Inhibition of transcription by dactinomycin reveals a new characteristic of immunogenic cell stress

Abstract Chemotherapy still constitutes the standard of care for the treatment of most neoplastic diseases. Certain chemotherapeutics from the oncological armamentarium are able to trigger pre‐mortem stress signals that lead to immunogenic cell death (ICD), thus inducing an antitumor immune response...

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Main Authors: Juliette Humeau, Allan Sauvat, Giulia Cerrato, Wei Xie, Friedemann Loos, Francesca Iannantuoni, Lucillia Bezu, Sarah Lévesque, Juliette Paillet, Jonathan Pol, Marion Leduc, Laurence Zitvogel, Hugues de Thé, Oliver Kepp, Guido Kroemer
Format: Article
Language:English
Published: Springer Nature 2020-04-01
Series:EMBO Molecular Medicine
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Online Access:https://doi.org/10.15252/emmm.201911622
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author Juliette Humeau
Allan Sauvat
Giulia Cerrato
Wei Xie
Friedemann Loos
Francesca Iannantuoni
Lucillia Bezu
Sarah Lévesque
Juliette Paillet
Jonathan Pol
Marion Leduc
Laurence Zitvogel
Hugues de Thé
Oliver Kepp
Guido Kroemer
author_facet Juliette Humeau
Allan Sauvat
Giulia Cerrato
Wei Xie
Friedemann Loos
Francesca Iannantuoni
Lucillia Bezu
Sarah Lévesque
Juliette Paillet
Jonathan Pol
Marion Leduc
Laurence Zitvogel
Hugues de Thé
Oliver Kepp
Guido Kroemer
author_sort Juliette Humeau
collection DOAJ
description Abstract Chemotherapy still constitutes the standard of care for the treatment of most neoplastic diseases. Certain chemotherapeutics from the oncological armamentarium are able to trigger pre‐mortem stress signals that lead to immunogenic cell death (ICD), thus inducing an antitumor immune response and mediating long‐term tumor growth reduction. Here, we used an established model, built on artificial intelligence to identify, among a library of 50,000 compounds, anticancer agents that, based on their molecular descriptors, were predicted to induce ICD. This algorithm led us to the identification of dactinomycin (DACT, best known as actinomycin D), a highly potent cytotoxicant and ICD inducer that mediates immune‐dependent anticancer effects in vivo. Since DACT is commonly used as an inhibitor of DNA to RNA transcription, we investigated whether other experimentally established or algorithm‐selected, clinically employed ICD inducers would share this characteristic. As a common leitmotif, a panel of pharmacological ICD stimulators inhibited transcription and secondarily translation. These results establish the inhibition of RNA synthesis as an initial event for ICD induction.
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spelling doaj-art-9ac05f98dda3489daa122aa6f33d4ae12025-08-20T04:03:01ZengSpringer NatureEMBO Molecular Medicine1757-46761757-46842020-04-0112512210.15252/emmm.201911622Inhibition of transcription by dactinomycin reveals a new characteristic of immunogenic cell stressJuliette Humeau0Allan Sauvat1Giulia Cerrato2Wei Xie3Friedemann Loos4Francesca Iannantuoni5Lucillia Bezu6Sarah Lévesque7Juliette Paillet8Jonathan Pol9Marion Leduc10Laurence Zitvogel11Hugues de Thé12Oliver Kepp13Guido Kroemer14Equipe ItemNumberlisée par la Ligue contre le Cancer, Sorbonne Université, INSERM UMR1138, Centre de Recherche des Cordeliers, Université de ParisEquipe ItemNumberlisée par la Ligue contre le Cancer, Sorbonne Université, INSERM UMR1138, Centre de Recherche des Cordeliers, Université de ParisEquipe ItemNumberlisée par la Ligue contre le Cancer, Sorbonne Université, INSERM UMR1138, Centre de Recherche des Cordeliers, Université de ParisEquipe ItemNumberlisée par la Ligue contre le Cancer, Sorbonne Université, INSERM UMR1138, Centre de Recherche des Cordeliers, Université de ParisEquipe ItemNumberlisée par la Ligue contre le Cancer, Sorbonne Université, INSERM UMR1138, Centre de Recherche des Cordeliers, Université de ParisEquipe ItemNumberlisée par la Ligue contre le Cancer, Sorbonne Université, INSERM UMR1138, Centre de Recherche des Cordeliers, Université de ParisEquipe ItemNumberlisée par la Ligue contre le Cancer, Sorbonne Université, INSERM UMR1138, Centre de Recherche des Cordeliers, Université de ParisEquipe ItemNumberlisée par la Ligue contre le Cancer, Sorbonne Université, INSERM UMR1138, Centre de Recherche des Cordeliers, Université de ParisEquipe ItemNumberlisée par la Ligue contre le Cancer, Sorbonne Université, INSERM UMR1138, Centre de Recherche des Cordeliers, Université de ParisEquipe ItemNumberlisée par la Ligue contre le Cancer, Sorbonne Université, INSERM UMR1138, Centre de Recherche des Cordeliers, Université de ParisEquipe ItemNumberlisée par la Ligue contre le Cancer, Sorbonne Université, INSERM UMR1138, Centre de Recherche des Cordeliers, Université de ParisFaculty of Medicine Kremlin Bicêtre, Université Paris Sud, Paris SaclayCollege de France, INSERM UMR 1050, CNRS UMR 7241, PSL UniversityEquipe ItemNumberlisée par la Ligue contre le Cancer, Sorbonne Université, INSERM UMR1138, Centre de Recherche des Cordeliers, Université de ParisEquipe ItemNumberlisée par la Ligue contre le Cancer, Sorbonne Université, INSERM UMR1138, Centre de Recherche des Cordeliers, Université de ParisAbstract Chemotherapy still constitutes the standard of care for the treatment of most neoplastic diseases. Certain chemotherapeutics from the oncological armamentarium are able to trigger pre‐mortem stress signals that lead to immunogenic cell death (ICD), thus inducing an antitumor immune response and mediating long‐term tumor growth reduction. Here, we used an established model, built on artificial intelligence to identify, among a library of 50,000 compounds, anticancer agents that, based on their molecular descriptors, were predicted to induce ICD. This algorithm led us to the identification of dactinomycin (DACT, best known as actinomycin D), a highly potent cytotoxicant and ICD inducer that mediates immune‐dependent anticancer effects in vivo. Since DACT is commonly used as an inhibitor of DNA to RNA transcription, we investigated whether other experimentally established or algorithm‐selected, clinically employed ICD inducers would share this characteristic. As a common leitmotif, a panel of pharmacological ICD stimulators inhibited transcription and secondarily translation. These results establish the inhibition of RNA synthesis as an initial event for ICD induction.https://doi.org/10.15252/emmm.201911622dactinomycineIF2α phosphorylationimmunogenic cell deathtranscriptiontranslation
spellingShingle Juliette Humeau
Allan Sauvat
Giulia Cerrato
Wei Xie
Friedemann Loos
Francesca Iannantuoni
Lucillia Bezu
Sarah Lévesque
Juliette Paillet
Jonathan Pol
Marion Leduc
Laurence Zitvogel
Hugues de Thé
Oliver Kepp
Guido Kroemer
Inhibition of transcription by dactinomycin reveals a new characteristic of immunogenic cell stress
EMBO Molecular Medicine
dactinomycin
eIF2α phosphorylation
immunogenic cell death
transcription
translation
title Inhibition of transcription by dactinomycin reveals a new characteristic of immunogenic cell stress
title_full Inhibition of transcription by dactinomycin reveals a new characteristic of immunogenic cell stress
title_fullStr Inhibition of transcription by dactinomycin reveals a new characteristic of immunogenic cell stress
title_full_unstemmed Inhibition of transcription by dactinomycin reveals a new characteristic of immunogenic cell stress
title_short Inhibition of transcription by dactinomycin reveals a new characteristic of immunogenic cell stress
title_sort inhibition of transcription by dactinomycin reveals a new characteristic of immunogenic cell stress
topic dactinomycin
eIF2α phosphorylation
immunogenic cell death
transcription
translation
url https://doi.org/10.15252/emmm.201911622
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