Small RNA Sequencing Identifies PIWI-Interacting RNAs Deregulated in Glioblastoma-piR-9491 and piR-12488 Reduce Tumor Cell Colonies In Vitro
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
34485142
PubMed Central
PMC8415021
DOI
10.3389/fonc.2021.707017
Knihovny.cz E-zdroje
- Klíčová slova
- PIWI-interacting RNA, diagnosis, glioblastoma, piRNA, prognosis,
- Publikační typ
- časopisecké články MeSH
Glioblastoma (GBM) is the most frequently occurring primary malignant brain tumor of astrocytic origin. To change poor prognosis, it is necessary to deeply understand the molecular mechanisms of gliomagenesis and identify new potential biomarkers and therapeutic targets. PIWI-interacting RNAs (piRNAs) help in maintaining genome stability, and their deregulation has already been observed in many tumors. Recent studies suggest that these molecules could also play an important role in the glioma biology. To determine GBM-associated piRNAs, we performed small RNA sequencing analysis in the discovery set of 19 GBM and 11 non-tumor brain samples followed by TaqMan qRT-PCR analyses in the independent set of 77 GBM and 23 non-tumor patients. Obtained data were subsequently bioinformatically analyzed. Small RNA sequencing revealed 58 significantly deregulated piRNA molecules in GBM samples in comparison with non-tumor brain tissues. Deregulation of piR-1849, piR-9491, piR-12487, and piR-12488 was successfully confirmed in the independent groups of patients and controls (all p < 0.0001), and piR-9491 and piR-12488 reduced GBM cells' ability to form colonies in vitro. In addition, piR-23231 was significantly associated with the overall survival of the GBM patients treated with Stupp regimen (p = 0.007). Our results suggest that piRNAs could be a novel promising diagnostic and prognostic biomarker in GBM potentially playing important roles in gliomagenesis.
Central European Institute of Technology Masaryk University Brno Czechia
Department of Biology Faculty of Medicine Masaryk University Brno Czechia
Department of Comprehensive Cancer Care Masaryk Memorial Cancer Institute Brno Czechia
Department of Neurosurgery University Hospital Brno Brno Czechia
Department of Neurosurgery University Hospital Hradec Kralove Hradec Kralove Czechia
Department of Neurosurgery University Hospital Ostrava Ostrava Czechia
Department of Oncology and Radiotherapy University Hospital Hradec Kralove Hradec Kralove Czechia
Department of Pathology University Hospital Brno Brno Czechia
The Fingerland Department of Pathology University Hospital Hradec Kralove Hradec Kralove Czechia
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Sasmita AO, Wong YP, Ling APK. Biomarkers and Therapeutic Advances in Glioblastoma Multiforme. Asia Pac J Clin Oncol (2018) 14:40–51. 10.1111/ajco.12756 PubMed DOI
Wesseling P, Capper D. WHO 2016 Classification of Gliomas. Neuropathol Appl Neurobiol (2018) 44:139–50. 10.1111/nan.12432 PubMed DOI
Ohgaki H, Kleihues P. The Definition of Primary and Secondary Glioblastoma. Clin Cancer Res (2013) 19:764–72. 10.1158/1078-0432.CCR-12-3002 PubMed DOI
Ostrom QT, Bauchet L, Davis FG, Deltour I, Fisher JL, Langer CE, et al. . The Epidemiology of Glioma in Adults: A “State of the Science” Review. Neuro Oncol (2014) 16:896–913. 10.1093/neuonc/nou087 PubMed DOI PMC
Alexander BM, Cloughesy TF. Adult Glioblastoma. JCO (2017) 35:2402–9. 10.1200/JCO.2017.73.0119 PubMed DOI
Ross RJ, Weiner MM, Lin H. PIWI Proteins and PIWI-Interacting RNAs in the Soma. Nature (2014) 505:353–9. 10.1038/nature12987 PubMed DOI PMC
Iwasaki YW, Siomi MC, Siomi H. PIWI-Interacting RNA: Its Biogenesis and Functions. Annu Rev Biochem (2015) 84:405–33. 10.1146/annurev-biochem-060614-034258 PubMed DOI
Han YN, Li Y, Xia SQ, Zhang YY, Zheng JH, Li W. PIWI Proteins and PIWI-Interacting RNA: Emerging Roles in Cancer. Cell Physiol Biochem (2017) 44:1–20. 10.1159/000484541 PubMed DOI
Jacobs DI, Qin Q, Fu A, Chen Z, Zhou J, Zhu Y. piRNA-8041 Is Downregulated in Human Glioblastoma and Suppresses Tumor Growth In Vitro and In Vivo . Oncotarget (2018) 9:37616–20. 10.18632/oncotarget.26331 PubMed DOI PMC
Sana J, Busek P, Fadrus P, Besse A, Radova L, Vecera M, et al. . Identification of microRNAs Differentially Expressed in Glioblastoma Stem-Like Cells and Their Association With Patient Survival. Sci Rep (2018) 8:2836. 10.1038/s41598-018-20929-6 PubMed DOI PMC
Omuro A. Glioblastoma and Other Malignant Gliomas: A Clinical Review. JAMA (2013) 310:1842. 10.1001/jama.2013.280319 PubMed DOI
Wen PY, Kesari S. Malignant Gliomas in Adults. N Engl J Med (2008) 359:492–507. 10.1056/NEJMra0708126 PubMed DOI
Moyano M, Stefani G. piRNA Involvement in Genome Stability and Human Cancer. J Hematol Oncol (2015) 8:38. 10.1186/s13045-015-0133-5 PubMed DOI PMC
Assumpção CB, Calcagno DQ, Araújo TMT, dos Santos SEB, dos Santos AKCR, Riggins GJ, et al. . The Role of piRNA and Its Potential Clinical Implications in Cancer. Epigenomics (2015) 7:975–84. 10.2217/epi.15.37 PubMed DOI PMC
Leng X, Ma J, Liu Y, Shen S, Yu H, Zheng J, et al. . Mechanism of piR-DQ590027/MIR17HG Regulating the Permeability of Glioma Conditioned Normal BBB. J Exp Clin Cancer Res (2018) 37:246. 10.1186/s13046-018-0886-0 PubMed DOI PMC
Liu X, Zheng J, Xue Y, Yu H, Gong W, Wang P, et al. . PIWIL3/OIP5-AS1/miR-367-3p/CEBPA Feedback Loop Regulates the Biological Behavior of Glioma Cells. Theranostics (2018) 8:1084–105. 10.7150/thno.21740 PubMed DOI PMC
Shen S, Yu H, Liu X, Chen J, Zhao L, Xue Y, et al. . PIWIL1/piRNA-DQ593109 Regulates the Permeability of the Blood-Tumor Barrier via the MEG3/miR-330-5p/RUNX3 Axis. Mol Ther Nucleic Acids (2018) 10:412–25. 10.1016/j.omtn.2017.12.020 PubMed DOI PMC
Mei Y, Wang Y, Kumari P, Shetty AC, Clark D, MacKerell AD, et al. . A piRNA-Like Small RNA Interacts With and Modulates P-ERM Proteins in Human Somatic Cells. Nat Commun (2015) 6:7316. 10.1038/ncomms8316 PubMed DOI PMC
Weng W, Li H, Goel A. Piwi-Interacting RNAs (piRNAs) and Cancer: Emerging Biological Concepts and Potential Clinical Implications. Biochim Biophys Acta (BBA) - Rev Cancer (2019) 1871:160–9. 10.1016/j.bbcan.2018.12.005 PubMed DOI PMC
Hashim A, Rizzo F, Marchese G, Ravo M, Tarallo R, Nassa G, et al. . RNA Sequencing Identifies Specific PIWI-Interacting Small Non-Coding RNA Expression Patterns in Breast Cancer. Oncotarget (2014) 5:9901–10. 10.18632/oncotarget.2476 PubMed DOI PMC
Huang G, Hu H, Xue X, Shen S, Gao E, Guo G, et al. . Altered Expression of piRNAs and Their Relation With Clinicopathologic Features of Breast Cancer. Clin Transl Oncol (2013) 15:563–8. 10.1007/s12094-012-0966-0 PubMed DOI
Chu H, Hui G, Yuan L, Shi D, Wang Y, Du M, et al. . Identification of Novel piRNAs in Bladder Cancer. Cancer Lett (2015) 356:561–7. 10.1016/j.canlet.2014.10.004 PubMed DOI
Yan H, Wu Q-L, Sun C-Y, Ai L-S, Deng J, Zhang L, et al. . piRNA-823 Contributes to Tumorigenesis by Regulating De Novo DNA Methylation and Angiogenesis in Multiple Myeloma. Leukemia (2015) 29:196–206. 10.1038/leu.2014.135 PubMed DOI
Cheng J, Deng H, Xiao B, Hou H, Zhou F, Shen Z, et al. . piR-823, a Novel Non-Coding Small RNA, Demonstrates In Vitro and In Vivo Tumor Suppressive Activity in Human Gastric Cancer Cells. Cancer Lett (2012) 315:12–7. 10.1016/j.canlet.2011.10.004 PubMed DOI
Hallal S, Khani SE, Wei H, Lee MYT, Sim H-W, Sy J, et al. . Deep Sequencing of Small RNAs From Neurosurgical Extracellular Vesicles Substantiates miR-486-3p as a Circulating Biomarker That Distinguishes Glioblastoma From Lower-Grade Astrocytoma Patients. Int J Mol Sci (2020) 21(14):4954. 10.3390/ijms21144954 PubMed DOI PMC
Tosar JP, Rovira C, Cayota A. Non-Coding RNA Fragments Account for the Majority of Annotated piRNAs Expressed in Somatic Non-Gonadal Tissues. Commun Biol (2018) 1:2. 10.1038/s42003-017-0001-7 PubMed DOI PMC