Oligodendrocyte precursor cells engulf synapses during circuit remodeling in mice

Auguste, Yohan S. S.; Ferro, Austin; Kahng, Jessica A.; Xavier, André Machado; Dixon, Jessica R.; Vrudhula, Uma; Nichitiu, Anne-Sarah; Rosado, Daniele; Wee, Tse-Luen; Pedmale, Ullas V.; Cheadle, Lucas

doi:10.1038/s41593-022-01170-x

Cited by 74 publications

(51 citation statements)

References 24 publications

(33 reference statements)

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“…One should recognize that synaptic transmission is no longer unique to neurons but also involves mutual crosstalk between glial cells and neurons at the synaptic level in the control of brain functions. Recently, Auguste et al reported that OPCs engulf thalamocortical synapses in the developing and adult mouse visual cortex and that such OPC‐mediated synapse elimination is beneficial to sensory experience during neural circuit refinement, indicating that diverse functions of OPCs are constantly being revealed (Auguste et al, 2022). Thus, glia, as indispensable neural cells in the brain, play crucial roles in neuronal circuitry and actively modulate synaptic transmission under both physiological and pathological conditions including, among many others, neurodegenerative, mood, and memory disorders.…”

Section: Discussionmentioning

confidence: 99%

Interactions of glial cells with neuronal synapses, from astrocytes to microglia and oligodendrocyte lineage cells

Liu

Shen

Zhang

et al. 2023

Glia

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The mammalian brain is a complex organ comprising neurons, glia, and more than 1 × 1014 synapses. Neurons are a heterogeneous group of electrically active cells, which form the framework of the complex circuitry of the brain. However, glial cells, which are primarily divided into astrocytes, microglia, oligodendrocytes (OLs), and oligodendrocyte precursor cells (OPCs), constitute approximately half of all neural cells in the mammalian central nervous system (CNS) and mainly provide nutrition and tropic support to neurons in the brain. In the last two decades, the concept of “tripartite synapses” has drawn great attention, which emphasizes that astrocytes are an integral part of the synapse and regulate neuronal activity in a feedback manner after receiving neuronal signals. Since then, synaptic modulation by glial cells has been extensively studied and substantially revised. In this review, we summarize the latest significant findings on how glial cells, in particular, microglia and OL lineage cells, impact and remodel the structure and function of synapses in the brain. Our review highlights the cellular and molecular aspects of neuron‐glia crosstalk and provides additional information on how aberrant synaptic communication between neurons and glia may contribute to neural pathologies.

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Section: Discussionmentioning

confidence: 99%

Interactions of glial cells with neuronal synapses, from astrocytes to microglia and oligodendrocyte lineage cells

Liu

Shen

Zhang

et al. 2023

Glia

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“…Alternatively, or in addition, enhanced OLP proliferation and the consequent increase in OLP population density, which persisted for at least 2 weeks post-training in the white matter, might itself lead to improved cognitive performance. There are reports that immature OL lineage cells in zebrafish (Marisca et al, 2020;Xiao et al, 2022) and mice (Buchanan et al, 2021;Auguste et al, 2022) can exert effects on neurons that are unrelated to myelination, including synaptic pruning by OLPs (Buchanan et al, 2021;Auguste et al, 2022). It is conceivable that such non-canonical effects could have a lasting impact on neural circuitry even if the responsible OL lineage cells are eventually eliminated.…”

Section: Discussionmentioning

confidence: 99%

Oligodendrocyte dynamics dictate individual performance outcomes of working memory training in mice

Shimizu

Nayar

Swire

et al. 2023

Preprint

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Motor skill learning stimulates and requires generation of myelinating oligodendrocytes (OLs) from their precursors. We asked whether OL production is also required for non- motor learning and cognition, using T-maze and radial arm maze tasks that tax spatial working memory. Maze training stimulated OL production in the medial prefrontal cortex, anterior corpus callosum (genu), hippocampus and fimbria; myelin sheath formation was also stimulated in the genu. Genetic blockade of OL differentiation and neo-myelination in Myrf conditional knockout mice strongly impaired training-induced improvements in maze performance. Remarkably, working memory performance of individual mice correlated closely with the scale of OL precursor proliferation and OL generation in their genu and anterior cingulate cortex during training, indicating a key role for adaptive OL genesis and myelination in cognitive processing.

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“…Both NPCs and OPCs can also act as phagocytes. Dcx + (Doublecortin) neuroblasts, which are derived from NPCs and represent committed proliferative progenitors that are destined to differentiate into neurons, phagocytose dead neurons, whereas OPCs can phagocytose myelin debris and prune synapses; properties typically attributed to microglia and macrophages (Lu et al, 2011;Falcão et al, 2018;Auguste et al, 2022). NPCs and OPCs also directly react to frontiersin.org de Almeida et al 10.3389/fncel.2023.1130205 neuroinflammatory environment through chemokine and cytokine receptors that they express, and actively participate in modulating the inflammatory environment by secreting chemokines and cytokines (Watson et al, 2020(Watson et al, , 2021Belenguer et al, 2021;Shariq et al, 2021;Willis et al, 2022;Dittmann et al, 2023).…”

Section: "Immune" Roles Of Npcs In Cns Development and Regenerationmentioning

confidence: 99%

Regulation of microglia function by neural stem cells

Almeida

Goodkey

Voronova

2023

Front. Cell. Neurosci.

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Neural stem and precursor cells (NPCs) build and regenerate the central nervous system (CNS) by maintaining their pool (self-renewal) and differentiating into neurons, astrocytes, and oligodendrocytes (multipotency) throughout life. This has inspired research into pro-regenerative therapies that utilize transplantation of exogenous NPCs or recruitment of endogenous adult NPCs for CNS regeneration and repair. Recent advances in single-cell RNA sequencing and other “omics” have revealed that NPCs express not just traditional progenitor-related genes, but also genes involved in immune function. Here, we review how NPCs exert immunomodulatory function by regulating the biology of microglia, immune cells that are present in NPC niches and throughout the CNS. We discuss the role of transplanted and endogenous NPCs in regulating microglia fates, such as survival, proliferation, migration, phagocytosis and activation, in the developing, injured and degenerating CNS. We also provide a literature review on NPC-specific mediators that are responsible for modulating microglia biology. Our review highlights the immunomodulatory properties of NPCs and the significance of these findings in the context of designing pro-regenerative therapies for degenerating and diseased CNS.

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Oligodendrocyte precursor cells engulf synapses during circuit remodeling in mice

Cited by 74 publications

References 24 publications

Interactions of glial cells with neuronal synapses, from astrocytes to microglia and oligodendrocyte lineage cells

Interactions of glial cells with neuronal synapses, from astrocytes to microglia and oligodendrocyte lineage cells

Oligodendrocyte dynamics dictate individual performance outcomes of working memory training in mice

Regulation of microglia function by neural stem cells

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