Microglia activation triggers astrocyte-mediated modulation of excitatory neurotransmission
Fine control of neuronal activity is crucial to rapidly adjust to subtle changes of the environment. This fine tuning was thought to be purely neuronal until the discovery that astrocytes are active players of synaptic transmission. In the adult hippocampus, microglia are the other major glial cell...
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| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 109; no. 4; pp. 1009 - 1010 |
|---|---|
| Main Authors | , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences
24.01.2012
National Acad Sciences |
| Series | PNAS Plus |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Fine control of neuronal activity is crucial to rapidly adjust to subtle changes of the environment. This fine tuning was thought to be purely neuronal until the discovery that astrocytes are active players of synaptic transmission. In the adult hippocampus, microglia are the other major glial cell type. Microglia are highly dynamic and closely associated with neurons and astrocytes. They react rapidly to modifications of their environment and are able to release molecules known to control neuronal function and synaptic transmission. Therefore, microglia display functional features of synaptic partners, but their involvement in the regulation of synaptic transmission has not yet been addressed. We have used a combination of pharmacological approaches with electrophysiological analysis on acute hippocampal slices and ATP assays in purified cell cultures to show that activation of microglia induces a rapid increase of spontaneous excitatory postsynaptic currents. We found that this modulation is mediated by binding of ATP to P2Y1R located on astrocytes and is independent of TNFα or NOS2. Our data indicate that, on activation, microglia cells rapidly release small amounts of ATP, and astrocytes, in turn, amplified this release. Finally, P2Y1 stimulation of astrocytes increased excitatory postsynaptic current frequency through a metabotropic glutamate receptor 5-dependent mechanism. These results indicate that microglia are genuine regulators of neurotransmission and place microglia as upstream partners of astrocytes. Because pathological activation of microglia and alteration of neurotransmission are two early symptoms of most brain diseases, our work also provides a basis for understanding synaptic dysfunction in neuronal diseases. |
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| AbstractList | Fine control of neuronal activity is crucial to rapidly adjust to subtle changes of the environment. This fine tuning was thought to be purely neuronal until the discovery that astrocytes are active players of synaptic transmission. In the adult hippocampus, microglia are the other major glial cell type. Microglia are highly dynamic and closely associated with neurons and astrocytes. They react rapidly to modifications of their environment and are able to release molecules known to control neuronal function and synaptic transmission. Therefore, microglia display functional features of synaptic partners, but their involvement in the regulation of synaptic transmission has not yet been addressed. We have used a combination of pharmacological approaches with electrophysiological analysis on acute hippocampal slices and ATP assays in purified cell cultures to show that activation of microglia induces a rapid increase of spontaneous excitatory postsynaptic currents. We found that this modulation is mediated by binding of ATP to P2Y1R located on astrocytes and is independent of TNF alpha or NOS2. Our data indicate that, on activation, microglia cells rapidly release small amounts of ATP, and astrocytes, in turn, amplified this release. Finally, P2Y1 stimulation of astrocytes increased excitatory postsynaptic current frequency through a metabotropic glutamate receptor 5-dependent mechanism. These results indicate that microglia are genuine regulators of neurotransmission and place microglia as upstream partners of astrocytes. Because pathological activation of microglia and alteration of neurotransmission are two early symptoms of most brain diseases, our work also provides a basis for understanding synaptic dysfunction in neuronal diseases. Fine control of neuronal activity is crucial to rapidly adjust to subtle changes of the environment. This fine tuning was thought to be purely neuronal until the discovery that astrocytes are active players of synaptic transmission. In the adult hippocampus, microglia are the other major glial cell type. Microglia are highly dynamic and closely associated with neurons and astrocytes. They react rapidly to modifications of their environment and are able to release molecules known to control neuronal function and synaptic transmission. Therefore, microglia display functional features of synaptic partners, but their involvement in the regulation of synaptic transmission has not yet been addressed. We have used a combination of pharmacological approaches with electrophysiological analysis on acute hippocampal slices and ATP assays in purified cell cultures to show that activation of microglia induces a rapid increase of spontaneous excitatory postsynaptic currents. We found that this modulation is mediated by binding of ATP to P2Y1R located on astrocytes and is independent of TNFα or NOS2. Our data indicate that, on activation, microglia cells rapidly release small amounts of ATP, and astrocytes, in turn, amplified this release. Finally, P2Y1 stimulation of astrocytes increased excitatory postsynaptic current frequency through a metabotropic glutamate receptor 5-dependent mechanism. These results indicate that microglia are genuine regulators of neurotransmission and place microglia as upstream partners of astrocytes. Because pathological activation of microglia and alteration of neurotransmission are two early symptoms of most brain diseases, our work also provides a basis for understanding synaptic dysfunction in neuronal diseases. Fine control of neuronal activity is crucial to rapidly adjust to subtle changes of the environment. This fine tuning was thought to be purely neuronal until the discovery that astrocytes are active players of synaptic transmission. In the adult hippocampus, microglia are the other major glial cell type. Microglia are highly dynamic and closely associated with neurons and astrocytes. They react rapidly to modifications of their environment and are able to release molecules known to control neuronal function and synaptic transmission. Therefore, microglia display functional features of synaptic partners, but their involvement in the regulation of synaptic transmission has not yet been addressed. We have used a combination of pharmacological approaches with electrophysiological analysis on acute hippocampal slices and ATP assays in purified cell cultures to show that activation of microglia induces a rapid increase of spontaneous excitatory postsynaptic currents. We found that this modulation is mediated by binding of ATP to P2Y1R located on astrocytes and is independent of TNFα or NOS2. Our data indicate that, on activation, microglia cells rapidly release small amounts of ATP, and astrocytes, in turn, amplified this release. Finally, P2Y1 stimulation of astrocytes increased excitatory postsynaptic current frequency through a metabotropic glutamate receptor 5-dependent mechanism. These results indicate that microglia are genuine regulators of neurotransmission and place microglia as upstream partners of astrocytes. Because pathological activation of microglia and alteration of neurotransmission are two early symptoms of most brain diseases, our work also provides a basis for understanding synaptic dysfunction in neuronal diseases. Author Summary This study indicates that microglial cells can control neuronal activity through astrocytes as intermediaries. We also found that, when the excitation vs. inhibition balance is challenged, LPS application can increase the propensity for seizure-like activity. In conclusion, TLR4 activation modulates neuronal activity through the intermediaries microglia and astrocytes. The discovery of a growing number of endogenous TLR4 ligands, such as Heat Shock Protein 60 (HSP60), fibronectin, and fibrinogen, indicates that the signaling pathway described in this study might be relevant under many physiological conditions and in most CNS pathologies. A pharmacological approach, which uses various compounds or drugs to experimentally understand a process, indicated that microglial stimulation by LPS was insensitive to tetrodotoxin, a blocker of action potential and one (2,3-dihydroxy-6-nitro-7-sulfamoyl-benzo[f]quinoxaline-2,3-dione) that specifically targets synapses containing the AMPA-type glutamate receptors. Additional investigations of these signaling pathways indicated that ATP played a central role in this communication, because an ATP competitor blocked the LPS-induced neuronal response. We were able to more specifically show that the neuronal response required the protein G-coupled purinergic metabotropic receptors P2Y1. In the hippocampus, P2Y1 receptors are only present on inhibitory interneurons (i.e., neurons inhibiting neural signaling) and astrocytes. The involvement of interneurons was ruled out, because we found that inhibitory synapses were not involved in the neuronal response to microglial activation. In contrast, application of fluoroacetate, a metabolic poison that is taken up only by astrocytes and frequently used to inhibit astrocytic functions ( 4 , 5 ), completely abolished the LPS-induced increase in the frequency of spontaneous synaptic events. Because the release of ATP by microglia was poorly documented, we used a combination of pure microglial and pure astrocyte cell cultures to monitor ATP release by using a specially designed assay system. We confirmed that LPS specifically acts on microglia, because the microglial cultures but not the astrocyte cultures responded to LPS by a release of ATP. This finding was also supported by the application of LPS on organotypic slice cultures lacking microglia. In such slices, LPS failed to increase neuronal activity, whereas the P2Y1 receptor agonist mimicked the LPS-induced neuronal modulation. Finally, with the acute hippocampal slices, we were able to show that astrocytes recruited by microglial ATP modulated neuronal activity at AMPA receptor-containing synapses by glutamate acting on metabotropic glutamate receptors. This conclusion was reached after a series of experiments. First, we stimulated microglia by using an LPS, a toll-like receptor 4 (TLR4) ligand, commonly used as a proinflammatory agent. We simultaneously recorded the spontaneous synaptic activity of neurons in acute hippocampal slices, slices containing a region of the brain involved in memory formation, by using a method known as patch-clamp recording. We found that microglial activation induces a rapid and transient increase in the frequency of excitatory synaptic events but no associated change in their amplitude, suggesting an increased neurotransmitter release from the presynaptic terminals. We confirmed the involvement of TLR4 signaling, because the response to LPS was absent in slices from mice lacking the TLR4 protein. Although the rapid kinetic response to LPS seemed to be incompatible with an inflammatory response, we challenged the inflammatory pathway by using minocycline. This widely used antiinflammatory agent prevented the response to LPS. These results indicate that LPS-induced neuronal response is mediated through the classical TLR4 signaling pathway. In the CNS, the communication between neurons occurs mostly at synapses. At these critical meeting points, one neuron (the presynaptic neuron) sends a signal to another neuron (the postsynaptic neuron) across a gap known as the synaptic cleft. During synaptic transmission, the presynaptic neuron releases neurotransmitters (i.e., small molecules that act as signals between nerve cells) such as glutamate into the synaptic cleft. The neurotransmitter then binds to specific receptors located on the postsynaptic neurons to elicit a postsynaptic potential. However, the communication between neurons is more complex than this simple one-way messaging. Fine modulation of synaptic transmission in mammals requires retrograde signaling, wherein the postsynaptic nerve communicates with the presynaptic nerve. This modulation has long been thought to be purely neuronal, involving solely the pre- and postsynaptic cells. However, since the mid-1990s, the role of astrocytes, a subtype of glial (support) cell, in the fine tuning of neurotransmission has been shown. Indeed, astrocytes, which were primarily known to clear neurotransmitters from the synaptic cleft, were also shown to release neurotransmitters such as glutamate or ATP, commonly known as the energy currency of the cell, to modulate neuronal activity ( 1 – 4 ). In this study, we show that a second type of glial cell, the microglia (referred to as the macrophages of the central nervous system), recruits astrocytes to modulate neuronal activity at an early step in the inflammatory process ( Fig. P1 ). Fine control of neuronal activity is crucial to rapidly adjust to subtle changes of the environment. This fine tuning was thought to be purely neuronal until the discovery that astrocytes are active players of synaptic transmission. In the adult hippocampus, microglia are the other major glial cell type. Microglia are highly dynamic and closely associated with neurons and astrocytes. They react rapidly to modifications of their environment and are able to release molecules known to control neuronal function and synaptic transmission. Therefore, microglia display functional features of synaptic partners, but their involvement in the regulation of synaptic transmission has not yet been addressed. We have used a combination of pharmacological approaches with electrophysiological analysis on acute hippocampal slices and ATP assays in purified cell cultures to show that activation of microglia induces a rapid increase of spontaneous excitatory postsynaptic currents. We found that this modulation is mediated by binding of ATP to P2Y1R located on astrocytes and is independent of TNFα or NOS2. Our data indicate that, on activation, microglia cells rapidly release small amounts of ATP, and astrocytes, in turn, amplified this release. Finally, P2Y1 stimulation of astrocytes increased excitatory postsynaptic current frequency through a metabotropic glutamate receptor 5-dependent mechanism. These results indicate that microglia are genuine regulators of neurotransmission and place microglia as upstream partners of astrocytes. Because pathological activation of microglia and alteration of neurotransmission are two early symptoms of most brain diseases, our work also provides a basis for understanding synaptic dysfunction in neuronal diseases. [PUBLICATION ABSTRACT] |
| Author | Pascual, Olivier Rostaing, Philippe Achour, Sarrah Ben Triller, Antoine Bessis, Alain |
| Author_xml | – sequence: 1 givenname: Olivier surname: Pascual fullname: Pascual, Olivier – sequence: 2 givenname: Sarrah Ben surname: Achour fullname: Achour, Sarrah Ben – sequence: 3 givenname: Philippe surname: Rostaing fullname: Rostaing, Philippe – sequence: 4 givenname: Antoine surname: Triller fullname: Triller, Antoine – sequence: 5 givenname: Alain surname: Bessis fullname: Bessis, Alain |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/22167804$$D View this record in MEDLINE/PubMed |
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| SubjectTerms | Adenosine triphosphatase Adenosine Triphosphate - metabolism Analysis of Variance Animals Astrocytes Astrocytes - metabolism Astrocytes - physiology Astrocytes - ultrastructure ATP Biological Sciences Blotting, Western Brain diseases Brain slice preparation Cell culture Data processing DNA Primers - genetics Electrophysiology Excitatory postsynaptic potentials Excitatory Postsynaptic Potentials - physiology Fluorescent Antibody Technique Glial cells Glutamic acid receptors (metabotropic) Hippocampus Hippocampus - physiology Immunohistochemistry Mice Mice, Inbred C57BL Mice, Knockout Microglia Microglia - metabolism Microglia - physiology Microglia - ultrastructure Microscopy, Confocal Microscopy, Electron Neuromodulation Neurons Neurotransmission Neurotransmitters PNAS Plus PNAS PLUS (AUTHOR SUMMARIES) Real-Time Polymerase Chain Reaction Receptor, Metabotropic Glutamate 5 Receptors, Metabotropic Glutamate - metabolism Receptors, Purinergic P2Y1 - metabolism Synaptic transmission Tumor necrosis factor- alpha |
| Title | Microglia activation triggers astrocyte-mediated modulation of excitatory neurotransmission |
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