Ucp2-dependent microglia-neuronal coupling controls ventral hippocampal circuit function and anxiety-like behavior

Microglia have been implicated in synapse remodeling by phagocytosis of synaptic elements in the adult brain, but the mechanisms involved in the regulation of this process are ill-defined. By examining microglia-neuronal interaction in the ventral hippocampus, we found a significant reduction in spi...

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Published inMolecular psychiatry Vol. 26; no. 7; pp. 2740 - 2752
Main Authors Yasumoto, Yuki, Stoiljkovic, Milan, Kim, Jung Dae, Sestan-Pesa, Matija, Gao, Xiao-Bing, Diano, Sabrina, Horvath, Tamas L.
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.07.2021
Nature Publishing Group
Subjects
14/28
631/378
631/80
64/60
9/74
Animal cognition
Animals
Antibodies
Anxiety
Behavior
Behavioral Sciences
Biological Psychology
Brain
Care and treatment
Diagnosis
Electrophysiology
Female
Gene expression
Health aspects
Hippocampus
Immediate Communication
Laboratory animals
Male
Medicine
Medicine & Public Health
Mice
Mice, Knockout
Microglia
Microscopy
Mitochondria
Mitochondrial uncoupling protein 2
Neural Pathways
Neurons
Neurosciences
Parahippocampal region
Phagocytes
Phagocytosis
Pharmacotherapy
Physiological aspects
Psychiatry
Reactive oxygen species
Synapses
Uncoupling Protein 2 - genetics
United States
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Abstract Microglia have been implicated in synapse remodeling by phagocytosis of synaptic elements in the adult brain, but the mechanisms involved in the regulation of this process are ill-defined. By examining microglia-neuronal interaction in the ventral hippocampus, we found a significant reduction in spine synapse number during the light phase of the light/dark cycle accompanied by increased microglia-synapse contacts and an elevated amount of microglial phagocytic inclusions. This was followed by a transient rise in microglial production of reactive oxygen species (ROS) and a concurrent increase in expression of uncoupling protein 2 ( Ucp2 ), a regulator of mitochondrial ROS generation. Conditional ablation of Ucp2 from microglia hindered phasic elimination of spine synapses with consequent accumulations of ROS and lysosome-lipid droplet complexes, which resulted in hippocampal neuronal circuit dysfunctions assessed by electrophysiology, and altered anxiety-like behavior. These observations unmasked a novel and chronotypical interaction between microglia and neurons involved in the control of brain functions.
AbstractList Microglia have been implicated in synapse remodeling by phagocytosis of synaptic elements in the adult brain, but the mechanisms involved in the regulation of this process are ill-defined. By examining microglia-neuronal interaction in the ventral hippocampus, we found a significant reduction in spine synapse number during the light phase of the light/dark cycle accompanied by increased microglia-synapse contacts and an elevated amount of microglial phagocytic inclusions. This was followed by a transient rise in microglial production of reactive oxygen species (ROS) and a concurrent increase in expression of uncoupling protein 2 (Ucp2), a regulator of mitochondrial ROS generation. Conditional ablation of Ucp2 from microglia hindered phasic elimination of spine synapses with consequent accumulations of ROS and lysosome-lipid droplet complexes, which resulted in hippocampal neuronal circuit dysfunctions assessed by electrophysiology, and altered anxiety-like behavior. These observations unmasked a novel and chronotypical interaction between microglia and neurons involved in the control of brain functions.
Microglia have been implicated in synapse remodeling by phagocytosis of synaptic elements in the adult brain, but the mechanisms involved in the regulation of this process are ill-defined. By examining microglia-neuronal interaction in the ventral hippocampus, we found a significant reduction in spine synapse number during the light phase of the light/dark cycle accompanied by increased microglia-synapse contacts and an elevated amount of microglial phagocytic inclusions. This was followed by a transient rise in microglial production of reactive oxygen species (ROS) and a concurrent increase in expression of uncoupling protein 2 ( Ucp2 ), a regulator of mitochondrial ROS generation. Conditional ablation of Ucp2 from microglia hindered phasic elimination of spine synapses with consequent accumulations of ROS and lysosome-lipid droplet complexes, which resulted in hippocampal neuronal circuit dysfunctions assessed by electrophysiology, and altered anxiety-like behavior. These observations unmasked a novel and chronotypical interaction between microglia and neurons involved in the control of brain functions.
Microglia have been implicated in synapse remodeling by phagocytosis of synaptic elements in the adult brain, but the mechanisms involved in the regulation of this process are ill-defined. By examining microglia-neuronal interaction in the ventral hippocampus, we found a significant reduction in spine synapse number during the light phase of the light/dark cycle accompanied by increased microglia-synapse contacts and an elevated amount of microglial phagocytic inclusions. This was followed by a transient rise in microglial production of reactive oxygen species (ROS) and a concurrent increase in expression of uncoupling protein 2 (Ucp2), a regulator of mitochondrial ROS generation. Conditional ablation of Ucp2 from microglia hindered phasic elimination of spine synapses with consequent accumulations of ROS and lysosome-lipid droplet complexes, which resulted in hippocampal neuronal circuit dysfunctions assessed by electrophysiology, and altered anxiety-like behavior. These observations unmasked a novel and chronotypical interaction between microglia and neurons involved in the control of brain functions.Microglia have been implicated in synapse remodeling by phagocytosis of synaptic elements in the adult brain, but the mechanisms involved in the regulation of this process are ill-defined. By examining microglia-neuronal interaction in the ventral hippocampus, we found a significant reduction in spine synapse number during the light phase of the light/dark cycle accompanied by increased microglia-synapse contacts and an elevated amount of microglial phagocytic inclusions. This was followed by a transient rise in microglial production of reactive oxygen species (ROS) and a concurrent increase in expression of uncoupling protein 2 (Ucp2), a regulator of mitochondrial ROS generation. Conditional ablation of Ucp2 from microglia hindered phasic elimination of spine synapses with consequent accumulations of ROS and lysosome-lipid droplet complexes, which resulted in hippocampal neuronal circuit dysfunctions assessed by electrophysiology, and altered anxiety-like behavior. These observations unmasked a novel and chronotypical interaction between microglia and neurons involved in the control of brain functions.
Audience Academic
Author Kim, Jung Dae
Horvath, Tamas L.
Yasumoto, Yuki
Sestan-Pesa, Matija
Gao, Xiao-Bing
Stoiljkovic, Milan
Diano, Sabrina
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Snippet Microglia have been implicated in synapse remodeling by phagocytosis of synaptic elements in the adult brain, but the mechanisms involved in the regulation of...
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SubjectTerms 14/28
631/378
631/80
64/60
9/74
Animal cognition
Animals
Antibodies
Anxiety
Behavior
Behavioral Sciences
Biological Psychology
Brain
Care and treatment
Diagnosis
Electrophysiology
Female
Gene expression
Health aspects
Hippocampus
Immediate Communication
Laboratory animals
Male
Medicine
Medicine & Public Health
Mice
Mice, Knockout
Microglia
Microscopy
Mitochondria
Mitochondrial uncoupling protein 2
Neural Pathways
Neurons
Neurosciences
Parahippocampal region
Phagocytes
Phagocytosis
Pharmacotherapy
Physiological aspects
Psychiatry
Reactive oxygen species
Synapses
Uncoupling Protein 2 - genetics
Title Ucp2-dependent microglia-neuronal coupling controls ventral hippocampal circuit function and anxiety-like behavior
URI https://link.springer.com/article/10.1038/s41380-021-01105-1
https://www.ncbi.nlm.nih.gov/pubmed/33879866
https://www.proquest.com/docview/2580805677
https://www.proquest.com/docview/2516223387
https://pubmed.ncbi.nlm.nih.gov/PMC8056795
Volume 26
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