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Role of small extracellular-vesicle microRNA-302f in endometriosis-associated ovarian cancer

ABSTRACT: Background: Tumor microenvironment is well known to have a key role in tumor development. Extracellular vesicles are capable in cell signaling transduction and important in regulation of tumor microenvironment. Objective: To investigate whether peritoneal fluid–derived extracellular vesicles help regulate the tumor microenvironment in the malignant transformation of endometriosis. Methods: Samples of peritoneal fluid were taken from women with benign gynecological disease, endometriosis, or endometriosis-associated ovarian cancer. Small extracellular vesicles in the samples were isolated via ultracentrifugation and characterized by western blotting, transmission electron microscopy, and nanoparticle tracking. A global microRNA (miRNA) expression profile array was used to analyze miRNA abundance in peritoneal fluid–derived small extracellular vesicles. Candidate miRNAs were quantified by reverse transcription PCR to assess their potential role in cell migration. Results: A total of 22 miRNAs were identified from the analysis of miRNAs in peritoneal fluid–derived small extracellular vesicles from patients with endometriosis or endometriosis-associated ovarian cancer. We confirmed that each miRNA was expressed in various ovarian cell lines. The miRNA miR-302f was consistently highly expressed in both clinical specimens and ovarian cell lines from patients with endometriosis, yet expression was relatively low in specimens and cell lines from patients with endometriosis-associated ovarian cancer. A bio-functional assay revealed that miR-302f regulates cell migration. Finally, the possible target mRNAs of miR-302f were identified in the Gene Expression Omnibus database. Conclusions: These data may provide a basis for the development of novel therapeutic strategies for endometriosis-associated ovarian cancer patients by downregulating PDGFRA abundance in cancer cells via overexpression of miR-302f.

ORGANISM(S): Homo sapiens

PROVIDER: GSE307729 | GEO | 2026/01/14

REPOSITORIES: GEO

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Project description:Background: Newer 3D culturing approaches are a promising way to better mimic the in vivo tumor microenvironment and to study the interactions between the heterogeneous cell populations of glioblastoma multiforme. Like many other tumors, glioblastoma uses extracellular vesicles as an intercellular communication system to prepare surrounding tissue for invasive tumor growth. However, little is known about the effects of 3D culture on extracellular vesicles. The aim of this study was to comprehensively characterise extracellular vesicles in 3D organoid models and compare them to conventional 2D cell culture systems.Methods: Primary glioblastoma cells were cultured as 2D and 3D organoid models. Extracellular vesicles were obtained by precipitation and immunoaffinity, with the latter allowing targeted isolation of the CD9/CD63/CD81 vesicle subpopulation. Comprehensive vesicle characterisation was performed and miRNA expression profiles were generated by smallRNA-sequencing. In silico analysis of differentially regulated miRNAs was performed to identify mRNA targets and corresponding signaling pathways. The tumor cell media and extracellular vesicle proteome were analysed by high-resolution mass spectrometry.Results: We observed an increased concentration of extracellular vesicles in 3D organoid cultures. Differential gene expression analysis further revealed the regulation of twelve miRNAs in 3D tumor organoid cultures (with nine miRNAs down and three miRNAs upregulated). MiR-23a-3p, known to be involved in glioblastoma invasion, was significantly increased in 3D. MiR-7-5p, which counteracts glioblastoma malignancy, was significantly decreased. Moreover, we identified four miRNAs (miR- 323a-3p, miR-382-5p, miR-370-3p, miR-134-5p) located within the DLK1-DIO3 domain, a cancer associated genomic region, suggesting a possible importance of this region in glioblastoma progression. Overrepresentation analysis identified alterations of extracellular vesicle cargo in 3D organoids, including representation of several miRNA targets and proteins primarily implicated in the immune response.Conclusion: Our results show that 3D glioblastoma organoid models secrete extracellular vesicles with an altered cargo compared to corresponding conventional 2D cultures. Extracellular vesicles from 3D cultures were found to contain signaling molecules associated with the immune regulatory signaling pathways and as such could potentially change the surrounding microenvironment towards tumor progression and immunosuppressive conditions. These findings suggest the use of 3D glioblastoma models for further clinical biomarker studies as well as investigation of new therapeutic options.

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Role of small extracellular-vesicle microRNA-302f in endometriosis-associated ovarian cancer

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