Interferon regulates neural stem cell function at all ages by orchestrating mTOR and cell cycle

Abstract Stem cells show intrinsic interferon signalling, which protects them from viral infections at all ages. In the ageing brain, interferon signalling also reduces the ability of stem cells to activate. Whether these functions are linked and at what time interferons start taking on a role in st...

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Main Authors: Damian Carvajal Ibañez, Maxim Skabkin, Jooa Hooli, Santiago Cerrizuela, Manuel Göpferich, Adrien Jolly, Katrin Volk, Marc Zumwinkel, Matilde Bertolini, Gianluca Figlia, Thomas Höfer, Guenter Kramer, Simon Anders, Aurelio A Teleman, Anna Marciniak‐Czochra, Ana Martin‐Villalba
Format: Article
Language:English
Published: Springer Nature 2023-01-01
Series:EMBO Molecular Medicine
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Online Access:https://doi.org/10.15252/emmm.202216434
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author Damian Carvajal Ibañez
Maxim Skabkin
Jooa Hooli
Santiago Cerrizuela
Manuel Göpferich
Adrien Jolly
Katrin Volk
Marc Zumwinkel
Matilde Bertolini
Gianluca Figlia
Thomas Höfer
Guenter Kramer
Simon Anders
Aurelio A Teleman
Anna Marciniak‐Czochra
Ana Martin‐Villalba
author_facet Damian Carvajal Ibañez
Maxim Skabkin
Jooa Hooli
Santiago Cerrizuela
Manuel Göpferich
Adrien Jolly
Katrin Volk
Marc Zumwinkel
Matilde Bertolini
Gianluca Figlia
Thomas Höfer
Guenter Kramer
Simon Anders
Aurelio A Teleman
Anna Marciniak‐Czochra
Ana Martin‐Villalba
author_sort Damian Carvajal Ibañez
collection DOAJ
description Abstract Stem cells show intrinsic interferon signalling, which protects them from viral infections at all ages. In the ageing brain, interferon signalling also reduces the ability of stem cells to activate. Whether these functions are linked and at what time interferons start taking on a role in stem cell functioning is unknown. Additionally, the molecular link between interferons and activation in neural stem cells and how this relates to progenitor production is not well understood. Here we combine single‐cell transcriptomics, RiboSeq and mathematical models of interferon to show that this pathway is important for proper stem cell function at all ages in mice. Interferon orchestrates cell cycle and mTOR activity to post‐transcriptionally repress Sox2 and induces quiescence. The interferon response then decreases in the subsequent maturation states. Mathematical simulations indicate that this regulation is beneficial for the young and harmful for the old brain. Our study establishes molecular mechanisms of interferon in stem cells and interferons as genuine regulators of stem cell homeostasis and a potential therapeutic target to repair the ageing brain.
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institution Kabale University
issn 1757-4676
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language English
publishDate 2023-01-01
publisher Springer Nature
record_format Article
series EMBO Molecular Medicine
spelling doaj-art-c039cae925bd4fe8acd4f4d3519e3e362025-08-20T03:46:28ZengSpringer NatureEMBO Molecular Medicine1757-46761757-46842023-01-0115411810.15252/emmm.202216434Interferon regulates neural stem cell function at all ages by orchestrating mTOR and cell cycleDamian Carvajal Ibañez0Maxim Skabkin1Jooa Hooli2Santiago Cerrizuela3Manuel Göpferich4Adrien Jolly5Katrin Volk6Marc Zumwinkel7Matilde Bertolini8Gianluca Figlia9Thomas Höfer10Guenter Kramer11Simon Anders12Aurelio A Teleman13Anna Marciniak‐Czochra14Ana Martin‐Villalba15Division of Molecular Neurobiology, German Cancer Research Center (DKFZ)Division of Molecular Neurobiology, German Cancer Research Center (DKFZ)Division of Molecular Neurobiology, German Cancer Research Center (DKFZ)Division of Molecular Neurobiology, German Cancer Research Center (DKFZ)Division of Molecular Neurobiology, German Cancer Research Center (DKFZ)Division of Theoretical Systems Biology, German Cancer Research Center (DKFZ)Division of Molecular Neurobiology, German Cancer Research Center (DKFZ)Division of Molecular Neurobiology, German Cancer Research Center (DKFZ)Center for Molecular Biology of Heidelberg University (ZMBH) & German Cancer Research Center (DKFZ), DKFZ‐ZMBH AllianceFaculty of Biosciences, Heidelberg UniversityDivision of Theoretical Systems Biology, German Cancer Research Center (DKFZ)Center for Molecular Biology of Heidelberg University (ZMBH) & German Cancer Research Center (DKFZ), DKFZ‐ZMBH AllianceBioquant, Heidelberg UniversityDivision of Signal Transduction in Cancer and Metabolism, German Cancer Research Center (DKFZ)Institute of Applied Mathematics, Heidelberg UniversityDivision of Molecular Neurobiology, German Cancer Research Center (DKFZ)Abstract Stem cells show intrinsic interferon signalling, which protects them from viral infections at all ages. In the ageing brain, interferon signalling also reduces the ability of stem cells to activate. Whether these functions are linked and at what time interferons start taking on a role in stem cell functioning is unknown. Additionally, the molecular link between interferons and activation in neural stem cells and how this relates to progenitor production is not well understood. Here we combine single‐cell transcriptomics, RiboSeq and mathematical models of interferon to show that this pathway is important for proper stem cell function at all ages in mice. Interferon orchestrates cell cycle and mTOR activity to post‐transcriptionally repress Sox2 and induces quiescence. The interferon response then decreases in the subsequent maturation states. Mathematical simulations indicate that this regulation is beneficial for the young and harmful for the old brain. Our study establishes molecular mechanisms of interferon in stem cells and interferons as genuine regulators of stem cell homeostasis and a potential therapeutic target to repair the ageing brain.https://doi.org/10.15252/emmm.202216434ageingdormancyinterferonmTORstem cells
spellingShingle Damian Carvajal Ibañez
Maxim Skabkin
Jooa Hooli
Santiago Cerrizuela
Manuel Göpferich
Adrien Jolly
Katrin Volk
Marc Zumwinkel
Matilde Bertolini
Gianluca Figlia
Thomas Höfer
Guenter Kramer
Simon Anders
Aurelio A Teleman
Anna Marciniak‐Czochra
Ana Martin‐Villalba
Interferon regulates neural stem cell function at all ages by orchestrating mTOR and cell cycle
EMBO Molecular Medicine
ageing
dormancy
interferon
mTOR
stem cells
title Interferon regulates neural stem cell function at all ages by orchestrating mTOR and cell cycle
title_full Interferon regulates neural stem cell function at all ages by orchestrating mTOR and cell cycle
title_fullStr Interferon regulates neural stem cell function at all ages by orchestrating mTOR and cell cycle
title_full_unstemmed Interferon regulates neural stem cell function at all ages by orchestrating mTOR and cell cycle
title_short Interferon regulates neural stem cell function at all ages by orchestrating mTOR and cell cycle
title_sort interferon regulates neural stem cell function at all ages by orchestrating mtor and cell cycle
topic ageing
dormancy
interferon
mTOR
stem cells
url https://doi.org/10.15252/emmm.202216434
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