Astrocytes mediate synapse elimination through MEGF10 and MERTK pathways
To achieve its precise neural connectivity, the developing mammalian nervous system undergoes extensive activity-dependent synapse remodelling. Recently, microglial cells have been shown to be responsible for a portion of synaptic pruning, but the remaining mechanisms remain unknown. Here we report...
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| Published in | Nature (London) Vol. 504; no. 7480; pp. 394 - 400 |
|---|---|
| Main Authors | , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
19.12.2013
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0028-0836 1476-4687 1476-4687 |
| DOI | 10.1038/nature12776 |
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| Abstract | To achieve its precise neural connectivity, the developing mammalian nervous system undergoes extensive activity-dependent synapse remodelling. Recently, microglial cells have been shown to be responsible for a portion of synaptic pruning, but the remaining mechanisms remain unknown. Here we report a new role for astrocytes in actively engulfing central nervous system synapses. This process helps to mediate synapse elimination, requires the MEGF10 and MERTK phagocytic pathways, and is strongly dependent on neuronal activity. Developing mice deficient in both astrocyte pathways fail to refine their retinogeniculate connections normally and retain excess functional synapses. Finally, we show that in the adult mouse brain, astrocytes continuously engulf both excitatory and inhibitory synapses. These studies reveal a novel role for astrocytes in mediating synapse elimination in the developing and adult brain, identify MEGF10 and MERTK as critical proteins in the synapse remodelling underlying neural circuit refinement, and have important implications for understanding learning and memory as well as neurological disease processes.
This study describes comprehensive synaptic engulfment by astrocytes, mediating synapse elimination in an activity-dependent manner; this elimination process involves the MEGF10 and MERTK phagocytic pathways and persists into adulthood, with mutant mice that lack these pathways in astrocytes exhibiting a failure to refine retinogeniculate connections during development.
Astrocytes involved in synapse elimination
Synapse elimination is an important aspect of brain development in which the number of synaptic contacts is reduced in an activity-dependent manner. Glial cells — non-neural cells that perform a variety of roles in the brain — were recently shown to have a role in synapse remodelling, with the phagocytic microglia responsible for a certain proportion of connection refinement, with little else known regarding the mechanisms underlying this. Here, Won-Suk Chung
et al
. describe comprehensive synaptic engulfment by astrocytes, mediating synapse elimination in an activity-dependent manner. This elimination process involved the MEGF10 and MERTK phagocytic pathways, with transgenic animals lacking these pathways in astrocytes exhibiting a failure to refine retinogeniculate connections during development. These mechanisms also extend into adulthood. This work has implications for our understanding of learning and memory as well as neurological disease processes. |
|---|---|
| AbstractList | To achieve its precise neural connectivity, the developing mammalian nervous system undergoes extensive activity-dependent synapse remodelling. Recently, microglial cells have been shown to be responsible for a portion of synaptic pruning, but the remaining mechanisms remain unknown. Here we report a new role for astrocytes in actively engulfing central nervous system synapses. This process helps to mediate synapse elimination, requires the MEGF10 and MERTK phagocytic pathways, and is strongly dependent on neuronal activity. Developing mice deficient in both astrocyte pathways fail to refine their retinogeniculate connections normally and retain excess functional synapses. Finally, we show that in the adult mouse brain, astrocytes continuously engulf both excitatory and inhibitory synapses. These studies reveal a novel role for astrocytes in mediating synapse elimination in the developing and adult brain, identify MEGF10 and MERTK as critical proteins in the synapse remodelling underlying neural circuit refinement, and have important implications for understanding learning and memory as well as neurological disease processes. To achieve its precise neural connectivity, the developing mammalian nervous system undergoes extensive activity-dependent synapse remodelling. Recently, microglial cells have been shown to be responsible for a portion of synaptic pruning, but the remaining mechanisms remain unknown. Here we report a new role for astrocytes in actively engulfing central nervous system synapses. This process helps to mediate synapse elimination, requires the MEGF10 and MERTK phagocytic pathways, and is strongly dependent on neuronal activity. Developing mice deficient in both astrocyte pathways fail to refine their retinogeniculate connections normally and retain excess functional synapses. Finally, we show that in the adult mouse brain, astrocytes continuously engulf both excitatory and inhibitory synapses. These studies reveal a novel role for astrocytes in mediating synapse elimination in the developing and adult brain, identify MEGF10 and MERTK as critical proteins in the synapse remodelling underlying neural circuit refinement, and have important implications for understanding learning and memory as well as neurological disease processes. This study describes comprehensive synaptic engulfment by astrocytes, mediating synapse elimination in an activity-dependent manner; this elimination process involves the MEGF10 and MERTK phagocytic pathways and persists into adulthood, with mutant mice that lack these pathways in astrocytes exhibiting a failure to refine retinogeniculate connections during development. Astrocytes involved in synapse elimination Synapse elimination is an important aspect of brain development in which the number of synaptic contacts is reduced in an activity-dependent manner. Glial cells -- non-neural cells that perform a variety of roles in the brain -- were recently shown to have a role in synapse remodelling, with the phagocytic microglia responsible for a certain proportion of connection refinement, with little else known regarding the mechanisms underlying this. Here, Won-Suk Chung et al. describe comprehensive synaptic engulfment by astrocytes, mediating synapse elimination in an activity-dependent manner. This elimination process involved the MEGF10 and MERTK phagocytic pathways, with transgenic animals lacking these pathways in astrocytes exhibiting a failure to refine retinogeniculate connections during development. These mechanisms also extend into adulthood. This work has implications for our understanding of learning and memory as well as neurological disease processes. To achieve its precise neural connectivity, the developing mammalian nervous system undergoes extensive activity-dependent synapse remodelling. Recently, microglial cells have been shown to be responsible for a portion of synaptic pruning, but the remaining mechanisms remain unknown. Here we report a new role for astrocytes in actively engulfing central nervous system synapses. This process helps to mediate synapse elimination, requires the MEGF10 and MERTK phagocytic pathways, and is strongly dependent on neuronal activity. Developing mice deficient in both astrocyte pathways fail to refine their retinogeniculate connections normally and retain excess functional synapses. Finally, we show that in the adult mouse brain, astrocytes continuously engulf both excitatory and inhibitory synapses. These studies reveal a novel role for astrocytes in mediating synapse elimination in the developing and adult brain, identify MEGF10 and MERTK as critical proteins in the synapse remodelling underlying neural circuit refinement, and have important implications for understanding learning and memory as well as neurological disease processes. [PUBLICATION ABSTRACT] To achieve its precise neural connectivity, the developing mammalian nervous system undergoes extensive activity-dependent synapse remodelling. Recently, microglial cells have been shown to be responsible for a portion of synaptic pruning, but the remaining mechanisms remain unknown. Here we report a new role for astrocytes in actively engulfing central nervous system synapses. This process helps to mediate synapse elimination, requires the MEGF10 and MERTK phagocytic pathways, and is strongly dependent on neuronal activity. Developing mice deficient in both astrocyte pathways fail to refine their retinogeniculate connections normally and retain excess functional synapses. Finally, we show that in the adult mouse brain, astrocytes continuously engulf both excitatory and inhibitory synapses. These studies reveal a novel role for astrocytes in mediating synapse elimination in the developing and adult brain, identify MEGF10 and MERTK as critical proteins in the synapse remodelling underlying neural circuit refinement, and have important implications for understanding learning and memory as well as neurological disease processes. This study describes comprehensive synaptic engulfment by astrocytes, mediating synapse elimination in an activity-dependent manner; this elimination process involves the MEGF10 and MERTK phagocytic pathways and persists into adulthood, with mutant mice that lack these pathways in astrocytes exhibiting a failure to refine retinogeniculate connections during development. Astrocytes involved in synapse elimination Synapse elimination is an important aspect of brain development in which the number of synaptic contacts is reduced in an activity-dependent manner. Glial cells — non-neural cells that perform a variety of roles in the brain — were recently shown to have a role in synapse remodelling, with the phagocytic microglia responsible for a certain proportion of connection refinement, with little else known regarding the mechanisms underlying this. Here, Won-Suk Chung et al . describe comprehensive synaptic engulfment by astrocytes, mediating synapse elimination in an activity-dependent manner. This elimination process involved the MEGF10 and MERTK phagocytic pathways, with transgenic animals lacking these pathways in astrocytes exhibiting a failure to refine retinogeniculate connections during development. These mechanisms also extend into adulthood. This work has implications for our understanding of learning and memory as well as neurological disease processes. To achieve its precise neural connectivity, the developing mammalian nervous system undergoes extensive activity-dependent synapse remodelling. Recently, microglial cells have been shown to be responsible for a portion of synaptic pruning, but the remaining mechanisms remain unknown. Here we report a new role for astrocytes in actively engulfing central nervous system synapses. This process helps to mediate synapse elimination, requires the MEGF10 and MERTK phagocytic pathways, and is strongly dependent on neuronal activity. Developing mice deficient in both astrocyte pathways fail to refine their retinogeniculate connections normally and retain excess functional synapses. Finally, we show that in the adult mouse brain, astrocytes continuously engulf both excitatory and inhibitory synapses. These studies reveal a novel role for astrocytes in mediating synapse elimination in the developing and adult brain, identify MEGF10 and MERTK as critical proteins in the synapse remodelling underlying neural circuit refinement, and have important implications for understanding learning and memory as well as neurological disease processes.To achieve its precise neural connectivity, the developing mammalian nervous system undergoes extensive activity-dependent synapse remodelling. Recently, microglial cells have been shown to be responsible for a portion of synaptic pruning, but the remaining mechanisms remain unknown. Here we report a new role for astrocytes in actively engulfing central nervous system synapses. This process helps to mediate synapse elimination, requires the MEGF10 and MERTK phagocytic pathways, and is strongly dependent on neuronal activity. Developing mice deficient in both astrocyte pathways fail to refine their retinogeniculate connections normally and retain excess functional synapses. Finally, we show that in the adult mouse brain, astrocytes continuously engulf both excitatory and inhibitory synapses. These studies reveal a novel role for astrocytes in mediating synapse elimination in the developing and adult brain, identify MEGF10 and MERTK as critical proteins in the synapse remodelling underlying neural circuit refinement, and have important implications for understanding learning and memory as well as neurological disease processes. To achieve its precise neural connectivity, the developing mammalian nervous system undergoes extensive activity-dependent synapse remodeling. Recently microglial cells have been shown to be responsible for a portion of synaptic remodeling, but the remaining mechanisms remain mysterious. Here we report a new role for astrocytes in actively engulfing CNS synapses. This process helps to mediate synapse elimination, requires the Megf10 and Mertk phagocytic pathways, and is strongly dependent on neuronal activity. Developing mice deficient in both astrocyte pathways fail to normally refine their retinogeniculate connections and retain excess functional synapses. Lastly, we show that in the adult mouse brain, astrocytes continuously engulf both excitatory and inhibitory synapses. These studies reveal a novel role for astrocytes in mediating synapse elimination in the developing and adult brain, identify Megf10 and Mertk as critical players in the synapse remodeling underlying neural circuit refinement, and have important implications for understanding learning and memory as well as neurological disease processes. |
| Audience | Academic |
| Author | Chakraborty, Chandrani Wang, Gordon X. Chen, Chinfei Foo, Lynette C. Smith, Stephen J. Clarke, Laura E. Joung, Julia Stafford, Benjamin K. Chung, Won-Suk Barres, Ben A. Sher, Alexander Thompson, Andrew |
| AuthorAffiliation | 2 Department of Molecular and Cellular Physiology, Stanford University, School of Medicine, Stanford, CA 94305, USA 3 Department of Ophthalmology and Visual Sciences, University of Michigan, Ann Arbor, MI 48105, USA 5 Institute of Molecular and Cell Biology, AStar, 61 Biopolis Drive, Proteos Building, Singapore 138673 4 Santa Cruz Institute of Particle Physic and Department of Physics, University of California, Santa Cruz, CA 95064 6 Children's Hospital, Harvard Medical School, 300 Longwood Ave., CLS12250, Boston, MA 02115 1 Department of Neurobiology, Stanford University, School of Medicine, Stanford, CA 94305, USA |
| AuthorAffiliation_xml | – name: 3 Department of Ophthalmology and Visual Sciences, University of Michigan, Ann Arbor, MI 48105, USA – name: 5 Institute of Molecular and Cell Biology, AStar, 61 Biopolis Drive, Proteos Building, Singapore 138673 – name: 1 Department of Neurobiology, Stanford University, School of Medicine, Stanford, CA 94305, USA – name: 4 Santa Cruz Institute of Particle Physic and Department of Physics, University of California, Santa Cruz, CA 95064 – name: 6 Children's Hospital, Harvard Medical School, 300 Longwood Ave., CLS12250, Boston, MA 02115 – name: 2 Department of Molecular and Cellular Physiology, Stanford University, School of Medicine, Stanford, CA 94305, USA |
| Author_xml | – sequence: 1 givenname: Won-Suk surname: Chung fullname: Chung, Won-Suk email: wschung@stanford.edu organization: Department of Neurobiology, Stanford University, School of Medicine – sequence: 2 givenname: Laura E. surname: Clarke fullname: Clarke, Laura E. organization: Department of Neurobiology, Stanford University, School of Medicine – sequence: 3 givenname: Gordon X. surname: Wang fullname: Wang, Gordon X. organization: Department of Molecular and Cellular Physiology, Stanford University, School of Medicine – sequence: 4 givenname: Benjamin K. surname: Stafford fullname: Stafford, Benjamin K. organization: Department of Ophthalmology and Visual Sciences, University of Michigan – sequence: 5 givenname: Alexander surname: Sher fullname: Sher, Alexander organization: Santa Cruz Institute of Particle Physic and Department of Physics, University of California – sequence: 6 givenname: Chandrani surname: Chakraborty fullname: Chakraborty, Chandrani organization: Department of Neurobiology, Stanford University, School of Medicine – sequence: 7 givenname: Julia surname: Joung fullname: Joung, Julia organization: Department of Neurobiology, Stanford University, School of Medicine – sequence: 8 givenname: Lynette C. surname: Foo fullname: Foo, Lynette C. organization: Institute of Molecular and Cell Biology, A Star, 61 Biopolis Drive, Proteos Building, 138673 Singapore – sequence: 9 givenname: Andrew surname: Thompson fullname: Thompson, Andrew organization: Children’s Hospital, Harvard Medical School, 300 Longwood Avenue, CLS12250, Boston, Massachusetts 02115, USA – sequence: 10 givenname: Chinfei surname: Chen fullname: Chen, Chinfei organization: Children’s Hospital, Harvard Medical School, 300 Longwood Avenue, CLS12250, Boston, Massachusetts 02115, USA – sequence: 11 givenname: Stephen J. surname: Smith fullname: Smith, Stephen J. organization: Department of Molecular and Cellular Physiology, Stanford University, School of Medicine – sequence: 12 givenname: Ben A. surname: Barres fullname: Barres, Ben A. organization: Department of Neurobiology, Stanford University, School of Medicine |
| BackLink | http://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=28051841$$DView record in Pascal Francis https://www.ncbi.nlm.nih.gov/pubmed/24270812$$D View this record in MEDLINE/PubMed |
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| CODEN | NATUAS |
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| Keywords | Neuroglia Memory Rodentia Central nervous system Nervous system Astrocyte Protein Encephalon Microglia Learning Vertebrata Synapse Acquisition process Mammalia Mouse Animal Development |
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| Snippet | To achieve its precise neural connectivity, the developing mammalian nervous system undergoes extensive activity-dependent synapse remodelling. Recently,... To achieve its precise neural connectivity, the developing mammalian nervous system undergoes extensive activity-dependent synapse remodeling. Recently... |
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| SubjectTerms | 13/1 13/106 13/31 13/51 14/19 14/28 631/378/2596/1308 64/110 9/74 Animals Astrocytes Astrocytes - cytology Astrocytes - metabolism Biological and medical sciences Brain - cytology c-Mer Tyrosine Kinase Cellular signal transduction Central nervous system Fundamental and applied biological sciences. Psychology Gene expression Health aspects Humanities and Social Sciences In Vitro Techniques Insects Kinases Laboratory animals Lateral Thalamic Nuclei - cytology Lateral Thalamic Nuclei - metabolism Learning - physiology Membrane Proteins - deficiency Membrane Proteins - genetics Membrane Proteins - metabolism Mice Mice, Transgenic Microscopy multidisciplinary Neural circuitry Neural Pathways - cytology Neural Pathways - metabolism Phagocytosis Physiological aspects Protein expression Proteins Proto-Oncogene Proteins - deficiency Proto-Oncogene Proteins - genetics Proto-Oncogene Proteins - metabolism Receptor Protein-Tyrosine Kinases - deficiency Receptor Protein-Tyrosine Kinases - genetics Receptor Protein-Tyrosine Kinases - metabolism Retina - physiology Science Synapses Synapses - metabolism Vertebrates: nervous system and sense organs |
| Title | Astrocytes mediate synapse elimination through MEGF10 and MERTK pathways |
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