MiR-200c sensitizes Olaparib-resistant ovarian cancer cells by targeting Neuropilin 1
Identifieur interne : 000110 ( an2020/Analysis ); précédent : 000109; suivant : 000111MiR-200c sensitizes Olaparib-resistant ovarian cancer cells by targeting Neuropilin 1
Auteurs : Enrica Vescarelli [Italie] ; Giulia Gerini [Italie] ; Francesca Megiorni [Italie] ; Eleni Anastasiadou [Italie] ; Paola Pontecorvi [Italie] ; Luciana Solito [Italie] ; Claudia De Vitis [Italie] ; Simona Camero [Italie] ; Claudia Marchetti [Italie] ; Rita Mancini [Italie] ; Pierluigi Benedetti Panici [Italie] ; Carlo Dominici [Italie] ; Ferdinando Romano [Italie] ; Antonio Angeloni [Italie] ; Cinzia Marchese [Italie] ; Simona Ceccarelli [Italie]Source :
- Journal of Experimental & Clinical Cancer Research : CR [ 0392-9078 ] ; 2020.
Abstract
Ovarian cancer (OC) is the most lethal gynecological malignancy and the second leading cause of cancer-related death in women. Treatment with PARP inhibitors (PARPi), such as Olaparib, has been recently introduced for OC patients, but resistance may occur and underlying mechanisms are still poorly understood. The aim of this study is to identify target genes within the tumor cells that might cause resistance to Olaparib. We focused on Neuropilin 1 (NRP1), a transmembrane receptor expressed in OC and correlated with poor survival, which has been also proposed as a key molecule in OC multidrug resistance.
Using three OC cell lines (UWB, UWB-BRCA and SKOV3) as model systems, we evaluated the biological and molecular effects of Olaparib on OC cell growth, cell cycle, DNA damage and apoptosis/autophagy induction, through MTT and colony forming assays, flow cytometry, immunofluorescence and Western blot analyses. We evaluated NRP1 expression in OC specimens and cell lines by Western blot and qRT-PCR, and used RNA interference to selectively inhibit NRP1. To identify miR-200c as a regulator of NRP1, we used miRNA target prediction algorithms and Pearsons’ correlation analysis in biopsies from OC patients. Then, we used a stable transfection approach to overexpress miR-200c in Olaparib-resistant cells.
We observed that NRP1 is expressed at high levels in resistant cells (SKOV3) and is upmodulated in partially sensitive cells (UWB-BRCA) upon prolonged Olaparib treatment, leading to poor drug response. Our results show that the selective inhibition of NRP1 is able to overcome Olaparib resistance in SKOV3 cells. Moreover, we demonstrated that miR-200c can target NRP1 in OC cells, causing its downmodulation, and that miR-200c overexpression is a valid approach to restore Olaparib sensitivity in OC resistant cells.
These data demonstrate that miR-200c significantly enhanced the anti-cancer efficacy of Olaparib in drug-resistant OC cells. Thus, the combination of Olaparib with miRNA-based therapy may represent a promising treatment for drug resistant OC, and our data may help in designing novel precision medicine trials for optimizing the clinical use of PARPi.
Url:
DOI: 10.1186/s13046-019-1490-7
PubMed: 31898520
PubMed Central: 6939329
Affiliations:
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uniqKey="Vescarelli E" first="Enrica" last="Vescarelli">Enrica Vescarelli</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="GRID">grid.7841.a</institution-id><institution>Department of Experimental Medicine,</institution><institution>Sapienza University of Rome,</institution></institution-wrap>Viale Regina Elena 324, 00161 Rome, Italy</nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Viale Regina Elena 324, 00161 Rome</wicri:regionArea><placeName><settlement type="city">Rome</settlement><region nuts="2">Latium</region></placeName></affiliation></author><author><name sortKey="Gerini, Giulia" sort="Gerini, Giulia" uniqKey="Gerini G" first="Giulia" last="Gerini">Giulia Gerini</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="GRID">grid.7841.a</institution-id><institution>Department of Experimental Medicine,</institution><institution>Sapienza University of Rome,</institution></institution-wrap>Viale Regina Elena 324, 00161 Rome, Italy</nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Viale Regina Elena 324, 00161 Rome</wicri:regionArea><placeName><settlement type="city">Rome</settlement><region nuts="2">Latium</region></placeName></affiliation></author><author><name sortKey="Megiorni, Francesca" sort="Megiorni, Francesca" uniqKey="Megiorni F" first="Francesca" last="Megiorni">Francesca Megiorni</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="GRID">grid.7841.a</institution-id><institution>Department of Experimental Medicine,</institution><institution>Sapienza University of Rome,</institution></institution-wrap>Viale Regina Elena 324, 00161 Rome, Italy</nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Viale Regina Elena 324, 00161 Rome</wicri:regionArea><placeName><settlement type="city">Rome</settlement><region nuts="2">Latium</region></placeName></affiliation></author><author><name sortKey="Anastasiadou, Eleni" sort="Anastasiadou, Eleni" uniqKey="Anastasiadou E" first="Eleni" last="Anastasiadou">Eleni Anastasiadou</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="GRID">grid.7841.a</institution-id><institution>Department of Experimental Medicine,</institution><institution>Sapienza University of Rome,</institution></institution-wrap>Viale Regina Elena 324, 00161 Rome, Italy</nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Viale Regina Elena 324, 00161 Rome</wicri:regionArea><placeName><settlement type="city">Rome</settlement><region nuts="2">Latium</region></placeName></affiliation></author><author><name sortKey="Pontecorvi, Paola" sort="Pontecorvi, Paola" uniqKey="Pontecorvi P" first="Paola" last="Pontecorvi">Paola Pontecorvi</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="GRID">grid.7841.a</institution-id><institution>Department of Experimental Medicine,</institution><institution>Sapienza University of Rome,</institution></institution-wrap>Viale Regina Elena 324, 00161 Rome, Italy</nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Viale Regina Elena 324, 00161 Rome</wicri:regionArea><placeName><settlement type="city">Rome</settlement><region nuts="2">Latium</region></placeName></affiliation></author><author><name sortKey="Solito, Luciana" sort="Solito, Luciana" uniqKey="Solito L" first="Luciana" last="Solito">Luciana Solito</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="GRID">grid.7841.a</institution-id><institution>Department of Experimental Medicine,</institution><institution>Sapienza University of Rome,</institution></institution-wrap>Viale Regina Elena 324, 00161 Rome, Italy</nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Viale Regina Elena 324, 00161 Rome</wicri:regionArea><placeName><settlement type="city">Rome</settlement><region nuts="2">Latium</region></placeName></affiliation></author><author><name sortKey="De Vitis, Claudia" sort="De Vitis, Claudia" uniqKey="De Vitis C" first="Claudia" last="De Vitis">Claudia De Vitis</name><affiliation wicri:level="1"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="GRID">grid.7841.a</institution-id><institution>Department of Clinical and Molecular Medicine,</institution><institution>Sapienza University of Rome,</institution></institution-wrap>00161 Rome, Italy</nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>00161 Rome</wicri:regionArea></affiliation></author><author><name sortKey="Camero, Simona" sort="Camero, Simona" uniqKey="Camero S" first="Simona" last="Camero">Simona Camero</name><affiliation wicri:level="1"><nlm:aff id="Aff3"><institution-wrap><institution-id 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Public Health and Infectious Diseases,</institution><institution>Sapienza University of Rome,</institution></institution-wrap>00185 Rome, Italy</nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>00185 Rome</wicri:regionArea></affiliation></author><author><name sortKey="Angeloni, Antonio" sort="Angeloni, Antonio" uniqKey="Angeloni A" first="Antonio" last="Angeloni">Antonio Angeloni</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="GRID">grid.7841.a</institution-id><institution>Department of Experimental Medicine,</institution><institution>Sapienza University of Rome,</institution></institution-wrap>Viale Regina Elena 324, 00161 Rome, Italy</nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Viale Regina Elena 324, 00161 Rome</wicri:regionArea><placeName><settlement type="city">Rome</settlement><region nuts="2">Latium</region></placeName></affiliation></author><author><name sortKey="Marchese, Cinzia" sort="Marchese, Cinzia" uniqKey="Marchese C" first="Cinzia" last="Marchese">Cinzia Marchese</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="GRID">grid.7841.a</institution-id><institution>Department of Experimental Medicine,</institution><institution>Sapienza University of Rome,</institution></institution-wrap>Viale Regina Elena 324, 00161 Rome, Italy</nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Viale Regina Elena 324, 00161 Rome</wicri:regionArea><placeName><settlement type="city">Rome</settlement><region nuts="2">Latium</region></placeName></affiliation></author><author><name sortKey="Ceccarelli, Simona" sort="Ceccarelli, Simona" uniqKey="Ceccarelli S" first="Simona" last="Ceccarelli">Simona Ceccarelli</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="GRID">grid.7841.a</institution-id><institution>Department of Experimental Medicine,</institution><institution>Sapienza University of Rome,</institution></institution-wrap>Viale Regina Elena 324, 00161 Rome, Italy</nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Viale Regina Elena 324, 00161 Rome</wicri:regionArea><placeName><settlement type="city">Rome</settlement><region nuts="2">Latium</region></placeName></affiliation></author></analytic><series><title level="j">Journal of Experimental & Clinical Cancer Research : CR</title><idno type="ISSN">0392-9078</idno><idno type="eISSN">1756-9966</idno><imprint><date when="2020">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Background</title><p id="Par1">Ovarian cancer (OC) is the most lethal gynecological malignancy and the second leading cause of cancer-related death in women. Treatment with PARP inhibitors (PARPi), such as Olaparib, has been recently introduced for OC patients, but resistance may occur and underlying mechanisms are still poorly understood. The aim of this study is to identify target genes within the tumor cells that might cause resistance to Olaparib. We focused on Neuropilin 1 (NRP1), a transmembrane receptor expressed in OC and correlated with poor survival, which has been also proposed as a key molecule in OC multidrug resistance.</p></sec><sec><title>Methods</title><p id="Par2">Using three OC cell lines (UWB, UWB-BRCA and SKOV3) as model systems, we evaluated the biological and molecular effects of Olaparib on OC cell growth, cell cycle, DNA damage and apoptosis/autophagy induction, through MTT and colony forming assays, flow cytometry, immunofluorescence and Western blot analyses. We evaluated NRP1 expression in OC specimens and cell lines by Western blot and qRT-PCR, and used RNA interference to selectively inhibit NRP1. To identify miR-200c as a regulator of NRP1, we used miRNA target prediction algorithms and Pearsons’ correlation analysis in biopsies from OC patients. Then, we used a stable transfection approach to overexpress miR-200c in Olaparib-resistant cells.</p></sec><sec><title>Results</title><p id="Par3">We observed that NRP1 is expressed at high levels in resistant cells (SKOV3) and is upmodulated in partially sensitive cells (UWB-BRCA) upon prolonged Olaparib treatment, leading to poor drug response. Our results show that the selective inhibition of NRP1 is able to overcome Olaparib resistance in SKOV3 cells. Moreover, we demonstrated that miR-200c can target NRP1 in OC cells, causing its downmodulation, and that miR-200c overexpression is a valid approach to restore Olaparib sensitivity in OC resistant cells.</p></sec><sec><title>Conclusions</title><p id="Par4">These data demonstrate that miR-200c significantly enhanced the anti-cancer efficacy of Olaparib in drug-resistant OC cells. Thus, the combination of Olaparib with miRNA-based therapy may represent a promising treatment for drug resistant OC, and our data may help in designing novel precision medicine trials for optimizing the clinical use of PARPi.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Reid, Bm" uniqKey="Reid B">BM Reid</name></author><author><name sortKey="Permuth, Jb" uniqKey="Permuth J">JB Permuth</name></author><author><name sortKey="Sellers, Ta" uniqKey="Sellers T">TA Sellers</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hennessy, Bt" uniqKey="Hennessy B">BT Hennessy</name></author><author><name sortKey="Coleman, Rl" uniqKey="Coleman R">RL Coleman</name></author><author><name sortKey="Markman, M" uniqKey="Markman M">M Markman</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Siegel, Rl" uniqKey="Siegel R">RL Siegel</name></author><author><name sortKey="Miller, 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Spoelstra</name></author></analytic></biblStruct></listBibl></div1></back></TEI><affiliations><list><country><li>Italie</li></country><region><li>Latium</li></region><settlement><li>Rome</li></settlement></list><tree><country name="Italie"><region name="Latium"><name sortKey="Vescarelli, Enrica" sort="Vescarelli, Enrica" uniqKey="Vescarelli E" first="Enrica" last="Vescarelli">Enrica Vescarelli</name></region><name sortKey="Anastasiadou, Eleni" sort="Anastasiadou, Eleni" uniqKey="Anastasiadou E" first="Eleni" last="Anastasiadou">Eleni Anastasiadou</name><name sortKey="Angeloni, Antonio" sort="Angeloni, Antonio" uniqKey="Angeloni A" first="Antonio" last="Angeloni">Antonio Angeloni</name><name sortKey="Benedetti Panici, Pierluigi" sort="Benedetti Panici, Pierluigi" uniqKey="Benedetti Panici P" first="Pierluigi" last="Benedetti Panici">Pierluigi Benedetti Panici</name><name sortKey="Camero, Simona" sort="Camero, Simona" uniqKey="Camero S" first="Simona" last="Camero">Simona Camero</name><name sortKey="Ceccarelli, Simona" sort="Ceccarelli, Simona" uniqKey="Ceccarelli S" first="Simona" last="Ceccarelli">Simona Ceccarelli</name><name sortKey="De Vitis, Claudia" sort="De Vitis, Claudia" uniqKey="De Vitis C" first="Claudia" last="De Vitis">Claudia De Vitis</name><name sortKey="Dominici, Carlo" sort="Dominici, Carlo" uniqKey="Dominici C" first="Carlo" last="Dominici">Carlo Dominici</name><name sortKey="Gerini, Giulia" sort="Gerini, Giulia" uniqKey="Gerini G" first="Giulia" last="Gerini">Giulia Gerini</name><name sortKey="Mancini, Rita" sort="Mancini, Rita" uniqKey="Mancini R" first="Rita" last="Mancini">Rita Mancini</name><name sortKey="Marchese, Cinzia" sort="Marchese, Cinzia" uniqKey="Marchese C" first="Cinzia" last="Marchese">Cinzia Marchese</name><name sortKey="Marchetti, Claudia" sort="Marchetti, Claudia" uniqKey="Marchetti C" first="Claudia" last="Marchetti">Claudia Marchetti</name><name sortKey="Megiorni, Francesca" sort="Megiorni, Francesca" uniqKey="Megiorni F" first="Francesca" last="Megiorni">Francesca Megiorni</name><name sortKey="Pontecorvi, Paola" sort="Pontecorvi, Paola" uniqKey="Pontecorvi P" first="Paola" last="Pontecorvi">Paola Pontecorvi</name><name sortKey="Romano, Ferdinando" sort="Romano, Ferdinando" uniqKey="Romano F" first="Ferdinando" last="Romano">Ferdinando Romano</name><name sortKey="Solito, Luciana" sort="Solito, Luciana" uniqKey="Solito L" first="Luciana" last="Solito">Luciana Solito</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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