The CDK12–BRCA1 signaling axis mediates dinaciclib‐associated radiosensitivity through p53‐mediated cellular senescence

Pan‐cyclin‐dependent‐kinase (CDK) inhibitors are a new class of targeted therapies that can act on multiple CDKs, with dinaciclib being one of the most promising compounds. Although used as a monotherapy, an interesting approach could be to combine it with radiotherapy. Here, we show that dinaciclib...

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Main Authors: Natalia García Flores, Diego M. Fernández‐Aroca, Cristina Garnés‐García, Andrés Domínguez‐Calvo, Jaime Jiménez‐Suárez, Sebastià Sabater, Pablo Fernández‐Aroca, Ignacio Andrés, Francisco J. Cimas, Guillermo deCárcer, Borja Belandia, Ignacio Palmero, Pablo Huertas, María José Ruiz‐Hidalgo, Ricardo Sánchez‐Prieto
Format: Article
Language:English
Published: Wiley 2025-04-01
Series:Molecular Oncology
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Online Access:https://doi.org/10.1002/1878-0261.13773
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author Natalia García Flores
Diego M. Fernández‐Aroca
Cristina Garnés‐García
Andrés Domínguez‐Calvo
Jaime Jiménez‐Suárez
Sebastià Sabater
Pablo Fernández‐Aroca
Ignacio Andrés
Francisco J. Cimas
Guillermo deCárcer
Borja Belandia
Ignacio Palmero
Pablo Huertas
María José Ruiz‐Hidalgo
Ricardo Sánchez‐Prieto
author_facet Natalia García Flores
Diego M. Fernández‐Aroca
Cristina Garnés‐García
Andrés Domínguez‐Calvo
Jaime Jiménez‐Suárez
Sebastià Sabater
Pablo Fernández‐Aroca
Ignacio Andrés
Francisco J. Cimas
Guillermo deCárcer
Borja Belandia
Ignacio Palmero
Pablo Huertas
María José Ruiz‐Hidalgo
Ricardo Sánchez‐Prieto
author_sort Natalia García Flores
collection DOAJ
description Pan‐cyclin‐dependent‐kinase (CDK) inhibitors are a new class of targeted therapies that can act on multiple CDKs, with dinaciclib being one of the most promising compounds. Although used as a monotherapy, an interesting approach could be to combine it with radiotherapy. Here, we show that dinaciclib increases radiosensitivity in some experimental models of lung and colon cancer (A549 or HCT 116) but not in others (H1299 or HT‐29). Dinaciclib did not alter serine‐protein kinase ATM signalling or cell cycle profiling after ionising‐radiation exposure, which have been described for other CDK inhibitors. Interestingly, in terms of apoptosis, although the combination renders a clear increase, no potentiation of the ionising‐radiation‐induced apoptosis was observed. Mechanistically, inhibition of CDK12 by dinaciclib diminishes BRCA1 expression, which decreases homologous recombination (HR) and probably promotes the nonhomologous end joining repair process (NHEJ), which ultimately promotes the induction of ionising‐radiation‐associated cellular senescence in a TP53‐dependent manner, explaining the lack of effect observed in some experimental models. In conclusion, our report proposes a molecular mechanism, based on the signalling axis CDK12–BRCA1, involved in this newly identified therapeutic effect of dinaciclib, although other players implicated in HR should not be discarded. In addition, our data provide a rationale for more selective and personalised chemo/radiotherapy treatment according to the genetic background of the tumour.
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spelling doaj-art-44ead440b44148e1b0741c44d9fcf0df2025-08-20T02:16:21ZengWileyMolecular Oncology1574-78911878-02612025-04-011941265128010.1002/1878-0261.13773The CDK12–BRCA1 signaling axis mediates dinaciclib‐associated radiosensitivity through p53‐mediated cellular senescenceNatalia García Flores0Diego M. Fernández‐Aroca1Cristina Garnés‐García2Andrés Domínguez‐Calvo3Jaime Jiménez‐Suárez4Sebastià Sabater5Pablo Fernández‐Aroca6Ignacio Andrés7Francisco J. Cimas8Guillermo deCárcer9Borja Belandia10Ignacio Palmero11Pablo Huertas12María José Ruiz‐Hidalgo13Ricardo Sánchez‐Prieto14Laboratorio de Oncología Molecular, Unidad de Medicina Molecular, Instituto de Biomedicina Universidad de Castilla‐La Mancha Albacete SpainLaboratorio de Oncología Molecular, Unidad de Medicina Molecular, Instituto de Biomedicina Universidad de Castilla‐La Mancha Albacete SpainLaboratorio de Oncología Molecular, Unidad de Medicina Molecular, Instituto de Biomedicina Universidad de Castilla‐La Mancha Albacete SpainFacultad de Biología Universidad de Sevilla SpainLaboratorio de Oncología Molecular, Unidad de Medicina Molecular, Instituto de Biomedicina Universidad de Castilla‐La Mancha Albacete SpainServicio de Oncología Radioterápica Complejo Hospitalario Universitario de Albacete SpainLaboratorio de Oncología Molecular, Unidad de Medicina Molecular, Instituto de Biomedicina Universidad de Castilla‐La Mancha Albacete SpainServicio de Oncología Radioterápica Complejo Hospitalario Universitario de Albacete SpainLaboratorio de Oncología Molecular, Unidad de Medicina Molecular, Instituto de Biomedicina Universidad de Castilla‐La Mancha Albacete SpainUnidad de Biomedicina de la UCLM, Unidad asociada al CSIC Albacete SpainUnidad de Biomedicina de la UCLM, Unidad asociada al CSIC Albacete SpainLaboratorio de Senescencia Celular y Supresión Tumoral, Departamento de Biología del Cáncer Instituto de Investigaciones Biomédicas Sols‐Morreale (CSIC‐UAM) Madrid SpainFacultad de Biología Universidad de Sevilla SpainLaboratorio de Oncología Molecular, Unidad de Medicina Molecular, Instituto de Biomedicina Universidad de Castilla‐La Mancha Albacete SpainLaboratorio de Oncología Molecular, Unidad de Medicina Molecular, Instituto de Biomedicina Universidad de Castilla‐La Mancha Albacete SpainPan‐cyclin‐dependent‐kinase (CDK) inhibitors are a new class of targeted therapies that can act on multiple CDKs, with dinaciclib being one of the most promising compounds. Although used as a monotherapy, an interesting approach could be to combine it with radiotherapy. Here, we show that dinaciclib increases radiosensitivity in some experimental models of lung and colon cancer (A549 or HCT 116) but not in others (H1299 or HT‐29). Dinaciclib did not alter serine‐protein kinase ATM signalling or cell cycle profiling after ionising‐radiation exposure, which have been described for other CDK inhibitors. Interestingly, in terms of apoptosis, although the combination renders a clear increase, no potentiation of the ionising‐radiation‐induced apoptosis was observed. Mechanistically, inhibition of CDK12 by dinaciclib diminishes BRCA1 expression, which decreases homologous recombination (HR) and probably promotes the nonhomologous end joining repair process (NHEJ), which ultimately promotes the induction of ionising‐radiation‐associated cellular senescence in a TP53‐dependent manner, explaining the lack of effect observed in some experimental models. In conclusion, our report proposes a molecular mechanism, based on the signalling axis CDK12–BRCA1, involved in this newly identified therapeutic effect of dinaciclib, although other players implicated in HR should not be discarded. In addition, our data provide a rationale for more selective and personalised chemo/radiotherapy treatment according to the genetic background of the tumour.https://doi.org/10.1002/1878-0261.13773BRCA1CDK12dinaciclibradiosensitivitysenescence
spellingShingle Natalia García Flores
Diego M. Fernández‐Aroca
Cristina Garnés‐García
Andrés Domínguez‐Calvo
Jaime Jiménez‐Suárez
Sebastià Sabater
Pablo Fernández‐Aroca
Ignacio Andrés
Francisco J. Cimas
Guillermo deCárcer
Borja Belandia
Ignacio Palmero
Pablo Huertas
María José Ruiz‐Hidalgo
Ricardo Sánchez‐Prieto
The CDK12–BRCA1 signaling axis mediates dinaciclib‐associated radiosensitivity through p53‐mediated cellular senescence
Molecular Oncology
BRCA1
CDK12
dinaciclib
radiosensitivity
senescence
title The CDK12–BRCA1 signaling axis mediates dinaciclib‐associated radiosensitivity through p53‐mediated cellular senescence
title_full The CDK12–BRCA1 signaling axis mediates dinaciclib‐associated radiosensitivity through p53‐mediated cellular senescence
title_fullStr The CDK12–BRCA1 signaling axis mediates dinaciclib‐associated radiosensitivity through p53‐mediated cellular senescence
title_full_unstemmed The CDK12–BRCA1 signaling axis mediates dinaciclib‐associated radiosensitivity through p53‐mediated cellular senescence
title_short The CDK12–BRCA1 signaling axis mediates dinaciclib‐associated radiosensitivity through p53‐mediated cellular senescence
title_sort cdk12 brca1 signaling axis mediates dinaciclib associated radiosensitivity through p53 mediated cellular senescence
topic BRCA1
CDK12
dinaciclib
radiosensitivity
senescence
url https://doi.org/10.1002/1878-0261.13773
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