Differential transcriptome response to proton versus X-ray radiation reveals novel candidate targets for combinatorial PT therapy in lymphoma.

Lymphoma PPARgamma Proton therapy Radiobiology Radiotherapy Transcriptome

Journal

Radiotherapy and oncology : journal of the European Society for Therapeutic Radiology and Oncology
ISSN: 1879-0887
Titre abrégé: Radiother Oncol
Pays: Ireland
ID NLM: 8407192

Informations de publication

Date de publication:
02 2021
Historique:
received: 15 01 2020
revised: 09 10 2020
accepted: 15 10 2020
pubmed: 24 10 2020
medline: 24 4 2021
entrez: 23 10 2020
Statut: ppublish

Résumé

Knowledge of biological responses to proton therapy (PT) in comparison to X-ray remains in its infancy. Identification of PT specific molecular signals is an important opportunity for the discovery of biomarkers and synergistic drugs to advance clinical application. Since PT is used for the treatment of lymphoma, we report here transcriptomic responses of lymphoma cell lines to PT vs X-ray and identify potential therapeutic targets. Two lymphoma cell lines of human (BL41) and murine (J3D) origin were irradiated by X-ray and PT. Differential transcriptome regulation was quantified by RNA sequencing for each radiation type at 12 hours post irradiation. Gene-set enrichment analysis revealed deregulated molecular pathways and putative targets for lymphoma cell sensitization to PT. Transcriptomic gene set enrichment analyses uncovered pathways that contribute to the unfolded protein response (UPR) and mitochondrial transport. Functional validation at multiple time points demonstrated increased UPR activation and decreased protein translation, perhaps due to increased oxidative stress and oxidative protein damage after PT. PPARgamma was identified as a potential regulator of the PT transcriptomic response. Inhibition of PPARgamma by two compounds, T0070907 and SR2595, sensitized lymphoma cells to PT. Proton vs X-ray radiation leads to the transcriptional regulation of a specific subset of genes in line with diminished protein translation and UPR activation that may be due to oxidative stress. This study demonstrates that different radiation qualities trigger distinct cellular responses in lymphoma cells, and identifies PPARgamma inhibition as a potential strategy for the sensitization of lymphoma to PT.

Sections du résumé

BACKGROUND AND PURPOSE
Knowledge of biological responses to proton therapy (PT) in comparison to X-ray remains in its infancy. Identification of PT specific molecular signals is an important opportunity for the discovery of biomarkers and synergistic drugs to advance clinical application. Since PT is used for the treatment of lymphoma, we report here transcriptomic responses of lymphoma cell lines to PT vs X-ray and identify potential therapeutic targets.
MATERIALS AND METHODS
Two lymphoma cell lines of human (BL41) and murine (J3D) origin were irradiated by X-ray and PT. Differential transcriptome regulation was quantified by RNA sequencing for each radiation type at 12 hours post irradiation. Gene-set enrichment analysis revealed deregulated molecular pathways and putative targets for lymphoma cell sensitization to PT.
RESULTS
Transcriptomic gene set enrichment analyses uncovered pathways that contribute to the unfolded protein response (UPR) and mitochondrial transport. Functional validation at multiple time points demonstrated increased UPR activation and decreased protein translation, perhaps due to increased oxidative stress and oxidative protein damage after PT. PPARgamma was identified as a potential regulator of the PT transcriptomic response. Inhibition of PPARgamma by two compounds, T0070907 and SR2595, sensitized lymphoma cells to PT.
CONCLUSIONS
Proton vs X-ray radiation leads to the transcriptional regulation of a specific subset of genes in line with diminished protein translation and UPR activation that may be due to oxidative stress. This study demonstrates that different radiation qualities trigger distinct cellular responses in lymphoma cells, and identifies PPARgamma inhibition as a potential strategy for the sensitization of lymphoma to PT.

Identifiants

pubmed: 33096164
pii: S0167-8140(20)30860-4
doi: 10.1016/j.radonc.2020.10.024
pii:
doi:

Substances chimiques

Protons 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

293-303

Informations de copyright

Copyright © 2020 The Authors. Published by Elsevier B.V. All rights reserved.

Auteurs

Mathieu Sertorio (M)

Division of Oncology, Cincinnati Children's Hospital Medical Center, Cincinnati, USA; Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, USA. Electronic address: Mathieu.Sertorio@cchmc.org.

Ali Nowrouzi (A)

Heidelberg Ion-Beam Therapy Center (HIT), Department of Radiation Oncology, Heidelberg University Hospital (UKHD), Germany; German Cancer Consortium (DKTK) Core Center, Clinical Cooperation Units (CCU) Translational Radiation Oncology and Radiation Oncology, National Center for Tumor Diseases (NCT), German Cancer Research Center (DKFZ), Heidelberg, Germany; Heidelberg Institute of Radiation Oncology (HIRO), National Center for Radiation Research in Oncology (NCRO), German Cancer Research Center (DKFZ) and Heidelberg University Hospital (UKHD), Germany; Division of Molecular and Translational Radiation Oncology, Heidelberg Medical Faculty (HDMF), Heidelberg University, Germany.

Mahdi Akbarpour (M)

Heidelberg Ion-Beam Therapy Center (HIT), Department of Radiation Oncology, Heidelberg University Hospital (UKHD), Germany; German Cancer Consortium (DKTK) Core Center, Clinical Cooperation Units (CCU) Translational Radiation Oncology and Radiation Oncology, National Center for Tumor Diseases (NCT), German Cancer Research Center (DKFZ), Heidelberg, Germany; Heidelberg Institute of Radiation Oncology (HIRO), National Center for Radiation Research in Oncology (NCRO), German Cancer Research Center (DKFZ) and Heidelberg University Hospital (UKHD), Germany; Division of Molecular and Translational Radiation Oncology, Heidelberg Medical Faculty (HDMF), Heidelberg University, Germany.

Kashish Chetal (K)

Division of Biomedical Informatics, Cincinnati Children's Hospital Medical Center, Cincinnati, USA.

Nathan Salomonis (N)

Division of Biomedical Informatics, Cincinnati Children's Hospital Medical Center, Cincinnati, USA; Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, USA.

Stephan Brons (S)

Heidelberg Institute of Radiation Oncology (HIRO), National Center for Radiation Research in Oncology (NCRO), German Cancer Research Center (DKFZ) and Heidelberg University Hospital (UKHD), Germany.

Anthony Mascia (A)

Department of Radiation Oncology, University of Cincinnati College of Medicine, USA.

Dan Ionascu (D)

Department of Radiation Oncology, University of Cincinnati College of Medicine, USA.

Shelby McCauley (S)

Division of Oncology, Cincinnati Children's Hospital Medical Center, Cincinnati, USA.

Taylor Kupneski (T)

Division of Oncology, Cincinnati Children's Hospital Medical Center, Cincinnati, USA.

Andreas Köthe (A)

Division of Oncology, Cincinnati Children's Hospital Medical Center, Cincinnati, USA.

Jürgen Debus (J)

Heidelberg Ion-Beam Therapy Center (HIT), Department of Radiation Oncology, Heidelberg University Hospital (UKHD), Germany; German Cancer Consortium (DKTK) Core Center, Clinical Cooperation Units (CCU) Translational Radiation Oncology and Radiation Oncology, National Center for Tumor Diseases (NCT), German Cancer Research Center (DKFZ), Heidelberg, Germany; Heidelberg Institute of Radiation Oncology (HIRO), National Center for Radiation Research in Oncology (NCRO), German Cancer Research Center (DKFZ) and Heidelberg University Hospital (UKHD), Germany; Division of Molecular and Translational Radiation Oncology, Heidelberg Medical Faculty (HDMF), Heidelberg University, Germany.

John P Perentesis (JP)

Division of Oncology, Cincinnati Children's Hospital Medical Center, Cincinnati, USA; Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, USA.

Amir Abdollahi (A)

Heidelberg Ion-Beam Therapy Center (HIT), Department of Radiation Oncology, Heidelberg University Hospital (UKHD), Germany; German Cancer Consortium (DKTK) Core Center, Clinical Cooperation Units (CCU) Translational Radiation Oncology and Radiation Oncology, National Center for Tumor Diseases (NCT), German Cancer Research Center (DKFZ), Heidelberg, Germany; Heidelberg Institute of Radiation Oncology (HIRO), National Center for Radiation Research in Oncology (NCRO), German Cancer Research Center (DKFZ) and Heidelberg University Hospital (UKHD), Germany; Division of Molecular and Translational Radiation Oncology, Heidelberg Medical Faculty (HDMF), Heidelberg University, Germany.

Yi Zheng (Y)

Division of Experimental Hematology, Cincinnati Children's Hospital Medical Center, Cincinnati, USA; Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, USA. Electronic address: Yi.Zheng@cchmc.org.

Susanne I Wells (SI)

Division of Oncology, Cincinnati Children's Hospital Medical Center, Cincinnati, USA; Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, USA. Electronic address: Susanne.Wells@cchmc.org.

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