HDAC1 fine-tunes Th17 polarization in vivo to restrain tissue damage in fungal infections

Summary: Histone deacetylases (HDACs) contribute to shaping many aspects of T cell lineage functions in anti-infective surveillance; however, their role in fungus-specific immune responses remains poorly understood. Using a T cell-specific deletion of HDAC1, we uncover its critical role in limiting...

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Main Authors: Philipp Penninger, Helena Brezovec, Irina Tsymala, Magdalena Teufl, Trinh Phan-Canh, Tamires Bitencourt, Marie Brinkmann, Walter Glaser, Wilfried Ellmeier, Michael Bonelli, Karl Kuchler
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:Cell Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S2211124724013445
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author Philipp Penninger
Helena Brezovec
Irina Tsymala
Magdalena Teufl
Trinh Phan-Canh
Tamires Bitencourt
Marie Brinkmann
Walter Glaser
Wilfried Ellmeier
Michael Bonelli
Karl Kuchler
author_facet Philipp Penninger
Helena Brezovec
Irina Tsymala
Magdalena Teufl
Trinh Phan-Canh
Tamires Bitencourt
Marie Brinkmann
Walter Glaser
Wilfried Ellmeier
Michael Bonelli
Karl Kuchler
author_sort Philipp Penninger
collection DOAJ
description Summary: Histone deacetylases (HDACs) contribute to shaping many aspects of T cell lineage functions in anti-infective surveillance; however, their role in fungus-specific immune responses remains poorly understood. Using a T cell-specific deletion of HDAC1, we uncover its critical role in limiting polarization toward Th17 by restricting expression of the cytokine receptors gp130 and transforming growth factor β receptor 2 (TGF-βRII) in a fungus-specific manner, thus limiting Stat3 and Smad2/3 signaling. Controlled release of interleukin-17A (IL-17A) and granulocyte-macrophage colony-stimulating factor (GM-CSF) is vital to minimize apoptotic processes in renal tubular epithelial cells in vitro and in vivo. Consequently, animals harboring excess Th17-polarized HDCA1-deficient CD4+ T cells develop increased kidney pathology upon invasive Candida albicans infection. Importantly, pharmacological inhibition of class I HDACs similarly increased IL-17A release by both mouse and human CD4+ T cells. Collectively, this work shows that HDAC1 controls T cell polarization, thus playing a critical role in the antifungal immune defense and infection outcomes.
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spelling doaj-art-f28f3f111aae4ea7a61d8ea5f2b710a62025-08-20T02:22:34ZengElsevierCell Reports2211-12472024-12-01431211499310.1016/j.celrep.2024.114993HDAC1 fine-tunes Th17 polarization in vivo to restrain tissue damage in fungal infectionsPhilipp Penninger0Helena Brezovec1Irina Tsymala2Magdalena Teufl3Trinh Phan-Canh4Tamires Bitencourt5Marie Brinkmann6Walter Glaser7Wilfried Ellmeier8Michael Bonelli9Karl Kuchler10Max Perutz Labs, Vienna BioCenter Campus (VBC), Dr.-Bohr-Gasse 9, 1030, Vienna, Austria; Medical University of Vienna, Center for Medical Biochemistry, Dr.-Bohr-Gasse 9, 1030, Vienna, AustriaMax Perutz Labs, Vienna BioCenter Campus (VBC), Dr.-Bohr-Gasse 9, 1030, Vienna, Austria; Medical University of Vienna, Center for Medical Biochemistry, Dr.-Bohr-Gasse 9, 1030, Vienna, AustriaMax Perutz Labs, Vienna BioCenter Campus (VBC), Dr.-Bohr-Gasse 9, 1030, Vienna, Austria; Medical University of Vienna, Center for Medical Biochemistry, Dr.-Bohr-Gasse 9, 1030, Vienna, AustriaMax Perutz Labs, Vienna BioCenter Campus (VBC), Dr.-Bohr-Gasse 9, 1030, Vienna, Austria; Medical University of Vienna, Center for Medical Biochemistry, Dr.-Bohr-Gasse 9, 1030, Vienna, AustriaMax Perutz Labs, Vienna BioCenter Campus (VBC), Dr.-Bohr-Gasse 9, 1030, Vienna, Austria; Medical University of Vienna, Center for Medical Biochemistry, Dr.-Bohr-Gasse 9, 1030, Vienna, AustriaMax Perutz Labs, Vienna BioCenter Campus (VBC), Dr.-Bohr-Gasse 9, 1030, Vienna, Austria; CCRI – St. Anna Children's Cancer Research Institute, Vienna, AustriaMedical University of Vienna, Division of Rheumatology, Department of Internal Medicine III, 1090 Vienna, AustriaMax Perutz Labs, Vienna BioCenter Campus (VBC), Dr.-Bohr-Gasse 9, 1030, Vienna, Austria; Medical University of Vienna, Center for Medical Biochemistry, Dr.-Bohr-Gasse 9, 1030, Vienna, AustriaMedical University of Vienna, Center for Pathophysiology, Infectiology and Immunology, Institute of Immunology, 1090 Vienna, AustriaMedical University of Vienna, Division of Rheumatology, Department of Internal Medicine III, 1090 Vienna, AustriaMax Perutz Labs, Vienna BioCenter Campus (VBC), Dr.-Bohr-Gasse 9, 1030, Vienna, Austria; Medical University of Vienna, Center for Medical Biochemistry, Dr.-Bohr-Gasse 9, 1030, Vienna, Austria; Corresponding authorSummary: Histone deacetylases (HDACs) contribute to shaping many aspects of T cell lineage functions in anti-infective surveillance; however, their role in fungus-specific immune responses remains poorly understood. Using a T cell-specific deletion of HDAC1, we uncover its critical role in limiting polarization toward Th17 by restricting expression of the cytokine receptors gp130 and transforming growth factor β receptor 2 (TGF-βRII) in a fungus-specific manner, thus limiting Stat3 and Smad2/3 signaling. Controlled release of interleukin-17A (IL-17A) and granulocyte-macrophage colony-stimulating factor (GM-CSF) is vital to minimize apoptotic processes in renal tubular epithelial cells in vitro and in vivo. Consequently, animals harboring excess Th17-polarized HDCA1-deficient CD4+ T cells develop increased kidney pathology upon invasive Candida albicans infection. Importantly, pharmacological inhibition of class I HDACs similarly increased IL-17A release by both mouse and human CD4+ T cells. Collectively, this work shows that HDAC1 controls T cell polarization, thus playing a critical role in the antifungal immune defense and infection outcomes.http://www.sciencedirect.com/science/article/pii/S2211124724013445CP: Immunology
spellingShingle Philipp Penninger
Helena Brezovec
Irina Tsymala
Magdalena Teufl
Trinh Phan-Canh
Tamires Bitencourt
Marie Brinkmann
Walter Glaser
Wilfried Ellmeier
Michael Bonelli
Karl Kuchler
HDAC1 fine-tunes Th17 polarization in vivo to restrain tissue damage in fungal infections
Cell Reports
CP: Immunology
title HDAC1 fine-tunes Th17 polarization in vivo to restrain tissue damage in fungal infections
title_full HDAC1 fine-tunes Th17 polarization in vivo to restrain tissue damage in fungal infections
title_fullStr HDAC1 fine-tunes Th17 polarization in vivo to restrain tissue damage in fungal infections
title_full_unstemmed HDAC1 fine-tunes Th17 polarization in vivo to restrain tissue damage in fungal infections
title_short HDAC1 fine-tunes Th17 polarization in vivo to restrain tissue damage in fungal infections
title_sort hdac1 fine tunes th17 polarization in vivo to restrain tissue damage in fungal infections
topic CP: Immunology
url http://www.sciencedirect.com/science/article/pii/S2211124724013445
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