MiRNA-mRNA integrative analysis reveals epigenetically regulated and prognostic miR-103a with a role in migration and invasion of carboplatin-resistant ovarian cancer cells that acquired mesenchymal-like phenotype
DNA methylation, histone modifications, and miRNAs affect ovarian cancer (OC) progression and therapy response. Identification of epigenetically downregulated miRNAs in drug-resistant OC cell lines with a possible role in drug resistance and/or drug-induced mesenchymal-like phenotype. MiRNA profilin...
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Published in | Biomedicine & pharmacotherapy Vol. 166; p. 115349 |
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Main Authors | , , , , , , , , , |
Format | Journal Article |
Language | English |
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Elsevier Masson SAS
01.10.2023
Elsevier |
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Abstract | DNA methylation, histone modifications, and miRNAs affect ovarian cancer (OC) progression and therapy response.
Identification of epigenetically downregulated miRNAs in drug-resistant OC cell lines with a possible role in drug resistance and/or drug-induced mesenchymal-like phenotype.
MiRNA profiling was performed on parental and carboplatin-resistant OC cells, MES-OV and MES-OV CBP. RT-qPCR validation, epigenetic modulation and other CBP-resistant OC cell lines were used to select miRNAs of interest. The integration of miRNA-predicted target genes and differentially expressed genes (DEGs), pathway and functional analysis were used for forecasting their biological role. Data mining was performed to determine their possible prognostic and predictive values.
MiRNA profiling revealed 48 downregulated miRNAs in OC cells whose drug sensitivity and metastatic potential were impacted by epigenetic modulators. Of the fourteen selected, nine were validated as changed, and seven of these restored their expression upon treatment with epigenetic inhibitors. Only three had similar expression patterns in other OC cell lines. MiRNA-mRNA integrative analysis resulted in 56 target DEGs. Pathway analysis revealed that these genes are involved in cell adhesion, migration, and invasion. The functional analysis confirmed the role of miR-103a–3p, miR-17–5p and miR-107 in cell invasion, while data mining showed their prognostic and predictive values. Only miR-103a–3p was epigenetically regulated at the constitutive level.
High throughput miRNA and cDNA profiling coupled with pathway analysis and data mining delivered evidence for miRNAs which can be epigenetically regulated in drug-resistant, mesenchymal-like OC cells as possible markers to combat therapy-induced short overall survival and tumor metastatic potential.
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•Microarray analysis identifies 77 differentially expressed miRNAs in drug resistant EOC cells.•Epigenetic modulators impact cells’ drug response and metastatic capacity.•Downregulated miR-103a, 17 and 107 are shared feature of several resistant EOC cell lines and has a prognostic value.•MiRNA-mRNA integrative analysis reveals signaling pathways involved in metastasis.•Epigenetically regulated miR-103a is involved in metastasis but not drug response. |
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AbstractList | BACKGROUNDDNA methylation, histone modifications, and miRNAs affect ovarian cancer (OC) progression and therapy response. PURPOSEIdentification of epigenetically downregulated miRNAs in drug-resistant OC cell lines with a possible role in drug resistance and/or drug-induced mesenchymal-like phenotype. METHODSMiRNA profiling was performed on parental and carboplatin-resistant OC cells, MES-OV and MES-OV CBP. RT-qPCR validation, epigenetic modulation and other CBP-resistant OC cell lines were used to select miRNAs of interest. The integration of miRNA-predicted target genes and differentially expressed genes (DEGs), pathway and functional analysis were used for forecasting their biological role. Data mining was performed to determine their possible prognostic and predictive values. RESULTSMiRNA profiling revealed 48 downregulated miRNAs in OC cells whose drug sensitivity and metastatic potential were impacted by epigenetic modulators. Of the fourteen selected, nine were validated as changed, and seven of these restored their expression upon treatment with epigenetic inhibitors. Only three had similar expression patterns in other OC cell lines. MiRNA-mRNA integrative analysis resulted in 56 target DEGs. Pathway analysis revealed that these genes are involved in cell adhesion, migration, and invasion. The functional analysis confirmed the role of miR-103a-3p, miR-17-5p and miR-107 in cell invasion, while data mining showed their prognostic and predictive values. Only miR-103a-3p was epigenetically regulated at the constitutive level. CONCLUSIONHigh throughput miRNA and cDNA profiling coupled with pathway analysis and data mining delivered evidence for miRNAs which can be epigenetically regulated in drug-resistant, mesenchymal-like OC cells as possible markers to combat therapy-induced short overall survival and tumor metastatic potential. Background: DNA methylation, histone modifications, and miRNAs affect ovarian cancer (OC) progression and therapy response. Purpose: Identification of epigenetically downregulated miRNAs in drug-resistant OC cell lines with a possible role in drug resistance and/or drug-induced mesenchymal-like phenotype. Methods: MiRNA profiling was performed on parental and carboplatin-resistant OC cells, MES-OV and MES-OV CBP. RT-qPCR validation, epigenetic modulation and other CBP-resistant OC cell lines were used to select miRNAs of interest. The integration of miRNA-predicted target genes and differentially expressed genes (DEGs), pathway and functional analysis were used for forecasting their biological role. Data mining was performed to determine their possible prognostic and predictive values. Results: MiRNA profiling revealed 48 downregulated miRNAs in OC cells whose drug sensitivity and metastatic potential were impacted by epigenetic modulators. Of the fourteen selected, nine were validated as changed, and seven of these restored their expression upon treatment with epigenetic inhibitors. Only three had similar expression patterns in other OC cell lines. MiRNA-mRNA integrative analysis resulted in 56 target DEGs. Pathway analysis revealed that these genes are involved in cell adhesion, migration, and invasion. The functional analysis confirmed the role of miR-103a–3p, miR-17–5p and miR-107 in cell invasion, while data mining showed their prognostic and predictive values. Only miR-103a–3p was epigenetically regulated at the constitutive level. Conclusion: High throughput miRNA and cDNA profiling coupled with pathway analysis and data mining delivered evidence for miRNAs which can be epigenetically regulated in drug-resistant, mesenchymal-like OC cells as possible markers to combat therapy-induced short overall survival and tumor metastatic potential. DNA methylation, histone modifications, and miRNAs affect ovarian cancer (OC) progression and therapy response. Identification of epigenetically downregulated miRNAs in drug-resistant OC cell lines with a possible role in drug resistance and/or drug-induced mesenchymal-like phenotype. MiRNA profiling was performed on parental and carboplatin-resistant OC cells, MES-OV and MES-OV CBP. RT-qPCR validation, epigenetic modulation and other CBP-resistant OC cell lines were used to select miRNAs of interest. The integration of miRNA-predicted target genes and differentially expressed genes (DEGs), pathway and functional analysis were used for forecasting their biological role. Data mining was performed to determine their possible prognostic and predictive values. MiRNA profiling revealed 48 downregulated miRNAs in OC cells whose drug sensitivity and metastatic potential were impacted by epigenetic modulators. Of the fourteen selected, nine were validated as changed, and seven of these restored their expression upon treatment with epigenetic inhibitors. Only three had similar expression patterns in other OC cell lines. MiRNA-mRNA integrative analysis resulted in 56 target DEGs. Pathway analysis revealed that these genes are involved in cell adhesion, migration, and invasion. The functional analysis confirmed the role of miR-103a–3p, miR-17–5p and miR-107 in cell invasion, while data mining showed their prognostic and predictive values. Only miR-103a–3p was epigenetically regulated at the constitutive level. High throughput miRNA and cDNA profiling coupled with pathway analysis and data mining delivered evidence for miRNAs which can be epigenetically regulated in drug-resistant, mesenchymal-like OC cells as possible markers to combat therapy-induced short overall survival and tumor metastatic potential. [Display omitted] •Microarray analysis identifies 77 differentially expressed miRNAs in drug resistant EOC cells.•Epigenetic modulators impact cells’ drug response and metastatic capacity.•Downregulated miR-103a, 17 and 107 are shared feature of several resistant EOC cell lines and has a prognostic value.•MiRNA-mRNA integrative analysis reveals signaling pathways involved in metastasis.•Epigenetically regulated miR-103a is involved in metastasis but not drug response. |
ArticleNumber | 115349 |
Author | Kralj, Juran Culig, Zoran Orešković, Slavko Babić, Ivan Zhang, Wei Pernar Kovač, Margareta Brozovic, Anamaria Banović, Vladimir Tadić, Vanja Milković Periša, Marija |
Author_xml | – sequence: 1 givenname: Margareta surname: Pernar Kovač fullname: Pernar Kovač, Margareta organization: Division of Molecular Biology, Ruđer Bošković Institute, Bijenička cesta 54, HR-10000 Zagreb, Croatia – sequence: 2 givenname: Vanja surname: Tadić fullname: Tadić, Vanja organization: Division of Molecular Biology, Ruđer Bošković Institute, Bijenička cesta 54, HR-10000 Zagreb, Croatia – sequence: 3 givenname: Juran orcidid: 0000-0002-0991-9414 surname: Kralj fullname: Kralj, Juran organization: Division of Molecular Biology, Ruđer Bošković Institute, Bijenička cesta 54, HR-10000 Zagreb, Croatia – sequence: 4 givenname: Marija surname: Milković Periša fullname: Milković Periša, Marija organization: University Hospital Centre Zagreb, Department of Pathology and Cytology, Petrova ulica 13, HR-10000 Zagreb, Croatia – sequence: 5 givenname: Slavko surname: Orešković fullname: Orešković, Slavko organization: Department of Obstetrics and Gynecology, University Hospital Center Zagreb, Petrova 13, HR-10000 Zagreb, Croatia – sequence: 6 givenname: Ivan surname: Babić fullname: Babić, Ivan organization: Department of Obstetrics and Gynecology, University Hospital Center Zagreb, Petrova 13, HR-10000 Zagreb, Croatia – sequence: 7 givenname: Vladimir surname: Banović fullname: Banović, Vladimir organization: Department of Obstetrics and Gynecology, University Hospital Center Zagreb, Petrova 13, HR-10000 Zagreb, Croatia – sequence: 8 givenname: Wei orcidid: 0000-0002-8475-3143 surname: Zhang fullname: Zhang, Wei organization: Department of Engineering Mechanics, Dalian University of Technology, Linggong Road 2, 116024 Dalian, China – sequence: 9 givenname: Zoran surname: Culig fullname: Culig, Zoran organization: Department of Urology, Medical University of Innsbruck, Anichstrasse 35, A-6020 Innsbruck, Austria – sequence: 10 givenname: Anamaria orcidid: 0000-0002-6820-2173 surname: Brozovic fullname: Brozovic, Anamaria email: brozovic@irb.hr organization: Division of Molecular Biology, Ruđer Bošković Institute, Bijenička cesta 54, HR-10000 Zagreb, Croatia |
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Keywords | Biomarkers Epithelial-mesenchymal transition MicroRNA Epigenetic regulation Drug resistance Ovarian cancer |
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Identification of epigenetically downregulated... BACKGROUNDDNA methylation, histone modifications, and miRNAs affect ovarian cancer (OC) progression and therapy response. PURPOSEIdentification of... Background: DNA methylation, histone modifications, and miRNAs affect ovarian cancer (OC) progression and therapy response. Purpose: Identification of... |
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SubjectTerms | Biomarkers Drug resistance Epigenetic regulation Epithelial-mesenchymal transition MicroRNA Ovarian cancer |
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Title | MiRNA-mRNA integrative analysis reveals epigenetically regulated and prognostic miR-103a with a role in migration and invasion of carboplatin-resistant ovarian cancer cells that acquired mesenchymal-like phenotype |
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