Cited by 335Neuroinflammation and Neurodegeneration MechanismsNeuroscience and Neuropharmacology ResearchRetinal Imaging and Analysis

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Microglial Morphology and Dynamic Behavior Is Regulated by Ionotropic Glutamatergic and GABAergic Neurotransmission

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Fontainhas, Aurora M., Wang, Minhua, Liang, Katharine J., Chen, Shan, Mettu, Pradeep, Damani, Mausam, Fariss, Robert N., Li, Wei, Wong, Wai T.·2011·PLoS ONE

DOI 10.1371/journal.pone.0015973PMC PMC3026789

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Abstract

PURPOSE: Microglia represent the primary resident immune cells in the CNS, and have been implicated in the pathology of neurodegenerative diseases. Under basal or "resting" conditions, microglia possess ramified morphologies and exhibit dynamic surveying movements in their processes. Despite the prominence of this phenomenon, the function and regulation of microglial morphology and dynamic behavior are incompletely understood. We investigate here whether and how neurotransmission regulates "resting" microglial morphology and behavior. METHODS: We employed an ex vivo mouse retinal explant system in which endogenous neurotransmission and dynamic microglial behavior are present. We utilized live-cell time-lapse confocal imaging to study the morphology and behavior of GFP-labeled retinal microglia in response to neurotransmitter agonists and antagonists. Patch clamp electrophysiology and immunohistochemical localization of glutamate receptors were also used to investigate direct-versus-indirect effects of neurotransmission by microglia. RESULTS: Retinal microglial morphology and dynamic behavior were not cell-autonomously regulated but are instead modulated by endogenous neurotransmission. Morphological parameters and process motility were differentially regulated by different modes of neurotransmission and were increased by ionotropic glutamatergic neurotransmission and decreased by ionotropic GABAergic neurotransmission. These neurotransmitter influences on retinal microglia were however unlikely to be directly mediated; local applications of neurotransmitters were unable to elicit electrical responses on microglia patch-clamp recordings and ionotropic glutamatergic receptors were not located on microglial cell bodies or processes by immunofluorescent labeling. Instead, these influences were mediated indirectly via extracellular ATP, released in response to glutamatergic neurotransmission through probenecid-sensitive pannexin hemichannels. CONCLUSIONS: Our results demonstrate that neurotransmission plays an endogenous role in regulating the morphology and behavior of "resting" microglia in the retina. These findings illustrate a mode of constitutive signaling between the neural and immune compartments of the CNS through which immune cells may be regulated in concert with levels of neural activity.

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Authors: Fontainhas, A. M., Wang, M., Liang, K. J., Chen, S., Mettu, P., Damani, M., Fariss, R. N., Li, W., & Wong, W. T.
Affiliations: National Institutes of Health (US)
Corresponding author: Wong, Wai T.
ORCID: Liang, Katharine J.
Chen, Shan
Fariss, Robert N.
Wong, Wai T.
Venue: PLoS ONE
Publisher: Public Library of Science (PLoS)
Published: 2011-01-25
Volume: 6
Issue: 1
Pages: e15973
ISSN: 1932-6203 (ISSN-L)
DOI: 10.1371/journal.pone.0015973
PMC: PMC3026789
OpenAlex: W1997602206
Cited by: 334
References: 57
Citations by year: 2026: 8 · 2025: 12 · 2024: 15 · 2023: 18 · 2022: 20 · 2021: 44 · 2020: 30 · 2019: 28 · 2018: 19 · 2017: 27 · 2016: 28 · 2015: 21 · 2014: 20 · 2013: 24 · 2012: 12
FWCI: 11.32
Type: journal article
Language: en
Open access: gold
doi.org
Licence: public-domain
creativecommons.org/publicdomain/zero/1.0/ (unspecified)
Locations: PLoS ONE (publishedVersion, public-domain)
PubMed Central (publishedVersion, public-domain)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Figshare (submittedVersion, cc-by)
Funders: National Eye Institute
Topics: Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Retinal Imaging and Analysis
Keywords: microglia, microglial morphology, microglial motility, resting microglia, retinal microglia, extracellular ATP, glutamate receptors, neuroimmune signaling, neurodegenerative diseases
MeSH terms: Animals, Immune System, Synaptic Transmission, Retina, Microglia, Receptors, GABA, Microscopy, Video, Cell Shape, Green Fluorescent Proteins, Mice, Receptors, Ionotropic Glutamate, In Vitro Techniques

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Microglial Morphology and Dynamic Behavior Is Regulated by Ionotropic Glutamatergic and GABAergic Neurotransmission

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