Local externalization of phosphatidylserine mediates developmental synaptic pruning by microglia
Neuronal circuit assembly requires the fine balance between synapse formation and elimination. Microglia, through the elimination of supernumerary synapses, have an established role in this process. While the microglial receptor TREM2 and the soluble complement proteins C1q and C3 are recognized as...
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| Veröffentlicht in: | The EMBO journal Jg. 39; H. 16; S. e105380 - n/a |
|---|---|
| Hauptverfasser: | , , , , , , , , , , , , , , , , |
| Format: | Journal Article |
| Sprache: | Englisch |
| Veröffentlicht: |
London
Nature Publishing Group UK
17.08.2020
Springer Nature B.V John Wiley and Sons Inc |
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| ISSN: | 0261-4189, 1460-2075, 1460-2075 |
| Online-Zugang: | Volltext |
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| Abstract | Neuronal circuit assembly requires the fine balance between synapse formation and elimination. Microglia, through the elimination of supernumerary synapses, have an established role in this process. While the microglial receptor TREM2 and the soluble complement proteins C1q and C3 are recognized as key players, the neuronal molecular components that specify synapses to be eliminated are still undefined. Here, we show that exposed phosphatidylserine (PS) represents a neuronal “eat‐me” signal involved in microglial‐mediated pruning. In hippocampal neuron and microglia co‐cultures, synapse elimination can be partially prevented by blocking accessibility of exposed PS using Annexin V or through microglial loss of TREM2.
In vivo
, PS exposure at both hippocampal and retinogeniculate synapses and engulfment of PS‐labeled material by microglia occurs during established developmental periods of microglial‐mediated synapse elimination. Mice deficient in C1q, which fail to properly refine retinogeniculate connections, have elevated presynaptic PS exposure and reduced PS engulfment by microglia. These data provide mechanistic insight into microglial‐mediated synapse pruning and identify a novel role of developmentally regulated neuronal PS exposure that is common among developing brain structures.
Synopsis
Microglia help refine developing neural circuits through the elimination of supernumerary synapses. Here we show that exposed phosphatidylserine on pre‐ and postsynaptic membranes functions as an “eat‐me” signal contributing to microglial‐mediated synapse pruning. Phosphatidylserine exposure at both hippocampal and retinogeniculate synapses coincides with the onset of synapse elimination and PS engulfment by microglia.
Microglia‐mediated synapse elimination is dependent on TREM2 and exposed phosphatidylserine
in vitro
.
Exposed phosphatidylserine is developmentally regulated across periods of pruning in both hippocampus and visual system.
In vivo
developmental phosphatidylserine exposure is not caspase 3‐dependent.
Loss of C1q leads to elevated phosphatidylserine‐positive presynaptic inputs and reduced microglia engulfment.
Graphical Abstract
Exposed phosphatidylserine on pre‐ and postsynaptic membranes functions as an “eat‐me” signal contributing to microglia‐mediated synapse pruning. |
|---|---|
| AbstractList | Neuronal circuit assembly requires the fine balance between synapse formation and elimination. Microglia, through the elimination of supernumerary synapses, have an established role in this process. While the microglial receptor TREM2 and the soluble complement proteins C1q and C3 are recognized as key players, the neuronal molecular components that specify synapses to be eliminated are still undefined. Here, we show that exposed phosphatidylserine (PS) represents a neuronal "eat-me" signal involved in microglial-mediated pruning. In hippocampal neuron and microglia co-cultures, synapse elimination can be partially prevented by blocking accessibility of exposed PS using Annexin V or through microglial loss of TREM2. In vivo, PS exposure at both hippocampal and retinogeniculate synapses and engulfment of PS-labeled material by microglia occurs during established developmental periods of microglial-mediated synapse elimination. Mice deficient in C1q, which fail to properly refine retinogeniculate connections, have elevated presynaptic PS exposure and reduced PS engulfment by microglia. These data provide mechanistic insight into microglial-mediated synapse pruning and identify a novel role of developmentally regulated neuronal PS exposure that is common among developing brain structures.Neuronal circuit assembly requires the fine balance between synapse formation and elimination. Microglia, through the elimination of supernumerary synapses, have an established role in this process. While the microglial receptor TREM2 and the soluble complement proteins C1q and C3 are recognized as key players, the neuronal molecular components that specify synapses to be eliminated are still undefined. Here, we show that exposed phosphatidylserine (PS) represents a neuronal "eat-me" signal involved in microglial-mediated pruning. In hippocampal neuron and microglia co-cultures, synapse elimination can be partially prevented by blocking accessibility of exposed PS using Annexin V or through microglial loss of TREM2. In vivo, PS exposure at both hippocampal and retinogeniculate synapses and engulfment of PS-labeled material by microglia occurs during established developmental periods of microglial-mediated synapse elimination. Mice deficient in C1q, which fail to properly refine retinogeniculate connections, have elevated presynaptic PS exposure and reduced PS engulfment by microglia. These data provide mechanistic insight into microglial-mediated synapse pruning and identify a novel role of developmentally regulated neuronal PS exposure that is common among developing brain structures. Neuronal circuit assembly requires the fine balance between synapse formation and elimination. Microglia, through the elimination of supernumerary synapses, have an established role in this process. While the microglial receptor TREM2 and the soluble complement proteins C1q and C3 are recognized as key players, the neuronal molecular components that specify synapses to be eliminated are still undefined. Here, we show that exposed phosphatidylserine (PS) represents a neuronal “eat‐me” signal involved in microglial‐mediated pruning. In hippocampal neuron and microglia co‐cultures, synapse elimination can be partially prevented by blocking accessibility of exposed PS using Annexin V or through microglial loss of TREM2. In vivo, PS exposure at both hippocampal and retinogeniculate synapses and engulfment of PS‐labeled material by microglia occurs during established developmental periods of microglial‐mediated synapse elimination. Mice deficient in C1q, which fail to properly refine retinogeniculate connections, have elevated presynaptic PS exposure and reduced PS engulfment by microglia. These data provide mechanistic insight into microglial‐mediated synapse pruning and identify a novel role of developmentally regulated neuronal PS exposure that is common among developing brain structures. Neuronal circuit assembly requires the fine balance between synapse formation and elimination. Microglia, through the elimination of supernumerary synapses, have an established role in this process. While the microglial receptor TREM2 and the soluble complement proteins C1q and C3 are recognized as key players, the neuronal molecular components that specify synapses to be eliminated are still undefined. Here, we show that exposed phosphatidylserine (PS) represents a neuronal “eat‐me” signal involved in microglial‐mediated pruning. In hippocampal neuron and microglia co‐cultures, synapse elimination can be partially prevented by blocking accessibility of exposed PS using Annexin V or through microglial loss of TREM2. In vivo , PS exposure at both hippocampal and retinogeniculate synapses and engulfment of PS‐labeled material by microglia occurs during established developmental periods of microglial‐mediated synapse elimination. Mice deficient in C1q, which fail to properly refine retinogeniculate connections, have elevated presynaptic PS exposure and reduced PS engulfment by microglia. These data provide mechanistic insight into microglial‐mediated synapse pruning and identify a novel role of developmentally regulated neuronal PS exposure that is common among developing brain structures. Synopsis Microglia help refine developing neural circuits through the elimination of supernumerary synapses. Here we show that exposed phosphatidylserine on pre‐ and postsynaptic membranes functions as an “eat‐me” signal contributing to microglial‐mediated synapse pruning. Phosphatidylserine exposure at both hippocampal and retinogeniculate synapses coincides with the onset of synapse elimination and PS engulfment by microglia. Microglia‐mediated synapse elimination is dependent on TREM2 and exposed phosphatidylserine in vitro . Exposed phosphatidylserine is developmentally regulated across periods of pruning in both hippocampus and visual system. In vivo developmental phosphatidylserine exposure is not caspase 3‐dependent. Loss of C1q leads to elevated phosphatidylserine‐positive presynaptic inputs and reduced microglia engulfment. Graphical Abstract Exposed phosphatidylserine on pre‐ and postsynaptic membranes functions as an “eat‐me” signal contributing to microglia‐mediated synapse pruning. Neuronal circuit assembly requires the fine balance between synapse formation and elimination. Microglia, through the elimination of supernumerary synapses, have an established role in this process. While the microglial receptor TREM2 and the soluble complement proteins C1q and C3 are recognized as key players, the neuronal molecular components that specify synapses to be eliminated are still undefined. Here, we show that exposed phosphatidylserine (PS) represents a neuronal “eat‐me” signal involved in microglial‐mediated pruning. In hippocampal neuron and microglia co‐cultures, synapse elimination can be partially prevented by blocking accessibility of exposed PS using Annexin V or through microglial loss of TREM2. In vivo, PS exposure at both hippocampal and retinogeniculate synapses and engulfment of PS‐labeled material by microglia occurs during established developmental periods of microglial‐mediated synapse elimination. Mice deficient in C1q, which fail to properly refine retinogeniculate connections, have elevated presynaptic PS exposure and reduced PS engulfment by microglia. These data provide mechanistic insight into microglial‐mediated synapse pruning and identify a novel role of developmentally regulated neuronal PS exposure that is common among developing brain structures. Synopsis Microglia help refine developing neural circuits through the elimination of supernumerary synapses. Here we show that exposed phosphatidylserine on pre‐ and postsynaptic membranes functions as an “eat‐me” signal contributing to microglial‐mediated synapse pruning. Phosphatidylserine exposure at both hippocampal and retinogeniculate synapses coincides with the onset of synapse elimination and PS engulfment by microglia. Microglia‐mediated synapse elimination is dependent on TREM2 and exposed phosphatidylserine in vitro. Exposed phosphatidylserine is developmentally regulated across periods of pruning in both hippocampus and visual system. In vivo developmental phosphatidylserine exposure is not caspase 3‐dependent. Loss of C1q leads to elevated phosphatidylserine‐positive presynaptic inputs and reduced microglia engulfment. Exposed phosphatidylserine on pre‐ and postsynaptic membranes functions as an “eat‐me” signal contributing to microglia‐mediated synapse pruning. Neuronal circuit assembly requires the fine balance between synapse formation and elimination. Microglia, through the elimination of supernumerary synapses, have an established role in this process. While the microglial receptor TREM2 and the soluble complement proteins C1q and C3 are recognized as key players, the neuronal molecular components that specify synapses to be eliminated are still undefined. Here, we show that exposed phosphatidylserine (PS) represents a neuronal “eat‐me” signal involved in microglial‐mediated pruning. In hippocampal neuron and microglia co‐cultures, synapse elimination can be partially prevented by blocking accessibility of exposed PS using Annexin V or through microglial loss of TREM2. In vivo, PS exposure at both hippocampal and retinogeniculate synapses and engulfment of PS‐labeled material by microglia occurs during established developmental periods of microglial‐mediated synapse elimination. Mice deficient in C1q, which fail to properly refine retinogeniculate connections, have elevated presynaptic PS exposure and reduced PS engulfment by microglia. These data provide mechanistic insight into microglial‐mediated synapse pruning and identify a novel role of developmentally regulated neuronal PS exposure that is common among developing brain structures. Exposed phosphatidylserine on pre‐ and postsynaptic membranes functions as an “eat‐me” signal contributing to microglia‐mediated synapse pruning. |
| Author | Scott‐Hewitt, Nicole Erreni, Marco Faggiani, Elisa Filipello, Fabia Perrucci, Fabio Tamborini, Matteo Carey, Alanna Schuetz, Lisa Theresia Mahoney, Matthew Jahn, Reinhard Stevens, Beth Witkowska, Agata Mason, Sydney Bizzotto, Matteo Passoni, Lorena Morini, Raffaella Matteoli, Michela |
| AuthorAffiliation | 7 Department of Molecular Pharmacology and Cell Biology Leibniz‐Forschungsinstitut für Molekulare Pharmakologie (FMP) Berlin Germany 8 University of Göttingen Göttingen Germany 4 Department of Biomedical Sciences Humanitas University Pieve Emanuele (MI) Italy 3 Laboratory of Pharmacology and Brain Pathology Neurocenter Humanitas Clinical and Research Center ‐ IRCCS Rozzano (MI) Italy 9 Howard Hughes Medical Institute Boston Children's Hospital Boston MA USA 10 CNR Institute of Neuroscience Milano Italy 11 Present address: Department of Neurology Washington University St. Louis MO USA 6 Laboratory of Neurobiology Max Planck Institute for Biophysical Chemistry Göttingen Germany 1 F.M. Kirby Center for Neurobiology Boston Children's Hospital Boston MA USA 2 Stanley Center for Psychiatric Research The Broad Institute of MIT and Harvard Cambridge MA USA 5 Unit of Advanced Optical Microscopy Humanitas Clinical and Research Center ‐ IRCCS Rozzano (MI) Italy |
| AuthorAffiliation_xml | – name: 3 Laboratory of Pharmacology and Brain Pathology Neurocenter Humanitas Clinical and Research Center ‐ IRCCS Rozzano (MI) Italy – name: 7 Department of Molecular Pharmacology and Cell Biology Leibniz‐Forschungsinstitut für Molekulare Pharmakologie (FMP) Berlin Germany – name: 11 Present address: Department of Neurology Washington University St. Louis MO USA – name: 2 Stanley Center for Psychiatric Research The Broad Institute of MIT and Harvard Cambridge MA USA – name: 9 Howard Hughes Medical Institute Boston Children's Hospital Boston MA USA – name: 5 Unit of Advanced Optical Microscopy Humanitas Clinical and Research Center ‐ IRCCS Rozzano (MI) Italy – name: 8 University of Göttingen Göttingen Germany – name: 4 Department of Biomedical Sciences Humanitas University Pieve Emanuele (MI) Italy – name: 10 CNR Institute of Neuroscience Milano Italy – name: 1 F.M. Kirby Center for Neurobiology Boston Children's Hospital Boston MA USA – name: 6 Laboratory of Neurobiology Max Planck Institute for Biophysical Chemistry Göttingen Germany |
| Author_xml | – sequence: 1 givenname: Nicole surname: Scott‐Hewitt fullname: Scott‐Hewitt, Nicole organization: F.M. Kirby Center for Neurobiology, Boston Children's Hospital, Stanley Center for Psychiatric Research, The Broad Institute of MIT and Harvard – sequence: 2 givenname: Fabio orcidid: 0000-0001-6810-471X surname: Perrucci fullname: Perrucci, Fabio organization: Laboratory of Pharmacology and Brain Pathology, Neurocenter, Humanitas Clinical and Research Center ‐ IRCCS, Department of Biomedical Sciences, Humanitas University – sequence: 3 givenname: Raffaella surname: Morini fullname: Morini, Raffaella organization: Laboratory of Pharmacology and Brain Pathology, Neurocenter, Humanitas Clinical and Research Center ‐ IRCCS – sequence: 4 givenname: Marco surname: Erreni fullname: Erreni, Marco organization: Unit of Advanced Optical Microscopy, Humanitas Clinical and Research Center ‐ IRCCS – sequence: 5 givenname: Matthew surname: Mahoney fullname: Mahoney, Matthew organization: F.M. Kirby Center for Neurobiology, Boston Children's Hospital – sequence: 6 givenname: Agata surname: Witkowska fullname: Witkowska, Agata organization: Laboratory of Neurobiology, Max Planck Institute for Biophysical Chemistry, Department of Molecular Pharmacology and Cell Biology, Leibniz‐Forschungsinstitut für Molekulare Pharmakologie (FMP) – sequence: 7 givenname: Alanna surname: Carey fullname: Carey, Alanna organization: F.M. Kirby Center for Neurobiology, Boston Children's Hospital – sequence: 8 givenname: Elisa surname: Faggiani fullname: Faggiani, Elisa organization: Laboratory of Pharmacology and Brain Pathology, Neurocenter, Humanitas Clinical and Research Center ‐ IRCCS – sequence: 9 givenname: Lisa Theresia orcidid: 0000-0003-4865-8218 surname: Schuetz fullname: Schuetz, Lisa Theresia organization: Department of Biomedical Sciences, Humanitas University – sequence: 10 givenname: Sydney surname: Mason fullname: Mason, Sydney organization: F.M. Kirby Center for Neurobiology, Boston Children's Hospital – sequence: 11 givenname: Matteo surname: Tamborini fullname: Tamborini, Matteo organization: Laboratory of Pharmacology and Brain Pathology, Neurocenter, Humanitas Clinical and Research Center ‐ IRCCS – sequence: 12 givenname: Matteo surname: Bizzotto fullname: Bizzotto, Matteo organization: Department of Biomedical Sciences, Humanitas University – sequence: 13 givenname: Lorena surname: Passoni fullname: Passoni, Lorena organization: Laboratory of Pharmacology and Brain Pathology, Neurocenter, Humanitas Clinical and Research Center ‐ IRCCS – sequence: 14 givenname: Fabia surname: Filipello fullname: Filipello, Fabia organization: Laboratory of Pharmacology and Brain Pathology, Neurocenter, Humanitas Clinical and Research Center ‐ IRCCS, Department of Biomedical Sciences, Humanitas University, Department of Neurology, Washington University – sequence: 15 givenname: Reinhard orcidid: 0000-0003-1542-3498 surname: Jahn fullname: Jahn, Reinhard organization: Laboratory of Neurobiology, Max Planck Institute for Biophysical Chemistry, University of Göttingen – sequence: 16 givenname: Beth orcidid: 0000-0003-4226-1201 surname: Stevens fullname: Stevens, Beth email: beth.stevens@childrens.harvard.edu organization: F.M. Kirby Center for Neurobiology, Boston Children's Hospital, Stanley Center for Psychiatric Research, The Broad Institute of MIT and Harvard, Howard Hughes Medical Institute, Boston Children's Hospital – sequence: 17 givenname: Michela orcidid: 0000-0002-3569-7843 surname: Matteoli fullname: Matteoli, Michela email: michela.matteoli@hunimed.eu organization: Laboratory of Pharmacology and Brain Pathology, Neurocenter, Humanitas Clinical and Research Center ‐ IRCCS, CNR Institute of Neuroscience |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32657463$$D View this record in MEDLINE/PubMed |
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| SubjectTerms | Animals Annexin V C1q Caspase-3 Circuits Coculture Techniques Complement C1q - genetics Complement C1q - metabolism Complement C3 - genetics Complement C3 - metabolism Complement component C1q Complement component C3 EMBO19 EMBO27 Exposure Hippocampus Hippocampus - metabolism Membrane Glycoproteins - genetics Membrane Glycoproteins - metabolism Mice Mice, Knockout Microglia Microglia - metabolism Neural networks Neurons - metabolism Phosphatidylserine Phosphatidylserines - genetics Phosphatidylserines - metabolism Pruning Receptors, Immunologic - genetics Receptors, Immunologic - metabolism Supernumerary Synapse elimination synapse pruning Synapses Synapses - genetics Synapses - metabolism Synaptogenesis TREM2 Visual pathways Visual system |
| Title | Local externalization of phosphatidylserine mediates developmental synaptic pruning by microglia |
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