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Redox potential defines functional states of adult hippocampal stem cells

Vijay S Adusumilli, Tara L Walker, Rupert W Overall, Gesa M Klatt, Salma A Zeidan, Tim J Fischer, Sara Zocher, Alex M Sykes, Susanne Reinhardt, View ORCID ProfileAndreas Dahl, Dilyana G Kirova, Jörg Mansfeld, Annette E Rünker, Gerd Kempermann
doi: https://doi.org/10.1101/606186
Vijay S Adusumilli
1German Center for Neurodegenerative Diseases (DZNE) Dresden, Dresden, Germany
2CRTD – Center for Regenerative Therapies Dresden, Technische Universität Dresden, Dresden, Germany
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Tara L Walker
1German Center for Neurodegenerative Diseases (DZNE) Dresden, Dresden, Germany
2CRTD – Center for Regenerative Therapies Dresden, Technische Universität Dresden, Dresden, Germany
6Queensland Brain Institute (QBI), The University of Queensland, Brisbane, Australia
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Rupert W Overall
1German Center for Neurodegenerative Diseases (DZNE) Dresden, Dresden, Germany
2CRTD – Center for Regenerative Therapies Dresden, Technische Universität Dresden, Dresden, Germany
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Gesa M Klatt
1German Center for Neurodegenerative Diseases (DZNE) Dresden, Dresden, Germany
2CRTD – Center for Regenerative Therapies Dresden, Technische Universität Dresden, Dresden, Germany
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Salma A Zeidan
1German Center for Neurodegenerative Diseases (DZNE) Dresden, Dresden, Germany
2CRTD – Center for Regenerative Therapies Dresden, Technische Universität Dresden, Dresden, Germany
4Cell Cycle, Biotechnology Center (Biotec), Technische Universität Dresden, Dresden, Germany
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Tim J Fischer
1German Center for Neurodegenerative Diseases (DZNE) Dresden, Dresden, Germany
2CRTD – Center for Regenerative Therapies Dresden, Technische Universität Dresden, Dresden, Germany
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Sara Zocher
1German Center for Neurodegenerative Diseases (DZNE) Dresden, Dresden, Germany
2CRTD – Center for Regenerative Therapies Dresden, Technische Universität Dresden, Dresden, Germany
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Alex M Sykes
5Max Planck Institute for Molecular Cell Biology and Genetics, Dresden, Germany
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Susanne Reinhardt
3DRESDEN Genome Center TU Dresden, Deep Sequencing Group, Center for Molecular and Cellular Bioengineering (CMCB) Technische Universität Dresden, Dresden, Germany
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Andreas Dahl
3DRESDEN Genome Center TU Dresden, Deep Sequencing Group, Center for Molecular and Cellular Bioengineering (CMCB) Technische Universität Dresden, Dresden, Germany
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  • ORCID record for Andreas Dahl
Dilyana G Kirova
4Cell Cycle, Biotechnology Center (Biotec), Technische Universität Dresden, Dresden, Germany
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Jörg Mansfeld
4Cell Cycle, Biotechnology Center (Biotec), Technische Universität Dresden, Dresden, Germany
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Annette E Rünker
1German Center for Neurodegenerative Diseases (DZNE) Dresden, Dresden, Germany
2CRTD – Center for Regenerative Therapies Dresden, Technische Universität Dresden, Dresden, Germany
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Gerd Kempermann
1German Center for Neurodegenerative Diseases (DZNE) Dresden, Dresden, Germany
2CRTD – Center for Regenerative Therapies Dresden, Technische Universität Dresden, Dresden, Germany
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  • For correspondence: gerd.kempermann@dzne.de
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Summary

Intracellular redox states regulate the balance between stem cell maintenance and activation. Increased levels of reactive oxygen species (ROS) are linked to proliferation and lineage specification. In contrast to this general principle, we show that in the hippocampus of adult mice it is the quiescent neural stem cells (NSCs) that maintain the highest ROS levels (hiROS). Classifying NSCs based on intracellular ROS content identified subpopulations with distinct molecular profiles, corresponding to functional states. Shifts in ROS content primed cells for a subsequent transition of cellular state, with lower cellular ROS content marking activity and differentiation. Physical activity, a known physiological activator of adult hippocampal neurogenesis, recruited the quiescent hiROS NSCs into proliferation via a transient Nox2-dependent ROS surge. In the absence of Nox2, baseline neurogenesis was unaffected, but the activity-induced increase in proliferation disappeared. These results describe a novel mechanism linking the modulation of cellular ROS by behavioral cues to the maintenance and activation of adult NSCs.

Highlights

  • Quiescent adult hippocampal stem cells are characterized by high intracellular ROS

  • Changes in intracellular ROS content precede changes in cellular state

  • Acute physical activity recruits quiescent cells into active proliferation

  • This recruitment is marked by a Nox2-dependent ROS spike in hiROS stem cells and represents an independent mode of cell cycle entry

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Posted April 12, 2019.
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Redox potential defines functional states of adult hippocampal stem cells
Vijay S Adusumilli, Tara L Walker, Rupert W Overall, Gesa M Klatt, Salma A Zeidan, Tim J Fischer, Sara Zocher, Alex M Sykes, Susanne Reinhardt, Andreas Dahl, Dilyana G Kirova, Jörg Mansfeld, Annette E Rünker, Gerd Kempermann
bioRxiv 606186; doi: https://doi.org/10.1101/606186
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Redox potential defines functional states of adult hippocampal stem cells
Vijay S Adusumilli, Tara L Walker, Rupert W Overall, Gesa M Klatt, Salma A Zeidan, Tim J Fischer, Sara Zocher, Alex M Sykes, Susanne Reinhardt, Andreas Dahl, Dilyana G Kirova, Jörg Mansfeld, Annette E Rünker, Gerd Kempermann
bioRxiv 606186; doi: https://doi.org/10.1101/606186

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