{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,30]],"date-time":"2026-07-30T18:19:41Z","timestamp":1785435581451,"version":"3.56.0"},"reference-count":72,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2026,6,18]],"date-time":"2026-06-18T00:00:00Z","timestamp":1781740800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Zhejiang Provincial Natural Science Foundation of China","award":["LTGD24H160007"],"award-info":[{"award-number":["LTGD24H160007"]}]},{"name":"Zhejiang Provincial Natural Science Foundation of China","award":["LMS25C040004"],"award-info":[{"award-number":["LMS25C040004"]}]},{"name":"Zhejiang Provincial Natural Science Foundation of China","award":["LTGY24C060003"],"award-info":[{"award-number":["LTGY24C060003"]}]},{"award":["LTGD24H160007"],"award-info":[{"award-number":["LTGD24H160007"]}],"id":[{"id":"https:\/\/ror.org\/04aqat463","id-type":"ROR","asserted-by":"publisher"}]},{"award":["LMS25C040004"],"award-info":[{"award-number":["LMS25C040004"]}],"id":[{"id":"https:\/\/ror.org\/04aqat463","id-type":"ROR","asserted-by":"publisher"}]},{"award":["LTGY24C060003"],"award-info":[{"award-number":["LTGY24C060003"]}],"id":[{"id":"https:\/\/ror.org\/04aqat463","id-type":"ROR","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"crossref","award":["82303104"],"award-info":[{"award-number":["82303104"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"crossref","award":["82403762"],"award-info":[{"award-number":["82403762"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"crossref"}]},{"award":["82303104"],"award-info":[{"award-number":["82303104"]}],"id":[{"id":"https:\/\/ror.org\/01h0zpd94","id-type":"ROR","asserted-by":"publisher"}]},{"award":["82403762"],"award-info":[{"award-number":["82403762"]}],"id":[{"id":"https:\/\/ror.org\/01h0zpd94","id-type":"ROR","asserted-by":"publisher"}]},{"name":"Fundamental Research Grant Scheme, Ministry of Higher Education of Malaysia","award":["FRGS\/1\/2023\/SKK03\/UM\/02\/2"],"award-info":[{"award-number":["FRGS\/1\/2023\/SKK03\/UM\/02\/2"]}]},{"DOI":"10.13039\/501100003787","name":"Natural Science Foundation of Hebei Province","doi-asserted-by":"crossref","award":["H2022201008"],"award-info":[{"award-number":["H2022201008"]}],"id":[{"id":"10.13039\/501100003787","id-type":"DOI","asserted-by":"crossref"}]},{"name":"General Research Project of the Education Department of Zhejiang Province","award":["2023RC306"],"award-info":[{"award-number":["2023RC306"]}]},{"name":"Zhejiang Provincial Science and Technology Achievement Transformation Project","award":["2024330001003347"],"award-info":[{"award-number":["2024330001003347"]}]},{"name":"Zhejiang Provincial Science and Technology Achievement Transformation Project","award":["2024330001003345"],"award-info":[{"award-number":["2024330001003345"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biomolecules"],"abstract":"<jats:p>Background: Acquired tolerance to temozolomide (TMZ) remains one of the main obstacles to enduring therapeutic success in glioblastoma (GBM). While tumor-derived extracellular vesicles are known to orchestrate therapy evasion by horizontally transferring molecules across the tumor microenvironment, the precise regulatory roles of specific exosomal circular RNAs (circRNAs) in establishing this refractory state require further elucidation. Methods: The expression of circ_0050688 in TMZ-resistant GBM clinical tissues and cell lines was evaluated. Exosomes derived from resistant cells were isolated and confirmed via transmission electron microscopy (TEM) and marker analysis. PKH67 fluorescent tracking was utilized to visually demonstrate exosome internalization by sensitive recipient cells. Biological functions, including the expression of the multidrug resistance protein P-glycoprotein (P-gp) and the proliferation marker Ki-67, were evaluated. The competing endogenous RNA mechanism was validated using RNA FISH, dual-luciferase reporters, and functional rescue experiments. In vivo efficacy was determined using subcutaneous xenograft mouse models. Results: Clinical and in vitro analyses revealed that circ_0050688 is upregulated in TMZ-refractory GBM, predicting adverse patient survival. Through PKH67-based tracing, we confirmed that resistant cells actively secrete circ_0050688-enriched exosomes, which are subsequently engulfed by drug-sensitive bystander cells. This vesicular transfer directly instigates a chemoresistant and highly proliferative phenotype, marked by elevated P-gp and Ki-67 levels. At the molecular level, circ_0050688 operates as a molecular decoy for miR-508-5p, thereby preventing the suppression of its downstream target, MDM2. Functionally, circ_0050688 depletion eradicated these aggressive traits and restored TMZ vulnerability across both cellular and murine xenograft models. Furthermore, rescue assays confirmed that this circ_0050688-driven chemoresistance is fundamentally dependent on the miR-508-5p\/MDM2 signaling axis. Conclusions: Current data uncover an intercellular signaling network driven by vesicular circ_0050688, which functions as a mobile oncogene to reshape the TMZ-refractory microenvironment. Targeting this exosomal circ_0050688\/miR-508-5p\/MDM2 network to suppress P-gp and Ki-67 expression represents a highly promising therapeutic strategy for refractory GBM.<\/jats:p>","DOI":"10.3390\/biom16060906","type":"journal-article","created":{"date-parts":[[2026,6,18]],"date-time":"2026-06-18T10:25:34Z","timestamp":1781778334000},"page":"906","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Exosomal circ_0050688 Shapes a Chemoresistant Microenvironment by Driving Spatial Resistance Spreading in Glioblastoma via the MDM2 Pathway"],"prefix":"10.3390","volume":"16","author":[{"given":"Qiang","family":"Li","sequence":"first","affiliation":[{"name":"School of Medicine, Taizhou University, Taizhou 318000, Zhejiang, China"},{"name":"Department of Pathology, Faculty of Medicine, Universiti Malaya, Kuala Lumpur 50603, Malaysia"},{"name":"Department of Psychosomatic, Taizhou Second People\u2019s Hospital, Affiliated to School of Medicine, Taizhou University, Taizhou 318000, Zhejiang, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jianglong","family":"Xu","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, Affiliated Hospital of Hebei University, Baoding 071000, Hebei, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuhao","family":"Zhang","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, Zhejiang Provincial People\u2019s Hospital, Affiliated to Hangzhou Medical College, Hangzhou 310014, Zhejiang, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Junbing","family":"Qian","sequence":"additional","affiliation":[{"name":"School of Medicine, Taizhou University, Taizhou 318000, Zhejiang, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Diana","family":"Bee-Lan Ong","sequence":"additional","affiliation":[{"name":"Department of Pathology, Faculty of Medicine, Universiti Malaya, Kuala Lumpur 50603, Malaysia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kein Seong","family":"Mun","sequence":"additional","affiliation":[{"name":"Department of Pathology, Faculty of Medicine, Universiti Malaya, Kuala Lumpur 50603, Malaysia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yiping","family":"Tang","sequence":"additional","affiliation":[{"name":"Department of Psychosomatic, Taizhou Second People\u2019s Hospital, Affiliated to School of Medicine, Taizhou University, Taizhou 318000, Zhejiang, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3386-1443","authenticated-orcid":false,"given":"Xiuchao","family":"Geng","sequence":"additional","affiliation":[{"name":"School of Medicine, Taizhou University, Taizhou 318000, Zhejiang, China"},{"name":"Department of Pathology, Faculty of Medicine, Universiti Malaya, Kuala Lumpur 50603, Malaysia"},{"name":"Department of Psychosomatic, Taizhou Second People\u2019s Hospital, Affiliated to School of Medicine, Taizhou University, Taizhou 318000, Zhejiang, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6843-9613","authenticated-orcid":false,"given":"Kean Chang","family":"Phang","sequence":"additional","affiliation":[{"name":"Department of Pathology, Faculty of Medicine, Universiti Malaya, Kuala Lumpur 50603, Malaysia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,6,18]]},"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","first-page":"209","article-title":"Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries","volume":"71","author":"Sung","year":"2021","journal-title":"CA Cancer. J. Clin."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"459","DOI":"10.1016\/S1470-2045(09)70025-7","article-title":"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","volume":"10","author":"Stupp","year":"2009","journal-title":"Lancet Oncol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"7204","DOI":"10.1111\/jcmm.16750","article-title":"Identification and characterization of N6-methyladenosine modification of circRNAs in glioblastoma","volume":"25","author":"Zhang","year":"2021","journal-title":"J. Cell. Mol. Med."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"5913","DOI":"10.1038\/s41467-023-41663-2","article-title":"Hypoxanthine phosphoribosyl transferase 1 metabolizes temozolomide to activate AMPK for driving chemoresistance of glioblastomas","volume":"14","author":"Yin","year":"2023","journal-title":"Nat. Commun."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"e2203958","DOI":"10.1002\/adma.202203958","article-title":"Brain co-delivery of temozolomide and cisplatin for combinatorial glioblastoma chemotherapy","volume":"34","author":"Zou","year":"2022","journal-title":"Adv. Mater."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"857","DOI":"10.1093\/neuonc\/noac242","article-title":"A novel compound EPIC-0412 reverses temozolomide resistance via inhibiting DNA repair\/MGMT in glioblastoma","volume":"25","author":"Zhao","year":"2023","journal-title":"Neuro. Oncol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"4330","DOI":"10.7150\/thno.71763","article-title":"PTRF\/Cavin-1 enhances chemo-resistance and promotes temozolomide efflux through extracellular vesicles in glioblastoma","volume":"12","author":"Yang","year":"2022","journal-title":"Theranostics"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"267","DOI":"10.2217\/epi-2019-0295","article-title":"Circular RNA: Biogenesis, degradation, functions and potential roles in mediating resistance to anticarcinogens","volume":"12","author":"Geng","year":"2020","journal-title":"Epigenomics"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1186\/s12943-019-0986-2","article-title":"Exo-circRNAs: A new paradigm for anticancer therapy","volume":"18","author":"Bai","year":"2019","journal-title":"Mol. Cancer"},{"key":"ref_11","first-page":"4291","article-title":"Whole-transcriptome sequencing with ceRNA regulation network construction and verification in glioblastoma","volume":"15","author":"Zeng","year":"2023","journal-title":"Am. J. Transl. Res."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"242","DOI":"10.1038\/s41392-020-00359-5","article-title":"Exosome-mediated metabolic reprogramming: The emerging role in tumor microenvironment remodeling and its influence on cancer progression","volume":"5","author":"Yang","year":"2020","journal-title":"Signal Transduct. Target. Ther."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1186\/s13046-023-02916-6","article-title":"Circular RNA circATP9A promotes non-small cell lung cancer progression by interacting with HuR and by promoting extracellular vesicles-mediated macrophage M2 polarization","volume":"42","author":"Yao","year":"2023","journal-title":"J. Exp. Clin. Cancer Res."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"111256","DOI":"10.1016\/j.brainresbull.2025.111256","article-title":"Exosome-based platforms for treatment of multiple sclerosis","volume":"222","author":"Zonouz","year":"2025","journal-title":"Brain Res. Bull."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"463","DOI":"10.1186\/s12951-024-02681-4","article-title":"Exosomes as therapeutic and drug delivery vehicle for neurodegenerative diseases","volume":"22","author":"Nouri","year":"2024","journal-title":"J. Nanobiotechnol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"287","DOI":"10.1002\/cac2.12275","article-title":"Essential roles of exosome and circRNA_101093 on ferroptosis desensitization in lung adenocarcinoma","volume":"42","author":"Zhang","year":"2022","journal-title":"Cancer Commun."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1186\/s13046-023-02642-z","article-title":"circMMD reduction following tumor treating fields inhibits glioblastoma progression through FUBP1\/FIR\/DVL1 and miR-15b-5p\/FZD6 signaling","volume":"42","author":"Xu","year":"2023","journal-title":"J. Exp. Clin. Cancer Res."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"242","DOI":"10.1186\/s13046-023-02816-9","article-title":"CircRNF10 triggers a positive feedback loop to facilitate progression of glioblastoma via redeploying the ferroptosis defense in GSCs","volume":"42","author":"Wang","year":"2023","journal-title":"J. Exp. Clin. Cancer Res."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"897","DOI":"10.1111\/cns.13821","article-title":"Hsa_circ_0072309 enhances autophagy and TMZ sensitivity in glioblastoma","volume":"28","author":"Yuan","year":"2022","journal-title":"CNS Neurosci. Ther."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1684","DOI":"10.1007\/s11064-016-1884-2","article-title":"MiR-508-5p inhibits the progression of glioma by targeting glycoprotein non-metastatic melanoma B","volume":"41","author":"Bao","year":"2016","journal-title":"Neurochem. Res."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"596","DOI":"10.1038\/s41419-022-05056-5","article-title":"Exosomal circWDR62 promotes temozolomide resistance and malignant progression through regulation of the miR-370-3p\/MGMT axis in glioma","volume":"13","author":"Geng","year":"2022","journal-title":"Cell Death Dis."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1016\/j.gendis.2016.04.007","article-title":"Temozolomide resistance in glioblastoma multiforme","volume":"3","author":"Lee","year":"2016","journal-title":"Genes Dis."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"112432","DOI":"10.1016\/j.cellsig.2026.112432","article-title":"Intercellular transfer of circ_0017636 via exosomal vehicles overcomes glioblastoma chemoresistance through ARRB1-mediated signaling restoration","volume":"143","author":"Li","year":"2026","journal-title":"Cell. Signal."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"bbac261","DOI":"10.1093\/bib\/bbac261","article-title":"Hiplot: A comprehensive and easy-to-use web service for boosting publication-ready biomedical data visualization","volume":"23","author":"Li","year":"2022","journal-title":"Brief. Bioinform."},{"key":"ref_25","first-page":"14.42.1","article-title":"Isolation and characterization of exosomes from cultures of tissue explants and cell lines","volume":"115","author":"Baranov","year":"2016","journal-title":"Curr. Protoc. Immunol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1535750","DOI":"10.1080\/20013078.2018.1535750","article-title":"Minimal information for studies of extracellular vesicles 2018 (MISEV2018): A position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines","volume":"7","author":"Thery","year":"2018","journal-title":"J. Extracell. Vesicles"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1186\/s13046-023-02620-5","article-title":"Targeting tumor exosomal circular RNA cSERPINE2 suppresses breast cancer progression by modulating MALT1-NF-\u03baB-IL-6 axis of tumor-associated macrophages","volume":"42","author":"Zhou","year":"2023","journal-title":"J. Exp. Clin. Cancer Res."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1038\/s41419-024-06695-6","article-title":"Glioblastoma stem cells deliver ABCB4 transcribed by ATF3 via exosomes conferring glioblastoma resistance to temozolomide","volume":"15","author":"Xu","year":"2024","journal-title":"Cell Death Dis."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Zhu, Y., Liu, X., Zhao, P., Zhao, H., Gao, W., and Wang, L. (2020). Celastrol suppresses glioma vasculogenic mimicry formation and angiogenesis by blocking the PI3K\/Akt\/mTOR signaling pathway. Front. Pharmacol., 11.","DOI":"10.3389\/fphar.2020.00025"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1016\/j.jconrel.2014.12.013","article-title":"Biodistribution and delivery efficiency of unmodified tumor-derived exosomes","volume":"199","author":"Smyth","year":"2015","journal-title":"J. Control. Release"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1016\/j.jconrel.2019.11.009","article-title":"Systemic delivery of microRNA-21 antisense oligonucleotides to the brain using T7-peptide decorated exosomes","volume":"317","author":"Kim","year":"2020","journal-title":"J. Control. Release"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Sullivan, P.M., Reed, S.J., Kalia, V., and Sarkar, S. (2021). Solid tumor microenvironment can harbor and support functional properties of memory T cells. Front. Immunol., 12.","DOI":"10.3389\/fimmu.2021.706150"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1186\/s12943-024-01968-2","article-title":"Bladder-cancer-derived exosomal circRNA_0013936 promotes suppressive immunity by up-regulating fatty acid transporter protein 2 and down-regulating receptor-interacting protein kinase 3 in PMN-MDSCs","volume":"23","author":"Shi","year":"2024","journal-title":"Mol. Cancer"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1038\/s41392-024-01814-3","article-title":"Cholangiocarcinoma combined with biliary obstruction: An exosomal circRNA signature for diagnosis and early recurrence monitoring","volume":"9","author":"Wen","year":"2024","journal-title":"Signal Transduct. Target. Ther."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"117027","DOI":"10.1016\/j.biopha.2024.117027","article-title":"New insights into the potential of exosomal circular RNAs in mediating cancer chemotherapy resistance and their clinical applications","volume":"177","author":"Li","year":"2024","journal-title":"Biomed. Pharmacother."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1378056","DOI":"10.1080\/20013078.2017.1378056","article-title":"Neutral sphingomyelinases control extracellular vesicles budding from the plasma membrane","volume":"6","author":"Menck","year":"2017","journal-title":"J. Extracell. Vesicles"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"520","DOI":"10.1016\/j.amjms.2023.02.014","article-title":"miR-508-5p serves as an anti-oncogene by targeting S100A16 to regulate AKT signaling and epithelial-mesenchymal transition process in lung adenocarcinoma cells","volume":"365","author":"Wu","year":"2023","journal-title":"Am. J. Med. Sci."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"40","DOI":"10.4149\/neo_2017_105","article-title":"miR-508-5p acts as an anti-oncogene by targeting MESDC1 in hepatocellular carcinoma","volume":"64","author":"Wu","year":"2017","journal-title":"Neoplasma"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"41128","DOI":"10.1074\/jbc.M206747200","article-title":"Inhibition of tumor necrosis factor-induced cell death in MCF7 by a novel inhibitor of neutral sphingomyelinase","volume":"277","author":"Luberto","year":"2002","journal-title":"J. Biol. Chem."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"3267","DOI":"10.1038\/onc.2013.297","article-title":"miR-508-5p regulates multidrug resistance of gastric cancer by targeting ABCB1 and ZNRD1","volume":"33","author":"Shang","year":"2014","journal-title":"Oncogene"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"106643","DOI":"10.1016\/j.leukres.2021.106643","article-title":"miR-324-3p and miR-508-5p expression levels could serve as potential diagnostic and multidrug-resistant biomarkers in childhood acute lymphoblastic leukemia","volume":"109","author":"Zamani","year":"2021","journal-title":"Leuk. Res."},{"key":"ref_42","first-page":"76","article-title":"MiR-508-5p is a prognostic marker and inhibits cell proliferation and migration in glioma","volume":"21","author":"Liu","year":"2017","journal-title":"Eur. Rev. Med. Pharmacol. Sci."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1038\/nrc3430","article-title":"MDM2, MDMX and p53 in oncogenesis and cancer therapy","volume":"13","author":"Wade","year":"2013","journal-title":"Nat. Rev. Cancer"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1080\/15384101.2018.1557489","article-title":"Interaction with AEG-1 and MDM2 is associated with glioma development and progression and correlates with poor prognosis","volume":"18","author":"Ding","year":"2019","journal-title":"Cell Cycle"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1186\/s10020-020-00193-z","article-title":"Primary resistance to first-generation EGFR-TKIs induced by MDM2 amplification in NSCLC","volume":"26","author":"Sun","year":"2020","journal-title":"Mol. Med."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1186\/s12929-024-01004-x","article-title":"Targeting MDM2 in malignancies is a promising strategy for overcoming resistance to anticancer immunotherapy","volume":"31","author":"Sun","year":"2024","journal-title":"J. Biomed. Sci."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1038\/s41698-025-01063-9","article-title":"Synergistic effect of MDM2 inhibitors and radiotherapy in endometrial cancer","volume":"9","author":"Vargas","year":"2025","journal-title":"npj Precis. Oncol."},{"key":"ref_48","first-page":"448","article-title":"Signals ahead: Balancing cancer detection innovation and evidence","volume":"29","author":"Watson","year":"2025","journal-title":"Clin. J. Oncol. Nurs."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"3211","DOI":"10.1007\/s12035-017-0569-4","article-title":"MDM2 degrades deacetylated nucleolin through ubiquitination to promote glioma stem-like cell enrichment for chemotherapeutic resistance","volume":"55","author":"Ko","year":"2018","journal-title":"Mol. Neurobiol."},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"You, W., Feng, J., Guo, L., Yan, J., and Yan, S. (2025). Selenium nanoparticle-delivered MDM2 inhibitor reactivates p53 and reprograms tumor immune microenvironment in colorectal cancer. Front. Immunol., 16.","DOI":"10.3389\/fimmu.2025.1684611"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1186\/s40425-019-0750-6","article-title":"MDM2 inhibitor APG-115 synergizes with PD-1 blockade through enhancing antitumor immunity in the tumor microenvironment","volume":"7","author":"Fang","year":"2019","journal-title":"J. Immunother. Cancer"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1186\/s12951-022-01609-0","article-title":"Exosomes in the tumor microenvironment of sarcoma: From biological functions to clinical applications","volume":"20","author":"Ye","year":"2022","journal-title":"J. Nanobiotechnol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1744","DOI":"10.1016\/j.cmet.2021.08.006","article-title":"Exosomes as mediators of intercellular crosstalk in metabolism","volume":"33","author":"Isaac","year":"2021","journal-title":"Cell Metab."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"11499","DOI":"10.1021\/jacs.3c02844","article-title":"Single exosome amperometric measurements reveal encapsulation of chemical messengers for intercellular communication","volume":"145","author":"Hu","year":"2023","journal-title":"J. Am. Chem. Soc."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"238","DOI":"10.1016\/j.ebiom.2019.03.016","article-title":"Exosomal transfer of miR-1238 contributes to temozolomide-resistance in glioblastoma","volume":"42","author":"Yin","year":"2019","journal-title":"EBioMedicine"},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Wu, X., Wang, X., Wang, J., Hao, Y., Liu, F., Wang, X., Yang, L., and Lu, Z. (2021). The roles of exosomes as future therapeutic agents and diagnostic tools for glioma. Front. Oncol., 11.","DOI":"10.3389\/fonc.2021.733529"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1038\/nbt.1807","article-title":"Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes","volume":"29","author":"Seow","year":"2011","journal-title":"Nat. Biotechnol."},{"key":"ref_58","doi-asserted-by":"crossref","unstructured":"Gecys, D., Kazlauskas, A., Gecyte, E., Pauziene, N., Kulakauskiene, D., Lukminaite, I., and Jekabsone, A. (2022). Internalisation of RGD-engineered extracellular vesicles by glioblastoma cells. Biology, 11.","DOI":"10.3390\/biology11101483"},{"key":"ref_59","doi-asserted-by":"crossref","unstructured":"Pozdniakova, N., Generalov, E., Shevelev, A., and Tarasova, O. (2025). RNA therapeutics: Delivery problems and solutions-a review. Pharmaceutics, 17.","DOI":"10.3390\/pharmaceutics17101305"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"2003","DOI":"10.1007\/s11095-014-1593-y","article-title":"Exosome delivered anticancer drugs across the blood-brain barrier for brain cancer therapy in Danio rerio","volume":"32","author":"Yang","year":"2015","journal-title":"Pharm. Res."},{"key":"ref_61","doi-asserted-by":"crossref","unstructured":"Banks, W.A., Sharma, P., Bullock, K.M., Hansen, K.M., Ludwig, N., and Whiteside, T.L. (2020). Transport of extracellular vesicles across the blood-brain barrier: Brain pharmacokinetics and effects of inflammation. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21124407"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"550","DOI":"10.1016\/j.cell.2015.12.028","article-title":"Molecular profiling reveals biologically discrete subsets and pathways of progression in diffuse glioma","volume":"164","author":"Ceccarelli","year":"2016","journal-title":"Cell"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"603","DOI":"10.1038\/nature11003","article-title":"The cancer cell line encyclopedia enables predictive modelling of anticancer drug sensitivity","volume":"483","author":"Barretina","year":"2012","journal-title":"Nature"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"4529","DOI":"10.2174\/0929867323666160926150820","article-title":"MDM2 increases drug resistance in cancer cells by inducing EMT independent of p53","volume":"23","author":"Sun","year":"2016","journal-title":"Curr. Med. Chem."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"716","DOI":"10.1038\/bjc.2014.325","article-title":"Structurally diverse MDM2-p53 antagonists act as modulators of MDR-1 function in neuroblastoma","volume":"111","author":"Chen","year":"2014","journal-title":"Br. J. Cancer"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"416","DOI":"10.1158\/0008-5472.CAN-08-1856","article-title":"Reversal of P-glycoprotein-mediated multidrug resistance by the murine double minute 2 antagonist nutlin-3","volume":"69","author":"Michaelis","year":"2009","journal-title":"Cancer Res."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"2980","DOI":"10.1038\/ncomms3980","article-title":"Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs","volume":"4","author":"Vazquez","year":"2013","journal-title":"Nat. Commun."},{"key":"ref_68","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_69","doi-asserted-by":"crossref","first-page":"eaau6977","DOI":"10.1126\/science.aau6977","article-title":"The biology, function, and biomedical applications of exosomes","volume":"367","author":"Kalluri","year":"2020","journal-title":"Science"},{"key":"ref_70","doi-asserted-by":"crossref","unstructured":"Busatto, S., Vilanilam, G., Ticer, T., Lin, W.L., Dickson, D.W., Shapiro, S., Bergese, P., and Wolfram, J. (2018). Tangential flow filtration for highly efficient concentration of extracellular vesicles from large volumes of fluid. Cells, 7.","DOI":"10.3390\/cells7120273"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"748","DOI":"10.1038\/s41565-021-00931-2","article-title":"Extracellular vesicles as a next-generation drug delivery platform","volume":"16","author":"Herrmann","year":"2021","journal-title":"Nat. Nanotechnol."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"e12510","DOI":"10.1002\/jev2.12510","article-title":"A critical systematic review of extracellular vesicle clinical trials","volume":"13","author":"Mizenko","year":"2024","journal-title":"J. Extracell. Vesicles"}],"container-title":["Biomolecules"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2218-273X\/16\/6\/906\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,6,26]],"date-time":"2026-06-26T10:07:11Z","timestamp":1782468431000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2218-273X\/16\/6\/906"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,6,18]]},"references-count":72,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2026,6]]}},"alternative-id":["biom16060906"],"URL":"https:\/\/doi.org\/10.3390\/biom16060906","relation":{},"ISSN":["2218-273X"],"issn-type":[{"value":"2218-273X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,6,18]]}}}