New tools for studying microglia in the mouse and human CNS
Open accessAbstract
Significance: Microglia are the tissue resident macrophages of the brain and spinal cord, implicated in important developmental, homeostatic, and disease processes, although our understanding of their roles is complicated by an inability to distinguish microglia from related cell types. Although they share many features with other macrophages, microglia have distinct developmental origins and functions. Here we validate a stable and robustly expressed microglial marker for both mouse and human, transmembrane protein 119 (Tmem119). We use custom-made antibodies against Tmem119 to perform deep RNA sequencing of developing microglia, and demonstrate that microglia mature by the second postnatal week in mice. The antibodies, cell isolation methods, and RNAseq profiles presented here will greatly facilitate our understanding of microglial function in health and disease.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
TMEM119 and P2RY12 have been shown to be expressed solely by microglial cells and not by infiltrating macrophages.
“TMEM119 and P2RY12 are especially useful, since they have been shown to be expressed solely by microglial cells and not by infiltrating macrophages [41,42,43].”
From Beyond Activation: Characterizing Microglial Functional Phenotypes (2021) · cites this paper as [41]
In “Macrophages After CNS Inflammation and Injury” (page not available), the paper reports that Tmem119 labels resident microglia but not infiltrating macrophages. It lists P2ry12 as a microglia-enriched candidate in “Tmem119 mRNA Expression Is Highly Enriched” (page not available), but does not establish that P2ry12 is expressed solely by microglia or absent from infiltrating macrophages. (LLM, conf=0.88)
Experimental — accuracy not yet measuredThe upregulation of inflammatory genes in microglia is not observed with a mechanical dissociation at 4°C.
“The phenomenon was not observed with a mechanical dissociation at 4°C (Bennett et al., 2016).”
From Single-cell resolution analysis of the crosstalk between chemogenically activated astrocytes and microglia (2020) · cites this paper as Bennett et al., 2016
The section on Tmem119-purified microglia describes mechanical brain homogenization, and “RNAseq Profiles Quality and Purity” reports significantly lower expression of inflammatory activation markers than in published profiles. It concludes that the procedure limits activation, not that inflammatory-gene upregulation is absent; our copy also does not specify dissociation at 4°C. Page numbers are unavailable in the indexed passages. (LLM, conf=0.86)
Experimental — accuracy not yet measuredEnzymatic dissociation of brain tissue at 37°C results in an upregulation of inflammatory genes in microglia.
“Research has also shown that the enzymatic dissociation of brain tissue at 37°C results in an upregulation of inflammatory genes in microglia.”
From Single-cell resolution analysis of the crosstalk between chemogenically activated astrocytes and microglia (2020) · cites this paper as Bennett et al., 2016
The section “RNAseq Profiles Quality and Purity: Lower Expression of Activation Marker Genes” reports lower expression of inflammatory activation markers in microglia isolated by the authors’ procedure than in published datasets that used enzymatic digestion or Percoll. It does not specify 37°C or establish that enzymatic dissociation itself caused the higher expression; the procedures differed in other ways too. The “Other Analyses: Microglial Activation” section attributes inflammatory-gene upregulation to LPS, not dissociation. Page numbers are unavailable in our copy. (LLM, conf=0.82)
Experimental — accuracy not yet measuredIl-1α, TNFα, and C1q are highly expressed specifically by microglia.
“All three of these cytokines are highly expressed specifically by microglia13,15, again suggesting a critical role for microglia in inducing A1 reactive astrocytes.”
From Neurotoxic reactive astrocytes are induced by activated microglia (2017) · cites this paper as [15]
In “Tmem119 mRNA Expression Is Highly Enriched in the CNS and Specific,” Il1a is listed among highly expressed microglia-enriched candidates. The RNA-seq section reports much higher C1q gene expression in microglia than in other myeloid cells, but also identifies C1q-positive macrophages. The activation section reports Tnf upregulation after LPS, not that TNFα is highly expressed specifically by microglia. No page numbers are supplied for these passages. (LLM, conf=0.88)
Experimental — accuracy not yet measuredTMEM119 is stably and specifically expressed in microglia and can be used to distinguish microglia from resident and infiltrating macrophages.
“TMEM119 has been shown to be stably and specifically expressed in microglia [41,44], and it can be used to distinguish microglia from resident and infiltrating macrophages [41].”
From Beyond Activation: Characterizing Microglial Functional Phenotypes (2021) · cites this paper as [41]
Rodent studies demonstrated TMEM119 expression in 98% of CD45lowCD11b+ cells in adult animals.
“while rodent studies even demonstrated an expression of 98% of CD45lowCD11b+ cells in adult animals [41].”
From Beyond Activation: Characterizing Microglial Functional Phenotypes (2021) · cites this paper as [41]
TMEM119 is a canonical microglia marker not expressed by other CNS resident macrophages.
“we performed in situ RNA labeling for TMEM119, a canonical microglia marker not expressed by other CNS resident macrophages (Bennett et al. 2016).”
From Depletion of Microglia Increases Cortical Oligodendrocyte Density During Remyelination (2026) · cites this paper as Bennett et al. 2016
Tmem119 is a microglia-specific marker.
“we co-stained for CD11b and for the transmembrane protein 119 (Tmem119), a microglia specific marker (M. L. Bennett et al., 2016).”
From Activated microglia drive demyelination via <scp>CSF1R</scp> signaling (2021) · cites this paper as M. L. Bennett et al., 2016
A low but significant number of donor-derived immune cells in the brain were Tmem119+, indicating that they had adopted a microglia-like phenotype.
“We thereby identified a low but significant number of donor-derived immune cells that were Tmem119+, indicating that they had adopted a microglia-like phenotype35 (Figure 2E).”
From TET2-mutant myeloid cells mitigate Alzheimer’s disease progression via CNS infiltration and enhanced phagocytosis in mice (2025) · cites this paper as [35]
SPI1, MS4A4A, MS4A6A, and SELL are specifically expressed in microglia based on RNA-Seq data.
“Further, SPI1, MS4A4A, MS4A6A, and SELL are specifically expressed in microglia based on RNA-Seq data29–31”
From A common haplotype lowers PU.1 expression in myeloid cells and delays onset of Alzheimer's disease (2017) · cites this paper as [30]
The sections on Tmem119-purified transcriptomes and microglial maturation describe RNA-seq profiling and identify other microglia-enriched genes, but do not identify SPI1, MS4A4A, MS4A6A, or SELL as specifically expressed in microglia. Searches for the four genes, including mouse-style capitalization, found no passage establishing the claim. Page numbers were not available in our copy. (LLM, conf=0.72)
Experimental — accuracy not yet measuredAnimal microglia are often inaccessible to real-time imaging and cannot fully reflect human biology.
“Animal microglia are often inaccessible to real-time imaging, and cannot fully reflect human biology.15–17”
From Tubular human brain organoids to model microglia-mediated neuroinflammation (2021) · cites this paper as [15]
The introduction describes difficulty distinguishing microglia from other immune cells, not a lack of access to real-time imaging. A later RNAseq discussion mentions transcranial two-photon imaging of mouse microglia, but does not establish how often imaging is possible. The passages examined also do not say that animal microglia cannot fully reflect human biology (searched: real-time imaging, live imaging, mouse–human differences). (LLM, conf=0.72)
Experimental — accuracy not yet measuredWAVE2 is expressed at high levels in microglia and vascular endothelial cells.
“WAVE2 is expressed at high levels in microglia and vascular endothelial cells14,15.”
From The WAVE complex in developmental and adulthood brain disorders (2025) · cites this paper as [15]
The RNA-seq profiles section discusses microglial gene expression and compares Pdgfb expression with endothelial cells, but it does not address WAVE2. Searches for WAVE2 and Wasf2 found no passage establishing high expression in either microglia or vascular endothelial cells; page numbers were not available in our copy. (LLM, conf=0.72)
Experimental — accuracy not yet measuredP2RY12 and TMEM119 are also expressed in human microglia.
“Several of these microglial genes were also observed in human microglia, including P2RY12 and TMEM119 (REFs25,33–36).”
From Microglial signatures and their role in health and disease (2018) · cites this paper as [35]
Microglia express lower CD45 than monocytes, allowing discrimination, and CD163 expression distinguishes microglia from perivascular macrophages.
“microglia express lower levels of receptor-type tyrosine-protein phosphatase C (PTPRC; also known as CD45) than monocytes, allowing these two cell types to be discriminated, whereas the expression of scavenger receptor cysteine-rich type 1 protein M130 (CD163) by microglia enables their distinction from perivascular macrophages35,44–47.”
From Microglial signatures and their role in health and disease (2018) · cites this paper as [35]
The Blue module contained several homeostatic microglial genes (Tmem119, P2ry12, Mtss1, Tgfbr1).
“Within these three AD modules, we observed enrichment of pro-inflammatory genes in the Magenta module (Ptgs2, Il12b, Tlr2, Hif1a, Cd69, Il1b, Cxcl16 and Irg1) and anti-inflammatory and phagocytic genes in the Yellow module (Igf1, Dpp7, Apoe, Spp1, Cd200r4 and Lpl) [38] while the Blue module contained several homeostatic microglial genes (Tmem119, P2ry12, Mtss1 and Tgfbr1, Fig. 2d) [39].”
From Identification and therapeutic modulation of a pro-inflammatory subset of disease-associated-microglia in Alzheimer’s disease (2018) · cites this paper as [39]
Region-specific bulk RNA-seq was performed on highly purified homeostatic microglia sorted with TMEM119 antibodies, which label over 90% of microglia in the adult brain.
“we performed region-specific bulk RNA-seq of highly purified homeostatic microglia sorted with TMEM119 antibodies, which label over 90% of microglia in the adult brain (Bennett et al., 2016).”
From Developmental Heterogeneity of Microglia and Brain Myeloid Cells Revealed by Deep Single-Cell RNA Sequencing (2019) · cites this paper as Bennett et al., 2016
A recently developed cell extraction protocol was used to minimize microglial activation.
“We used a recently developed protocol for cell extraction to minimize microglial activation (Bennett et al., 2016).”
From Developmental Heterogeneity of Microglia and Brain Myeloid Cells Revealed by Deep Single-Cell RNA Sequencing (2019) · cites this paper as Bennett et al., 2016
Yolk sac-derived microglia express Tmem119++, Sall1, Gpr56, and Apoe.
“Barres group recently identified Tmem119++/Sall1+/Gpr56+/Apoe+ as yolk sac-derived microglia, whereas hematopoietic stem cell-derived microglia-like cells express Tmem119+/Ms4a7+/Clec12a+/Apoe+++ suggesting lineage-specific microglia markers that can be useful in determining the origin of microglia [18, 19].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [19]
Lineage-specific microglial markers can be useful in determining the origin of microglia.
“suggesting lineage-specific microglia markers that can be useful in determining the origin of microglia [18, 19].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [19]
Hematopoietic stem cell-derived microglia-like cells express Tmem119, Ms4a7, Clec12a, and high Apoe.
“Barres group recently identified Tmem119++/Sall1+/Gpr56+/Apoe+ as yolk sac-derived microglia, whereas hematopoietic stem cell-derived microglia-like cells express Tmem119+/Ms4a7+/Clec12a+/Apoe+++ suggesting lineage-specific microglia markers that can be useful in determining the origin of microglia [18, 19].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [19]
Microglia express a unique set of genes distinct from infiltrating monocytes and other immune cells.
“Recent genomic and proteomic studies revealed microglia express a unique set of genes distinct from infiltrating monocytes and other immune cells [18, 19].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [19]
Mature pMGLs stained positive for markers of murine and human microglia, with TMEM119 and P2RY12 displaying broad membrane and punctate vesicular expression.
“Mature pMGLs stained positive for markers of murine and human microglia 10,11,29,30, with both TMEM119 and P2RY12 displaying a broad membrane and punctate vesicular expression pattern”
From Efficient derivation of microglia-like cells from human pluripotent stem cells (2016) · cites this paper as [10]
Microglia-like cells matching acutely isolated microglial signatures and following non-monocytic yolk sac ontogeny had not been reported from human pluripotent cells.
“However, generation of microglia-like cells matching the recently identified signatures of acutely isolated microglia 10,11, and following their non-monocytic yolk sac ontogeny 4, has not been reported from pluripotent human cells.”
From Efficient derivation of microglia-like cells from human pluripotent stem cells (2016) · cites this paper as [10]
In mouse, several microglia-specific genes are upregulated in brain-resident microglia through early postnatal development.
“In the mouse, several microglia-specific genes appear to be upregulated in brain-resident microglia through early postnatal development 10.”
From Efficient derivation of microglia-like cells from human pluripotent stem cells (2016) · cites this paper as [10]
Cx3cr1+ perivascular/meningeal macrophages, identified by low Tmem119, low Hexb, and high Mrc1, were excluded from single-cell analysis.
“Cx3cr1+ perivascular/meningeal macrophages were identified by low Tmem119, low Hexb, and high Mrc1 expression35,84 and excluded from single cell analysis (n=1-5 per plate).”
From Epigenetic regulation of brain region-specific microglia clearance activity (2018) · cites this paper as [84]
Addition of CD200 and CX3CL1 to iMGLs increased expression of select genes like COMT, CD52, and HLADRB5 while maintaining similar expression levels of core-microglial genes and AD-risk genes.
“The addition of CD200 and CX3CL1 to iMGLs increased the expression of select genes like COMT (Bennett et al., 2016)(Figure S5B), CD52, a cell surface receptor that binds Siglec-10 and interacts with DAP12 as part of the microglia sensome (Hickman et al., 2013) and HLADRB5, a member of the MHC II complex implicated in AD, while maintaining similar expression levels of core-microglial genes (e.g. P2”
From iPSC-derived human microglia-like cells to study neurological diseases (2017) · cites this paper as Bennett et al., 2016
Over 90% of CD11b+ cells in brains from 5xFAD Rubicon+/− and −/− mice were TMEM119+, and TMEM119+ cells isolated from 5xFAD Rubicon−/− mice had higher Iba1 expression compared to Rubicon+/− animals.
“We observed that over 90% of CD11b+ cells in brains from the 5xFAD Rubicon+/− and−/− mice were TMEM119+ (a microglia-specific marker (Bennett et al., 2016)) (Fig. S5C,D). Furthermore, the TMEM119+ cells isolated from 5xFAD Rubicon−/− mice had higher Iba1 expression compared to Rubicon+/− animals (Fig. S5E).”
From LC3-Associated Endocytosis Facilitates β-Amyloid Clearance and Mitigates Neurodegeneration in Murine Alzheimer’s Disease (2019) · cites this paper as Bennett et al., 2016
The identification of the transmembrane protein TMEM119 as a specific marker of microglia has enabled global gene expression profiling of highly pure preparations of microglia.
“In particular, the identification of the transmembrane protein TMEM119 as a specific marker of microglia has enabled global gene expression profiling of highly pure preparations of microglia (9).”
From The Transcriptional Landscape of Microglial Genes in Aging and Neurodegenerative Disease (2019) · cites this paper as [9]
TMEM119 is a highly specific and well-validated marker of brain-derived microglia in both mice and humans.
“We analyzed TMEM119 in bulk human brain tissue data from the Allen Brain Institute (13) because it is a highly specific and well-validated marker of brain-derived microglia in both mice and humans.”
From The Transcriptional Landscape of Microglial Genes in Aging and Neurodegenerative Disease (2019) · cites this paper as [9]
TMEM119 appears to exhibit stable expression even in response to a variety of inflammatory conditions.
“and appears to exhibit stable expression even in response to a variety of inflammatory conditions (9, 96).”
From The Transcriptional Landscape of Microglial Genes in Aging and Neurodegenerative Disease (2019) · cites this paper as [9]
We utilized TMEM119 as a marker of microglial expression, which was shown in 2016 to be a highly specific marker of brain-derived microglia.
“Secondly, we utilized TMEM119 as a marker of microglial expression, which was shown in 2016 to be a highly specific marker of brain-derived microglia (9).”
From The Transcriptional Landscape of Microglial Genes in Aging and Neurodegenerative Disease (2019) · cites this paper as [9]
TMEM119 has been shown to be stably and selectively expressed in adult microglia.
“TMEM119 has been shown to be stably and selectively expressed in adult microglia (9, 95)”
From The Transcriptional Landscape of Microglial Genes in Aging and Neurodegenerative Disease (2019) · cites this paper as [9]
Genes previously identified to be associated specifically with microglia but not with blood monocytes showed similar expression in co-pMG and fetalMG.
“As a set, genes previously identified to be associated specifically with microglia but not with blood monocytes (Bennett et al., 2016, Butovsky et al., 2014, Melief et al., 2012) (Figure 2C) showed similar expression in co-pMG and fetalMG.”
From A highly efficient human pluripotent stem cell microglia model displays a neuronal-co-culture-specific expression profile and inflammatory response (2017) · cites this paper as Bennett et al., 2016
Mcm5 is an established regulator of microglial cell cycle that is strongly expressed during embryonic and early postnatal microglial development.
“Mcm5, an established regulator of microglial cell cycle that is strongly expressed during embryonic and early postnatal microglial development”
From Mouse microglia express unique miRNA-mRNA networks to facilitate age-specific functions in the developing central nervous system (2023) · cites this paper as [38]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Robinson, M. D., McCarthy, D. J., & Smyth, G. K. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btp616 · Cited by 41,364 · see citing works
Gene Expression Omnibus: NCBI gene expression and hybridization array data repository
Edgar, R. (2002) · Nucleic Acids Research · doi:10.1093/nar/30.1.207 · Cited by 13,288 · see citing works
Trapnell, C., Roberts, A., Goff, L. A., Pertea, G. M., Kim, D., Kelley, D. R., Pimentel, H., Salzberg, S. L., Rinn, J. L., & Pachter, L. S. (2012) · Nature Protocols · doi:10.1038/nprot.2012.016 · Cited by 11,930 · see citing works
Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo
Nimmerjahn, A., Kirchhoff, F., & Helmchen, F. (2005) · Science · doi:10.1126/science.1110647 · Cited by 5,827 · see citing works
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
Zhang, Y., Chen, K., Sloan, S. A., Bennett, M. L., Scholze, A. R., O'Keeffe, S., Phatnani, H. P., Guarnieri, P., Caneda, C., Ruderisch, N., et al. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.1860-14.2014 · Cited by 4,875 · cited 2× · see citing works
“We calculated percentile ranks for several canonical activation genes for our naïve and LPS-stimulated samples, as well as five published datasets (15, 17, 30, 33, 34); these datasets were generated using CD45 or Cx3cr1 rather than a specific microglia marker, such as Tmem119, and used enzymatic digestion or Percoll f…”
MethodSelf-citationMicroglia Sculpt Postnatal Neural Circuits in an Activity and Complement-Dependent Manner
Schafer, D. P., Lehrman, E. K., Kautzman, A. G., Koyama, R., Mardinly, A. R., Yamasaki, R., Ransohoff, R. M., Greenberg, M. E., Barres, B. A., & Stevens, B. (2012) · Neuron · doi:10.1016/j.neuron.2012.03.026 · Cited by 4,089 · cited 1× · see citing works
“Given the recently identified novel role for the complement cascade and microglia in synaptic phagocytosis in normal development and disease (48), we compared expression of relevant genes in microglia and CNS macrophages.”
BackgroundSelf-citationATP mediates rapid microglial response to local brain injury in vivo
Davalos, D., Grutzendler, J., Yang, G., Kim, J. V., Zuo, Y., Jung, S., Littman, D. R., Dustin, M. L., & Gan, W.-B. (2005) · Nature Neuroscience · doi:10.1038/nn1472 · Cited by 3,913 · see citing works
Fate Mapping Reveals Origins and Dynamics of Monocytes and Tissue Macrophages under Homeostasis
Yona, S., Kim, K.-W., Wolf, Y., Mildner, A., Varol, D., Breker, M., Strauss-Ayali, D., Viukov, S., Guilliams, M., Misharin, A., et al. (2013) · Immunity · doi:10.1016/j.immuni.2012.12.001 · Cited by 3,245 · see citing works
<i>TREM2</i> Variants in Alzheimer's Disease
Guerreiro, R., Wojtas, A., Bras, J., Carrasquillo, M., Rogaeva, E., Majounie, E., Cruchaga, C., Sassi, C., Kauwe, J. S. K., Younkin, S., et al. (2013) · New England Journal of Medicine · doi:10.1056/nejmoa1211851 · Cited by 3,020 · see citing works
Jung, S., Aliberti, J., Graemmel, P., Sunshine, M. J., Kreutzberg, G. W., Sher, A., & Littman, D. R. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.11.4106-4114.2000 · Cited by 2,632 · 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
Identification of a unique TGF-β–dependent molecular and functional signature in microglia
Butovsky, O., Jedrychowski, M. P., Moore, C. S., Cialic, R., Lanser, A. J., Gabriely, G., Koeglsperger, T., Dake, B., Wu, P. M., Doykan, C. E., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3599 · Cited by 2,543 · see citing works
jvenn: an interactive Venn diagram viewer
Bardou, P., Mariette, J., Escudié, F., Djemiel, C., & Klopp, C. (2014) · BMC Bioinformatics · doi:10.1186/1471-2105-15-293 · Cited by 2,506 · see citing works
Genomic analysis of reactive astrogliosis
Zamanian, J. L., Xu, L., Foo, L. C., Nouri, N., Zhou, L., Giffard, R. G., & Barres, B. A. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.6221-11.2012 · Cited by 2,404 · see citing works
Self-citationMartínez, F. O., Gordon, S., Locati, M., & Mantovani, A. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.10.7303 · Cited by 2,336 · see citing works
Pericyte Loss and Microaneurysm Formation in PDGF-B-Deficient Mice
Lindahl, P., Johansson, B. R., Levéen, P., & Betsholtz, C. (1997) · Science · doi:10.1126/science.277.5323.242 · Cited by 2,226 · see citing works
Tissue-Resident Macrophage Enhancer Landscapes Are Shaped by the Local Microenvironment
Lavin, Y., Winter, D., Blecher-Gonen, R., David, E., Keren-Shaul, H., Merad, M., Jung, S., & Amit, I. (2014) · Cell · doi:10.1016/j.cell.2014.11.018 · Cited by 2,167 · see citing works
Pericytes are required for blood–brain barrier integrity during embryogenesis
Daneman, R., Zhou, L., Kebede, A. A., & Barres, B. A. (2010) · Nature · doi:10.1038/nature09513 · Cited by 2,128 · see citing works
Self-citationthe 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 · see citing works
TREM2 Lipid Sensing Sustains the Microglial Response in an Alzheimer’s Disease Model
Wang, Y., Cella, M., Mallinson, K., Ulrich, J. D., Young, K. L., Robinette, M. L., Gilfillan, S., Krishnan, G. M., Sudhakar, S., Zinselmeyer, B. H., et al. (2015) · Cell · doi:10.1016/j.cell.2015.01.049 · Cited by 1,736 · see citing works
Local self-renewal can sustain CNS microglia maintenance and function throughout adult life
Ajami, B., Bennett, J. L., Krieger, C., Tetzlaff, W., & Rossi, F. M. V. (2007) · Nature Neuroscience · doi:10.1038/nn2014 · Cited by 1,643 · see citing works
Self-citationThe P2Y12 receptor regulates microglial activation by extracellular nucleotides
Haynes, S. E., Hollopeter, G., Yang, G., Kurpius, D., Dailey, M. E., Gan, W.-B., & Julius, D. (2006) · Nature Neuroscience · doi:10.1038/nn1805 · Cited by 1,542 · see citing works
Astrocytes mediate synapse elimination through MEGF10 and MERTK pathways
Chung, W.-S., Clarke, L. E., Wang, G. X., Stafford, B. K., Sher, A., Chakraborty, C., Joung, J., Foo, L. C., Thompson, A., Chen, C., et al. (2013) · Nature · doi:10.1038/nature12776 · Cited by 1,377 · cited 1× · see citing works
“Microglia also express significantly higher levels of opsonins (Pros1, Gas6) that promote synaptic phagocytosis by astrocytes (49).”
BackgroundSelf-citationGosselin, D., Link, V. M., Romanoski, C. E., Fonseca, G. J., Eichenfield, D. Z., Spann, N. J., Stender, J. D., Chun, H. B., Garner, H., Geissmann, F., et al. (2014) · Cell · doi:10.1016/j.cell.2014.11.023 · Cited by 1,307 · see citing works
Langenbach, R. J., Morham, S. G., Tiano, H. F., Loftin, C. D., Ghanayem, B. I., Chulada, P. C., Mahler, J. F., Lee, C. A., Goulding, E. H., Kluckman, K. D., et al. (1995) · Cell · doi:10.1016/0092-8674(95)90126-4 · Cited by 1,120 · 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
The 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 · see citing works
Microglia derive from progenitors, originating from the yolk sac, and which proliferate in the brain
Alliot, F., Godin, I., & Pessac, B. (1999) · Developmental Brain Research · doi:10.1016/s0165-3806(99)00113-3 · Cited by 884 · see citing works
Microglia: Scapegoat, saboteur, or something else?
Aguzzi, A., Barres, B. A., & Bennett, M. L. (2013) · Science · doi:10.1126/science.1227901 · Cited by 836 · see citing works
Self-citationCatechol-o-Methyltransferase, Cognition, and Psychosis: Val158Met and Beyond
Tunbridge, E. M., Harrison, P. J., & Weinberger, D. R. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.10.024 · Cited by 685 · see citing works
Laminin receptor on platelets is the integrin VLA-6
Sonnenberg, A., Modderman, P. W., & Hogervorst, F. B. L. (1988) · Nature · doi:10.1038/336487a0 · Cited by 678 · 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
Control of excitatory CNS synaptogenesis by astrocyte-secreted proteins Hevin and SPARC
Kucukdereli, H., Allen, N. J., Lee, A. T., Feng, A., Ozlu, M. I., Conatser, L. M., Chakraborty, C., Workman, G., Weaver, M., Sage, E. H., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1104977108 · Cited by 642 · see citing works
Self-citationBruttger, 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
Ford, A. L., Goodsall, A. L., Hickey, W. F., & Sedgwick, J. D. (1995) · The Journal of Immunology · doi:10.4049/jimmunol.154.9.4309 · Cited by 631 · see citing works
Perry, V. H., Brown, M. C., & Gordon, S. (1987) · The Journal of Experimental Medicine · doi:10.1084/jem.165.4.1218 · Cited by 604 · 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
Funk, C. D., Funk, L. B., Kennedy, M. E., Pong, A. S., & FitzGerald, G. A. (1991) · The FASEB Journal · doi:10.1096/fasebj.5.9.1907252 · Cited by 568 · see citing works
Genome-wide RNA-seq analysis of human and mouse platelet transcriptomes
Rowley, J. W., Oler, A. J., Tolley, N. D., Hunter, B. N., Low, E. N., Nix, D. A., Yost, C. C., Zimmerman, G. A., & Weyrich, A. S. (2011) · Blood · doi:10.1182/blood-2011-03-339705 · Cited by 562 · see citing works
Most Tissue-Resident Macrophages Except Microglia Are Derived from Fetal Hematopoietic Stem Cells
Sheng, J., Ruedl, C., & Karjalainen, K. (2015) · Immunity · doi:10.1016/j.immuni.2015.07.016 · Cited by 482 · see citing works
Defective oligodendrocyte development and severe hypomyelination in PDGF-A knockout mice
Fruttiger, M., Karlsson, L. K., Hall, A. C., Abramsson, A., Calver, A. R., Boström, H., Willetts, K. E., Bertold, C.-H., Heath, J. K., Betsholtz, C., et al. (1999) · Development · doi:10.1242/dev.126.3.457 · Cited by 440 · see citing works
Chen, Z., Jalabi, W., Shpargel, K. B., Farabaugh, K. T., Dutta, R., Yin, X., Kidd, G. J., Bergmann, C. C., Stohlman, S. A., & Trapp, B. D. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.0730-12.2012 · Cited by 432 · see citing works
Purinergic receptor P2RY12-dependent microglial closure of the injured blood–brain barrier
Lou, N., Takano, T., Pei, Y., Xavier, A. L., Goldman, S. A., & Nedergaard, M. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1520398113 · Cited by 364 · see citing works
Bone marrow derived elements and resident microglia in brain inflammation
Lassmann, H., Schmied, M. C., Vass, K., & Hickey, W. F. (1993) · Glia · doi:10.1002/glia.440070106 · Cited by 349 · see citing works
Echeverry, S., Shi, X. Q., & Zhang, J. (2008) · Pain · doi:10.1016/j.pain.2007.05.002 · Cited by 211 · see citing works
Capotondo, A., Milazzo, R., Politi, L. S., Quattrini, A., Palini, A. G., Plati, T., Merella, S., Nonis, A., Serio, C. D., Montini, E., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1205858109 · Cited by 207 · see citing works
Efficient isolation of live microglia with preserved phenotypes from adult mouse brain
Nikodémová, M., & Watters, J. J. (2012) · Journal of Neuroinflammation · doi:10.1186/1742-2094-9-147 · Cited by 165 · see citing works
Gehrmann, J., & Banati, R. B. (1995) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-199509000-00010 · Cited by 147 · see citing works
Hypoxanthine-Guanine Phosphoribosyltransferase Deficiency
Flier, J. S., Moore, M. J., Wilson, J. M., et al. (1983) · New England Journal of Medicine · doi:10.1056/nejm198310133091507 · Cited by 145 · see citing works
Isolation of brain and spinal cord mononuclear cells using percoll gradients.
Pino, P., & Cardona, A. (2011) · Journal of Visualized Experiments · doi:10.3791/2348 · Cited by 142 · see citing works
Sung, L., Gao, S., Shen, H., Yu, H. M., Song, Y., Marjani, S. L., Chang, C.-C., Inoue, K., Kuo, L., Lian, J., et al. (2006) · Nature Genetics · doi:10.1038/ng1895 · Cited by 123 · see citing works
Hisa, I., Inoue, Y., Hendy, G. N., Canaff, L., Kitazawa, R., Kitazawa, S., Komori, T., Sugimoto, T., Seino, S., & Kaji, H. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.179127 · Cited by 87 · see citing works
Intermediate filament change in astrocytes following mild cortical contusion
Baldwin, S. A., & Scheff, S. W. (1996) · Glia · doi:10.1002/(sici)1098-1136(199603)16:3 · Cited by 81 · see citing works
Tanaka, K.-I., Inoue, Y., Hendy, G. N., et al. (2012) · Bone · doi:10.1016/j.bone.2012.04.017 · Cited by 51 · see citing works
Hieronymus, T., Gust, T. C., Kirsch, R. D., Jorgas, T., Blendinger, G., Goncharenko, M., Supplitt, K., Rose‐John, S., Müller, A. M., & Zenke, M. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.5.2552 · Cited by 47 · see citing works
Isolation of Brain and Spinal Cord Mononuclear Cells Using Percoll Gradients
Pino, P. A., & Cardona, A. E. (2011) · Journal of Visualized Experiments · doi:10.3791/2348-v · Cited by 34 · see citing works
Peripheral Nerve Lesion Induces an Up-regulation of Spy1 in Rat Spinal Cord
Huang, Y., Liu, Y., Chen, Y., et al. (2008) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-008-9332-8 · Cited by 15 · see citing works
Flagged first, then by citations
Research works printed but not linked: 3
- Frank M, Wolburg H (1996) Cellular reactions at the lesion site after crushing of the rat optic nerve. Glia 16(3):227-240.
- Tremblay ME, et al. (2011) The role of microglia in the healthy brain. J Neurosci 31(45):16064-16069.
- Wilson JM, Young AB, Young AB, Kelley WN (1983) Hypoxanthine-guanine phos- phoribosyltransferase deficiency. The molecular basis of the clinical syndromes. N Engl J Med 309(15):900-910.
Cited by
Sorted by citations
Neurotoxic reactive astrocytes are induced by activated microglia
Liddelow, S. A., Guttenplan, K. A., Clarke, L. E., Bennett, F. C., Bohlen, C. J., Schirmer, L., Bennett, M. L., Münch, A. E., Chung, W.-S., Peterson, T. C., et al. (2017) · Nature · doi:10.1038/nature21029 · Cited by 7,971 · see citing works
Self-citationHammond, 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
Shared and distinct transcriptomic cell types across neocortical areas
Tasic, B., Yao, Z., Graybuck, L. T., Smith, K. A., Nguyen, T. N., Bertagnolli, D., Goldy, J., Garren, E., Economo, M. N., Viswanathan, S., et al. (2018) · Nature · doi:10.1038/s41586-018-0654-5 · Cited by 1,746 · see citing works
How neuroinflammation contributes to neurodegeneration
Ransohoff, R. M. (2016) · Science · doi:10.1126/science.aag2590 · Cited by 1,967 · 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
A polarizing question: do M1 and M2 microglia exist?
Ransohoff, R. M. (2016) · Nature Neuroscience · doi:10.1038/nn.4338 · Cited by 1,573 · 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
The central nervous system and the gut microbiome
Sharon, G., Sampson, T. R., Geschwind, D. H., & Mazmanian, S. K. (2016) · Cell · doi:10.1016/j.cell.2016.10.027 · Cited by 1,513 · see citing works
Marschallinger, J., Iram, T., Zardeneta, M., Lee, S. E., Lehallier, B., Haney, M. S., Pluvinage, J. V., Mathur, V., Hahn, O., Morgens, D. W., et al. (2020) · Nature Neuroscience · doi:10.1038/s41593-019-0566-1 · Cited by 1,384 · see citing works
A single-cell molecular map of mouse gastrulation and early organogenesis
Pijuan-Sala, B., Griffiths, J. A., Guibentif, C., Hiscock, T. W., Jawaid, W., Calero-Nieto, F. J., Mulas, C., Ibarra-Soria, X., Tyser, R. C. V., Ho, D. L. L., et al. (2019) · Nature · doi:10.1038/s41586-019-0933-9 · Cited by 1,033 · 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
iPSC-derived human microglia-like cells to study neurological diseases
Abud, E. M., Ramirez, R. N., Martinez, E. S., Healy, L. M., Nguyen, C. H. H., Newman, S. A., Yeromin, A. V., Scarfone, V. M., Marsh, S. E., Fimbres, C., et al. (2017) · Neuron · doi:10.1016/j.neuron.2017.03.042 · Cited by 1,154 · see citing works
Li, Q., Cheng, Z., Zhou, L., Darmanis, S., Neff, N. F., Okamoto, J., Gulati, G., Bennett, M. L., Sun, L. O., Clarke, L. E., et al. (2019) · Neuron · doi:10.1016/j.neuron.2018.12.006 · Cited by 1,129 · see citing works
Self-citationSpatial 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
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
Microglia in Alzheimer's disease
Sarlus, H., & Heneka, M. T. (2017) · Journal of Clinical Investigation · doi:10.1172/jci90606 · Cited by 911 · see citing works
Single-cell profiling identifies myeloid cell subsets with distinct fates during neuroinflammation
Jordão, M. J. C., Sankowski, R., Brendecke, S. M., Sagar, Locatelli, G., Tai, Y.-H., Tay, T. L., Schramm, E., Armbruster, S., Hagemeyer, N., et al. (2019) · Science · doi:10.1126/science.aat7554 · Cited by 843 · see citing works
Friedman, B. A., Srinivasan, K., Ayalon, G., Meilandt, W. J., Lin, H., Huntley, M. A., Cao, Y., Lee, S.-H., Haddick, P. C. G., Ngu, H., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2017.12.066 · Cited by 662 · see citing works
Loss of ‘homeostatic’ microglia and patterns of their activation in active multiple sclerosis
Zrzavy, T., Hametner, S., Wimmer, I., Butovsky, O., Weiner, H. L., & Lassmann, H. (2017) · Brain · doi:10.1093/brain/awx113 · Cited by 684 · 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
Self-citationEfficient derivation of microglia-like cells from human pluripotent stem cells
Muffat, J., Li, Y., Yuan, B., Mitalipova, M., Omer, A., Corcoran, S., Bakiasi, G., Tsai, L.-H., Aubourg, P., Ransohoff, R. M., et al. (2016) · Nature Medicine · doi:10.1038/nm.4189 · Cited by 651 · 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
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
Microglia and Central Nervous System–Associated Macrophages—From Origin to Disease Modulation
Prinz, M., Masuda, T., Wheeler, M. A., & Quintana, F. J. (2021) · Annual Review of Immunology · doi:10.1146/annurev-immunol-093019-110159 · Cited by 584 · see citing works
Haenseler, W., Sansom, S. N., Buchrieser, J., Newey, S. E., Moore, C. S., Nicholls, F. J., Chintawar, S., Schnell, C., Antel, J. P., Allen, N. D., et al. (2017) · Stem Cell Reports · doi:10.1016/j.stemcr.2017.05.017 · Cited by 593 · 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
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
A combination of ontogeny and CNS environment establishes microglial identity
Bennett, F. C., Bennett, M. L., Yaqoob, F., Mulinyawe, S. B., Grant, G. A., Hayden Gephart, M., Plowey, E. D., & Barres, B. A. (2018) · Neuron · doi:10.1016/j.neuron.2018.05.014 · Cited by 524 · see citing works
Self-citationGuidelines for the use of flow cytometry and cell sorting in immunological studies (third edition)
Cossarizza, A., Chang, H., Radbruch, A., Abrignani, S., Addo, R., Akdis, M., Andrä, I., Andreata, F., Annunziato, F., Arranz, E., et al. (2021) · European Journal of Immunology · doi:10.1002/eji.202170126 · Cited by 531 · 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
Mild respiratory COVID can cause multi-lineage neural cell and myelin dysregulation
Fernández-Castañeda, A., Lu, P., Geraghty, A. C., Song, E., Lee, M.-H., Wood, J., O’Dea, M. R., Dutton, S., Shamardani, K., Nwangwu, K., et al. (2022) · Cell · doi:10.1016/j.cell.2022.06.008 · Cited by 521 · see citing works
Self-citationControl of tumor-associated macrophages and T cells in glioblastoma via AHR and CD39
Takenaka, M. C., Gabriely, G., Rothhammer, V., Mascanfroni, I. D., Wheeler, M. A., Chao, C.-C., Gutiérrez-Vázquez, C., Kenison, J., Tjon, E. C., Barroso, A., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0370-y · Cited by 517 · see citing works
Heckmann, B. L., Teubner, B. J. W., Tummers, B., Boada-Romero, E., Harris, L., Yang, M., Guy, C. S., Zakharenko, S. S., & Green, D. R. (2019) · Cell · doi:10.1016/j.cell.2019.05.056 · Cited by 503 · see citing works
“We observed that over 90% of CD11b+ cells in brains from the 5xFAD Rubicon+/− and−/− mice were TMEM119+ (a microglia-specific marker (Bennett et al., 2016)) (Fig.”
Disease Progression-Dependent Effects of TREM2 Deficiency in a Mouse Model of Alzheimer's Disease
Jay, T. R., Hirsch, A. M., Broihier, M. L., Miller, C. M., Neilson, L. E., Ransohoff, R. M., Lamb, B. T., & Landreth, G. E. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.2110-16.2016 · Cited by 457 · see citing works
Microbiome–microglia connections via the gut–brain axis
Abdel-Haq, R., Schlachetzki, J. C. M., Glass, C. K., & Mazmanian, S. K. (2019) · Journal of Experimental Medicine · doi:10.1084/jem.20180794 · Cited by 471 · see citing works
A common haplotype lowers PU.1 expression in myeloid cells and delays onset of Alzheimer's disease
The International Genomics of Alzheimer's Project, Huang, K.-L., Initiative, T. A. D. N., Marcora, E., Pimenova, A. A., Di Narzo, A. F., Kapoor, M., Jin, S. C., Harari, O., Bertelsen, S., et al. (2017) · Nature Neuroscience · doi:10.1038/nn.4587 · Cited by 423 · see citing works
Rangaraju, S., Dammer, E. B., Raza, S. A., Rathakrishnan, P., Xiao, H., Gao, T., Duong, D. M., Pennington, M. W., Lah, J. J., Seyfried, N. T., et al. (2018) · Molecular Neurodegeneration · doi:10.1186/s13024-018-0254-8 · Cited by 430 · see citing works
Microglia use TAM receptors to detect and engulf amyloid β plaques
Huang, Y., Happonen, K. E., Burrola, P. G., O’Connor, C., Hah, N., Huang, L., Nimmerjahn, A., & Lemke, G. (2021) · Nature Immunology · doi:10.1038/s41590-021-00913-5 · Cited by 483 · 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
Self-citationNBB-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
CD22 blockade restores homeostatic microglial phagocytosis in ageing brains
Pluvinage, J. V., Haney, M. S., Smith, B. A. H., Sun, J., Iram, T., Bonanno, L., Li, L., Lee, D. P., Morgens, D. W., Yang, A. C., et al. (2019) · Nature · doi:10.1038/s41586-019-1088-4 · Cited by 459 · 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
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
Cignarella, F., Filipello, F., Bollman, B., Cantoni, C., Locca, A., Mikesell, R., Manis, M., Ibrahim, A., Deng, L., Benitez, B. A., et al. (2020) · Acta Neuropathologica · doi:10.1007/s00401-020-02193-z · Cited by 392 · see citing works
Directed differentiation of human pluripotent stem cells to microglia
Douvaras, P., Sun, B., Wang, M., Kruglikov, I., Lallos, G., Zimmer, M., Terrenoire, C., Zhang, B., Gandy, S., Schadt, E., et al. (2017) · Stem Cell Reports · doi:10.1016/j.stemcr.2017.04.023 · Cited by 381 · see citing works
NLRP3 inflammasome-driven pathways in depression: clinical and preclinical findings
Kaufmann, F. N., Costa, A. P., Ghisleni, G., Diaz, A. P., Rodrigues, A. L. S., Peluffo, H., & Kaster, M. P. (2017) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2017.03.002 · Cited by 370 · see citing works
IL-33 ameliorates Alzheimer's disease-like pathology and cognitive decline
Fu, A. K. Y., Hung, K.-W., Yuen, M. Y. F., Zhou, X., Mak, D. S. Y., Chan, I. C. W., Cheung, T. H., Zhang, B., Fu, W.-Y., Liew, F. Y., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1604032113 · Cited by 369 · 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
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
Immune Signaling in Neurodegeneration
Hammond, T. R., Marsh, S. E., & Stevens, B. (2019) · Immunity · doi:10.1016/j.immuni.2019.03.016 · Cited by 336 · see citing works
Microglia Phenotypes in Aging and Neurodegenerative Diseases
Wendimu, M. Y., & Hooks, S. B. (2022) · Cells · doi:10.3390/cells11132091 · Cited by 336 · see citing works
Neuroinflammation in frontotemporal dementia
Bright, F., Werry, E. L., Dobson-Stone, C., Piguet, O., Ittner, L. M., Halliday, G. M., Hodges, J. R., Kiernan, M. C., Loy, C. T., Kassiou, M., et al. (2019) · Nature Reviews Neurology · doi:10.1038/s41582-019-0231-z · Cited by 280 · see citing works
Knockout of reactive astrocyte activating factors slows disease progression in an ALS mouse model
Guttenplan, K. A., Weigel, M. K., Adler, D. I., Couthouis, J., Liddelow, S. A., Gitler, A. D., & Barres, B. A. (2020) · Nature Communications · doi:10.1038/s41467-020-17514-9 · Cited by 278 · see citing works
Self-citationBeyond Activation: Characterizing Microglial Functional Phenotypes
Lier, J., Streit, W. J., & Bechmann, I. (2021) · Cells · doi:10.3390/cells10092236 · Cited by 274 · see citing works
“In human brains, at least 50% of the IBA1-positive microglial population were positive for TMEM119 [45], while rodent studies even demonstrated an expression of 98% of CD45lowCD11b+ cells in adult animals [41].”
BackgroundUnger, M. S., Li, E., Scharnagl, L., Poupardin, R., Altendorfer, B., Mrowetz, H., Hutter-Paier, B., Weiger, T. M., Heneka, M. T., Attems, J., et al. (2020) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2020.05.070 · Cited by 248 · see citing works
Lee, J.-W., Nam, H., Kim, L. E., Jeon, Y., Min, H., Ha, S., Lee, Y., Kim, S.-Y., Lee, S. J., Kim, E.-K., et al. (2019) · Autophagy · doi:10.1080/15548627.2018.1556946 · Cited by 260 · see citing works
Microglial cell loss after ischemic stroke favors brain neutrophil accumulation
Otxoa-de-Amezaga, A., Miró-Mur, F., Pedragosa, J., Gallizioli, M., Justicia, C., Gaja-Capdevila, N., Ruíz-Jaen, F., Salas-Perdomo, A., Bosch, A., Calvo, M., et al. (2019) · Acta Neuropathologica · doi:10.1007/s00401-018-1954-4 · Cited by 258 · see citing works
Tmem119-EGFP and Tmem119-CreERT2 Transgenic Mice for Labeling and Manipulating Microglia
Kaiser, T., & Feng, G. (2019) · eneuro · doi:10.1523/eneuro.0448-18.2019 · Cited by 259 · see citing works
Harms, A. S., Thome, A. D., Yan, Z., Schonhoff, A. M., Williams, G. P., Li, X., Liu, Y., Qin, H., Benveniste, E. N., & Standaert, D. G. (2018) · Experimental Neurology · doi:10.1016/j.expneurol.2017.11.010 · Cited by 236 · see citing works
Morphology of Microglia Across Contexts of Health and Disease
Savage, J. C., Carrier, M., & Tremblay, M.-È. (2019) · Methods in Molecular Biology · doi:10.1007/978-1-4939-9658-2_2 · Cited by 232 · see citing works
Microglia affect α-synuclein cell-to-cell transfer in a mouse model of Parkinson’s disease
George, S., Rey, N. L., Tyson, T., Esquibel, C., Meyerdirk, L., Schulz, E., Pierce, S., Burmeister, A. R., Madaj, Z., Steiner, J. A., et al. (2019) · Molecular Neurodegeneration · doi:10.1186/s13024-019-0335-3 · Cited by 229 · see citing works
Microglia and Astrocytes in Disease: Dynamic Duo or Partners in Crime?
Liddelow, S. A., Marsh, S. E., & Stevens, B. (2020) · Trends in Immunology · doi:10.1016/j.it.2020.07.006 · Cited by 226 · see citing works
Self-citationUncovering sex differences of rodent microglia
Han, J., Fan, Y., Zhou, K., Blomgren, K., & Harris, R. A. (2021) · Journal of Neuroinflammation · doi:10.1186/s12974-021-02124-z · Cited by 224 · see citing works
Functional Studies of Missense TREM2 Mutations in Human Stem Cell-Derived Microglia
Brownjohn, P. W., Smith, J., Solanki, R., Lohmann, E., Houlden, H., Hardy, J., Dietmann, S., & Livesey, F. J. (2018) · Stem Cell Reports · doi:10.1016/j.stemcr.2018.03.003 · Cited by 193 · see citing works
Microglia and monocytes in inflammatory CNS disease: integrating phenotype and function
Spiteri, A. G., Wishart, C. L., Pamphlett, R., Locatelli, G., & King, N. J. C. (2022) · Acta Neuropathologica · doi:10.1007/s00401-021-02384-2 · Cited by 216 · see citing works
“Relative to BAM/CAMs, microglia uniquely express transmembrane protein 119 (TMEM119) [26], hexosaminidase subunit beta (Hexb) [174, 214, 215], P2Y G-protein-coupled 12 (P2RY12) [41], sialic acid-binding immunoglobulin-type lectin H (Siglec-H) and Spalt-like transcription factor 1 (Sall1) [45], express low levels of CD…”
BackgroundMethodCo-expression patterns of microglia markers Iba1, TMEM119 and P2RY12 in Alzheimer’s disease
Kenkhuis, B., Somarakis, A., Kleindouwel, L. R. T., van Roon-Mom, W. M. C., Höllt, T., & van der Weerd, L. (2022) · Neurobiology of Disease · doi:10.1016/j.nbd.2022.105684 · Cited by 188 · see citing works
Microglia in multiple sclerosis: Friend or foe
Guerrero, B. L., & Sicotte, N. L. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00374 · Cited by 215 · see citing works
TP53 gain-of-function mutation promotes inflammation in glioblastoma
Ham, S. W., Jeon, H.-Y., Jin, X., Kim, E.-J., Kim, J.-K., Shin, Y. J., Lee, Y., Kim, S. H., Lee, S. Y., Seo, S., et al. (2019) · Cell Death & Differentiation · doi:10.1038/s41418-018-0126-3 · Cited by 213 · see citing works
Plemel, J. R., Stratton, J. A., Michaels, N. J., Rawji, K. S., Zhang, E., Sinha, S., Baaklini, C. S., Dong, Y., Ho, M., Thorburn, K., et al. (2020) · Science Advances · doi:10.1126/sciadv.aay6324 · Cited by 208 · see citing works
Werner, Y., Mass, E., Ashok Kumar, P., Ulas, T., Händler, K., Horne, A., Klee, K., Lupp, A., Schütz, D., Saaber, F., et al. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-0585-y · Cited by 208 · see citing works
Neurons under T Cell Attack Coordinate Phagocyte-Mediated Synaptic Stripping
Di Liberto, G., Pantelyushin, S., Kreutzfeldt, M., Page, N., Musardo, S., Coras, R., Steinbach, K., Vincenti, I., Klimek, B., Lingner, T., et al. (2018) · Cell · doi:10.1016/j.cell.2018.07.049 · Cited by 195 · see citing works
Abels, E. R., Maas, S. L. N., Nieland, L., Wei, Z., Cheah, P. S., Tai, E., Kolsteeg, C.-J., Dusoswa, S. A., Ting, D. T., Hickman, S., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.08.036 · Cited by 199 · see citing works
Microglial immune checkpoint mechanisms
Deczkowska, A., Amit, I., & Schwartz, M. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0145-x · Cited by 185 · see citing works
Microglia in multiple sclerosis: protectors turn destroyers
Yong, V. W. (2022) · Neuron · doi:10.1016/j.neuron.2022.06.023 · Cited by 185 · see citing works
Iron loading is a prominent feature of activated microglia in Alzheimer’s disease patients
Kenkhuis, B., Somarakis, A., de Haan, L., Dzyubachyk, O., IJsselsteijn, M. E., de Miranda, N. F. C. C., Lelieveldt, B. P. F., Dijkstra, J., van Roon-Mom, W. M. C., Höllt, T., et al. (2021) · Acta Neuropathologica Communications · doi:10.1186/s40478-021-01126-5 · Cited by 184 · see citing works
Microglia and C9orf72 in neuroinflammation and ALS and frontotemporal dementia
Lall, D., & Baloh, R. H. (2017) · Journal of Clinical Investigation · doi:10.1172/jci90607 · Cited by 175 · see citing works
Oosterhof, N., Kuil, L. E., van der Linde, H. C., Burm, S. M., Berdowski, W., van Ijcken, W. F. J., van Swieten, J. C., Hol, E. M., Verheijen, M. H. G., & van Ham, T. J. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.06.113 · Cited by 178 · see citing works
Directed evolution of adeno-associated virus for efficient gene delivery to microglia
Lin, R., Zhou, Y., Yan, T., Wang, R., Li, H., Wu, Z., Zhang, X., Zhou, X., Zhao, F., Zhang, L., et al. (2022) · Nature Methods · doi:10.1038/s41592-022-01547-7 · Cited by 171 · see citing works
Microglia and Astrocyte Function and Communication: What Do We Know in Humans?
Garland, E. F., Hartnell, I. J., & Boche, D. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.824888 · Cited by 165 · see citing works
Zhan, L., Krabbe, G., Du, F., Jones, I., Reichert, M. C., Telpoukhovskaia, M., Kodama, L., Wang, C., Cho, S.-H., Sayed, F., et al. (2019) · PLOS Biology · doi:10.1371/journal.pbio.3000134 · Cited by 163 · see citing works
“(f-p) Relative gene expression of Mcm5 (f), Cdk1 (g), Nestin (h), Pmepa1(i), Smad7 (j), Mafb (k), Selplg (l), P2ry12 (m), Tmem119 (n), Trem2 (o) and Grn (p).”
BackgroundKlotho controls the brain-immune system interface in the choroid plexus
Zhu, L., Stein, L. R., Kim, D., Ho, K., Yu, G.-Q., Zhan, L., Larsson, T. E., & Mucke, L. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1808609115 · Cited by 148 · see citing works
Analyzing microglial phenotypes across neuropathologies: a practical guide
Schwabenland, M., Brück, W., Priller, J., Stadelmann, C., Lassmann, H., & Prinz, M. (2021) · Acta Neuropathologica · doi:10.1007/s00401-021-02370-8 · Cited by 149 · see citing works
Activated microglia drive demyelination via <scp>CSF1R</scp> signaling
Marzan, D. E., Brügger‐Verdon, V., West, B. L., Liddelow, S., Samanta, J., & Salzer, J. L. (2021) · Glia · doi:10.1002/glia.23980 · Cited by 147 · see citing works
“the identity of these cells during CUP-mediated demyelination, we co-stained for CD11b and for the transmembrane protein 119 (Tmem119), a microglia specific marker (Bennett et al., 2016).”
MethodSelf-citationSterling, J. K., Adetunji, M. O., Guttha, S., Bargoud, A. R., Uyhazi, K. E., Ross, A. G., Dunaief, J. L., & Cui, Q. N. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108271 · Cited by 148 · see citing works
Transcriptional profiling of microglia; current state of the art and future perspectives
Gerrits, E., Heng, Y., Boddeke, E. W. G. M., & Eggen, B. J. L. (2020) · Glia · doi:10.1002/glia.23767 · Cited by 140 · see citing works
Alzheimer’s disease phospholipase C-gamma-2 (PLCG2) protective variant is a functional hypermorph
Magno, L., Lessard, C. B., Martins, M., Lang, V., Cruz, P., Asi, Y., Katan, M., Bilsland, J., Lashley, T., Chakrabarty, P., et al. (2019) · Alzheimer's Research & Therapy · doi:10.1186/s13195-019-0469-0 · Cited by 143 · see citing works
An updated assessment of microglia depletion: current concepts and future directions
Han, J., Harris, R. A., & Zhang, X.-M. (2017) · Molecular Brain · doi:10.1186/s13041-017-0307-x · Cited by 141 · see citing works
Chhatbar, C., Detje, C. N., Grabski, E., Borst, K., Spanier, J., Ghita, L., Elliott, D. A., Jordão, M. J. C., Mueller, N., Sutton, J., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.09.003 · Cited by 141 · see citing works
Lehmann, M. L., Weigel, T. K., Poffenberger, C. N., & Herkenham, M. (2019) · The Journal of Neuroscience · doi:10.1523/jneurosci.0184-19.2019 · Cited by 138 · see citing works
Transcriptional and Epigenetic Regulation of Microglia in Health and Disease
Yeh, H., & Ikezu, T. (2019) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2018.11.004 · Cited by 135 · see citing works
Pinto, B., Morelli, G., Rastogi, M., Savardi, A., Fumagalli, A., Petretto, A., Bartolucci, M., Varea, E., Catelani, T., Contestabile, A., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.09.010 · Cited by 135 · see citing works
Jafar-nejad, P., Powers, B., Soriano, A., Zhao, H., Norris, D. A., Matson, J., DeBrosse-Serra, B., Watson, J., Narayanan, P., Chun, S. J., et al. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkaa1235 · Cited by 128 · see citing works
Walker, D. G., Tang, T. M., Mendsaikhan, A., Tooyama, I., Serrano, G. E., Sue, L. I., Beach, T. G., & Lue, L.-F. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21020678 · Cited by 128 · see citing works
Rangaraju, S., Raza, S. A., Li, N. X., Betarbet, R., Dammer, E. B., Duong, D., Lah, J. J., Seyfried, N. T., & Levey, A. I. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00405 · Cited by 126 · see citing works
Béland, L.-C., Markovinovic, A., Jakovac, H., De Marchi, F., Bilic, E., Mazzini, L., Kriz, J., & Munitic, I. (2020) · Brain Communications · doi:10.1093/braincomms/fcaa124 · Cited by 125 · see citing works
Chiot, A., Zaïdi, S., Iltis, C., Ribon, M., Berriat, F., Schiaffino, L., Jolly, A., de la Grange, P., Mallat, M., Bohl, D., et al. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-00718-z · Cited by 122 · see citing works
Systems-based proteomics to resolve the biology of Alzheimer’s disease beyond amyloid and tau
Rayaprolu, S., Higginbotham, L., Bagchi, P., Watson, C. M., Zhang, T., Levey, A. I., Rangaraju, S., & Seyfried, N. T. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-020-00840-3 · Cited by 118 · see citing works
Loss of IL-10 Promotes Differentiation of Microglia to a M1 Phenotype
Laffer, B., Bauer, D., Wasmuth, S., Busch, M., Jalilvand, T. V., Thanos, S., Meyer zu Hörste, G., Loser, K., Langmann, T., Heiligenhaus, A., et al. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00430 · Cited by 120 · see citing works
McMenamin, P. G., Saban, D. R., & Dando, S. J. (2019) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2018.12.002 · Cited by 115 · see citing works
- Authors
- Bennett, M. L., Bennett, F. C., Liddelow, S. A., Ajami, B., Zamanian, J. L., Fernhoff, N. B., Mulinyawe, S. B., Bohlen, C. J., Adil, A., Tucker, A., Weissman, I. L., Chang, E. F., Li, G., Grant, G. A., Hayden Gephart, M. G., & Barres, B. A.
- Affiliations
- Stanford Medicine (US)
- The University of Melbourne (AU)
- University of California, San Francisco (US)
- Department of Neurosurgery, Stanford University School of Medicine, Stanford, CA 94305
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2016-02-16
- Volume
- 113
- Issue
- 12
- Pages
- E1738-46
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC4812770
- OpenAlex
- W2280077905
- Cited by
- 1,804
- References
- 58
- Citations by year
- 2026: 98 · 2025: 122 · 2024: 175 · 2023: 184 · 2022: 241 · 2021: 251 · 2020: 228 · 2019: 189 · 2018: 174 · 2017: 110 · 2016: 30 · 2015: 1
- FWCI
- 91.86
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- HHS | NIH | National Institute of Child Health and Human Development (F31NS078813, R21HD075359)
- HHS | NIH | National Institute of Neurological Disorders and Stroke (R47DA15043, 5K08NS075144-05)
- HHS | NIH | National Institute of Mental Health (5T32MH019938-22)
- HHS | NIH | National Cancer Institute (F32HL115973-02)
- Department of Health, Australian Government | National Health and Medical Research Council (GNT1052961)
- 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
- microglia, TMEM119, monoclonal antibodies, microglia isolation, microglial development, postnatal maturation, microglial transcriptome, central nervous system injury, brain development, myeloid cells, neuroinflammation
- MeSH terms
- Aged, Animals, Antibodies, Monoclonal, Brain, Cell Division, Child, Humans, Lipopolysaccharides, Macrophages, Membrane Proteins, Middle Aged, Nerve Crush, Nerve Tissue Proteins, Organ Specificity, Rabbits, Sciatic Nerve, Temporal Lobe, Biomarkers, Sequence Analysis, RNA, Microglia, Mice, Knockout, Gene Expression Regulation, Developmental, Cell Lineage, Endotoxemia, Optic Nerve Injuries, Gene Expression Profiling, Mice, Transcriptome
About these checks
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
