Effects of microgravity on neural crest stem cells

Exposure to microgravity (μg) results in a range of systemic changes in the organism, but may also have beneficial cellular effects. In a previous study we detected increased proliferation capacity and upregulation of genes related to proliferation and survival in boundary cap neural crest stem cell...

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Main Authors: Yilin Han, Povilas Barasa, Lukas Zeger, Sara B. Salomonsson, Federica Zanotti, Marcel Egli, Barbara Zavan, Martina Trentini, Gunnar Florin, Alf Vaerneus, Håkan Aldskogius, Robert Fredriksson, Elena N. Kozlova
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-03-01
Series:Frontiers in Neuroscience
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Online Access:https://www.frontiersin.org/articles/10.3389/fnins.2024.1379076/full
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author Yilin Han
Povilas Barasa
Lukas Zeger
Sara B. Salomonsson
Federica Zanotti
Marcel Egli
Marcel Egli
Barbara Zavan
Martina Trentini
Gunnar Florin
Alf Vaerneus
Håkan Aldskogius
Robert Fredriksson
Elena N. Kozlova
author_facet Yilin Han
Povilas Barasa
Lukas Zeger
Sara B. Salomonsson
Federica Zanotti
Marcel Egli
Marcel Egli
Barbara Zavan
Martina Trentini
Gunnar Florin
Alf Vaerneus
Håkan Aldskogius
Robert Fredriksson
Elena N. Kozlova
author_sort Yilin Han
collection DOAJ
description Exposure to microgravity (μg) results in a range of systemic changes in the organism, but may also have beneficial cellular effects. In a previous study we detected increased proliferation capacity and upregulation of genes related to proliferation and survival in boundary cap neural crest stem cells (BC) after MASER14 sounding rocket flight compared to ground-based controls. However, whether these changes were due to μg or hypergravity was not clarified. In the current MASER15 experiment BCs were exposed simultaneously to μg and 1 g conditions provided by an onboard centrifuge. BCs exposed to μg displayed a markedly increased proliferation capacity compared to 1 g on board controls, and genetic analysis of BCs harvested 5 h after flight revealed an upregulation, specifically in μg-exposed BCs, of Zfp462 transcription factor, a key regulator of cell pluripotency and neuronal fate. This was associated with alterations in exosome microRNA content between μg and 1 g exposed MASER15 specimens. Since the specimens from MASER14 were obtained for analysis with 1 week’s delay, we examined whether gene expression and exosome content were different compared to the current MASER15 experiments, in which specimens were harvested 5 h after flight. The overall pattern of gene expression was different and Zfp462 expression was down-regulated in MASER14 BC μg compared to directly harvested specimens (MASER15). MicroRNA exosome content was markedly altered in medium harvested with delay compared to directly collected samples. In conclusion, our analysis indicates that even short exposure to μg alters gene expression, leading to increased BC capacity for proliferation and survival, lasting for a long time after μg exposure. With delayed harvest of specimens, a situation which may occur due to special post-flight circumstances, the exosome microRNA content is modified compared to fast specimen harvest, and the direct effects from μg exposure may be partially attenuated, whereas other effects can last for a long time after return to ground conditions.
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spelling doaj.art-29a260c75e7749388801e29b0260b6902024-04-10T13:15:27ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2024-03-011810.3389/fnins.2024.13790761379076Effects of microgravity on neural crest stem cellsYilin Han0Povilas Barasa1Lukas Zeger2Sara B. Salomonsson3Federica Zanotti4Marcel Egli5Marcel Egli6Barbara Zavan7Martina Trentini8Gunnar Florin9Alf Vaerneus10Håkan Aldskogius11Robert Fredriksson12Elena N. Kozlova13Department of Immunology, Genetics and Pathology, Uppsala University, Uppsala, SwedenInstitute of Biochemistry, Vilnius University, Vilnius, LithuaniaDepartment of Immunology, Genetics and Pathology, Uppsala University, Uppsala, SwedenDepartment of Pharmaceutical Bioscience, Uppsala University, Uppsala, SwedenDepartment of Translational Medicine, University of Ferrara, Ferrara, ItalySpace Biology Group, School of Engineering and Architecture, Institute of Medical Engineering, Lucerne University of Applied Sciences and Arts, Hergiswil, SwitzerlandNational Center for Biomedical Research in Space, Innovation Cluster Space and Aviation, University of Zurich, Zurich, SwitzerlandDepartment of Translational Medicine, University of Ferrara, Ferrara, ItalyDepartment of Translational Medicine, University of Ferrara, Ferrara, ItalySwedish Space Corporation, Solna, SwedenSwedish Space Corporation, Solna, SwedenDepartment of Immunology, Genetics and Pathology, Uppsala University, Uppsala, SwedenDepartment of Pharmaceutical Bioscience, Uppsala University, Uppsala, SwedenDepartment of Immunology, Genetics and Pathology, Uppsala University, Uppsala, SwedenExposure to microgravity (μg) results in a range of systemic changes in the organism, but may also have beneficial cellular effects. In a previous study we detected increased proliferation capacity and upregulation of genes related to proliferation and survival in boundary cap neural crest stem cells (BC) after MASER14 sounding rocket flight compared to ground-based controls. However, whether these changes were due to μg or hypergravity was not clarified. In the current MASER15 experiment BCs were exposed simultaneously to μg and 1 g conditions provided by an onboard centrifuge. BCs exposed to μg displayed a markedly increased proliferation capacity compared to 1 g on board controls, and genetic analysis of BCs harvested 5 h after flight revealed an upregulation, specifically in μg-exposed BCs, of Zfp462 transcription factor, a key regulator of cell pluripotency and neuronal fate. This was associated with alterations in exosome microRNA content between μg and 1 g exposed MASER15 specimens. Since the specimens from MASER14 were obtained for analysis with 1 week’s delay, we examined whether gene expression and exosome content were different compared to the current MASER15 experiments, in which specimens were harvested 5 h after flight. The overall pattern of gene expression was different and Zfp462 expression was down-regulated in MASER14 BC μg compared to directly harvested specimens (MASER15). MicroRNA exosome content was markedly altered in medium harvested with delay compared to directly collected samples. In conclusion, our analysis indicates that even short exposure to μg alters gene expression, leading to increased BC capacity for proliferation and survival, lasting for a long time after μg exposure. With delayed harvest of specimens, a situation which may occur due to special post-flight circumstances, the exosome microRNA content is modified compared to fast specimen harvest, and the direct effects from μg exposure may be partially attenuated, whereas other effects can last for a long time after return to ground conditions.https://www.frontiersin.org/articles/10.3389/fnins.2024.1379076/fullmicrogravityproliferationdelayed effectneural stem cellgene expressionexosomes
spellingShingle Yilin Han
Povilas Barasa
Lukas Zeger
Sara B. Salomonsson
Federica Zanotti
Marcel Egli
Marcel Egli
Barbara Zavan
Martina Trentini
Gunnar Florin
Alf Vaerneus
Håkan Aldskogius
Robert Fredriksson
Elena N. Kozlova
Effects of microgravity on neural crest stem cells
Frontiers in Neuroscience
microgravity
proliferation
delayed effect
neural stem cell
gene expression
exosomes
title Effects of microgravity on neural crest stem cells
title_full Effects of microgravity on neural crest stem cells
title_fullStr Effects of microgravity on neural crest stem cells
title_full_unstemmed Effects of microgravity on neural crest stem cells
title_short Effects of microgravity on neural crest stem cells
title_sort effects of microgravity on neural crest stem cells
topic microgravity
proliferation
delayed effect
neural stem cell
gene expression
exosomes
url https://www.frontiersin.org/articles/10.3389/fnins.2024.1379076/full
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