Multifaceted effects of oligodendroglial exosomes on neurons: impact on neuronal firing rate, signal transduction and gene regulation
Abstract
Exosomes are small membranous vesicles of endocytic origin that are released by almost every cell type. They exert versatile functions in intercellular communication important for many physiological and pathological processes. Recently, exosomes attracted interest with regard to their role in cell–cell communication in the nervous system. We have shown that exosomes released from oligodendrocytes upon stimulation with the neurotransmitter glutamate are internalized by neurons and enhance the neuronal stress tolerance. Here, we demonstrate that oligodendroglial exosomes also promote neuronal survival during oxygen–glucose deprivation, a model of cerebral ischaemia. We show the transfer from oligodendrocytes to neurons of superoxide dismutase and catalase, enzymes which are known to help cells to resist oxidative stress. Additionally, we identify various effects of oligodendroglial exosomes on neuronal physiology. Electrophysiological analysis using in vitro multi-electrode arrays revealed an increased firing rate of neurons exposed to oligodendroglial exosomes. Moreover, gene expression analysis and phosphorylation arrays uncovered differentially expressed genes and altered signal transduction pathways in neurons after exosome treatment. Our study thus provides new insight into the broad spectrum of action of oligodendroglial exosomes and their effects on neuronal physiology. The exchange of extracellular vesicles between neural cells may exhibit remarkable potential to impact brain performance.
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The miRNA cargo of EVs produced by astrocytes and oligodendrocytes may regulate the expression of neuronal genes.
“Importantly, the miRNA cargo of EVs produced by astrocytes and oligodendrocytes may also regulate the expression of neuronal genes”
From Glia-to-neuron transfer of miRNAs via extracellular vesicles: a new mechanism underlying inflammation-induced synaptic alterations (2018) · cites this paper as [27]
Cites
limma: Linear Models for Microarray Data
Smyth, G. K. (2005) · Statistics for Biology and Health · doi:10.1007/0-387-29362-0_23 · Cited by 5,796 · see citing works
Exosomes are released by cultured cortical neurones
Fauré, J., Lachenal, G., Court, M., Hirrlinger, J., Chatellard-Causse, C., Blot, B., Grange, J., Schoehn, G., Goldberg, Y., Boyer, V., et al. (2006) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2005.12.003 · Cited by 896 · see citing works
Axonal loss and neuroinflammation caused by peroxisome-deficient oligodendrocytes
Kassmann, C. M., Lappe-Siefke, C., Baes, M., Brügger, B., Mildner, A., Werner, H. B., Natt, O., Michaelis, T., Prinz, M., Frahm, J., et al. (2007) · Nature Genetics · doi:10.1038/ng2070 · Cited by 357 · see citing works
Identification of Dynamically Regulated MicroRNA and mRNA Networks in Developing Oligodendrocytes
Lau, P., Verrier, J. D., Nielsen, J. A., Johnson, K. R., Notterpek, L., & Hudson, L. D. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.1932-08.2008 · Cited by 252 · see citing works
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Extracellular vesicles round off communication in the nervous system
Budnik, V., Ruiz-Cañada, C., & Wendler, F. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2015.29 · Cited by 712 · see citing works
Brites, D., & Fernandes, A. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00476 · Cited by 599 · see citing works
“The removal of plasma membrane by ectocytosis is compensated by the fusion of MVBs as a compensatory exocytic process of preformed intracellular vesicles (Sadallah et al., 2011; Cocucci and Meldolesi, 2015).”
BackgroundPrada, I., Gabrielli, M., Turola, E., Iorio, A., D’Arrigo, G., Parolisi, R., De Luca, M., Pacifici, M., Bastoni, M., Lombardi, M., et al. (2018) · Acta Neuropathologica · doi:10.1007/s00401-017-1803-x · Cited by 312 · see citing works
Extracellular Vesicles in Brain Tumors and Neurodegenerative Diseases
Ciregia, F., Urbani, A., & Palmisano, G. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00276 · Cited by 110 · see citing works
Pistono, C., Bister, N., Stanová, I., & Malm, T. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.623771 · Cited by 75 · see citing works
Filannino, F. M., Panaro, M. A., Benameur, T., Pizzolorusso, I., & Porro, C. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25031629 · Cited by 60 · see citing works
Marangon, D., Caporale, N., Boccazzi, M., Abbracchio, M. P., Testa, G., & Lecca, D. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.748849 · Cited by 34 · see citing works
Role of Glia-Derived Extracellular Vesicles in Neurodegenerative Diseases
Li, T., Tan, X., Li, S., Al-Nusaif, M., & Le, W. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.765395 · Cited by 33 · see citing works
Epothilone D inhibits microglia-mediated spread of alpha-synuclein aggregates
Valdinocci, D., Grant, G. D., Dickson, T. C., & Pountney, D. L. (2018) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2018.04.006 · Cited by 20 · see citing works
Engineered Extracellular Vesicles/Exosomes as a New Tool against Neurodegenerative Diseases
Ferrantelli, F., Chiozzini, C., Leone, P., Manfredi, F., & Federico, M. (2020) · Pharmaceutics · doi:10.3390/pharmaceutics12060529 · Cited by 17 · see citing works
Ghosh, S., & Ghosh, S. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.878058 · Cited by 13 · see citing works
- Authors
- Fröhlich, D., Kuo, W. P., Frühbeis, C., Sun, J.-J., Zehendner, C. M., Luhmann, H. J., Pinto, S., Toedling, J., Trotter, J., & Krämer-Albers, E.-M.
- Venue
- Philosophical Transactions of the Royal Society B: Biological Sciences
- Publisher
- The Royal Society
- Published
- 2014-09-26
- Volume
- 369
- Issue
- 1652
- Pages
- 20130510
- ISSN
- 0962-8436
- 1471-2970
- Cited by
- 274
- References
- 4
- Language
- en
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