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Oligodendrocyte-derived exosomes promote axonal transport and axonal long-term maintenance

Carsten Frühbeis, View ORCID ProfileWen Ping Kuo-Elsner, Kerstin Barth, View ORCID ProfileLeticia Peris, View ORCID ProfileStefan Tenzer, Wiebke Möbius, Hauke B. Werner, Klaus-Armin Nave, View ORCID ProfileDominik Fröhlich, View ORCID ProfileEva-Maria Krämer-Albers
doi: https://doi.org/10.1101/2019.12.20.884171
Carsten Frühbeis
1Institute of Developmental Biology and Neurobiology, Biology of Extracellular Vesicles Group, University of Mainz, 55099 Mainz, Germany
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Wen Ping Kuo-Elsner
1Institute of Developmental Biology and Neurobiology, Biology of Extracellular Vesicles Group, University of Mainz, 55099 Mainz, Germany
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Kerstin Barth
1Institute of Developmental Biology and Neurobiology, Biology of Extracellular Vesicles Group, University of Mainz, 55099 Mainz, Germany
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Leticia Peris
2University Grenoble Alpes, Inserm, U1216, Grenoble Institut Neurosciences, 38000 Grenoble, France
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Stefan Tenzer
3Institute of Immunology, University of Mainz, 55131 Mainz, Germany
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Wiebke Möbius
4Max Planck Institute of Experimental Medicine, Göttingen, Germany
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Hauke B. Werner
4Max Planck Institute of Experimental Medicine, Göttingen, Germany
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Klaus-Armin Nave
4Max Planck Institute of Experimental Medicine, Göttingen, Germany
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Dominik Fröhlich
1Institute of Developmental Biology and Neurobiology, Biology of Extracellular Vesicles Group, University of Mainz, 55099 Mainz, Germany
5Translational Neuroscience Facility and Department of Physiology, School of Medical Sciences, University of New South Wales, Sydney, NSW, Australia
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Eva-Maria Krämer-Albers
1Institute of Developmental Biology and Neurobiology, Biology of Extracellular Vesicles Group, University of Mainz, 55099 Mainz, Germany
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  • For correspondence: emkraemer@uni-mainz.de
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Abstract

Neurons extend long axons that require maintenance and are susceptible to degeneration. Long-term integrity of axons depends on intrinsic mechanisms including axonal transport and extrinsic support from adjacent glial cells. The mechanisms of support provided by myelinating oligodendrocytes to underlying axons are only partly understood. Oligodendrocytes release extracellular vesicles (EVs) with properties of exosomes, which upon delivery to neurons improve neuronal viability in vitro. Here, we show that oligodendroglial exosomes support neurons by promoting fast axonal transport, most strikingly under conditions of oxidative stress and nutrient deprivation. Interestingly, oligodendroglial exosome secretion is impaired in two mouse mutants exhibiting secondary axonal degeneration due to oligodendrocyte-specific gene defects. Mutant oligodendrocytes release less exosomes that share a common signature of underrepresented proteins. Notably, mutant exosomes lack the ability to support nutrient deprived neurons and to promote axonal transport. Together, these findings indicate that glia to neuron exosome transfer promotes neuronal long-term maintenance by facilitating axonal transport, providing a novel mechanistic link between myelin diseases and secondary loss of axonal integrity.

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Posted December 20, 2019.
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Oligodendrocyte-derived exosomes promote axonal transport and axonal long-term maintenance
Carsten Frühbeis, Wen Ping Kuo-Elsner, Kerstin Barth, Leticia Peris, Stefan Tenzer, Wiebke Möbius, Hauke B. Werner, Klaus-Armin Nave, Dominik Fröhlich, Eva-Maria Krämer-Albers
bioRxiv 2019.12.20.884171; doi: https://doi.org/10.1101/2019.12.20.884171
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Oligodendrocyte-derived exosomes promote axonal transport and axonal long-term maintenance
Carsten Frühbeis, Wen Ping Kuo-Elsner, Kerstin Barth, Leticia Peris, Stefan Tenzer, Wiebke Möbius, Hauke B. Werner, Klaus-Armin Nave, Dominik Fröhlich, Eva-Maria Krämer-Albers
bioRxiv 2019.12.20.884171; doi: https://doi.org/10.1101/2019.12.20.884171

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