Combination drug screen targeting glioblastoma core vulnerabilities reveals pharmacological synergisms.

Cancer vulnerabilities Drug combination screening Glioblastoma Pharmacological synergisms Target deconvolution

Journal

EBioMedicine
ISSN: 2352-3964
Titre abrégé: EBioMedicine
Pays: Netherlands
ID NLM: 101647039

Informations de publication

Date de publication:
Sep 2023
Historique:
received: 21 12 2022
revised: 26 07 2023
accepted: 27 07 2023
medline: 18 9 2023
pubmed: 13 8 2023
entrez: 12 8 2023
Statut: ppublish

Résumé

Pharmacological synergisms are an attractive anticancer strategy. However, with more than 5000 approved-drugs and compounds in clinical development, identifying synergistic treatments represents a major challenge. High-throughput screening was combined with target deconvolution and functional genomics to reveal targetable vulnerabilities in glioblastoma. The role of the top gene hit was investigated by RNA interference, transcriptomics and immunohistochemistry in glioblastoma patient samples. Drug combination screen using a custom-made library of 88 compounds in association with six inhibitors of the identified glioblastoma vulnerabilities was performed to unveil pharmacological synergisms. Glioblastoma 3D spheroid, organotypic ex vivo and syngeneic orthotopic mouse models were used to validate synergistic treatments. Nine targetable vulnerabilities were identified in glioblastoma and the top gene hit RRM1 was validated as an independent prognostic factor. The associations of CHK1/MEK and AURKA/BET inhibitors were identified as the most potent amongst 528 tested pairwise drug combinations and their efficacy was validated in 3D spheroid models. The high synergism of AURKA/BET dual inhibition was confirmed in ex vivo and in vivo glioblastoma models, without detectable toxicity. Our work provides strong pre-clinical evidence of the efficacy of AURKA/BET inhibitor combination in glioblastoma and opens new therapeutic avenues for this unmet medical need. Besides, we established the proof-of-concept of a stepwise approach aiming at exploiting drug poly-pharmacology to unveil druggable cancer vulnerabilities and to fast-track the identification of synergistic combinations against refractory cancers. This study was funded by institutional grants and charities.

Sections du résumé

BACKGROUND BACKGROUND
Pharmacological synergisms are an attractive anticancer strategy. However, with more than 5000 approved-drugs and compounds in clinical development, identifying synergistic treatments represents a major challenge.
METHODS METHODS
High-throughput screening was combined with target deconvolution and functional genomics to reveal targetable vulnerabilities in glioblastoma. The role of the top gene hit was investigated by RNA interference, transcriptomics and immunohistochemistry in glioblastoma patient samples. Drug combination screen using a custom-made library of 88 compounds in association with six inhibitors of the identified glioblastoma vulnerabilities was performed to unveil pharmacological synergisms. Glioblastoma 3D spheroid, organotypic ex vivo and syngeneic orthotopic mouse models were used to validate synergistic treatments.
FINDINGS RESULTS
Nine targetable vulnerabilities were identified in glioblastoma and the top gene hit RRM1 was validated as an independent prognostic factor. The associations of CHK1/MEK and AURKA/BET inhibitors were identified as the most potent amongst 528 tested pairwise drug combinations and their efficacy was validated in 3D spheroid models. The high synergism of AURKA/BET dual inhibition was confirmed in ex vivo and in vivo glioblastoma models, without detectable toxicity.
INTERPRETATION CONCLUSIONS
Our work provides strong pre-clinical evidence of the efficacy of AURKA/BET inhibitor combination in glioblastoma and opens new therapeutic avenues for this unmet medical need. Besides, we established the proof-of-concept of a stepwise approach aiming at exploiting drug poly-pharmacology to unveil druggable cancer vulnerabilities and to fast-track the identification of synergistic combinations against refractory cancers.
FUNDING BACKGROUND
This study was funded by institutional grants and charities.

Identifiants

pubmed: 37572644
pii: S2352-3964(23)00317-1
doi: 10.1016/j.ebiom.2023.104752
pmc: PMC10433015
pii:
doi:

Substances chimiques

Aurora Kinase A EC 2.7.11.1
Antineoplastic Agents 0
Drug Combinations 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

104752

Informations de copyright

Copyright © 2023 The Author(s). Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors have declared no conflict of interest.

Auteurs

Jérémy Ariey-Bonnet (J)

Aix Marseille Université, Centre National de la Recherche Scientifique (CNRS), Institut National de la Santé et de la Recherche Médicale (INSERM), Institut Paoli Calmettes, Centre de Recherche en Cancérologie de Marseille (CRCM), Marseille, France.

Raphael Berges (R)

Aix Marseille Université, CNRS, UMR 7051, INP, Inst Neurophysiopathol, Marseille, France.

Marie-Pierre Montero (MP)

Aix Marseille Université, Centre National de la Recherche Scientifique (CNRS), Institut National de la Santé et de la Recherche Médicale (INSERM), Institut Paoli Calmettes, Centre de Recherche en Cancérologie de Marseille (CRCM), Marseille, France.

Baptiste Mouysset (B)

Aix Marseille Université, Centre National de la Recherche Scientifique (CNRS), Institut National de la Santé et de la Recherche Médicale (INSERM), Institut Paoli Calmettes, Centre de Recherche en Cancérologie de Marseille (CRCM), Marseille, France.

Patricia Piris (P)

Aix Marseille Université, Centre National de la Recherche Scientifique (CNRS), Institut National de la Santé et de la Recherche Médicale (INSERM), Institut Paoli Calmettes, Centre de Recherche en Cancérologie de Marseille (CRCM), Marseille, France.

Kevin Muller (K)

Aix Marseille Université, Centre National de la Recherche Scientifique (CNRS), Institut National de la Santé et de la Recherche Médicale (INSERM), Institut Paoli Calmettes, Centre de Recherche en Cancérologie de Marseille (CRCM), Marseille, France.

Guillaume Pinna (G)

Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, University Paris-Sud, Université Paris-Saclay, Gif-sur-Yvette F-91198, France.

Tim W Failes (TW)

Children's Cancer Institute, Lowy Cancer Research Centre, UNSW Sydney, Sydney, NSW 2052, Australia; ACRF Drug Discovery Centre for Childhood Cancer, Children's Cancer Institute, Lowy Cancer Research Centre, UNSW Sydney, Sydney, NSW 2052, Australia.

Greg M Arndt (GM)

Children's Cancer Institute, Lowy Cancer Research Centre, UNSW Sydney, Sydney, NSW 2052, Australia; ACRF Drug Discovery Centre for Childhood Cancer, Children's Cancer Institute, Lowy Cancer Research Centre, UNSW Sydney, Sydney, NSW 2052, Australia.

Philippe Morando (P)

Aix Marseille Université, CNRS, UMR 7051, INP, Inst Neurophysiopathol, Marseille, France.

Nathalie Baeza-Kallee (N)

Aix Marseille Université, CNRS, UMR 7051, INP, Inst Neurophysiopathol, Marseille, France.

Carole Colin (C)

Aix Marseille Université, CNRS, UMR 7051, INP, Inst Neurophysiopathol, Marseille, France.

Olivier Chinot (O)

Aix-Marseille University, Assistance Publique-Hopitaux de Marseille, Centre Hospitalo-Universitaire Timone, Service de Neuro-Oncologie, Marseille, France.

Diane Braguer (D)

Aix Marseille Université, CNRS, UMR 7051, INP, Inst Neurophysiopathol, Marseille, France.

Xavier Morelli (X)

Aix Marseille Université, Centre National de la Recherche Scientifique (CNRS), Institut National de la Santé et de la Recherche Médicale (INSERM), Institut Paoli Calmettes, Centre de Recherche en Cancérologie de Marseille (CRCM), Marseille, France.

Nicolas André (N)

Aix Marseille Université, Centre National de la Recherche Scientifique (CNRS), Institut National de la Santé et de la Recherche Médicale (INSERM), Institut Paoli Calmettes, Centre de Recherche en Cancérologie de Marseille (CRCM), Marseille, France; Pediatric Oncology and Hematology Department, Hôpital pour Enfant de La Timone, AP-HM, Marseille, France; Metronomics Global Health Initiative, Marseille 13385, France.

Manon Carré (M)

Aix Marseille Université, Centre National de la Recherche Scientifique (CNRS), Institut National de la Santé et de la Recherche Médicale (INSERM), Institut Paoli Calmettes, Centre de Recherche en Cancérologie de Marseille (CRCM), Marseille, France.

Emeline Tabouret (E)

Aix Marseille Université, CNRS, UMR 7051, INP, Inst Neurophysiopathol, Marseille, France; Aix-Marseille University, Assistance Publique-Hopitaux de Marseille, Centre Hospitalo-Universitaire Timone, Service de Neuro-Oncologie, Marseille, France.

Dominique Figarella-Branger (D)

Aix Marseille Université, CNRS, UMR 7051, INP, Inst Neurophysiopathol, Marseille, France.

Marion Le Grand (M)

Aix Marseille Université, Centre National de la Recherche Scientifique (CNRS), Institut National de la Santé et de la Recherche Médicale (INSERM), Institut Paoli Calmettes, Centre de Recherche en Cancérologie de Marseille (CRCM), Marseille, France. Electronic address: marion.le-grand@inserm.fr.

Eddy Pasquier (E)

Aix Marseille Université, Centre National de la Recherche Scientifique (CNRS), Institut National de la Santé et de la Recherche Médicale (INSERM), Institut Paoli Calmettes, Centre de Recherche en Cancérologie de Marseille (CRCM), Marseille, France; Metronomics Global Health Initiative, Marseille 13385, France. Electronic address: eddy.pasquier@inserm.fr.

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Classifications MeSH