Gene expression and molecular pathway analyses differentiate immunotherapy-induced myositis from spontaneous dermatomyositis

Abstract Immune checkpoint inhibitor therapy (ICI)-induced myositis (irMyositis) occurs in about 1% of patients treated with anti-PD1 or anti-CTLA-4 antibodies and can be debilitating or even fatal. We compared gene expression profiles from skeletal muscle biopsies between irMyositis patients, patie...

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Main Authors: Magdalena Röckel, Luca Musella, Corinna Preusse, Josefine Radke, Lisa Zimmer, Kai-Martin Thoms, Florentia Dimitriou, Matthias Endres, Wolfgang Böhmerle, Waltraud Fröhlich, Sami Tayb-Boulahfa, Sarah Leonard-Louis, Yves Allenbach, Carola Berking, Werner Stenzel, Samuel Knauss, Julio Vera, Lucie Heinzerling
Format: Article
Language:English
Published: Nature Portfolio 2025-08-01
Series:Scientific Reports
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Online Access:https://doi.org/10.1038/s41598-025-11944-5
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author Magdalena Röckel
Luca Musella
Corinna Preusse
Josefine Radke
Lisa Zimmer
Kai-Martin Thoms
Florentia Dimitriou
Matthias Endres
Wolfgang Böhmerle
Waltraud Fröhlich
Sami Tayb-Boulahfa
Sarah Leonard-Louis
Yves Allenbach
Carola Berking
Werner Stenzel
Samuel Knauss
Julio Vera
Lucie Heinzerling
author_facet Magdalena Röckel
Luca Musella
Corinna Preusse
Josefine Radke
Lisa Zimmer
Kai-Martin Thoms
Florentia Dimitriou
Matthias Endres
Wolfgang Böhmerle
Waltraud Fröhlich
Sami Tayb-Boulahfa
Sarah Leonard-Louis
Yves Allenbach
Carola Berking
Werner Stenzel
Samuel Knauss
Julio Vera
Lucie Heinzerling
author_sort Magdalena Röckel
collection DOAJ
description Abstract Immune checkpoint inhibitor therapy (ICI)-induced myositis (irMyositis) occurs in about 1% of patients treated with anti-PD1 or anti-CTLA-4 antibodies and can be debilitating or even fatal. We compared gene expression profiles from skeletal muscle biopsies between irMyositis patients, patients with spontaneous dermatomyositis (DM, comprising anti-Mi2-positive and anti-TIF1-γ-positive subtypes), and non-diseased controls (NDC). We used the NanoString nCounter PanCancer Immune Profiling Panel to perform differential gene expression (DGE) and pathway enrichment analyses. We identified 93 differentially expressed genes (DEGs) across conditions. Gene set enrichment analysis (GSEA) suggested activation of interferon gamma (type-II IFN) and interferon alpha/beta (type-I IFN) signaling in irMyositis and DM, respectively. For instance, type-II IFN was upregulated exclusively in irMyositis when compared to DM, which conversely showed upregulation of effector genes downstream type-I IFN. The observed fold-change of a subset of 33 genes drove the GSEA. We further characterized the DEGs using network interaction and expression correlation analyses. This allowed us to describe potential differences between regulatory hubs and cells involved in irMyositis susceptible to ICI effects. For example, the downregulation of FOXP3 we observed together with the upregulation of the chemokine CCL14 in irMyositis may have been a consequence of T cell activation upon ICI therapy. The gene expression correlation and putative molecular interactions set irMyositis apart from DM, particularly with respect to IFN response and DGE of interactors of ICI protein targets (CTLA4, PD-1, PD-L1). Our results suggest new avenues for understanding immunotherapy-related adverse events.
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spelling doaj-art-43feb3b5afa24ad99f2a613fb4fd99c82025-08-20T04:02:45ZengNature PortfolioScientific Reports2045-23222025-08-0115111710.1038/s41598-025-11944-5Gene expression and molecular pathway analyses differentiate immunotherapy-induced myositis from spontaneous dermatomyositisMagdalena Röckel0Luca Musella1Corinna Preusse2Josefine Radke3Lisa Zimmer4Kai-Martin Thoms5Florentia Dimitriou6Matthias Endres7Wolfgang Böhmerle8Waltraud Fröhlich9Sami Tayb-Boulahfa10Sarah Leonard-Louis11Yves Allenbach12Carola Berking13Werner Stenzel14Samuel Knauss15Julio Vera16Lucie Heinzerling17Department of Dermatology, Uniklinikum ErlangenDepartment of Dermatology, Uniklinikum ErlangenCharité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Department of NeuropathologyCharité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Department of NeuropathologyDepartment of Dermatology, Venerology and Allergology, Universitätsklinikum EssenUniversity Medical Center GoettingenDepartment of Dermatology, University Hospital ZürichCharité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Department of NeurologyCharité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Department of NeurologyDepartment of Dermatology, Uniklinikum ErlangenDepartment of Internal Medicine and Clinical Immunology, Pitié-Salpêtrière University HospitalDepartment of Neuropathology, Sorbonne University ParisDepartment of Internal Medicine and Clinical Immunology, Pitié-Salpêtrière University HospitalDepartment of Dermatology, Uniklinikum ErlangenCharité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Department of NeuropathologyCharité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Department of NeurologyDepartment of Dermatology, Uniklinikum ErlangenDepartment of Dermatology, Uniklinikum ErlangenAbstract Immune checkpoint inhibitor therapy (ICI)-induced myositis (irMyositis) occurs in about 1% of patients treated with anti-PD1 or anti-CTLA-4 antibodies and can be debilitating or even fatal. We compared gene expression profiles from skeletal muscle biopsies between irMyositis patients, patients with spontaneous dermatomyositis (DM, comprising anti-Mi2-positive and anti-TIF1-γ-positive subtypes), and non-diseased controls (NDC). We used the NanoString nCounter PanCancer Immune Profiling Panel to perform differential gene expression (DGE) and pathway enrichment analyses. We identified 93 differentially expressed genes (DEGs) across conditions. Gene set enrichment analysis (GSEA) suggested activation of interferon gamma (type-II IFN) and interferon alpha/beta (type-I IFN) signaling in irMyositis and DM, respectively. For instance, type-II IFN was upregulated exclusively in irMyositis when compared to DM, which conversely showed upregulation of effector genes downstream type-I IFN. The observed fold-change of a subset of 33 genes drove the GSEA. We further characterized the DEGs using network interaction and expression correlation analyses. This allowed us to describe potential differences between regulatory hubs and cells involved in irMyositis susceptible to ICI effects. For example, the downregulation of FOXP3 we observed together with the upregulation of the chemokine CCL14 in irMyositis may have been a consequence of T cell activation upon ICI therapy. The gene expression correlation and putative molecular interactions set irMyositis apart from DM, particularly with respect to IFN response and DGE of interactors of ICI protein targets (CTLA4, PD-1, PD-L1). Our results suggest new avenues for understanding immunotherapy-related adverse events.https://doi.org/10.1038/s41598-025-11944-5Gene expression profilesImmune Related adverse eventsImmune checkpoint inhibitor therapyMyositisAnti-PD1/PD L1Anti-CTLA-4
spellingShingle Magdalena Röckel
Luca Musella
Corinna Preusse
Josefine Radke
Lisa Zimmer
Kai-Martin Thoms
Florentia Dimitriou
Matthias Endres
Wolfgang Böhmerle
Waltraud Fröhlich
Sami Tayb-Boulahfa
Sarah Leonard-Louis
Yves Allenbach
Carola Berking
Werner Stenzel
Samuel Knauss
Julio Vera
Lucie Heinzerling
Gene expression and molecular pathway analyses differentiate immunotherapy-induced myositis from spontaneous dermatomyositis
Scientific Reports
Gene expression profiles
Immune Related adverse events
Immune checkpoint inhibitor therapy
Myositis
Anti-PD1/PD L1
Anti-CTLA-4
title Gene expression and molecular pathway analyses differentiate immunotherapy-induced myositis from spontaneous dermatomyositis
title_full Gene expression and molecular pathway analyses differentiate immunotherapy-induced myositis from spontaneous dermatomyositis
title_fullStr Gene expression and molecular pathway analyses differentiate immunotherapy-induced myositis from spontaneous dermatomyositis
title_full_unstemmed Gene expression and molecular pathway analyses differentiate immunotherapy-induced myositis from spontaneous dermatomyositis
title_short Gene expression and molecular pathway analyses differentiate immunotherapy-induced myositis from spontaneous dermatomyositis
title_sort gene expression and molecular pathway analyses differentiate immunotherapy induced myositis from spontaneous dermatomyositis
topic Gene expression profiles
Immune Related adverse events
Immune checkpoint inhibitor therapy
Myositis
Anti-PD1/PD L1
Anti-CTLA-4
url https://doi.org/10.1038/s41598-025-11944-5
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