-6","article-title":"Understanding the Roles and Regulation Patterns of CircRNA on Its Host Gene in Tumorigenesis and Tumor Progression","volume":"42","author":"Wei","year":"2023","journal-title":"J. Exp. Clin. Cancer Res."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"1443","DOI":"10.1261\/rna.067132.118","article-title":"Rat BodyMap Transcriptomes Reveal Unique Circular RNA Features across Tissue Types and Developmental Stages","volume":"24","author":"Zhou","year":"2018","journal-title":"RNA"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"172","DOI":"10.1186\/s13046-018-0838-8","article-title":"CircFBLIM1 Act as a CeRNA to Promote Hepatocellular Cancer Progression by Sponging MiR-346","volume":"37","author":"Bai","year":"2018","journal-title":"J. Exp. Clin. Cancer Res."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"342","DOI":"10.1186\/s12935-022-02754-0","article-title":"A Review on the Role of Mir-16-5p in the Carcinogenesis","volume":"22","author":"Khoshbakht","year":"2022","journal-title":"Cancer Cell Int."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"10807","DOI":"10.2147\/OTT.S250369","article-title":"MicroRNA-16 Inhibits Glioblastoma Growth in Orthotopic Model by Targeting Cyclin D1 and WIP1","volume":"13","author":"Wang","year":"2020","journal-title":"Onco Targets Ther."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1111\/nan.12532","article-title":"MiR-16-5p Is Frequently down-Regulated in Astrocytic Gliomas and Modulates Glioma Cell Proliferation, Apoptosis and Response to Cytotoxic Therapy","volume":"45","author":"Krell","year":"2019","journal-title":"Neuropathol. Appl. Neurobiol."},{"key":"ref_69","doi-asserted-by":"crossref","unstructured":"Bonaf\u00e9, G.A., Dos Santos, J.S., Ziegler, J.V., Umezawa, K., Ribeiro, M.L., Rocha, T., and Ortega, M.M. (2019). Growth Inhibitory Effects of Dipotassium Glycyrrhizinate in Glioblastoma Cell Lines by Targeting MicroRNAs Through the NF-\u039aB Signaling Pathway. Front. Cell Neurosci., 13.","DOI":"10.3389\/fncel.2019.00216"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1038\/s41389-020-00295-7","article-title":"Diethyldithiocarbamate-Copper Complex (CuET) Inhibits Colorectal Cancer Progression via MiR-16-5p and 15b-5p\/ALDH1A3\/PKM2 Axis-Mediated Aerobic Glycolysis Pathway","volume":"10","author":"Huang","year":"2021","journal-title":"Oncogenesis"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"787","DOI":"10.1007\/s00432-019-02849-8","article-title":"Serum MiR-16 as a Potential Biomarker for Human Cancer Diagnosis: Results from a Large-Scale Population","volume":"145","author":"Huang","year":"2019","journal-title":"J. Cancer Res. Clin. Oncol."},{"key":"ref_72","doi-asserted-by":"crossref","unstructured":"Reis, P.P., Drigo, S.A., Carvalho, R.F., Lopez Lapa, R.M., Felix, T.F., Patel, D., Cheng, D., Pintilie, M., Liu, G., and Tsao, M.-S. (2020). Circulating MiR-16-5p, MiR-92a-3p, and MiR-451a in Plasma from Lung Cancer Patients: Potential Application in Early Detection and a Regulatory Role in Tumorigenesis Pathways. Cancers, 12.","DOI":"10.3390\/cancers12082071"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"92","DOI":"10.2174\/1567202619666220406084947","article-title":"Melatonin Inhibits the Malignant Progression of Glioblastoma via Regulating MiR-16-5p\/PIM1","volume":"19","author":"Yan","year":"2022","journal-title":"Curr. Neurovasc Res."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"200782","DOI":"10.1016\/j.omton.2024.200782","article-title":"Noncoding RNA Landscape and Their Emerging Roles as Biomarkers and Therapeutic Targets in Meningioma","volume":"32","author":"Joshi","year":"2024","journal-title":"Mol. Ther. Oncol."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"e355","DOI":"10.1016\/j.wneu.2019.12.182","article-title":"MicroRNA-195 Functions as a Tumor Suppressor by Directly Targeting Fatty Acid Synthase in Malignant Meningioma","volume":"136","author":"Song","year":"2020","journal-title":"World Neurosurg."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1111\/apm.12079","article-title":"Significance of COX-2 and VEGF Expression in Histopathologic Grading and Invasiveness of Meningiomas","volume":"122","author":"Lee","year":"2014","journal-title":"APMIS"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"1102","DOI":"10.1002\/1097-0142(20000901)89:5<1102::AID-CNCR20>3.0.CO;2-L","article-title":"Recurrence of Meningiomas","volume":"89","author":"Yamasaki","year":"2000","journal-title":"Cancer"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"104438","DOI":"10.1016\/j.yexmp.2020.104438","article-title":"MiR-195 Suppression Alleviates Apoptosis and Oxidative Stress in CCl4-Induced ALI in Mice by Targeting Pim-1","volume":"115","author":"Yang","year":"2020","journal-title":"Exp. Mol. Pathol."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"1661","DOI":"10.1093\/infdis\/jiv760","article-title":"Inhibition of MicroRNA 195 Prevents Apoptosis and Multiple-Organ Injury in Mouse Models of Sepsis","volume":"213","author":"Zheng","year":"2016","journal-title":"J. Infect. Dis."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"D222","DOI":"10.1093\/nar\/gkab1079","article-title":"MiRTarBase Update 2022: An Informative Resource for Experimentally Validated MiRNA-Target Interactions","volume":"50","author":"Huang","year":"2022","journal-title":"Nucleic Acids Res."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"D204","DOI":"10.1093\/nar\/gkab1101","article-title":"MirGeneDB 2.1: Toward a Complete Sampling of All Major Animal Phyla","volume":"50","author":"Fromm","year":"2022","journal-title":"Nucleic Acids Res."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"W154","DOI":"10.1093\/nar\/gkad431","article-title":"DIANA-MiRPath v4.0: Expanding Target-Based MiRNA Functional Analysis in Cell-Type and Tissue Contexts","volume":"51","author":"Tastsoglou","year":"2023","journal-title":"Nucleic Acids Res."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"D92","DOI":"10.1093\/nar\/gkt1248","article-title":"StarBase v2.0: Decoding MiRNA-CeRNA, MiRNA-NcRNA and Protein-RNA Interaction Networks from Large-Scale CLIP-Seq Data","volume":"42","author":"Li","year":"2014","journal-title":"Nucleic Acids Res."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"D1193","DOI":"10.1093\/nar\/gkad949","article-title":"CircRNADisease v2.0: An Updated Resource for High-Quality Experimentally Supported CircRNA-Disease Associations","volume":"52","author":"Sun","year":"2024","journal-title":"Nucleic Acids Res."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1080\/15476286.2015.1128065","article-title":"CircInteractome: A Web Tool for Exploring Circular RNAs and Their Interacting Proteins and MicroRNAs","volume":"13","author":"Dudekula","year":"2016","journal-title":"RNA Biol."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"D129","DOI":"10.1093\/nar\/gkae1036","article-title":"MiRNATissueAtlas 2025: An Update to the Uniformly Processed and Annotated Human and Mouse Non-Coding RNA Tissue Atlas","volume":"53","author":"Rishik","year":"2025","journal-title":"Nucleic Acids Res."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/26\/17\/8263\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T18:32:55Z","timestamp":1760034775000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/26\/17\/8263"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,8,26]]},"references-count":86,"journal-issue":{"issue":"17","published-online":{"date-parts":[[2025,9]]}},"alternative-id":["ijms26178263"],"URL":"https:\/\/doi.org\/10.3390\/ijms26178263","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,8,26]]}}}