Colony-Stimulating Factor 1 Receptor Signaling Is Necessary for Microglia Viability, Unmasking a Microglia Progenitor Cell in the Adult Brain
Open accessAbstract
The colony-stimulating factor 1 receptor (CSF1R) is a key regulator of myeloid lineage cells. Genetic loss of the CSF1R blocks the normal population of resident microglia in the brain that originates from the yolk sac during early development. However, the role of CSF1R signaling in microglial homeostasis in the adult brain is largely unknown. To this end, we tested the effects of selective CSF1R inhibitors on microglia in adult mice. Surprisingly, extensive treatment results in elimination of ∼99% of all microglia brain-wide, showing that microglia in the adult brain are physiologically dependent upon CSF1R signaling. Mice depleted of microglia show no behavioral or cognitive abnormalities, revealing that microglia are not necessary for these tasks. Finally, we discovered that the microglia-depleted brain completely repopulates with new microglia within 1 week of inhibitor cessation. Microglial repopulation throughout the CNS occurs through proliferation of nestin-positive cells that then differentiate into microglia.
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After inhibiting CSF-1R, the resident microglia display elevated proliferation and inflammation markers.
“In addition, it was reported that after inhibiting CSF-1R, the resident microglia display elevated proliferation and inflammation markers (64, 65)”
From Arresting the bad seed: HDAC3 regulates proliferation of different microglia after ischemic stroke (2024) · cites this paper as [65]
In Results (‘CSF1R inhibitors dramatically reduce microglia numbers in the adult brain’; page unavailable), inhibition prevented an LPS-induced increase in the inflammatory marker IBA1 and markedly reduced microglial numbers. Results (‘Rapid restoration of CNS microglia following drug removal’; page unavailable) place the proliferation marker Ki67 in newly repopulating cells after inhibitor withdrawal, not in resident microglia during inhibition. (LLM, conf=0.88)
Checked by a reasoning model — may be wrong.
Experimental — accuracy not yet measuredTgfbr2 and Csf1r play an essential signaling role in microglia development, with absence or inhibition causing marked reduction or complete absence of microglia.
“Tgfbr2 and Csf1r have also been demonstrated to play an essential signaling role in microglia development, where the absence of these genes or inhibition of their signaling shows marked reduction or complete absence of microglia”
From Cross-Species Single-Cell Analysis Reveals Divergence of the Primate Microglia Program (2019) · cites this paper as Elmore et al., 2014
The Introduction (page not provided) says microglial development depends on CSF1R and that CSF1R-knockout mice are devoid of microglia. The Discussion reports that CSF1R inhibition eliminates virtually all microglia in the adult CNS. Our copy does not support the claim about Tgfbr2; searches for Tgfbr2 and transforming growth factor beta receptor 2 found no relevant passage. (LLM, conf=0.90)
Experimental — accuracy not yet measuredPLX treatment near completely eliminates microglia in the healthy brain after about 1 week, and cessation of PLX treatment is followed by a rapid rebound in microglia numbers after about 1 week.
“Treatment with PLX is a highly effective and well tolerated strategy, with near complete elimination of microglia in the healthy brain after ~ 1 week. Cessation of PLX treatment is followed by a rapid (~ 1 week) rebound in microglia numbers.”
From Activated microglia drive demyelination via <scp>CSF1R</scp> signaling (2021) · cites this paper as Monica R. P. Elmore et al., 2014
The Results sections on early repopulation and rapid restoration report that microglia rebound after PLX3397 withdrawal, exceeding control numbers by seven days in aged mice. But the seven-day treatment experiment eliminated about 70% of microglia, not nearly all; the paper reports essentially microglia-devoid brains after 21 days of treatment. The claimed timing of near-complete elimination is therefore not supported. (LLM, conf=0.88)
Experimental — accuracy not yet measuredWithdrawal of PLX5622 treatment results in rapid and robust repopulation of microglia via self-renewal.
“Withdrawal of PLX5622 treatment is known to result in a rapid and robust repopulation of microglia via self-renewal (28, 29)”
From Microglia depletion exacerbates demyelination and impairs remyelination in a neurotropic coronavirus infection (2020) · cites this paper as [28]
The Results section, “Early microglial repopulation events,” reports rapid repopulation after withdrawal of PLX3397, not PLX5622. The Results section, “Surviving microglia cannot solely account for repopulation,” says surviving microglia alone cannot explain it and points to a CNS progenitor cell; thus the claimed self-renewal mechanism is not fully supported. (LLM, conf=0.90)
Experimental — accuracy not yet measuredCSF-1, IL-34, and TGF-β1 have been shown to play important roles in microglial proliferation and/or survival.
“because these cytokines have been shown to play important roles in microglial proliferation and/or survival [43, 44].”
From IL-1β-driven amyloid plaque clearance is associated with an expansion of transcriptionally reprogrammed microglia (2019) · cites this paper as [44]
The Discussion ('Dependence of microglia on CSF1R signaling in the adult brain'; page not supplied) reports reduced microglial densities in mice lacking CSF-1 or IL-34 and finds that adult microglia depend on CSF1R signaling for survival. Our copy does not establish a role for TGF-β1 in microglial proliferation or survival; its References list a TGF-β1 study concerning macrophages instead. (LLM, conf=0.88)
Experimental — accuracy not yet measured
The microglia population is rapidly reconstituted by resident cells after genetic or pharmacological ablation of microglia.
“the microglia population was found to be rapidly reconstituted by resident cells after genetic or pharmacological ablation of microglia (Bruttger et al., 2015; Elmore et al., 2014).”
From Pu.1/Spi1 dosage controls the turnover and maintenance of microglia in zebrafish and mammals (2025) · cites this paper as Elmore et al., 2014
Unlike non-plaque-associated or PU.1high plaque-associated microglia, the PU.1low subpopulation appears independent of the activity of the essential microglial survival receptor CSF1R.
“Unlike non-plaque-associated (distal microglia; Extended Data Fig. 1b) or PU.1high plaque-associated microglia, this subpopulation appears independent of the activity of the essential microglial survival receptor CSF1R26,27 (Fig. 1d,e and Extended Data Fig. 1b–d).”
From Lymphoid gene expression supports neuroprotective microglia function (2025) · cites this paper as [26]
Previous studies identified the capacity of microglia to repopulate following experimental depletion in healthy, aged, irradiated, or neurodegenerating brain, but this feature can also serve to reinstate microglia after naturally occurring death following white matter injury, while regulating microglia activation.
“Although previous studies identified the capacity of microglia to repopulate following experimental depletion in healthy13–15, aged17, irradiated18, or neurodegenerating brain19, we show that this feature can also serve to reinstate microglia after naturally occurring death following white matter injury, while regulating microglia activation.”
From Central nervous system regeneration is driven by microglia necroptosis and repopulation (2019) · cites this paper as [14]
Genetic defects in CSF1R and pharmacological blockade of CSF1R drastically reduce microglia numbers.
“Genetic defects in CSF1R and pharmacological blockade of CSF1R drastically reduce microglia numbers (5, 6).”
From Microglia Function in the Central Nervous System During Health and Neurodegeneration (2017) · cites this paper as [6]
Microglia interact with and modulate neuronal and synaptic elements, with direct effects on learning and memory.
“evidence indicates that these cells interact with and modulate neuronal and synaptic elements, with direct effects on learning and memory [14], [15], [16], [17], [18], [19].”
From Microglia facilitate loss of perineuronal nets in the Alzheimer's disease brain (2020) · cites this paper as [14]
Microglia express and are critically dependent upon signaling through the myeloid CSF1/IL-34 receptor CSF1R for survival.
“Microglia express and are critically dependent upon signaling through the myeloid CSF1/IL-34 receptor CSF1R for survival [14].”
From Microglia facilitate loss of perineuronal nets in the Alzheimer's disease brain (2020) · cites this paper as [14]
Microglial depletion enhances performance in certain memory tasks in healthy adult mice.
“Microglial depletion also enhances performance in certain memory tasks [12, 14, 16] and prevents the forgetting of remote memories, and in association, the dissociation of memory engram cells in healthy adult mice [18].”
From Microglia facilitate loss of perineuronal nets in the Alzheimer's disease brain (2020) · cites this paper as [14]
Microglial CSF1R signalling is essential for their survival and has become a thoroughly tested and highly replicated model for targeted elimination of microglia.
“Microglial CSF1R signalling is essential to their survival and has become a thoroughly tested and highly replicated model for targeted elimination of microglia (Elmore et al. , 2014; Asai et al. , 2015; Dagher et al. , 2015; Rice et al. , 2015; Acharya et al. , 2016; Feng et al. , 2016; Spangenberg et al. , 2016; Stafford et al. , 2016; Szalay et al. , 2016; Li et al. , 2017; Bennett et al. , 2018”
From Microglial depletion prevents extracellular matrix changes and striatal volume reduction in a model of Huntington's disease (2020) · cites this paper as Elmore et al., 2014
A pharmacological method based on CSF1R inhibition can eliminate virtually all (>99%) microglia from the murine brain for several months.
“Previously, we developed a pharmacological method to eliminate virtually all ( 99%) microglia from the murine brain for several months at a time (Elmore et al. , 2014; Dagher et al. , 2015), based on inhibition of colony-stimulating factor 1 receptor (CSF1Ri).”
From Microglial depletion prevents extracellular matrix changes and striatal volume reduction in a model of Huntington's disease (2020) · cites this paper as Elmore et al., 2014
Microglia are critically dependent on CSF1R signaling for their survival.
“As we previously demonstrated, microglia are critically dependent on CSF1R signaling for their survival17”
From Sustained microglial depletion with CSF1R inhibitor impairs parenchymal plaque development in an Alzheimer’s disease model (2019) · cites this paper as [17]
The long-term absence of microglia is not detrimental to murine cognitive function and may be beneficial.
“indicating that the long-term absence of microglia is not detrimental to murine cognitive function and may be beneficial, at least in this assay, which is consistent with our prior findings17,18.”
From Sustained microglial depletion with CSF1R inhibitor impairs parenchymal plaque development in an Alzheimer’s disease model (2019) · cites this paper as [17]
PLX5622 has a brain penetrance of ~20% in mice, rats, dogs, and monkeys, compared to ~5% for PLX3397.
“In vivo PLX5622 demonstrated desirable PK properties in mice, rats, dogs, and monkeys (Supplementary Table 5), with a brain penetrance of ~20% (compared to ~5% for PLX339717; Supplementary Table 6).”
From Sustained microglial depletion with CSF1R inhibitor impairs parenchymal plaque development in an Alzheimer’s disease model (2019) · cites this paper as [17]
PLX5622-treated wild-type mice tended to spend more time in the platform zone compared to wild-type mice in the MWM probe trial.
“In the MWM probe trial, PLX5622-treated wild-type mice tended to spend more time in the platform zone compared to wild-type mice (Fig. 3k), indicating that the long-term absence of microglia is not detrimental to murine cognitive function and may be beneficial, at least in this assay, which is consistent with our prior findings17,18.”
From Sustained microglial depletion with CSF1R inhibitor impairs parenchymal plaque development in an Alzheimer’s disease model (2019) · cites this paper as [17]
Microglia can be indefinitely depleted via the continued administration of CSF1R inhibitors, and the microglial compartment can also be repopulated upon CSF1R inhibitor withdrawal.
“While microglia can be indefinitely depleted via the continued administration of CSF1R inhibitors, the microglial compartment can also be repopulated upon CSF1R inhibitor withdrawal17,40,41.”
From Sustained microglial depletion with CSF1R inhibitor impairs parenchymal plaque development in an Alzheimer’s disease model (2019) · cites this paper as [17]
PLX3397 at 75 ppm provides robust peripheral CSF1R inhibition without microglial elimination.
“We further examined the role of peripheral CSF1R inhibition on AD pathology by treating 1.5-month-old 5xFAD mice until 5 months of age with PLX3397 (75 ppm) chow (Fig. 7a) – a formulation that provides robust peripheral CSF1R inhibition without microglial elimination17.”
From Sustained microglial depletion with CSF1R inhibitor impairs parenchymal plaque development in an Alzheimer’s disease model (2019) · cites this paper as [17]
Inhibition of CSF1R causes depletion of microglia.
“Recent studies that have used an anti-CSF1R antibody187 and PLX3397 to block CSF1R suggest that inhibition of CSF1R causes the depletion of microglia188.”
From Microglial signatures and their role in health and disease (2018) · cites this paper as [188]
Microglia repopulate rapidly after being depleted pharmacologically.
“This report shows rapid repopulation of microglia following pharmacological depletion.”
From Microglial signatures and their role in health and disease (2018) · cites this paper as [188]
No sign of BBB injury, as assessed by IgG penetration into the brain parenchyma, is found after PLX3397 treatment.
“No sign of blood brain barrier (BBB) injury, as assessed by IgG penetration into the brain parenchyma was found similarly to earlier observations24.”
From Microglia protect against brain injury and their selective elimination dysregulates neuronal network activity after stroke (2016) · cites this paper as [24]
A single intraperitoneal injection of 20 mg/kg PLX3397 does not lead to microglia depletion.
“This regimen yields higher PLX3397 levels than that needed to maintain depletion of microglia24, but does not lead to microglia depletion.”
From Microglia protect against brain injury and their selective elimination dysregulates neuronal network activity after stroke (2016) · cites this paper as [24]
Absence of microglia does not lead to increased leukocyte recruitment to the brain 24 h and 72 h after cerebral ischaemia.
“Absence of microglia did not lead to increased leukocyte recruitment to the brain 24 h (Fig. 1i) and 72 h (Supplementary Fig. 5) after cerebral ischaemia or inflammation as observed previously by others after hippocampal injury24.”
From Microglia protect against brain injury and their selective elimination dysregulates neuronal network activity after stroke (2016) · cites this paper as [24]
PLX3397 is quickly cleared from central and peripheral tissues.
“Since PLX3397 is quickly cleared from central and peripheral tissues24, the PLX3397 diet was withdrawn for 24 h after 21 days of microglia depletion in a separate group of animals, after which microglia remained fully depleted, but only trace amounts of the drug were detected in the brain24.”
From Microglia protect against brain injury and their selective elimination dysregulates neuronal network activity after stroke (2016) · cites this paper as [24]
High-dose treatment with a brain-penetrant CSF1R kinase inhibitor reversibly depletes microglia, an effect that has no apparent gross deleterious results in healthy mice.
“High-dose treatment with a brain-penetrant CSF1R kinase inhibitor reversibly depletes microglia, an effect that has no apparent gross deleterious results in healthy mice, but that provides a powerful tool for inferring the various roles of microglia in more detail24.”
From Microglia protect against brain injury and their selective elimination dysregulates neuronal network activity after stroke (2016) · cites this paper as [24]
Previous observations using the same approach demonstrated a lack of illness and behavioural alterations in microglia-depleted animals.
“This is in line with previous observations using the same approach24, which also demonstrated a lack of illness and behavioural alterations in microglia-depleted animals2432.”
From Microglia protect against brain injury and their selective elimination dysregulates neuronal network activity after stroke (2016) · cites this paper as [24]
Acute treatment with a PLX3397 dose higher than that needed to block microglial repopulation did not result in depletion of microglia.
“In addition, acute treatment with a PLX3397 dose higher than that needed to block microglial repopulation24 did not result in depletion of microglia and did not alter brain injury.”
From Microglia protect against brain injury and their selective elimination dysregulates neuronal network activity after stroke (2016) · cites this paper as [24]
In agreement with earlier results, we have not found any obvious behavioural alterations, weight loss or sign of illness in mice fed a PLX3397 diet for 3 weeks or longer.
“In agreement with earlier results24, we have not found any obvious behavioural alterations, weight loss or sign of illness in mice fed a PLX3397 diet for 3 weeks or longer.”
From Microglia protect against brain injury and their selective elimination dysregulates neuronal network activity after stroke (2016) · cites this paper as [24]
Acute treatment with a PLX3397 dose higher than that needed to block microglial repopulation did not alter brain injury.
“In addition, acute treatment with a PLX3397 dose higher than that needed to block microglial repopulation24 did not result in depletion of microglia and did not alter brain injury.”
From Microglia protect against brain injury and their selective elimination dysregulates neuronal network activity after stroke (2016) · cites this paper as [24]
Withdrawal of PLX3397 for 24 h reduces drug concentrations to below detection level.
“withdrawal of PLX3397 for 24 h, which reduces drug concentrations to below detection level24”
From Microglia protect against brain injury and their selective elimination dysregulates neuronal network activity after stroke (2016) · cites this paper as [24]
Elimination of EGFP+Iba1+ cells by PLEX5622 was due to programmed cell death of microglia.
“indicating that elimination of EGFP+Iba1+ cells was due to programmed cell death of microglia as previously reported (Elmore et al., 2014)”
From Local cues establish and maintain region-specific phenotypes of basal ganglia microglia (2017) · cites this paper as Elmore et al., 2014
Microglia can be efficiently ablated in mice by chronic treatment with PLX5622, a pharmacological inhibitor of CSF1R, which is required for microglia survival.
“Microglia can be efficiently ablated in mice by chronic treatment with PLX5622 (PLX), a pharmacological inhibitor of the colony stimulating factor 1 receptor, CSF1R, which is required for microglia survival24.”
From Epigenetic regulation of brain region-specific microglia clearance activity (2018) · cites this paper as [24]
Pharmacological blockade of CSF1 receptors impairs microglial survival and can completely remove microglia from the mouse brain.
“Pharmacological blockade of CSF1 receptors has been shown to impair microglial survival and can completely remove microglia from the mouse brain (53–55).”
From <i>Trem2</i> promotes anti-inflammatory responses in microglia and is suppressed under pro-inflammatory conditions (2020) · cites this paper as [53]
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Cites
Fate Mapping Analysis Reveals That Adult Microglia Derive from Primitive Macrophages
Ginhoux, F., Greter, M., Leboeuf, M., Nandi, S., See, P., Gokhan, S., Mehler, M. F., Conway, S. J., Ng, L. G., Stanley, E. R., et al. (2010) · Science · doi:10.1126/science.1194637 · Cited by 5,175 · see citing works
Triple-Transgenic Model of Alzheimer’s Disease with Plaques and Tangles
Oddo, S., Caccamo, A., Shepherd, J. D., Murphy, M. P., Golde, T. E., Kayed, R., Metherate, R., Mattson, M. P., Akbari, Y., & LaFerla, F. M. (2003) · Neuron · doi:10.1016/s0896-6273(03)00434-3 · Cited by 4,126 · see citing works
Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor
Parkhurst, C. N., Yang, G., Ninan, I., Savas, J. N., Yates, J. R., Lafaille, J. J., Hempstead, B. L., Littman, D. R., & Gan, W.-B. (2013) · Cell · doi:10.1016/j.cell.2013.11.030 · Cited by 2,599 · see citing works
Hashimoto, D., Chow, A., Noizat, C., Teo, P., Beasley, M. B., Leboeuf, M., Becker, C. D., See, P., Price, J., Lucas, D., et al. (2013) · Immunity · doi:10.1016/j.immuni.2013.04.004 · Cited by 2,311 · cited 1× · see citing works
“In the periphery, macrophage populations are thought to be replenished by circulating monocytes derived from multipotent HSCs found in the bone marrow, although this view has been challenged (Hashimoto et al., 2013; Sieweke and Allen, 2013).”
the Immunological Genome Consortium, Gautier, E. L., Shay, T., Miller, J., Greter, M., Jakubzick, C., Ivanov, S., Helft, J., Chow, A., Elpek, K. G., et al. (2012) · Nature Immunology · doi:10.1038/ni.2419 · Cited by 1,972 · cited 4× · see citing works
“Reductions in known microglial-associated genes were most common in the 1-day recovery group compared with controls, including recently identified microglial-selective genes p2ry13, Siglech, and slc2a5 (Chiu et al., 2013; Gautier et al., 2012).”
BackgroundInfluentialDeNardo, D. G., Brennan, D. J., Rexhepaj, E., Ruffell, B., Shiao, S. L., Madden, S. F., Gallagher, W. M., Wadhwani, N., Keil, S. D., Junaid, S. A., et al. (2011) · Cancer Discovery · doi:10.1158/2159-8274.cd-10-0028 · Cited by 1,715 · see citing works
Self-citationMicroglia emerge from erythromyeloid precursors via Pu.1- and Irf8-dependent pathways
Kierdorf, K., Erny, D., Goldmann, T., Sander, V., Schulz, C., Perdiguero, E. G., Wieghofer, P., Heinrich, A., Riemke, P., Hölscher, C., et al. (2013) · Nature Neuroscience · doi:10.1038/nn.3318 · Cited by 1,457 · see citing works
Zhan, Y., Paolicelli, R. C., Sforazzini, F., Weinhard, L., Bolasco, G., Pagani, F., Vyssotski, A. L., Bifone, A., Gozzi, A., Ragozzino, D., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3641 · Cited by 1,236 · see citing works
Debris clearance by microglia: an essential link between degeneration and regeneration
Neumann, H., Kotter, M. R., & Franklin, R. J. M. (2008) · Brain · doi:10.1093/brain/awn109 · Cited by 1,111 · see citing works
Microglia in the adult brain arise from Ly-6ChiCCR2+ monocytes only under defined host conditions
Mildner, A., Schmidt, H., Nitsche, M., Merkler, D., Hanisch, U.-K., Mack, M., Heikenwalder, M., Brück, W., Priller, J., & Prinz, M. (2007) · Nature Neuroscience · doi:10.1038/nn2015 · Cited by 1,089 · see citing works
Infiltrating monocytes trigger EAE progression, but do not contribute to the resident microglia pool
Ajami, B., Bennett, J. L., Krieger, C., McNagny, K. M., & Rossi, F. M. V. (2011) · Nature Neuroscience · doi:10.1038/nn.2887 · Cited by 1,061 · see citing works
Wang, Y., Szretter, K. J., Vermi, W., Gilfillan, S., Rossini, C., Cella, M., Barrow, A. D., Diamond, M. S., & Colonna, M. (2012) · Nature Immunology · doi:10.1038/ni.2360 · Cited by 1,011 · see citing works
The use of ATP bioluminescence as a measure of cell proliferation and cytotoxicity
Crouch, S. P. M., Kozlowski, R., Slater, K. J., & Fletcher, J. (1993) · Journal of Immunological Methods · doi:10.1016/0022-1759(93)90011-u · Cited by 926 · see citing works
Discovery of a Cytokine and Its Receptor by Functional Screening of the Extracellular Proteome
Lin, H., Lee, E., Hestir, K., Leo, C., Huang, M., Bosch, E., Halenbeck, R., Wu, G., Zhou, A. J., Behrens, D., et al. (2008) · Science · doi:10.1126/science.1154370 · Cited by 815 · see citing works
Chiu, I. M., Morimoto, E. T. A., Goodarzi, H., Liao, J. T., O’Keeffe, S., Phatnani, H. P., Muratet, M., Carroll, M. C., Levy, S., Tavazoie, S., et al. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.06.018 · Cited by 651 · see citing works
Erblich, B., Zhu, L., Etgen, A. M., Dobrenis, K., & Pollard, J. W. (2011) · PLoS ONE · doi:10.1371/journal.pone.0026317 · Cited by 649 · see citing works
Greter, M., Lelios, I., Pelczar, P., Hoeffel, G., Price, J., Leboeuf, M., Kündig, T. M., Frei, K., Ginhoux, F., Merad, M., et al. (2012) · Immunity · doi:10.1016/j.immuni.2012.11.001 · Cited by 630 · see citing works
CX3CR1 deficiency leads to impairment of hippocampal cognitive function and synaptic plasticity
Rogers, J. T., Morganti, J. M., Bachstetter, A. D., Hudson, C. E., Peters, M. M., Grimmig, B. A., Weeber, E. J., Bickford, P. C., & Gemma, C. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.3667-11.2011 · Cited by 624 · see citing works
Saederup, N., Cardona, A. E., Croft, K., Mizutani, M., Cotleur, A. C., Tsou, C.-L., Ransohoff, R. M., & Charo, I. F. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013693 · Cited by 599 · see citing works
Beyond stem cells: self-renewal of differentiated macrophages
Sieweke, M. H., & Allen, J. E. (2013) · Science · doi:10.1126/science.1242974 · Cited by 503 · see citing works
Coniglio, S. J., Eugenin, E., Dobrenis, K., Stanley, E. R., West, B. L., Symons, M. H., & Segall, J. E. (2012) · Molecular Medicine · doi:10.2119/molmed.2011.00217 · Cited by 429 · see citing works
Self-citationNandi, S., Gökhan, Ş., Dai, X.-M., Wei, S., Enikolopov, G., Lin, H., Mehler, M. F., & Stanley, E. R. (2012) · Developmental Biology · doi:10.1016/j.ydbio.2012.03.026 · Cited by 341 · see citing works
Inhibition of CSF-1 Receptor Improves the Antitumor Efficacy of Adoptive Cell Transfer Immunotherapy
Mok, S., Koya, R. C., Tsui, C. T., Xu, J., Robert, L., Wu, L., Graeber, T. G., West, B. L., Bollag, G. E., & Ribas, A. (2013) · Cancer Research · doi:10.1158/0008-5472.can-13-1816 · Cited by 311 · see citing works
Self-citationPositive Feedback Between PU.1 and the Cell Cycle Controls Myeloid Differentiation
Kueh, H. Y., Champhekar, A., Nutt, S. L., Elowitz, M. B., & Rothenberg, E. V. (2013) · Science · doi:10.1126/science.1240831 · Cited by 273 · see citing works
Conway, J. G., McDonald, B., Parham, J. H., Keith, B. R., Rusnak, D. W., Shaw, E., Jansen, M., Lin, P., Payne, A. J., Crosby, R. M., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0502000102 · Cited by 251 · see citing works
van der Meer, P., Ulrich, A. M., González‐Scarano, F., & Lavi, E. (2000) · Experimental and Molecular Pathology · doi:10.1006/exmp.2000.2336 · Cited by 174 · see citing works
Prada, C. E., Jousma, E., Rizvi, T. A., Wu, J., Dunn, R. S., Mayes, D. A., Cancelas, J. A., Dombi, E., Kim, M., West, B. L., et al. (2012) · Acta Neuropathologica · doi:10.1007/s00401-012-1056-7 · Cited by 143 · see citing works
Self-citationNeely, K. M., Green, K. N., & LaFerla, F. M. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.5156-10.2010 · Cited by 141 · see citing works
Self-citationRegulation of microglia development and homeostasis.
Greter, M., & Merad, M. (2013) · Glia · doi:10.1002/glia.22408 · Cited by 141 · see citing works
Banisadr, G., Gosselin, R., Méchighel, P., Rostène, W. H., Kitabgi, P., & Parsadaniantz, S. M. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20729 · Cited by 135 · see citing works
Conditional deletion of the colony stimulating factor-1 receptor (c-fms proto-oncogene) in mice
Li, J., Chen, K., Zhu, L., & Pollard, J. W. (2006) · genesis · doi:10.1002/dvg.20219 · Cited by 128 · see citing works
Colony-Stimulating Factor-1 Receptor Inhibitors for the Treatment of Cancer and Inflammatory Disease
Patel, S., & Player, M. R. (2009) · Current Topics in Medicinal Chemistry · doi:10.2174/156802609789007327 · Cited by 125 · see citing works
Węgiel, J., Wı́sniewski, H. M., Dziewiątkowski, J., Tarnawski, M. J., Kozielski, R., Trenkner, E., & Wiktor-Jędrzejczak, W. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00618-0 · Cited by 120 · see citing works
Expression of nestin after traumatic brain injury in rat brain
Kaya, S. S., Mahmood, A., Li, Y., Yavuz, E., & Chopp, M. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01757-6 · Cited by 118 · see citing works
Microglia, a potential source of neurons, astrocytes, and oligodendrocytes
Yokoyama, A., Yang, L., Itoh, S., Mori, K., & Tanaka, J. (2003) · Glia · doi:10.1002/glia.10306 · Cited by 105 · see citing works
Chin, B. Y., Petrache, I., Choi, A. M. K., & Choi, M. E. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.16.11362 · Cited by 100 · see citing works
Design and pharmacology of a highly specific dual FMS and KIT kinase inhibitor
Zhang, C., Ibrahim, P. N., Zhang, J., Burton, E. A., Habets, G. G. M., Zhang, Y., Powell, B., West, B. L., Matusow, B., Tsang, G., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1219457110 · Cited by 98 · see citing works
Self-citationOhno, H., Kubo, K., Murooka, H., Kobayashi, Y., Nishitoba, T., Shibuya, M., Yoneda, T., & Isoe, T. (2006) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-05-0313 · Cited by 96 · see citing works
Generation of microglial cells from mouse embryonic stem cells
Beutner, C., Roy, K., Linnartz, B., Napoli, I., & Neumann, H. (2010) · Nature Protocols · doi:10.1038/nprot.2010.90 · Cited by 85 · see citing works
Chiţu, V., Nacu, V., Charles, J. F., Henne, W. M., McMahon, H. T., Nandi, S., Ketchum, H., Harris, R., Nakamura, M. C., & Stanley, E. R. (2012) · Blood · doi:10.1182/blood-2012-04-425595 · Cited by 78 · see citing works
Delayed Bone Regeneration Is Linked to Chronic Inflammation in Murine Muscular Dystrophy
Abou-Khalil, R., Yang, F. F., Mortreux, M., Lieu, S., Yu, Y., Wurmser, M., Pereira, C., Relaix, F., Miclau, T., Marcucio, R., et al. (2013) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.2038 · Cited by 65 · see citing works
In Situ Dividing and Phagocytosing Retinal Microglia Express Nestin, Vimentin, and NG2 In Vivo
Wohl, S. G., Schmeer, C., Friese, T., Witte, O., & Isenmann, S. (2011) · PLoS ONE · doi:10.1371/journal.pone.0022408 · Cited by 62 · see citing works
ST101 induces a novel 17kDa APP cleavage that precludes Aβ generation in vivo
Green, K. N., Khashwji, H., Estrada, T., & LaFerla, F. M. (2011) · Annals of Neurology · doi:10.1002/ana.22325 · Cited by 34 · see citing works
Self-citationCornelis, S., Bruynooghe, Y., Loo, G., Saelens, X., Vandenabeele, P., & Beyaert, R. (2005) · Oncogene · doi:10.1038/sj.onc.1208401 · Cited by 30 · see citing works
c-Fms Signaling Mediates Neurofibromatosis Type-1 Osteoclast Gain-In-Functions
He, Y., Rhodes, S. D., Shi, C., Wu, X., Yuan, J., Yang, X., Jiang, L., Li, X., Takahashi, N., Xu, M., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0046900 · Cited by 20 · see citing works
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Microglia Function in the Central Nervous System During Health and Neurodegeneration
Colonna, M., & Butovsky, O. (2017) · Annual Review of Immunology · doi:10.1146/annurev-immunol-051116-052358 · Cited by 2,894 · see citing works
Hammond, T. R., Dufort, C., Dissing-Olesen, L., Giera, S., Young, A., Wysoker, A., Walker, A. J., Segel, M., Nemesh, J., Saunders, A., et al. (2018) · doi:10.1101/406140 · Cited by 2,225 · see citing works
Microglia and macrophages in brain homeostasis and disease
Li, Q., & Barres, B. A. (2018) · Nature Reviews Immunology · doi:10.1038/nri.2017.125 · Cited by 1,999 · see citing works
Microglia in Alzheimer’s disease
Hansen, D. V., Hanson, J. E., & Sheng, M. (2018) · Journal of Cell Biology · doi:10.1083/jcb.201709069 · Cited by 1,935 · see citing works
The Microenvironmental Landscape of Brain Tumors
Quail, D. F., & Joyce, J. A. (2017) · Cancer Cell · doi:10.1016/j.ccell.2017.02.009 · Cited by 1,875 · see citing works
Microglia emerge as central players in brain disease
Salter, M. W., & Stevens, B. (2017) · Nature Medicine · doi:10.1038/nm.4397 · Cited by 1,767 · see citing works
The role of microglia and macrophages in glioma maintenance and progression
Hambardzumyan, D., Gutmann, D. H., & Kettenmann, H. (2016) · Nature Neuroscience · doi:10.1038/nn.4185 · Cited by 1,683 · see citing works
Neuroinflammation: The Devil Is in the Details
DiSabato, D. J., Quan, N., & Godbout, J. P. (2016) · Journal of Neurochemistry · doi:10.1111/jnc.13607 · Cited by 1,640 · see citing works
Microglia in neurodegenerative diseases: mechanism and potential therapeutic targets
Gao, C., Jiang, J., Tan, Y., & Chen, S. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01588-0 · Cited by 1,616 · see citing works
Depletion of microglia and inhibition of exosome synthesis halt tau propagation
Asai, H., Ikezu, S., Tsunoda, S., Medalla, M., Luebke, J., Haydar, T., Wolozin, B., Butovsky, O., Kügler, S., & Ikezu, T. (2015) · Nature Neuroscience · doi:10.1038/nn.4132 · Cited by 1,591 · see citing works
Microglia Biology: One Century of Evolving Concepts
Prinz, M., Jung, S., & Priller, J. (2019) · Cell · doi:10.1016/j.cell.2019.08.053 · Cited by 1,525 · see citing works
An environment-dependent transcriptional network specifies human microglia identity
Gosselin, D., Skola, D., Coufal, N. G., Holtman, I. R., Schlachetzki, J. C. M., Sajti, E., Jaeger, B. N., O’Connor, C., Fitzpatrick, C., Pasillas, M. P., et al. (2017) · Science · doi:10.1126/science.aal3222 · Cited by 1,220 · see citing works
“Microglia share many traits with other subsets of tissue-resident macrophages, including dependence on the CSF1 receptor for differentiation and survival (18, 20), a requirement for PU.”
BackgroundVan Hove, H., Martens, L., Scheyltjens, I., De Vlaminck, K., Pombo Antunes, A. R., De Prijck, S., Vandamme, N., De Schepper, S., Van Isterdael, G., Scott, C. L., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0393-4 · Cited by 1,160 · see citing works
Microglial signatures and their role in health and disease
Butovsky, O., & Weiner, H. L. (2018) · Nature Reviews Neuroscience · doi:10.1038/s41583-018-0057-5 · Cited by 1,046 · see citing works
Colony-stimulating factor 1 receptor (CSF1R) inhibitors in cancer therapy
Cannarile, M. A., Weisser, M., Jacob, W., Jegg, A.-M., Ries, C. H., & Rüttinger, D. (2017) · Journal for ImmunoTherapy of Cancer · doi:10.1186/s40425-017-0257-y · Cited by 1,029 · see citing works
Overview of General and Discriminating Markers of Differential Microglia Phenotypes
Jurga, A. M., Paleczna, M., & Kuter, K. Z. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.00198 · Cited by 1,000 · see citing works
Negative feedback control of neuronal activity by microglia
Badimon, A., Strasburger, H. J., Ayata, P., Chen, X., Nair, A., Ikegami, A., Hwang, P., Chan, A. T., Graves, S. M., Uweru, J. O., et al. (2020) · Nature · doi:10.1038/s41586-020-2777-8 · Cited by 979 · see citing works
Developmental and Functional Heterogeneity of Monocytes
Guilliams, M., Mildner, A., & Yona, S. (2018) · Immunity · doi:10.1016/j.immuni.2018.10.005 · Cited by 973 · see citing works
Macrophages: Development and Tissue Specialization
Varol, C., Mildner, A., & Jung, S. (2015) · Annual Review of Immunology · doi:10.1146/annurev-immunol-032414-112220 · Cited by 962 · see citing works
Spatial Transcriptomics and In Situ Sequencing to Study Alzheimer’s Disease
Chen, W.-T., Lu, A., Craessaerts, K., Pavie, B., Sala Frigerio, C., Corthout, N., Qian, X., Laláková, J., Kühnemund, M., Voytyuk, I., et al. (2020) · Cell · doi:10.1016/j.cell.2020.06.038 · Cited by 949 · see citing works
Spangenberg, E., Severson, P. L., Hohsfield, L. A., Crapser, J., Zhang, J., Burton, E. A., Zhang, Y., Spevak, W., Lin, J., Phan, N. Y., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-11674-z · Cited by 939 · see citing works
Self-citationLöscher, W., Potschka, H., Sisodiya, S. M., & Vezzani, A. (2020) · Pharmacological Reviews · doi:10.1124/pr.120.019539 · Cited by 928 · see citing works
Microglia in neuropathic pain: cellular and molecular mechanisms and therapeutic potential
Inoue, K., & Tsuda, M. (2018) · Nature Reviews Neuroscience · doi:10.1038/nrn.2018.2 · Cited by 908 · see citing works
Microglia in the TBI brain: The good, the bad, and the dysregulated
Loane, D. J., & Kumar, A. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2015.08.018 · Cited by 816 · see citing works
Microglia: Immune and non-immune functions
Borst, K., Dumas, A. A., & Prinz, M. (2021) · Immunity · doi:10.1016/j.immuni.2021.09.014 · Cited by 804 · see citing works
Mechanisms of immunotherapy resistance: lessons from glioblastoma
Jackson, C. M., Choi, J. H., & Lim, M. K. (2019) · Nature Immunology · doi:10.1038/s41590-019-0433-y · Cited by 760 · see citing works
Coupled Proliferation and Apoptosis Maintain the Rapid Turnover of Microglia in the Adult Brain
Askew, K., Li, K., Olmos-Alonso, A., Garcia-Moreno, F., Liang, Y., Richardson, P., Tipton, T., Chapman, M. A., Riecken, K., Beccari, S., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2016.12.041 · Cited by 726 · see citing works
Pombo Antunes, A. R., Scheyltjens, I., Lodi, F., Messiaen, J., Antoranz, A., Duerinck, J., Kancheva, D., Martens, L., De Vlaminck, K., Van Hove, H., et al. (2021) · Nature Neuroscience · doi:10.1038/s41593-020-00789-y · Cited by 704 · see citing works
Spangenberg, E. E., Lee, R. J., Najafi, A. R., Rice, R. A., Elmore, M. R. P., Blurton-Jones, M., West, B. L., & Green, K. N. (2016) · Brain · doi:10.1093/brain/aww016 · Cited by 695 · see citing works
Self-citationSkull and vertebral bone marrow are myeloid cell reservoirs for the meninges and CNS parenchyma
Cugurra, A., Mamuladze, T., Rustenhoven, J., Dykstra, T., Beroshvili, G., Greenberg, Z. J., Baker, W., Papadopoulos, Z., Drieu, A., Blackburn, S., et al. (2021) · Science · doi:10.1126/science.abf7844 · Cited by 681 · see citing works
Cellular and Molecular Identity of Tumor-Associated Macrophages in Glioblastoma
Chen, Z., Feng, X., Herting, C. J., Garcia, V. A., Nie, K., Pong, W. W., Rasmussen, R. D., Dwivedi, B., Seby, S., Wolf, S. A., et al. (2017) · Cancer Research · doi:10.1158/0008-5472.can-16-2310 · Cited by 675 · see citing works
Bohlen, C. J., Bennett, F. C., Tucker, A. F., Collins, H. Y., Mulinyawe, S. B., & Barres, B. A. (2017) · Neuron · doi:10.1016/j.neuron.2017.04.043 · Cited by 676 · see citing works
Integrating neuroimmune systems in the neurobiology of depression
Wohleb, E. S., Franklin, T., Iwata, M., & Duman, R. S. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2016.69 · Cited by 668 · see citing works
Redox lipid reprogramming commands susceptibility of macrophages and microglia to ferroptotic death
Kapralov, A. A., Yang, Q., Dar, H. H., Tyurina, Y. Y., Anthonymuthu, T. S., Kim, R., Croix, C. M. S., Mikulska‐Ruminska, K., Liu, B., Shrivastava, I. H., et al. (2020) · Nature Chemical Biology · doi:10.1038/s41589-019-0462-8 · Cited by 657 · see citing works
Sex-specific features of microglia from adult mice
Villa, A., Gelosa, P., Castiglioni, L., Cimino, M., Rizzi, N., Pepe, G., Lolli, F., Marcello, E., Sironi, L., Vegeto, E., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.05.048 · Cited by 651 · see citing works
Bruttger, J., Karram, K., Wörtge, S., Regen, T., Marini, F., Hoppmann, N., Klein, M., Blank, T., Yona, S., Wolf, Y., et al. (2015) · Immunity · doi:10.1016/j.immuni.2015.06.012 · Cited by 634 · see citing works
Valdearcos, M., Robblee, M. M., Benjamin, D. I., Nomura, D. K., Xu, A. W., & Koliwad, S. K. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.11.018 · Cited by 629 · see citing works
Microglia are an essential component of the neuroprotective scar that forms after spinal cord injury
Bellver‐Landete, V., Bretheau, F., Mailhot, B., Vallières, N., Lessard, M., Janelle, M.-E., Vernoux, N., Tremblay, M., Führmann, T., Shoichet, M. S., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-08446-0 · Cited by 627 · see citing works
Holtman, I. R., Raj, D. D., Miller, J. A., Schaafsma, W., Yin, Z., Brouwer, N., Wes, P. D., Möller, T., Orre, M., Kamphuis, W., et al. (2015) · Acta Neuropathologica Communications · doi:10.1186/s40478-015-0203-5 · Cited by 619 · see citing works
Butowski, N. A., Colman, H., de Groot, J., Omuro, A. M. P., Nayak, L., Wen, P. Y., Cloughesy, T. F., Marimuthu, A., Haidar, S., Perry, A., et al. (2015) · Neuro-Oncology · doi:10.1093/neuonc/nov245 · Cited by 593 · see citing works
Self-citationA new fate mapping system reveals context-dependent random or clonal expansion of microglia
Tay, T. L., Mai, D., Dautzenberg, J., Fernández-Klett, F., Lin, G., Sagar, Datta, M., Drougard, A., Stempfl, T., Ardura-Fabregat, A., et al. (2017) · Nature Neuroscience · doi:10.1038/nn.4547 · Cited by 597 · see citing works
Norden, D. M., Trojanowski, P. J., Villanueva, E., Navarro, E., & Godbout, J. P. (2015) · Glia · doi:10.1002/glia.22930 · Cited by 596 · see citing works
Microglia in Neuroinflammation and Neurodegeneration: From Understanding to Therapy
Muzio, L., Viotti, A., & Martino, G. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.742065 · Cited by 581 · see citing works
Szalay, G., Martinecz, B., Lénárt, N., Környei, Z., Orsolits, B., Judák, L., Császár, E., Fekete, R., West, B. L., Katona, G., et al. (2016) · Nature Communications · doi:10.1038/ncomms11499 · Cited by 573 · see citing works
Self-citationMicroglial regional heterogeneity and its role in the brain
Tan, Y.-L., Yuan, Y., & Tian, L. (2020) · Molecular Psychiatry · doi:10.1038/s41380-019-0609-8 · Cited by 571 · see citing works
Sall1 is a transcriptional regulator defining microglia identity and function
Buttgereit, A., Lelios, I., Yu, X., Vrohlings, M., Krakoski, N. R., Gautier, E. L., Nishinakamura, R., Becher, B., & Greter, M. (2016) · Nature Immunology · doi:10.1038/ni.3585 · Cited by 570 · see citing works
Astrocytic and microglial cells as the modulators of neuroinflammation in Alzheimer’s disease
Singh, D. (2022) · Journal of Neuroinflammation · doi:10.1186/s12974-022-02565-0 · Cited by 569 · see citing works
Tay, T. L., Savage, J. C., Hui, C. W., Bisht, K., & Tremblay, M. (2017) · The Journal of Physiology · doi:10.1113/jp272134 · Cited by 562 · see citing works
Injured sensory neuron–derived CSF1 induces microglial proliferation and DAP12-dependent pain
Guan, Z., Kuhn, J., Wang, X., Colquitt, B. M., Solórzano, C., Vaman, S., Guan, A. K., Evans-Reinsch, Z., Braz, J. M., Devor, M. G., et al. (2015) · Nature Neuroscience · doi:10.1038/nn.4189 · Cited by 554 · see citing works
Huang, Y., Xu, Z., Xiong, S., Sun, F., Qin, G., Hu, G., Wang, J., Zhao, L., Liang, Y.-X., Wu, T., et al. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0090-8 · Cited by 560 · see citing works
Hagemeyer, N., Hanft, K.-M., Akriditou, M.-A., Unger, N., Park, E. S., Stanley, E. R., Staszewski, O., Dimou, L., & Prinz, M. (2017) · Acta Neuropathologica · doi:10.1007/s00401-017-1747-1 · Cited by 558 · see citing works
Retinal microglia: Just bystander or target for therapy?
Karlstetter, M., Scholz, R., Rutar, M., Wong, W. T., Provis, J. M., & Langmann, T. (2014) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2014.11.004 · Cited by 550 · see citing works
Microglial subtypes: diversity within the microglial community
Stratoulias, V., Venero, J. L., Tremblay, M., & Joseph, B. (2019) · The EMBO Journal · doi:10.15252/embj.2019101997 · Cited by 536 · see citing works
A novel microglial subset plays a key role in myelinogenesis in developing brain
Wlodarczyk, A., Holtman, I. R., Krueger, M., Yogev, N., Bruttger, J., Khorooshi, R., Benmamar‐Badel, A., de Boer‐Bergsma, J. J., Martin, N. A., Karram, K., et al. (2017) · The EMBO Journal · doi:10.15252/embj.201696056 · Cited by 535 · see citing works
Olmos-Alonso, A., Schetters, S. T. T., Sri, S., Askew, K., Mancuso, R., Vargas-Caballero, M., Holscher, C., Perry, V. H., & Gomez-Nicola, D. (2016) · Brain · doi:10.1093/brain/awv379 · Cited by 532 · see citing works
Bain, C. C., Hawley, C. A., Garner, H., Scott, C. L., Schridde, A., Steers, N. J., Mack, M., Joshi, A., Guilliams, M., Mowat, A. M. I., et al. (2016) · Nature Communications · doi:10.1038/ncomms11852 · Cited by 527 · see citing works
Microglial exosomes facilitate α-synuclein transmission in Parkinson’s disease
Guo, M., Wang, J., Zhao, Y., Feng, Y., Han, S., Dong, Q., Cui, M., & Tieu, K. (2020) · Brain · doi:10.1093/brain/awaa090 · Cited by 522 · see citing works
Glioblastoma: defining tumor niches
Hambardzumyan, D., & Bergers, G. (2015) · Trends in Cancer · doi:10.1016/j.trecan.2015.10.009 · Cited by 522 · see citing works
Repopulating Microglia Promote Brain Repair in an IL-6-Dependent Manner
Willis, E. F., MacDonald, K. P. A., Nguyen, Q. H., Garrido, A. L., Gillespie, E. R., Harley, S. B. R., Bartlett, P. F., Schroder, W. A., Yates, A. G., Anthony, D. C., et al. (2020) · Cell · doi:10.1016/j.cell.2020.02.013 · Cited by 520 · see citing works
The Indispensable Roles of Microglia and Astrocytes during Brain Development
Reemst, K., Noctor, S. C., Lucassen, P. J., & Hol, E. M. (2016) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2016.00566 · Cited by 516 · see citing works
Yu, X., Liu, H., Hamel, K. A., Morvan, M. G., Yu, S. W., Leff, J., Guan, Z., Braz, J. M., & Basbaum, A. I. (2020) · Nature Communications · doi:10.1038/s41467-019-13839-2 · Cited by 508 · see citing works
Establishment and Maintenance of the Macrophage Niche
Guilliams, M., Thierry, G. R., Bonnardel, J., & Bajenoff, M. (2020) · Immunity · doi:10.1016/j.immuni.2020.02.015 · Cited by 512 · see citing works
Microglial P2Y12 is necessary for synaptic plasticity in mouse visual cortex
Sipe, G. O., Lowery, Tremblay, M.-È., Kelly, E. A., Lamantia, C. E., & Majewska, A. K. (2016) · Nature Communications · doi:10.1038/ncomms10905 · Cited by 512 · see citing works
Dagher, N. N., Najafi, A. R., Kayala, K. M. N., Elmore, M. R. P., White, T. E., Medeiros, R., West, B. L., & Green, K. N. (2015) · Journal of Neuroinflammation · doi:10.1186/s12974-015-0366-9 · Cited by 505 · see citing works
Self-citationGlial Cells and Their Function in the Adult Brain: A Journey through the History of Their Ablation
Jäkel, S., & Dimou, L. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00024 · Cited by 501 · see citing works
Systematic phenotyping and characterization of the 5xFAD mouse model of Alzheimer’s disease.
Forner, S., Kawauchi, S., Balderrama-Gutierrez, G., Kramár, E. A., Matheos, D. P., Phan, J., Javonillo, D. I., Tran, K. M., Hingco, E., da Cunha, C., et al. (2021) · Scientific Data · doi:10.1038/s41597-021-01054-y · Cited by 501 · see citing works
Self-citationMicroglia and Beyond: Innate Immune Cells As Regulators of Brain Development and Behavioral Function
Lenz, K. M., & Nelson, L. H. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00698 · Cited by 491 · see citing works
Valdearcos, M., Douglass, J. D., Robblee, M. M., Dorfman, M. D., Stifler, D. R., Bennett, M. L., Gerritse, I., Fasnacht, R., Barres, B. A., Thaler, J. P., et al. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.05.015 · Cited by 477 · see citing works
Cross-Species Single-Cell Analysis Reveals Divergence of the Primate Microglia Program
Geirsdottir, L., David, E., Keren-Shaul, H., Weiner, A., Bohlen, S. C., Neuber, J., Balic, A., Giladi, A., Sheban, F., Dutertre, C.-A., et al. (2019) · Cell · doi:10.1016/j.cell.2019.11.010 · Cited by 461 · see citing works
Epigenetic regulation of brain region-specific microglia clearance activity
Ayata, P., Badimon, A., Strasburger, H. J., Duff, M. K., Montgomery, S. E., Loh, Y.-H. E., Ebert, A., Pimenova, A. A., Ramirez, B. R., Chan, A. T., et al. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0192-3 · Cited by 460 · see citing works
McQuade, A., Coburn, M., Tu, C. H., Hasselmann, J., Davtyan, H., & Blurton-Jones, M. (2018) · Molecular Neurodegeneration · doi:10.1186/s13024-018-0297-x · Cited by 449 · see citing works
Microglia drive APOE-dependent neurodegeneration in a tauopathy mouse model
Shi, Y., Manis, M., Long, J., Wang, K., Sullivan, P. M., Remolina Serrano, J., Hoyle, R., & Holtzman, D. M. (2019) · Journal of Experimental Medicine · doi:10.1084/jem.20190980 · Cited by 448 · see citing works
NBB-Psy, Böttcher, C., Schlickeiser, S., Sneeboer, M. A. M., Kunkel, D., Knop, A., Paza, E., Fidzinski, P., Kraus, L., Snijders, G. J. L., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-018-0290-2 · Cited by 436 · see citing works
Immune Microenvironment in Glioblastoma Subtypes
Chen, Z., & Hambardzumyan, D. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01004 · Cited by 430 · see citing works
Microglia-organized scar-free spinal cord repair in neonatal mice
Li, Y., He, X., Kawaguchi, R., Zhang, Y., Wang, Q., Monavarfeshani, A., Yang, Z., Chen, B., Shi, Z., Meng, H., et al. (2020) · Nature · doi:10.1038/s41586-020-2795-6 · Cited by 434 · see citing works
Local cues establish and maintain region-specific phenotypes of basal ganglia microglia
De Biase, L. M., Schuebel, K. E., Fusfeld, Z. H., Jair, K., Hawes, I. A., Cimbro, R., Zhang, H.-Y., Liu, Q.-R., Shen, H., Xi, Z.-X., et al. (2017) · Neuron · doi:10.1016/j.neuron.2017.06.020 · Cited by 432 · see citing works
Roles of microglia in brain development, tissue maintenance and repair
Michell‐Robinson, M. A., Touil, H., Healy, L. M., Owen, D. R., Durafourt, B. A., Bar‐Or, A., Antel, J. P., & Moore, C. S. (2015) · Brain · doi:10.1093/brain/awv066 · Cited by 421 · see citing works
TREM2 in Neurodegenerative Diseases
Jay, T. R., von Saucken, V. E., & Landreth, G. E. (2017) · Molecular Neurodegeneration · doi:10.1186/s13024-017-0197-5 · Cited by 427 · see citing works
Estrogens, Neuroinflammation, and Neurodegeneration
Villa, A., Vegeto, E., Poletti, A., & Maggi, A. (2016) · Endocrine Reviews · doi:10.1210/er.2016-1007 · Cited by 423 · see citing works
Dark microglia: A new phenotype predominantly associated with pathological states
Bisht, K., Sharma, K. P., Lecours, C., Gabriela Sánchez, M., El Hajj, H., Milior, G., Olmos‐Alonso, A., Gómez‐Nicola, D., Luheshi, G., Vallières, L., et al. (2016) · Glia · doi:10.1002/glia.22966 · Cited by 421 · see citing works
Wohleb, E. S., McKim, D. B., Sheridan, J. F., & Godbout, J. P. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00447 · Cited by 420 · see citing works
Chen, Z., & Trapp, B. D. (2015) · Journal of Neurochemistry · doi:10.1111/jnc.13062 · Cited by 413 · see citing works
Norden, D. M., Muccigrosso, M. M., & Godbout, J. P. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.10.028 · Cited by 413 · see citing works
Cronk, J. C., Filiano, A. J., Louveau, A., Marin, I., Marsh, R., Ji, E., Goldman, D. H., Smirnov, I., Geraci, N., Acton, S., et al. (2018) · Journal of Experimental Medicine · doi:10.1084/jem.20180247 · Cited by 412 · see citing works
Marsh, S. E., Abud, E. M., Lakatos, A., Karimzadeh, A., Yeung, S. T., Davtyan, H., Fote, G. M., Lau, L., Weinger, J. G., Lane, T. E., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1525466113 · Cited by 411 · see citing works
Sosna, J., Philipp, S., Albay, R., Reyes-Ruiz, J. M., Baglietto-Vargas, D., LaFerla, F. M., & Glabe, C. G. (2018) · Molecular Neurodegeneration · doi:10.1186/s13024-018-0244-x · Cited by 406 · see citing works
Microglia turnover with aging and in an Alzheimer’s model via long-term in vivo single-cell imaging
Füger, P., Hefendehl, J. K., Veeraraghavalu, K., Wendeln, A.-C., Schlosser, C., Obermüller, U., Wegenast-Braun, B. M., Neher, J. J., Martus, P., Kohsaka, S., et al. (2017) · Nature Neuroscience · doi:10.1038/nn.4631 · Cited by 401 · see citing works
Immune cell regulation of glia during CNS injury and disease
Greenhalgh, A. D., David, S., & Bennett, F. C. (2020) · Nature reviews. Neuroscience · doi:10.1038/s41583-020-0263-9 · Cited by 398 · see citing works
Rojo, R., Raper, A., Ozdemir, D. D., Lefèvre, L., Grabert, K., Wollscheid-Lengeling, E., Bradford, B. M., Caruso, M., Gažová, I., Sánchez, A., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-11053-8 · Cited by 372 · see citing works
Witcher, K. G., Bray, C. E., Chunchai, T., Zhao, F., O'Neil, S. M., Gordillo, A. J., Campbell, W. A., McKim, D. B., Liu, X., Dziabis, J. E., et al. (2021) · The Journal of Neuroscience · doi:10.1523/jneurosci.2469-20.2020 · Cited by 387 · see citing works
The pro-remyelination properties of microglia in the central nervous system
Lloyd, A. F., & Miron, V. E. (2019) · Nature Reviews Neurology · doi:10.1038/s41582-019-0184-2 · Cited by 381 · see citing works
Astrocytes phagocytose adult hippocampal synapses for circuit homeostasis
Lee, J.-H., Kim, J. S., Noh, S., Lee, H., Lee, S. Y., Mun, J. Y., Park, H., & Chung, W. (2020) · Nature · doi:10.1038/s41586-020-03060-3 · Cited by 387 · see citing works
Elmore, M. R. P., Hohsfield, L. A., Kramár, E. A., Soreq, L., Lee, R. J., Pham, S. T., Najafi, A. R., Spangenberg, E. E., Wood, M. A., West, B. L., et al. (2018) · Aging Cell · doi:10.1111/acel.12832 · Cited by 380 · see citing works
Self-citationDevelopment of a Chimeric Model to Study and Manipulate Human Microglia In Vivo
Hasselmann, J., Coburn, M. A., England, W., Figueroa Velez, D. X., Kiani Shabestari, S., Tu, C. H., McQuade, A., Kolahdouzan, M., Echeverria, K., Claes, C., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.07.002 · Cited by 380 · see citing works
Immune responses to human fungal pathogens and therapeutic prospects
Lionakis, M. S., Drummond, R. A., & Hohl, T. M. (2023) · Nature Reviews Immunology · doi:10.1038/s41577-022-00826-w · Cited by 379 · see citing works
Gibson, E. M., Nagaraja, S., Ocampo, A., Tam, L. T., Wood, L. S., Pallegar, P. N., Greene, J. J., Geraghty, A. C., Goldstein, A. K., Ni, L., et al. (2019) · Cell · doi:10.1016/j.cell.2018.10.049 · Cited by 372 · see citing works
Zhong, L., Xu, Y., Zhuo, R., Wang, T., Wang, K., Huang, R., Wang, D., Gao, Y., Zhu, Y., Sheng, X., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-09118-9 · Cited by 371 · see citing works
Microglia: Architects of the Developing Nervous System
Frost, J. L., & Schafer, D. P. (2016) · Trends in Cell Biology · doi:10.1016/j.tcb.2016.02.006 · Cited by 362 · see citing works
McKim, D. B., Weber, M. D., Niraula, A., Sawicki, C. M., Liu, X., Jarrett, B. L., Ramirez-Chan, K., Wang, Y., Roeth, R. M., Sucaldito, A. D., et al. (2018) · Molecular Psychiatry · doi:10.1038/mp.2017.64 · Cited by 365 · see citing works
Microglia: Agents of the CNS Pro-Inflammatory Response
Rodríguez-Gómez, J. A., Kavanagh, E., Engskog-Vlachos, P., Engskog, M. K. R., Herrera, A. J., Espinosa-Oliva, A. M., Joseph, B., Hajji, N., Venero, J. L., & Burguillos, M. A. (2020) · Cells · doi:10.3390/cells9071717 · Cited by 365 · see citing works
- Authors
- Elmore, M. R. P., Najafi, A. R., Koike, M. A., Dagher, N. N., Spangenberg, E. E., Rice, R. A., Kitazawa, M., Matusow, B., Nguyen, H., West, B. L., & Green, K. N.
- Affiliations
- University of California, Irvine (US)
- University of California, Merced (US)
- Plexxikon (United States) (US)
- Corresponding author
- Green, Kim N.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2014-04
- Volume
- 82
- Issue
- 2
- Pages
- 380-397
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC4161285
- OpenAlex
- W2104431737
- Cited by
- 1,968
- References
- 46
- Citations by year
- 2026: 161 · 2025: 182 · 2024: 240 · 2023: 172 · 2022: 201 · 2021: 245 · 2020: 191 · 2019: 154 · 2018: 128 · 2017: 101 · 2016: 88 · 2015: 75 · 2014: 27
- FWCI
- 50.08
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institutes of Health (1R01NS083801, F31NS086409, UL1 TR000153)
- Whitehall Foundation
- National Institute of Neurological Disorders and Stroke
- American Federation for Aging Research
- Alzheimer's Association (AG00538)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Health Sciences › Medicine › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
- Keywords
- colony-stimulating factor 1 receptor, CSF1R signaling, microglia, CSF1R inhibitor, microglial depletion, microglial repopulation, nestin-positive cells, microglial proliferation, microglial differentiation, adult brain, microglial homeostasis, myeloid lineage
- MeSH terms
- Animals, Animals, Newborn, Brain, Enzyme Inhibitors, Gene Expression Regulation, Lipopolysaccharides, Male, Mice, Inbred C57BL, Mice, Transgenic, Nerve Tissue Proteins, Time Factors, Signal Transduction, Macrophage Colony-Stimulating Factor, Receptor, Macrophage Colony-Stimulating Factor, Cell Death, Microglia, Maze Learning, Cell Proliferation, Mice, Adult Stem Cells
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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