The DOI matches its Crossref record; 33 of the 33 references it cites were found in a registry or an index.
Deficiency of the Microglial Receptor CX3CR1 Impairs Postnatal Functional Development of Thalamocortical Synapses in the Barrel Cortex
Open accessAbstract
Accumulative evidence indicates that microglial cells influence the normal development of brain synapses. Yet, the mechanisms by which these immune cells target maturating synapses and influence their functional development at early postnatal stages remain poorly understood. Here, we analyzed the role of CX3CR1, a microglial receptor activated by the neuronal chemokine CX3CL1 (or fractalkine) which controls key functions of microglial cells. In the whisker-related barrel field of the mouse somatosensory cortex, we show that the recruitment of microglia to the sites where developing thalamocortical synapses are concentrated (i.e., the barrel centers) occurs only after postnatal day 5 and is controlled by the fractalkine/CX3CR1 signaling pathway. Indeed, at this developmental stage fractalkine is overexpressed within the barrels and CX3CR1 deficiency delays microglial cell recruitment into the barrel centers. Functional analysis of thalamocortical synapses shows that CX3CR1 deficiency also delays the functional maturation of postsynaptic glutamate receptors which normally occurs at these synapses between the first and second postnatal week. These results show that reciprocal interactions between neurons and microglial cells control the functional maturation of cortical synapses.
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“KO mice lacking fractalkine receptor show transient excitatory hyperconnectivity followed by weak synaptic multiplicity and reduced functional brain connectivity in adulthood11,12, suggesting that a failure to eliminate synapses at the correct developmental time prevents the normal strengthening of synaptic connections.”
From Microglia remodel synapses by presynaptic trogocytosis and spine head filopodia induction (2018) · cites this paper as [12]
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Synaptic Pruning by Microglia Is Necessary for Normal Brain Development
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“…be that MGCs, once inside TCA clusters, could contribute to the selection of synapses with a mature signature of their glutamate receptors (Yashiro and Philpot, 2008) by pruning immature synapses through phagocytosis (Paolicelli et al., 2011) in a complement-dependent manner (Schafer et al., 2012).”
BackgroundMicroglia: Active sensor and versatile effector cells in the normal and pathologic brain
Hanisch, U.-K., & Kettenmann, H. (2007) · Nature Neuroscience · doi:10.1038/nn1997 · Cited by 3,676 · cited 1×
“In the diseased adult CNS, several signaling pathways control the recruitment of microglia at sites of compromised homeostasis (Hanisch and Kettenmann, 2007; Ransohoff and Perry, 2009).”
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“In few experiments heterozygous CX3CR1 /eGFP mice of either sex were obtained by crossing CX3CR1 eGFP/eGFP (Jung et al., 2000) with wild-type C57BL/6J mice (Janvier).”
BackgroundMethodInfluentialNeurotrophins and their receptors: A convergence point for many signalling pathways
Chao, M. V. (2003) · Nature Reviews Neuroscience · doi:10.1038/nrn1078 · Cited by 2,298
Microglial physiology: unique stimuli, specialized responses
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BackgroundControl of microglial neurotoxicity by the fractalkine receptor
Cardona, A. E., Pioro, E. P., Sasse, M. E., Kostenko, V., Cardona, S. M., Dijkstra, I. M., Huang, D., Kidd, G., Dombrowski, S., Dutta, R., et al. (2006) · Nature Neuroscience · doi:10.1038/nn1715 · Cited by 1,531 · cited 1×
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“…local role of fractalkine in which cellular elements localized within the barrel hollows, possibly thalamic fibers, overexpress the chemokine at P5–P7 and thus favor directed migration of microglia (Harrison et al., 1998; Maciejewski-Lenoir et al., 1999) toward maturating thalamocortical synapses.”
BackgroundResultThe Role of Microglia in the Healthy Brain: Figure 1.
Tremblay, M.-È., Stevens, B., Sierra, A., Wake, H., Bessis, A., & Nimmerjahn, A. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.4158-11.2011 · Cited by 992 · cited 1×
“In rodents, experimental evidence shows that MGCs contribute to developmentally regulated neuronal apoptosis but also to synapse pruning (Mallat et al., 2005; Pont-Lezica et al., 2011; Schlegelmilch et al., 2011; Tremblay et al., 2011).”
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“MGC occupancy along with aspects of synaptic pruning/maturation are delayed in developing barrel fields (Hoshiko et al., 2012) and hippocampus (Paolicelli et al.”
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“Furthermore, similar findings have been observed that the immune-related complement proteins or CX3CR1 receptor expressed on microglia have important impacts on the synapse dysfunction(Hoshiko et al., 2012; Schafer et al., 2012).”
Segregation of Multimodal Inputs Into Discrete Midbrain Compartments During an Early Critical Period
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“…environmental stimulation to develop properly, such as the retinogeniculate system (Li et al., 2019; Schafer et al., 2012; Stevens et al., 2007), the barrel cortex (Hoshiko et al., 2012), somatosensory system (Miyamoto et al., 2016), and hippocampus (Paolicelli et al., 2011; Weinhard et al., 2018).”
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Non-invasive light flickering reinstates visual plasticity in adult mice via lipocalin 2
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Mendóza, R., Santos, J. M., Liu, X., Elmassry, M. M., Ji, G., Kiritoshi, T., Neugebauer, V., & Shen, C. (2026) · Molecules · doi:10.3390/molecules31010166 · Cited by 3
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Sadakata, M., Fujii, K., Kaneko, R., Hosoya, E., Sugimoto, H., Kawabata‐Iwakawa, R., Kasamatsu, T., Hongo, S., Koshidaka, Y., Takase, A., et al. (2024) · Journal of Neuroinflammation · doi:10.1186/s12974-024-03100-z · Cited by 4
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“24,30,45 The fractalkine ligand is developmentally regulated on OPCs, 46 and we published that fractalkine receptor signaling decreased microglia engulfment of OPCs in the developing corpus callosum.”
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CX3CR1 Does Not Universally Mediate Microglia-Neuron Crosstalk during Synaptic Plasticity
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“(2017) replicated previous work (Hoshiko et al., 2012) showing a transient delay in the entry of microglia into thalamocortical axon clusters in somatosensory cortex of Cx3cr1 KO mice.”
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BackgroundMicroglia contribute to excitatory synapse formation in developing mouse neocortex
Miyamoto, A. (2014) · SOKENDAI (Graduate University for Advanced Studies)
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“On the other hand, any insult that affects neuronal integrity and interrupts these signals, or even the lack of expression of these ligands in neurons is recognized by the microglia as a “eat me” signal and, therefore, triggers the activation of the microglia and promoting phagocytosis of neurons [54-56].”
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“54 These developmental changes in the features of the barrel cells and barrel cortex L4 may affect the stability and/or NMDAR-de-pendency of the barrel-cell dendritic patterns.”
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Additional file 1 of Maternal immunoglobulin G affects brain development of mouse offspring
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Metadata
- Authors
- Hoshiko, M., Arnoux, I., Avignone, E., Yamamoto, N., & Audinat, E.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- The University of Osaka (JP)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2012-10-24
- Volume
- 32
- Issue
- 43
- Pages
- 15106-15111
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6704837
- OpenAlex
- W1996055705
- Cited by
- 384
- References
- 33
- Citations by year
- 2026: 12 · 2025: 22 · 2024: 36 · 2023: 29 · 2022: 40 · 2021: 41 · 2020: 35 · 2019: 39 · 2018: 30 · 2017: 23 · 2016: 19 · 2015: 14 · 2014: 22 · 2013: 22
- FWCI
- 9.33
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Funders
- Uehara Memorial Foundation
- Ministry of Education, Culture, Sports, Science and Technology (23115102)
- Japan Society for the Promotion of Science (20021018)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- CX3CR1, fractalkine, microglia, synapse maturation, thalamocortical synapses, barrel cortex, postnatal development, microglial recruitment, glutamate receptors, microglia-neuron interaction, somatosensory cortex
- MeSH terms
- CX3C Chemokine Receptor 1, Age Factors, Animals, Animals, Newborn, Developmental Disabilities, Electric Stimulation, Female, Male, Mice, Inbred C57BL, Mice, Transgenic, Somatosensory Cortex, Synapses, Thalamus, Microglia, Gene Expression Regulation, Developmental, Excitatory Amino Acid Antagonists, Statistics, Nonparametric, GABA Antagonists, Excitatory Postsynaptic Potentials, Receptors, Chemokine, Green Fluorescent Proteins, Serotonin Plasma Membrane Transport Proteins, Mice, Chemokine CX3CL1, In Vitro Techniques
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