Radiomics, mirnomics, and radiomirRNomics in glioblastoma: defining tumor biology from shadow to light

References

• Stupp R, Mason WP, van den Bent MJ, et al.; European Organisation for Research and Treatment of Cancer Brain Tumor and Radiotherapy Groups; National Cancer Institute of Canada Clinical Trials Group. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352(10):987–996.
   PubMed Web of Science ®Google Scholar
• Stupp R, Hegi ME, Mason WP, et al.; European Organisation for Research and Treatment of Cancer Brain Tumour and Radiation Oncology Groups; National Cancer Institute of Canada Clinical Trials Group. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 2009;10(5):459–466.
   PubMed Web of Science ®Google Scholar
• Franceschi E, Minichillo S, Brandes AA. Pharmacotherapy of glioblastoma: established treatments and emerging concepts. CNS Drugs. 2017;31(8):675–684.
   PubMed Web of Science ®Google Scholar
• Brandes AA, Tosoni A, Franceschi E, et al. Recurrence pattern after temozolomide concomitant with and adjuvant to radiotherapy in newly diagnosed patients with glioblastoma: correlation with MGMT promoter methylation status. J Clin Oncol. 2009;27(8):1275–1279.
   PubMed Web of Science ®Google Scholar
• Di Nunno V, Franceschi E, Tosoni A, et al. Treatment of recurrent glioblastoma: state-of-the-art and future perspectives. Expert Rev Anticancer Ther. 2020;20(9):785–795.
   PubMed Web of Science ®Google Scholar
• Lu VM, Goyal A, Graffeo CS, et al. Survival benefit of maximal resection for glioblastoma reoperation in the temozolomide era: a meta-analysis. World Neurosurg. 2019;127:31–37.
   PubMed Web of Science ®Google Scholar
• Kazmi F, Soon YY, Leong YH, et al. Re-irradiation for recurrent glioblastoma (GBM): a systematic review and meta-analysis. J Neurooncol. 2019;142(1):79–90.
   PubMed Web of Science ®Google Scholar
• Brandes AA, Tosoni A, Cavallo G, et al.; GICNO. Temozolomide 3 weeks on and 1 week off as first-line therapy for recurrent glioblastoma: phase II study from gruppo italiano cooperativo di neuro-oncologia (GICNO). Br J Cancer. 2006;95(9):1155–1160.
   PubMed Web of Science ®Google Scholar
• Franceschi E, Lamberti G, Visani M, et al. Temozolomide rechallenge in recurrent glioblastoma: when is it useful? Future Oncol. 2018;14(11):1063–1069.
   PubMed Web of Science ®Google Scholar
• Franceschi E, Omuro AM, Lassman AB, et al. Salvage temozolomide for prior temozolomide responders. Cancer. 2005;104(11):2473–2476.
   PubMed Web of Science ®Google Scholar
• Weller M, Tabatabai G, Kästner B, et al.; DIRECTOR Study Group. MGMT promoter methylation is a strong prognostic biomarker for benefit from dose-intensified temozolomide rechallenge in progressive glioblastoma: the DIRECTOR trial. Clin Cancer Res. 2015;21(9):2057–2064.
   PubMed Web of Science ®Google Scholar
• Perry JR, Bélanger K, Mason WP, et al. Phase II trial of continuous dose-intense temozolomide in recurrent malignant glioma: RESCUE study. J Clin Oncol. 2010;28(12):2051–2057.
   PubMed Web of Science ®Google Scholar
• Brandes AA, Tosoni A, Franceschi E, et al. Fotemustine as second-line treatment for recurrent or progressive glioblastoma after concomitant and/or adjuvant temozolomide: a phase II trial of Gruppo Italiano Cooperativo di Neuro-Oncologia (GICNO). Cancer Chemother Pharmacol. 2009;64(4):769–775.
   PubMed Web of Science ®Google Scholar
• Louis DN, Perry A, Reifenberger G, et al. The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol. 2016;131(6):803–820.
   PubMed Web of Science ®Google Scholar
• Brandes AA, Franceschi E, Paccapelo A, et al. Role of MGMT methylation status at time of diagnosis and recurrence for patients with glioblastoma: clinical implications. Oncologist. 2017;22(4):432–437.
   PubMed Web of Science ®Google Scholar
• Sanson M, Marie Y, Paris S, et al. Isocitrate dehydrogenase 1 codon 132 mutation is an important prognostic biomarker in gliomas. J Clin Oncol. 2009;27(25):4150–4154.
   PubMed Web of Science ®Google Scholar
• Verhaak RG, Hoadley KA, Purdom E, et al.; Cancer Genome Atlas Research Network. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell. 2010;17(1):98–110.
   PubMed Web of Science ®Google Scholar
• Hegi ME, Diserens AC, Gorlia T, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med. 2005;352(10):997–1003.
   PubMed Web of Science ®Google Scholar
• Brandes AA, Franceschi E, Tosoni A, et al. MGMT promoter methylation status can predict the incidence and outcome of pseudoprogression after concomitant radiochemotherapy in newly diagnosed glioblastoma patients. J Clin Oncol. 2008;26(13):2192–2197.
   PubMed Web of Science ®Google Scholar
• Simon M, Hosen I, Gousias K, et al. TERT promoter mutations: a novel independent prognostic factor in primary glioblastomas. Neuro Oncol. 2015;17(1):45–52.
   PubMed Web of Science ®Google Scholar
• Eckel-Passow JE, Lachance DH, Molinaro AM, et al. Glioma groups based on 1p/19q, IDH, and TERT promoter mutations in tumors. N Engl J Med. 2015;372(26):2499–2508.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Dube C, Gibert M, et al. The p53 pathway in glioblastoma. Cancers (Basel). 2018;10(9):297.
   Web of Science ®Google Scholar
• Noushmehr H, Weisenberger DJ, Diefes K, et al.; Cancer Genome Atlas Research Network. Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell. 2010;17(5):510–522.
   PubMed Web of Science ®Google Scholar
• Reardon DA, Wen PY. Therapeutic advances in the treatment of glioblastoma: rationale and potential role of targeted agents. Oncologist. 2006;11(2):152–164.
   PubMed Web of Science ®Google Scholar
• Taal W, Oosterkamp HM, Walenkamp AM, et al. Single-agent bevacizumab or lomustine versus a combination of bevacizumab plus lomustine in patients with recurrent glioblastoma (BELOB trial): a randomised controlled phase 2 trial. Lancet Oncol. 2014;15(9):943–953.
   PubMed Web of Science ®Google Scholar
• Brandes AA, Finocchiaro G, Zagonel V, et al. AVAREG: a phase II, randomized, noncomparative study of fotemustine or bevacizumab for patients with recurrent glioblastoma. Neuro Oncol. 2016;18(9):1304–1312.
   PubMed Web of Science ®Google Scholar
• Brandes AA, Gil-Gil M, Saran F, et al. A randomized phase II trial (TAMIGA) evaluating the efficacy and safety of continuous bevacizumab through multiple lines of treatment for recurrent glioblastoma. Oncologist. 2019;24(4):521–528.
   PubMed Web of Science ®Google Scholar
• Brandes AA, Finocchiaro G, Zagonel V, et al. Early tumour shrinkage as a survival predictor in patients with recurrent glioblastoma treated with bevacizumab in the AVAREG randomized phase II study. Oncotarget. 2017;8(33):55575–55581.
   PubMedGoogle Scholar
• Wick W, Gorlia T, Bendszus M, et al. Lomustine and bevacizumab in progressive glioblastoma. N Engl J Med. 2017;377(20):1954–1963.
   PubMed Web of Science ®Google Scholar
• Reardon DA, Brandes AA, Omuro A, et al. Effect of nivolumab vs bevacizumab in patients with recurrent glioblastoma: the CheckMate 143 phase 3 randomized clinical trial. JAMA Oncol. 2020;6(7):1003–1010.
   PubMed Web of Science ®Google Scholar
• Brandes AA, Franceschi E, Tosoni A, et al. Epidermal growth factor receptor inhibitors in neuro-oncology: hopes and disappointments. Clin Cancer Res. 2008;14(4):957–960.
   PubMed Web of Science ®Google Scholar
• Mellinghoff IK, Wang MY, Vivanco I, et al. Molecular determinants of the response of glioblastomas to EGFR kinase inhibitors. N Engl J Med. 2005;353(19):2012–2024.
   PubMed Web of Science ®Google Scholar
• van den Bent MJ, Brandes AA, Rampling R, et al. Randomized phase II trial of erlotinib versus temozolomide or carmustine in recurrent glioblastoma: EORTC brain tumor group study 26034. J Clin Oncol. 2009;27(8):1268–1274.
   PubMed Web of Science ®Google Scholar
• de Groot JF, Gilbert MR, Aldape K, et al. Phase II study of carboplatin and erlotinib (Tarceva, OSI-774) in patients with recurrent glioblastoma. J Neurooncol. 2008;90(1):89–97.
   PubMed Web of Science ®Google Scholar
• Franceschi E, Cavallo G, Lonardi S, et al. Gefitinib in patients with progressive high-grade gliomas: a multicentre phase II study by Gruppo Italiano Cooperativo di Neuro-Oncologia (GICNO). Br J Cancer. 2007;96(7):1047–1051.
   PubMed Web of Science ®Google Scholar
• Reardon DA, Wen PY, Mellinghoff IK. Targeted molecular therapies against epidermal growth factor receptor: past experiences and challenges. Neuro Oncol. 2014;16(Suppl 8):viii7–13.
   PubMed Web of Science ®Google Scholar
• Di Nunno V, Franceschi E, Gatto L, et al. Predictive markers of immune response in glioblastoma: hopes and facts. Future Oncol. 2020;16(15):1053–1063.
   PubMed Web of Science ®Google Scholar
• Okada H, Weller M, Huang R, et al. Immunotherapy response assessment in neuro-oncology: a report of the RANO working group. Lancet Oncol. 2015;16(15):e534–e542.
   PubMedGoogle Scholar
• Brandes AA, Carpentier AF, Kesari S, et al. A phase II randomized study of galunisertib monotherapy or galunisertib plus lomustine compared with lomustine monotherapy in patients with recurrent glioblastoma. Neuro Oncol. 2016;18(8):1146–1156.
   PubMed Web of Science ®Google Scholar
• Hassn Mesrati M, Behrooz AB, Abuhamad Y, et al. Understanding glioblastoma biomarkers: knocking a mountain with a hammer. Cells. 2020;9(5):1236.
   Web of Science ®Google Scholar
• Szopa W, Burley TA, Kramer-Marek G, et al. Diagnostic and therapeutic biomarkers in glioblastoma: current status and future perspectives. Biomed Res Int. 2017;2017:8013575.
   PubMed Web of Science ®Google Scholar
• Lambin P, Leijenaar RTH, Deist TM, et al. Radiomics: the bridge between medical imaging and personalized medicine. Nat Rev Clin Oncol. 2017;14(12):749–762.
   PubMed Web of Science ®Google Scholar
• Fathi Kazerooni A, Bakas S, Saligheh Rad H, et al. Imaging signatures of glioblastoma molecular characteristics: a radiogenomics review. J Magn Reson Imaging. 2020;52(1):54–69.
   PubMed Web of Science ®Google Scholar
• Huang SW, Ali ND, Zhong L, et al. MicroRNAs as biomarkers for human glioblastoma: progress and potential. Acta Pharmacol Sin. 2018;39(9):1405–1413.
   PubMed Web of Science ®Google Scholar
• Lambin P, Rios-Velazquez E, Leijenaar R, et al. Radiomics: extracting more information from medical images using advanced feature analysis. Eur J Cancer. 2012;48(4):441–446.
   PubMed Web of Science ®Google Scholar
• Gatenby RA, Grove O, Gillies RJ. Quantitative imaging in cancer evolution and ecology. Radiology. 2013;269(1):8–15.
   PubMed Web of Science ®Google Scholar
• Hobbs SK, Shi G, Homer R, et al. Magnetic resonance image-guided proteomics of human glioblastoma multiforme. J Magn Reson Imaging. 2003;18(5):530–536.
   PubMed Web of Science ®Google Scholar
• Kickingereder P, Burth S, Wick A, et al. Radiomic profiling of glioblastoma: identifying an imaging predictor of patient survival with improved performance over established clinical and radiologic risk models. Radiology. 2016;280(3):880–889.
   PubMed Web of Science ®Google Scholar
• Bae S, Choi YS, Ahn SS, et al. Radiomic MRI phenotyping of glioblastoma: improving survival prediction. Radiology. 2018;289(3):797–806.
   PubMed Web of Science ®Google Scholar
• Park JE, Kim HS, Park SY, et al. Prediction of core signaling pathway by using diffusion- and perfusion-based MRI radiomics and next-generation sequencing in isocitrate dehydrogenase wild-type glioblastoma. Radiology. 2020;294(2):388–397.
   PubMed Web of Science ®Google Scholar
• Macfarlane LA, Murphy PR. MicroRNA: biogenesis, function and role in cancer. Curr Genomics. 2010;11(7):537–561.
   PubMed Web of Science ®Google Scholar
• Lin S, Gregory RI. MicroRNA biogenesis pathways in cancer. Nat Rev Cancer. 2015;15(6):321–333.
   PubMed Web of Science ®Google Scholar
• Calin GA, Sevignani C, Dumitru CD, et al. Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc Natl Acad Sci U S A. 2004;101(9):2999–3004.
   PubMed Web of Science ®Google Scholar
• Zhang L, Huang J, Yang N, et al. microRNAs exhibit high frequency genomic alterations in human cancer. Proc Natl Acad Sci U S A. 2006;103(24):9136–9141.
   PubMed Web of Science ®Google Scholar
• Lodes MJ, Caraballo M, Suciu D, et al. Detection of cancer with serum miRNAs on an oligonucleotide microarray. PLoS One. 2009;4(7):e6229.
   PubMed Web of Science ®Google Scholar
• Häusler SF, Keller A, Chandran PA, et al. Whole blood-derived miRNA profiles as potential new tools for ovarian cancer screening. Br J Cancer. 2010;103(5):693–700.
   PubMed Web of Science ®Google Scholar
• Hanke M, Hoefig K, Merz H, et al. A robust methodology to study urine microRNA as tumor marker: microRNA-126 and microRNA-182 are related to urinary bladder cancer. Urol Oncol. 2010;28(6):655–661.
   PubMed Web of Science ®Google Scholar
• Michael A, Bajracharya SD, Yuen PS, et al. Exosomes from human saliva as a source of microRNA biomarkers. Oral Dis. 2010;16(1):34–38.
   PubMed Web of Science ®Google Scholar
• Visani M, De Biase D, Marucci G, et al.; PERNO study group. Expression of 19 microRNAs in glioblastoma and comparison with other brain neoplasia of grades I-III. Mol Oncol. 2014;8(2):417–430.
   PubMed Web of Science ®Google Scholar
• Buruiană A, Florian ȘI, Florian AI, et al. The roles of miRNA in glioblastoma tumor cell communication: diplomatic and aggressive negotiations. Int J Mol Sci. 2020;21(6):1950.
   Web of Science ®Google Scholar
• Banelli B, Forlani A, Allemanni G, et al. MicroRNA in glioblastoma: an overview. Int J Genomics. 2017;2017:7639084.
   PubMed Web of Science ®Google Scholar
• Henriksen M, Johnsen KB, Olesen P, et al. MicroRNA expression signatures and their correlation with clinicopathological features in glioblastoma multiforme. Neuromolecular Med. 2014;16(3):565–577.
   PubMed Web of Science ®Google Scholar
• Kim TM, Huang W, Park R, et al. A developmental taxonomy of glioblastoma defined and maintained by MicroRNAs. Cancer Res. 2011;71(9):3387–3399.
   PubMed Web of Science ®Google Scholar
• Chinot OL, Wick W, Mason W, et al. Bevacizumab plus radiotherapy-temozolomide for newly diagnosed glioblastoma. N Engl J Med. 2014;370(8):709–722.
   PubMed Web of Science ®Google Scholar
• Chan JA, Krichevsky AM, Kosik KS. MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res. 2005;65(14):6029–6033.
   PubMed Web of Science ®Google Scholar
• Hermansen SK, Dahlrot RH, Nielsen BS, et al. MiR-21 expression in the tumor cell compartment holds unfavorable prognostic value in gliomas. J Neurooncol. 2013;111(1):71–81.
   PubMed Web of Science ®Google Scholar
• Shi J. Considering exosomal miR-21 as a biomarker for cancer. J Clin Med. 2016;5(4):42.
   Web of Science ®Google Scholar
• Fang L, Deng Z, Shatseva T, et al. MicroRNA miR-93 promotes tumor growth and angiogenesis by targeting integrin-β8. Oncogene. 2011;30(7):806–821.
   PubMed Web of Science ®Google Scholar
• Skalsky RL, Cullen BR, Borras C. Reduced expression of brain-enriched microRNAs in glioblastomas permits targeted regulation of a cell death gene. PLoS One. 2011;6(9):e24248.
   PubMed Web of Science ®Google Scholar
• Huang T, Wan X, Alvarez AA, et al. MIR93 (microRNA −93) regulates tumorigenicity and therapy response of glioblastoma by targeting autophagy. Autophagy. 2019;15(6):1100–1111.
   PubMed Web of Science ®Google Scholar
• Qiu S, Lin S, Hu D, et al. Interactions of miR-323/miR-326/miR-329 and miR-130a/miR-155/miR-210 as prognostic indicators for clinical outcome of glioblastoma patients. J Transl Med. 2013;11:10.
   PubMed Web of Science ®Google Scholar
• Agrawal R, Pandey P, Jha P, et al. Hypoxic signature of microRNAs in glioblastoma: insights from small RNA deep sequencing. BMC Genomics. 2014;15(1):686.
   PubMedGoogle Scholar
• Roth P, Wischhusen J, Happold C, et al. A specific miRNA signature in the peripheral blood of glioblastoma patients. J Neurochem. 2011;118(3):449–457.
   PubMed Web of Science ®Google Scholar
• Wang S, Mo Y, Midorikawa K, et al. The potent tumor suppressor miR-497 inhibits cancer phenotypes in nasopharyngeal carcinoma by targeting ANLN and HSPA4L. Oncotarget. 2015;6(34):35893–35907.
   PubMed Web of Science ®Google Scholar
• Wang Q, Li P, Li A, et al. Plasma specific miRNAs as predictive biomarkers for diagnosis and prognosis of glioma. J Exp Clin Cancer Res. 2012;31(1):97.
   PubMedGoogle Scholar
• Wu N, Lin X, Zhao X, et al. MiR-125b acts as an oncogene in glioblastoma cells and inhibits cell apoptosis through p53 and p38MAPK-independent pathways. Br J Cancer. 2013;109(11):2853–2863.
   PubMed Web of Science ®Google Scholar
• Kefas B, Godlewski J, Comeau L, et al. microRNA-7 inhibits the epidermal growth factor receptor and the Akt pathway and is down-regulated in glioblastoma. Cancer Res. 2008;68(10):3566–3572.
   PubMed Web of Science ®Google Scholar
• Gao H, Zhao H, Xiang W. Expression level of human miR-34a correlates with glioma grade and prognosis. J Neurooncol. 2013;113(2):221–228.
   PubMed Web of Science ®Google Scholar
• Guessous F, Zhang Y, Kofman A, et al. microRNA-34a is tumor suppressive in brain tumors and glioma stem cells. Cell Cycle. 2010;9(6):1031–1036.
   PubMed Web of Science ®Google Scholar
• Rivera-Díaz M, Miranda-Román MA, Soto D, et al. MicroRNA-27a distinguishes glioblastoma multiforme from diffuse and anaplastic astrocytomas and has prognostic value. Am J Cancer Res. 2014;5(1):201–218.
   PubMed Web of Science ®Google Scholar
• Jia Z, Wang K, Zhang A, et al. miR-19a and miR-19b overexpression in gliomas. Pathol Oncol Res. 2013;19(4):847–853.
   PubMed Web of Science ®Google Scholar
• Banzhaf-Strathmann J, Edbauer D. Good guy or bad guy: the opposing roles of microRNA 125b in cancer. Cell Commun Signal. 2014;12: 30.
   PubMed Web of Science ®Google Scholar
• Feliciano A, Castellvi J, Artero-Castro A, et al. miR-125b acts as a tumor suppressor in breast tumorigenesis via its novel direct targets ENPEP, CK2-α, CCNJ, and MEGF9. PLoS One. 2013;8(10):e76247.
   PubMed Web of Science ®Google Scholar
• Xia HF, He TZ, Liu CM, et al. MiR-125b expression affects the proliferation and apoptosis of human glioma cells by targeting Bmf. Cell Physiol Biochem. 2009;23(4–6):347–358.
   PubMedGoogle Scholar
• Regazzo G, Terrenato I, Spagnuolo M, et al. A restricted signature of serum miRNAs distinguishes glioblastoma from lower grade gliomas. J Exp Clin Cancer Res. 2016;35(1):124.
   PubMedGoogle Scholar
• Yan JJ, Zhang YN, Liao JZ, et al. MiR-497 suppresses angiogenesis and metastasis of hepatocellular carcinoma by inhibiting VEGFA and AEG-1. Oncotarget. 2015;6(30):29527–29542.
   PubMedGoogle Scholar
• Slaby O, Lakomy R, Fadrus P, et al. MicroRNA-181 family predicts response to concomitant chemoradiotherapy with temozolomide in glioblastoma patients. Neoplasma. 2010;57(3):264–269.
   PubMed Web of Science ®Google Scholar
• Lakomy R, Sana J, Hankeova S, et al. MiR-195, miR-196b, miR-181c, miR-21 expression levels and O-6-methylguanine-DNA methyltransferase methylation status are associated with clinical outcome in glioblastoma patients. Cancer Sci. 2011;102(12):2186–2190.
   PubMed Web of Science ®Google Scholar
• Hui W, Yuntao L, Lun L, et al. MicroRNA-195 inhibits the proliferation of human glioma cells by directly targeting cyclin D1 and cyclin E1. PLoS One. 2013;8(1):e54932.
   PubMed Web of Science ®Google Scholar
• Ujifuku K, Mitsutake N, Takakura S, et al. miR-195, miR-455-3p and miR-10a(*) are implicated in acquired temozolomide resistance in glioblastoma multiforme cells. Cancer Lett. 2010;296(2):241–248.
   PubMed Web of Science ®Google Scholar
• Tezcan G, Tunca B, Bekar A, et al. microRNA expression pattern modulates temozolomide response in GBM tumors with cancer stem cells. Cell Mol Neurobiol. 2014;34(5):679–692.
   PubMed Web of Science ®Google Scholar
• Malzkorn B, Wolter M, Liesenberg F, et al. Identification and functional characterization of microRNAs involved in the malignant progression of gliomas. Brain Pathol. 2010;20(3):529–550.
   Web of Science ®Google Scholar
• Tu Y, Gao X, Li G, et al. MicroRNA-218 inhibits glioma invasion, migration, proliferation, and cancer stem-like cell self-renewal by targeting the polycomb group gene Bmi1. Cancer Res. 2013;73(19):6046–6055.
   PubMed Web of Science ®Google Scholar
• Song L, Huang Q, Chen K, et al. miR-218 inhibits the invasive ability of glioma cells by direct downregulation of IKK-β. Biochem Biophys Res Commun. 2010;402(1):135–140.
   PubMed Web of Science ®Google Scholar
• Srinivasan S, Patric IR, Somasundaram K. A ten-microRNA expression signature predicts survival in glioblastoma. PLoS One. 2011;6(3):e17438.
   PubMed Web of Science ®Google Scholar
• Sin WC, Aftab Q, Bechberger JF, et al. Astrocytes promote glioma invasion via the gap junction protein connexin43. Oncogene. 2016;35:1504–1516.
   PubMed Web of Science ®Google Scholar
• Hong X, Sin WC, Harris AL, et al. Gap junctions modulate glioma invasion by direct transfer of microRNA. Oncotarget. 2015;6:15566–15577.
   PubMed Web of Science ®Google Scholar
• Ghosh Z, Chakrabarti J, Mallick B. miRNomics – the bioinformatics of microRNA genes. Biochem Biophys Res Commun. 2007;363(1):6–11.
   PubMed Web of Science ®Google Scholar
• Erhart F, Hackl M, Hahne H, et al. Combined proteomics/miRNomics of dendritic cell immunotherapy-treated glioblastoma patients as a screening for survival-associated factors. NPJ Vaccines. 2020;5:5.
   PubMed Web of Science ®Google Scholar
• Sun X, Ma X, Wang J, et al. Glioma stem cells-derived exosomes promote the angiogenic ability of endothelial cells through miR-21/VEGF signal. Oncotarget. 2017;8:36137.
   PubMedGoogle Scholar
• Papagiannakopoulos T, Shapiro A, Kosik KS. MicroRNA-21 targets a network of key tumor-suppressive pathways in glioblastoma cells. Cancer Res. 2008;68(19):8164–8172.
   PubMed Web of Science ®Google Scholar
• Wong ST, Zhang XQ, Zhuang JT, et al. MicroRNA-21 inhibition enhances in vitro chemosensitivity of temozolomide-resistant glioblastoma cells. Anticancer Res. 2012 Jul;32(7):2835–2841.
   PubMed Web of Science ®Google Scholar
• Pinker K, Shitano F, Sala E, et al. Background, current role, and potential applications of radiogenomics. J Magn Reson Imaging. 2018;47(3):604–620.
   PubMed Web of Science ®Google Scholar
• Diehn M, Nardini C, Wang DS, et al. Identification of noninvasive imaging surrogates for brain tumor gene-expression modules. Proc Natl Acad Sci U S A. 2008;105(13):5213–5218.
   PubMed Web of Science ®Google Scholar
• Pope WB, Chen JH, Dong J, et al. Relationship between gene expression and enhancement in glioblastoma multiforme: exploratory DNA microarray analysis. Radiology. 2008;249(1):268–277.
   PubMed Web of Science ®Google Scholar
• Itakura H, Achrol AS, Mitchell LA, et al. Magnetic resonance image features identify glioblastoma phenotypic subtypes with distinct molecular pathway activities. Sci Transl Med. 2015;7(303):303ra138.
   PubMed Web of Science ®Google Scholar
• Crisi G, Filice S. Predicting MGMT promoter methylation of glioblastoma from dynamic susceptibility contrast perfusion: a radiomic approach. J Neuroimaging. 2020;30(4):458–462.
   PubMed Web of Science ®Google Scholar
• Romano A, Calabria LF, Tavanti F, et al. Apparent diffusion coefficient obtained by magnetic resonance imaging as a prognostic marker in glioblastomas: correlation with MGMT promoter methylation status. Eur Radiol. 2013;23(2):513–520.
   PubMed Web of Science ®Google Scholar
• Chang P, Grinband J, Weinberg BD, et al. Deep-learning convolutional neural networks accurately classify genetic mutations in gliomas. AJNR Am J Neuroradiol. 2018;39(7):1201–1207.
   PubMed Web of Science ®Google Scholar
• Carrillo JA, Lai A, Nghiemphu PL, et al. Relationship between tumor enhancement, edema, IDH1 mutational status, MGMT promoter methylation, and survival in glioblastoma. AJNR Am J Neuroradiol. 2012;33(7):1349–1355.
   PubMed Web of Science ®Google Scholar
• Hong EK, Choi SH, Shin DJ, et al. Radiogenomics correlation between MR imaging features and major genetic profiles in glioblastoma. Eur Radiol. 2018;28(10):4350–4361.
   PubMed Web of Science ®Google Scholar
• Xi YB, Guo F, Xu ZL, et al. Radiomics signature: a potential biomarker for the prediction of MGMT promoter methylation in glioblastoma. J Magn Reson Imaging. 2018;47(5):1380–1387.
   PubMed Web of Science ®Google Scholar
• Foltyn M, Nieto Taborda KN, Neuberger U, et al. T2/FLAIR-mismatch sign for noninvasive detection of IDH-mutant 1p/19q non-codeleted gliomas: validity and pathophysiology. Neurooncol Adv. 2020;2(1):vdaa004.
   PubMedGoogle Scholar
• Gallivanone F, Cava C, Corsi F, et al. In silico approach for the definition of radiomiRNomic signatures for breast cancer differential diagnosis. Int J Mol Sci. 2019;20(23):5825.
   Web of Science ®Google Scholar
• Park JE, Park SY, Kim HJ, et al. Reproducibility and generalizability in radiomics modeling: possible strategies in radiologic and statistical perspectives. Korean J Radiol. 2019;20(7):1124–1137.
   PubMed Web of Science ®Google Scholar