Beta-blockers disrupt mitochondrial bioenergetics and increase radiotherapy efficacy independently of beta-adrenergic receptors in medulloblastoma.


Journal

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

Informations de publication

Date de publication:
Aug 2022
Historique:
received: 21 01 2022
revised: 20 06 2022
accepted: 22 06 2022
pubmed: 12 7 2022
medline: 17 8 2022
entrez: 11 7 2022
Statut: ppublish

Résumé

Medulloblastoma is the most frequent brain malignancy of childhood. The current multimodal treatment comes at the expense of serious and often long-lasting side effects. Drug repurposing is a strategy to fast-track anti-cancer therapy with low toxicity. Here, we showed the ability of β-blockers to potentiate radiotherapy in medulloblastoma with bad prognosis. Medulloblastoma cell lines, patient-derived xenograft cells, 3D spheroids and an innovative cerebellar organotypic model were used to identify synergistic interactions between β-blockers and ionising radiations. Gene expression profiles of β-adrenergic receptors were analysed in medulloblastoma samples from 240 patients. Signaling pathways were explored by RT-qPCR, RNA interference, western blotting and RNA sequencing. Medulloblastoma cell bioenergetics were evaluated by measuring the oxygen consumption rate, the extracellular acidification rate and superoxide production. Low concentrations of β-blockers significantly potentiated clinically relevant radiation protocols. Although patient biopsies showed detectable expression of β-adrenergic receptors, the ability of the repurposed drugs to potentiate ionising radiations did not result from the inhibition of the canonical signaling pathway. We highlighted that the efficacy of the combinatorial treatment relied on a metabolic catastrophe that deprives medulloblastoma cells of their adaptive bioenergetics capacities. This led to an overproduction of superoxide radicals and ultimately to an increase in ionising radiations-mediated DNA damages. These data provide the evidence of the efficacy of β-blockers as potentiators of radiotherapy in medulloblastoma, which may help improve the treatment and quality of life of children with high-risk brain tumours. This study was funded by institutional grants and charities.

Sections du résumé

BACKGROUND BACKGROUND
Medulloblastoma is the most frequent brain malignancy of childhood. The current multimodal treatment comes at the expense of serious and often long-lasting side effects. Drug repurposing is a strategy to fast-track anti-cancer therapy with low toxicity. Here, we showed the ability of β-blockers to potentiate radiotherapy in medulloblastoma with bad prognosis.
METHODS METHODS
Medulloblastoma cell lines, patient-derived xenograft cells, 3D spheroids and an innovative cerebellar organotypic model were used to identify synergistic interactions between β-blockers and ionising radiations. Gene expression profiles of β-adrenergic receptors were analysed in medulloblastoma samples from 240 patients. Signaling pathways were explored by RT-qPCR, RNA interference, western blotting and RNA sequencing. Medulloblastoma cell bioenergetics were evaluated by measuring the oxygen consumption rate, the extracellular acidification rate and superoxide production.
FINDINGS RESULTS
Low concentrations of β-blockers significantly potentiated clinically relevant radiation protocols. Although patient biopsies showed detectable expression of β-adrenergic receptors, the ability of the repurposed drugs to potentiate ionising radiations did not result from the inhibition of the canonical signaling pathway. We highlighted that the efficacy of the combinatorial treatment relied on a metabolic catastrophe that deprives medulloblastoma cells of their adaptive bioenergetics capacities. This led to an overproduction of superoxide radicals and ultimately to an increase in ionising radiations-mediated DNA damages.
INTERPRETATION CONCLUSIONS
These data provide the evidence of the efficacy of β-blockers as potentiators of radiotherapy in medulloblastoma, which may help improve the treatment and quality of life of children with high-risk brain tumours.
FUNDING BACKGROUND
This study was funded by institutional grants and charities.

Identifiants

pubmed: 35816899
pii: S2352-3964(22)00330-9
doi: 10.1016/j.ebiom.2022.104149
pmc: PMC9283511
pii:
doi:

Substances chimiques

Receptors, Adrenergic, beta 0
Superoxides 11062-77-4

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

104149

Informations de copyright

Copyright © 2022 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

Maïlys Rossi (M)

Centre de Recherche en Cancérologie de Marseille (CRCM), Aix-Marseille Université, CNRS, Inserm, Institut Paoli Calmettes, Marseille, France.

Julie Talbot (J)

Institut Curie, Inserm, CNRS, Université Paris-Saclay, Orsay, France.

Patricia Piris (P)

Centre de Recherche en Cancérologie de Marseille (CRCM), Aix-Marseille Université, CNRS, Inserm, Institut Paoli Calmettes, Marseille, France.

Marion Le Grand (ML)

Centre de Recherche en Cancérologie de Marseille (CRCM), Aix-Marseille Université, CNRS, Inserm, Institut Paoli Calmettes, Marseille, France.

Marie-Pierre Montero (MP)

Centre de Recherche en Cancérologie de Marseille (CRCM), Aix-Marseille Université, CNRS, Inserm, Institut Paoli Calmettes, Marseille, France.

Mélanie Matteudi (M)

Centre de Recherche en Cancérologie de Marseille (CRCM), Aix-Marseille Université, CNRS, Inserm, Institut Paoli Calmettes, Marseille, France.

Emilie Agavnian-Couquiaud (E)

Plateforme ICEP (CRCM), Aix-Marseille Université, CNRS, Inserm, Institut Paoli Calmettes, Marseille, France.

Romain Appay (R)

Service d'anatomie pathologique et de neuropathologie, Hôpital de la Timone, Assistance Publique-Hôpitaux de Marseille (APHM), Marseille, France.

Céline Keime (C)

Plateforme GenomEast, Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), CNRS, Inserm, Université de Strasbourg, Illkirch-Graffenstaden, France.

Daniel Williamson (D)

Wolfson Childhood Cancer Research Centre, Newcastle University Centre for Cancer, Newcastle upon Tyne, United Kingdom.

Duje Buric (D)

Institut Méditerranéen de Biodiversité et d'Écologie marine et continentale (IMBE), Aix-Marseille Université, CNRS, IRD, Avignon Université, Marseille, France.

Véronique Bourgarel (V)

Centre de Recherche en Cancérologie de Marseille (CRCM), Aix-Marseille Université, CNRS, Inserm, Institut Paoli Calmettes, Marseille, France.

Laetitia Padovani (L)

Service de Radiothérapie, Timone Hospital, Assistance Publique-Hopitaux de Marseille (AP-HM), Marseille, France.

Steven C Clifford (SC)

Wolfson Childhood Cancer Research Centre, Newcastle University Centre for Cancer, Newcastle upon Tyne, United Kingdom.

Olivier Ayrault (O)

Institut Curie, Inserm, CNRS, Université Paris-Saclay, Orsay, France.

Eddy Pasquier (E)

Centre de Recherche en Cancérologie de Marseille (CRCM), Aix-Marseille Université, CNRS, Inserm, Institut Paoli Calmettes, Marseille, France; Metronomics Global Health Initiative, Marseille, France.

Nicolas André (N)

Centre de Recherche en Cancérologie de Marseille (CRCM), Aix-Marseille Université, CNRS, Inserm, Institut Paoli Calmettes, Marseille, France; Metronomics Global Health Initiative, Marseille, France; Service d'Hématologie & Oncologie Pédiatrique, Timone Hospital, AP-HM, Marseille, France. Electronic address: nicolas.andre@ap-hm.fr.

Manon Carré (M)

Centre de Recherche en Cancérologie de Marseille (CRCM), Aix-Marseille Université, CNRS, Inserm, Institut Paoli Calmettes, Marseille, France. Electronic address: manon.carre@univ-amu.fr.

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