Microglia modulate gliotransmission through the regulation of VAMP2 proteins in astrocytes.
TIRF microscopy
glutamate
neuron-glia interaction
vesicular release
Journal
Glia
ISSN: 1098-1136
Titre abrégé: Glia
Pays: United States
ID NLM: 8806785
Informations de publication
Date de publication:
01 2021
01 2021
Historique:
received:
20
03
2019
revised:
12
06
2020
accepted:
15
06
2020
pubmed:
8
7
2020
medline:
3
2
2022
entrez:
8
7
2020
Statut:
ppublish
Résumé
Vesicular release is one of the release mechanisms of various signaling molecules. In neurons, the molecular machinery involved in vesicular release has been designed through evolution to trigger fast and synchronous release of neurotransmitters. Similar machinery with a slower kinetic and a slightly different molecular assembly allows astrocytes to release various transmitters such as adenosine triphosphate (ATP), glutamate, and D-serine. Astrocytes are important modulators of neurotransmission through gliotransmitter release. We recently demonstrated that microglia, another type of glia, release ATP to modulate synaptic transmission using astrocytes as intermediate. We now report that microglia regulate astrocytic gliotransmission through the regulation of SNARE proteins in astrocytes. Indeed, we found that gliotransmission triggered by P2Y1 agonist is impaired in slices from transgenic mice devoid of microglia. Using total internal reflection fluorescence imaging, we found that the vesicular release of gliotransmitter by astrocytes was different in cultures lacking microglia compared to vesicular release in astrocytes cocultured with microglia. Quantification of the kinetic of vesicular release indicates that the overall release appears to be faster in pure astrocyte cultures with more vesicles close to the membrane when compared to astrocytes cocultured with microglia. Finally, biochemical investigation of SNARE protein expression indicates an upregulation of VAMP2 in absence of microglia. Altogether, these results indicate that microglia seems to be involved in the regulation of an astrocytic phenotype compatible with proper gliotransmission. The mechanisms described in this study could be of importance for central nervous system diseases where microglia are activated.
Substances chimiques
SNARE Proteins
0
Vesicle-Associated Membrane Protein 2
0
vesicle-associated membrane protein 2, mouse
0
Adenosine Triphosphate
8L70Q75FXE
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
61-72Informations de copyright
© 2020 Wiley Periodicals LLC.
Références
Back, J., Dierich, A., Bronn, C., Kastner, P., & Chan, S. (2004). PU.1 determines the self-renewal capacity of erythroid progenitor cells. Blood, 103(10), 3615-3623. https://doi.org/10.1182/blood-2003-11-4089
Ben Achour, S., & Pascual, O. (2010). Glia: The many ways to modulate synaptic plasticity. Neurochemistry International, 57, 440-445. https://doi.org/10.1016/j.neuint.2010.02.013
Ben Achour, S., & Pascual, O. (2012). Astrocyte-Neuron Communication: Functional Consequences. Neurochemical Research, 37(11), 2464-2473. https://doi.org/10.1007/s11064-012-0807-0
Bouyssié, D., Hesse, A. M., Mouton-Barbosa, E., Rompais, M., Macron, C., Carapito, C., … Bruley, C. (2020). Proline: An efficient and user-friendly software suite for large-scale proteomics. Bioinformatics, 36, 3148-3155. https://doi.org/10.1093/bioinformatics/btaa118
Domercq, M., Brambilla, L., Pilati, E., Marchaland, J., Volterra, A., & Bezzi, P. (2006). P2Y1 receptor-evoked glutamate exocytosis from astrocytes: Control by tumor necrosis factor-alpha and prostaglandins. The Journal of Biological Chemistry, 281(41), 30684-30696.
Durkee, C. A., & Araque, A. (2019). Diversity and specificity of astrocyte-neuron communication. Neuroscience, 396, 73-78. https://doi.org/10.1016/j.neuroscience.2018.11.010
Fellin, T., Pascual, O., Gobbo, S., Pozzan, T., Haydon, P. G., & Carmignoto, G. (2004). Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors. Neuron, 43(5), 729-743.
Geisler, J. C., Corbin, K. L., Li, Q., Feranchak, A. P., Nunemaker, C. S., & Li, C. (2013). Vesicular nucleotide transporter-mediated ATP release regulates insulin secretion. Endocrinology, 154(2), 675-684. https://doi.org/10.1210/en.2012-1818
Hamilton, N. B., & Attwell, D. (2010). Do astrocytes really exocytose neurotransmitters? Nature Reviews. Neuroscience, 11(4), 227-238. https://doi.org/10.1038/nrn2803
Haydon, P. G. (2001). GLIA: Listening and talking to the synapse. Nature Reviews. Neuroscience, 2(3), 185-193.
Henneberger, C., Papouin, T., Oliet, S. H., & Rusakov, D. A. (2010). Long-term potentiation depends on release of D-serine from astrocytes. Nature, 463(7278), 232-236. https://doi.org/10.1038/nature08673
Jourdain, P., Bergersen, L. H., Bhaukaurally, K., Bezzi, P., Santello, M., Domercq, M., … Volterra, A. (2007). Glutamate exocytosis from astrocytes controls synaptic strength. Nature Neuroscience, 10(3), 331-339.
Li, D., Ropert, N., Koulakoff, A., Giaume, C., & Oheim, M. (2008). Lysosomes are the major vesicular compartment undergoing Ca2+-regulated exocytosis from cortical astrocytes. The Journal of Neuroscience, 28(30), 7648-7658. https://doi.org/10.1523/jneurosci.0744-08.2008
Maggi, L., Scianni, M., Branchi, I., D'Andrea, I., Lauro, C., & Limatola, C. (2011). CX3CR1 deficiency alters hippocampal-dependent plasticity phenomena blunting the effects of enriched environment. Frontiers in Cellular Neuroscience, 5(22), 5-22. https://doi.org/10.3389/fncel.2011.00022
Mothet, J.-P., Parent, A. l. T., Wolosker, H., Brady, R. O., Linden, D. J., Ferris, C. D., … Snyder, S. H. (2000). d-Serine is an endogenous ligand for the glycine site of the N-methyl-d-aspartate receptor. Proceedings of the National Academy of Sciences of the United States of America, 97(9), 4926-4931.
Nedergaard, M. (1994). Direct signaling from astrocytes to neurons in cultures of mammalian brain cells. Science, 263(5154), 1768-1771.
Pangrsic, T., Potokar, M., Stenovec, M., Kreft, M., Fabbretti, E., Nistri, A., … Zorec, R. (2007). Exocytotic release of ATP from cultured astrocytes. Journal of Biological Chemistry, 282(39), 28749-28758. https://doi.org/10.1074/jbc.M700290200
Papouin, T., Dunphy, J., Tolman, M., Foley, J. C., & Haydon, P. G. (2017). Astrocytic control of synaptic function. Philosophical Transactions of the Royal Society B: Biological Sciences, 372(1715), 20160154. https://doi.org/10.1098/rstb.2016.0154
Parkhurst, C. N., Yang, G., Ninan, I., Savas, J. N., Yates, J. R., III, Lafaille, J. J., … Gan, W.-B. (2013). Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell, 155(7), 1596-1609. https://doi.org/10.1016/j.cell.2013.11.030
Parpura, V., Basarsky, T. A., Liu, F., Jeftinija, K., Jeftinija, S., & Haydon, P. G. (1994). Glutamate-mediated astrocyte-neuron signalling. Nature, 369(6483), 744-747.
Pascual, O., Ben Achour, S., Rostaing, P., Triller, A., & Bessis, A. (2012). Microglia activation triggers astrocyte-mediated modulation of excitatory neurotransmission. Proceedings of the National Academy of Sciences, 109(4), E197-E205. https://doi.org/10.1073/pnas.1111098109
Pascual, O., Casper, K. B., Kubera, C., Zhang, J., Revilla-Sanchez, R., Sul, J. Y., … Haydon, P. G. (2005). Astrocytic purinergic signaling coordinates synaptic networks. Science, 310(5745), 113-116.
Pocock, J. M., & Kettenmann, H. (2007). Neurotransmitter receptors on microglia. Trends in Neurosciences, 30(10), 527-535.
Rogers, J. T., Morganti, J. M., Bachstetter, A. D., Hudson, C. E., Peters, M. M., Grimmig, B. A., … Gemma, C. (2011). CX3CR1 deficiency leads to impairment of hippocampal cognitive function and synaptic plasticity. The Journal of Neuroscience, 31(45), 16241-16250. https://doi.org/10.1523/jneurosci.3667-11.2011
Roumier, A., Pascual, O., Bechade, C., Wakselman, S., Poncer, J.-C., Real, E., … Bessis, A. (2008). Prenatal activation of microglia induces delayed impairment of glutamatergic synaptic function. PLoS One, 3(7), e2595.
Salvetti, A., Couté, Y., Epstein, A., Arata, L., Kraut, A., Navratil, V., … Greco, A. (2016). Nuclear functions of nucleolin through global proteomics and interactomic approaches. Journal of Proteome Research, 15(5), 1659-1669. https://doi.org/10.1021/acs.jproteome.6b00126
Santello, M., Bezzi, P., & Volterra, A. (2011). TNF[alpha] controls glutamatergic gliotransmission in the hippocampal dentate gyrus. Neuron, 69(5), 988-1001.
Schoch, S., Deák, F., Königstorfer, A., Mozhayeva, M., Sara, Y., Südhof, T. C., & Kavalali, E. T. (2001). SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science, 294(5544), 1117-1122. https://doi.org/10.1126/science.1064335
Schwarz, Y., Zhao, N., Kirchhoff, F., & Bruns, D. (2017). Astrocytes control synaptic strength by two distinct v-SNARE-dependent release pathways. Nature Neuroscience, 20(11), 1529-1539. https://doi.org/10.1038/nn.4647
Sheikhbahaei, S., Turovsky, E. A., Hosford, P. S., Hadjihambi, A., Theparambil, S. M., Liu, B., … Gourine, A. V. (2018). Astrocytes modulate brainstem respiratory rhythm-generating circuits and determine exercise capacity. Nature Communications, 9(1), 370. https://doi.org/10.1038/s41467-017-02723-6
Stoppini, L., Buchs, P. A., & Muller, D. (1991). A simple method for organotypic cultures of nervous tissue. Journal of Neuroscience Methods, 37(2), 173-182.
Suzuki, T., Hide, I., Ido, K., Kohsaka, S., Inoue, K., & Nakata, Y. (2004). Production and release of neuroprotective tumor necrosis factor by P2X7 receptor-activated microglia. The Journal of Neuroscience, 24(1), 1-7. https://doi.org/10.1523/jneurosci.3792-03.2004
Tao-Cheng, J. H., Pham, A., Yang, Y., Winters, C. A., Gallant, P. E., & Reese, T. S. (2015). Syntaxin 4 is concentrated on plasma membrane of astrocytes. Neuroscience, 286, 264-271. https://doi.org/10.1016/j.neuroscience.2014.11.054
Vanessa, S., David, B., & Andrea, V. (2011). SNARE protein expression in synaptic terminals and astrocytes in the adult hippocampus: A comparative analysis. Glia, 59(10), 1472-1488. https://doi.org/10.1002/glia.21190
Wieczorek, S., Combes, F., Lazar, C., Giai Gianetto, Q., Gatto, L., Dorffer, A., … Burger, T. (2017). DAPAR & ProStaR: Software to perform statistical analyses in quantitative discovery proteomics. Bioinformatics, 33(1), 135-136. https://doi.org/10.1093/bioinformatics/btw580
Zhang, Q., Fukuda, M., Van Bockstaele, E., Pascual, O., & Haydon, P. G. (2004). Synaptotagmin IV regulates glial glutamate release. Proceedings of the National Academy of Sciences of the United States of America, 101(25), 9441-9446.
Zorec, R., Araque, A., Carmignoto, G., Haydon, P. G., Verkhratsky, A., & Parpura, V. (2012). Astroglial excitability and gliotransmission: An appraisal of Ca2+ as a signalling route. ASN Neuro, 4(2), e00080. https://doi.org/10.1042/AN20110061
Zorec, R., Verkhratsky, A., Rodríguez, J. J., & Parpura, V. (2016). Astrocytic vesicles and gliotransmitters: Slowness of vesicular release and synaptobrevin2-laden vesicle nanoarchitecture. Neuroscience, 323, 67-75. https://doi.org/10.1016/j.neuroscience.2015.02.033