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Sensory lesioning induces microglial synapse elimination via ADAM10 and fractalkine signaling

ABSTRACT: Single-cell (inDrops) analysis of primary somatosensory cortex after early postnatal unilateral whisker lesioning

ORGANISM(S): Mus musculus

PROVIDER: GSE129150 | GEO | 2019/04/02

REPOSITORIES: GEO

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Sensory lesioning induces microglial synapse elimination via ADAM10 and fractalkine signaling

Project description:Sensory lesioning induces microglial synapse elimination via ADAM10 and fractalkine signaling

| PRJNA530236 | ENA

Sensory lesioning induces microglial synapse elimination via ADAM10 and fractalkine signaling.

Project description:Microglia rapidly respond to changes in neural activity and inflammation to regulate synaptic connectivity. The extracellular signals, particularly neuron-derived molecules, that drive these microglial functions at synapses remain a key open question. Here we show that whisker lesioning, known to dampen cortical activity, induces microglia-mediated synapse elimination. This synapse elimination is dependent on signaling by CX3CR1, the receptor for microglial fractalkine (also known as CXCL1), but not complement receptor 3. Furthermore, mice deficient in CX3CL1 have profound defects in synapse elimination. Single-cell RNA sequencing revealed that Cx3cl1 is derived from cortical neurons, and ADAM10, a metalloprotease that cleaves CX3CL1 into a secreted form, is upregulated specifically in layer IV neurons and in microglia following whisker lesioning. Finally, inhibition of ADAM10 phenocopies Cx3cr1-/- and Cx3cl1-/- synapse elimination defects. Together, these results identify neuron-to-microglia signaling necessary for cortical synaptic remodeling and reveal that context-dependent immune mechanisms are utilized to remodel synapses in the mammalian brain.

| S-EPMC6596419 | biostudies-literature

Microglia-astrocyte crosstalk regulates synapse remodeling via Wnt signaling

Project description:Unilateral whisker lesioning at age P4 leads to removal of thalamocortical synapses in layer IV of the barrel cortex over the course of the next 6 days. Synapse removal is mediated by microglia and induced by CX3CL1-CX3CR1 signaling between neurons and microglia. Downstream of CX3CL1-CX3CR1 activation, microglia induce astrocyte morphological changes and activation of canonical Wnt signaling in astrocytes. To explore the spatial pattern of microglia Wnt ligand expression and astrocyte Wnt receptor expression in astrocytes, we analyzed coronal sections containing the barrel cortex from 4 wild-type mice and 4 CX3CL1 knockout mice at 24 hours after whisker lesioning by multiplexed error-robust fluorescent in situ hybridization (MERFISH).

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Microglia-astrocyte crosstalk regulates synapse remodeling via Wnt signaling

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Vascular and perivascular cell profiling reveals the molecular and cellular bases of blood-brain barrier heterogeneity [scRNA-Seq]

Project description:Single cell (inDrops) RNA sequencing analysis of median eminence and somatosensory cortex in male, wild type mice

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Single-Cell Analysis of Sensory Experience Regulated Gene Expression in Mouse Visual Cortex

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A prenatal window for enhancing spatial resolution of cortical barrel maps

Project description:Precise mapping of peripheral inputs onto cortical areas is essential for accurate sensory processing. In the mouse primary somatosensory cortex, mystacial whiskers correspond to large, well-defined barrels, while upper lip whiskers form smaller, less distinct barrels. These differences are traditionally attributed to variations in whisker input type and receptor density, but prenatal activity and transcriptional programs also impact somatosensory map development independently of sensory experience. Here, we demonstrate that prenatal ablation of mystacial whiskers leads to a remapping of cortical territories, enhancing the functional and anatomical definition of upper lip whisker barrels. This reorganization occurs without altering peripheral receptor types. Instead, thalamic neurons that receive upper lip inputs adopt a mystacial-like transcriptional profile. Our findings unveil a regulated prenatal mechanism in the thalamus that ensures sufficient cortical barrel size and spatial resolution for sensory processing, irrespective of peripheral receptor type or density, highlighting a critical developmental process in sensory mapping.

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Schwann cell-secreted PGE2 promotes sensory neuron excitability during development [scRNAseq_Dataset1]

Project description:Electrical excitability—the ability to fire and propagate action potentials—is a signature feature of neurons. How neurons become excitable during development and whether excitability is an intrinsic property of neurons or requires signaling from glial cells remain unclear. Here, we demonstrate that Schwann cells, the most abundant glia in the peripheral nervous system, promote somatosensory neuron excitability during development. We find that Schwann cells secrete prostaglandin E2, which is necessary and sufficient to induce developing somatosensory neurons to express normal levels of genes required for neuronal function, including voltage gated sodium channels, and to fire action potential trains. In this scRNAseq study, we found that inactivating PGE2 synthesis in Schwann cells in vivo impaired somatosensory neuron maturation, with the most dramatic effects on nociceptor and proprioceptor somatosensory neuron subtypes.

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Schwann cell-secreted PGE2 promotes sensory neuron excitability during development [scRNAseq_Dataset2]

Project description:Electrical excitability—the ability to fire and propagate action potentials—is a signature feature of neurons. How neurons become excitable during development and whether excitability is an intrinsic property of neurons or requires signaling from glial cells remain unclear. Here, we demonstrate that Schwann cells, the most abundant glia in the peripheral nervous system, promote somatosensory neuron excitability during development. We find that Schwann cells secrete prostaglandin E2, which is necessary and sufficient to induce developing somatosensory neurons to express normal levels of genes required for neuronal function, including voltage gated sodium channels, and to fire action potential trains. In this scRNAseq study, we found that inactivating PGE2 synthesis in Schwann cells, in vivo, impaired somatosensory neuron maturation, with the most dramatic effects on nociceptor and proprioceptor somatosensory neuron subtypes.

2024-06-03 | GSE268625 | GEO

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