The DOI matches its Crossref record; 37 of the 37 references it cites were found in a registry or an index.
Spatial and temporal heterogeneity of mouse and human microglia at single-cell resolution
Open accessAbstract
Microglia have critical roles not only in neural development and homeostasis, but also in neurodegenerative and neuroinflammatory diseases of the central nervous system 1-4. These highly diverse and specialized functions may be executed by subsets of microglia that already exist in situ, or by specific subsets of microglia that develop from a homogeneous pool of cells on demand. However, little is known about the presence of spatially and temporally restricted subclasses of microglia in the central nervous system during development or disease. Here we combine massively parallel single-cell analysis, single-molecule fluorescence in situ hybridization, advanced immunohistochemistry and computational modelling to comprehensively characterize subclasses of microglia in multiple regions of the central nervous system during development and disease. Single-cell analysis of tissues of the central nervous system during homeostasis in mice revealed specific time- and region-dependent subtypes of microglia. Demyelinating and neurodegenerative diseases evoked context-dependent subtypes of microglia with distinct molecular hallmarks and diverse cellular kinetics. Corresponding clusters of microglia were also identified in healthy human brains, and the brains of patients with multiple sclerosis. Our data provide insights into the endogenous immune system of the central nervous system during development, homeostasis and disease, and may also provide new targets for the treatment of neurodegenerative and neuroinflammatory pathologies.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
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?
In the citing paper
“The two predominant modules for MG4 were ‘MS-associated’23 and ‘MIMS-foamy’25 (Fig. 5C).”
From CHIT1 at diagnosis predicts faster disability progression and reflects early microglial activation in multiple sclerosis (2024) · cites this paper as [23]
In the citing paper
“Genetic association studies have demonstrated the critical involvement of the microglial immune response in Alzheimer's disease (AD) pathogenesis.”
From Genetic variants of phospholipase C-γ2 alter the phenotype and function of microglia and confer differential risk for Alzheimer’s disease (2023) · cites this paper as [2]
In the citing paper
“A concerted effort to identify genes that confer altered risk for Alzheimer's disease (AD) is leading to the recognition that many disease-risk genes are associated with the microgliamediated immune response in the AD brain 1-3 .”
From Genetic variants of phospholipase C-γ2 alter the phenotype and function of microglia and confer differential risk for Alzheimer’s disease (2023) · cites this paper as [2]
In the citing paper
“Padi2 is enriched in subsets of microglia isolated from human MS tissue”
From Mouse microglia express unique miRNA-mRNA networks to facilitate age-specific functions in the developing central nervous system (2023) · cites this paper as [19]
In the citing paper
“Microglia are highly dynamic cells that are strongly influenced by different environmental signals which result in distinct phenotypes and functions across brain regions4–9.”
From Genetic analysis of the human microglial transcriptome across brain regions, aging and disease pathologies (2022) · cites this paper as [9]
In the citing paper
“Regional and age-related differences in microglial density, morphology, gene, and protein expression have previously been described for both animals and humans5,6,9,60,61.”
From Genetic analysis of the human microglial transcriptome across brain regions, aging and disease pathologies (2022) · cites this paper as [9]
In the citing paper
“There are several methodological differences (recruitment of tissue, studied brain region, postmortem delay, pH, age, diagnosis, medication use) that could interfere with the interpretation of comparisons between MiGA and other microglial datasets5,9,42.”
From Genetic analysis of the human microglial transcriptome across brain regions, aging and disease pathologies (2022) · cites this paper as [9]
In the citing paper
“These studies have largely concluded that microglia undergo the most prominent changes in diseased brains, due to a combination of increased microglia numbers along with a robust transcriptional activation signature on a per-microglia basis.”
From Human and mouse single-nucleus transcriptomics reveal TREM2-dependent and TREM2-independent cellular responses in Alzheimer’s disease (2020) · cites this paper as [9]
In the citing paper
“Single-cell transcriptomic studies reveal a relatively homogeneous adult microglia population, and greater heterogeneity of microglia states at different developmental stages, during aging and in pathological conditions (Hammond et al., 2019; Li et al., 2019; Masuda et al., 2019).”
From What is a cell type and how to define it? (2022) · cites this paper as Masuda et al., 2019
In the citing paper
“sc/snRNA-seq also provides insight into the diversity of glial cells including the oligodendrocyte lineage (Marques et al., 2016) and functional states of microglia (Masuda et al., 2019).”
From Single-Cell Sequencing of Brain Cell Transcriptomes and Epigenomes (2021) · cites this paper as Masuda et al., 2019
Citations
Cites
Fast and accurate short read alignment with Burrows-Wheeler transform
Li, H., & Durbin, R. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp324 · Cited by 58,607
STAR: ultrafast universal RNA-seq aligner
Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., & Gingeras, T. R. (2013) · Bioinformatics · doi:10.1093/bioinformatics/bts635 · Cited by 51,709
Integrating single-cell transcriptomic data across different conditions, technologies, and species
Butler, A., Hoffman, P., Smibert, P., Papalexi, E., & Satija, R. (2018) · Nature Biotechnology · doi:10.1038/nbt.4096 · Cited by 13,174
Fast and accurate long-read alignment with Burrows-Wheeler transform.
Li, H., & Durbin, R. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btp698 · Cited by 12,063
Complex heatmaps reveal patterns and correlations in multidimensional genomic data
Gu, Z., Eils, R., & Schlesner, M. (2016) · Bioinformatics · doi:10.1093/bioinformatics/btw313 · Cited by 10,037
A Unique Microglia Type Associated with Restricting Development of Alzheimer’s Disease
Keren-Shaul, H., Spinrad, A., Weiner, A., Matcovitch-Natan, O., Dvir-Szternfeld, R., Ulland, T. K., David, E., Baruch, K., Lara-Astaiso, D., Toth, B., et al. (2017) · Cell · doi:10.1016/j.cell.2017.05.018 · Cited by 5,493
The Subread aligner: fast, accurate and scalable read mapping by seed-and-vote
Liao, Y., Smyth, G. K., & Shi, W. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt214 · Cited by 3,064
Krasemann, S., Madore, C., Cialic, R., Baufeld, C., Calcagno, N., El Fatimy, R., Beckers, L., O’Loughlin, E., Xu, Y., Fanek, Z., et al. (2017) · Immunity · doi:10.1016/j.immuni.2017.08.008 · Cited by 2,979
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
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
Cited by
Sorted by citations
Items 101–200 of 1,000
Microglia regulation of central nervous system myelin health and regeneration
Kent, S. A., & Miron, V. E. (2024) · Nature Reviews Immunology · doi:10.1038/s41577-023-00907-4 · Cited by 183
Type-I-interferon-responsive microglia shape cortical development and behavior
Escoubas, C. C., Dorman, L. C., Nguyen, P. T., Lagares-Linares, C., Nakajo, H., Anderson, S. R., Barron, J. J., Wade, S. D., Cuevas, B., Vainchtein, I. D., et al. (2024) · Cell · doi:10.1016/j.cell.2024.02.020 · Cited by 179
Shi, Z., Yu, P., Lin, W., Chen, S., Hu, X., Chen, S., Cheng, J., Liu, Q., Yang, Y., Li, S., et al. (2023) · Neuron · doi:10.1016/j.neuron.2022.12.009 · Cited by 182
Microglia as hackers of the matrix: sculpting synapses and the extracellular space
Crapser, J. D., Arreola, M. A., Tsourmas, K. I., & Green, K. N. (2021) · Cellular & Molecular Immunology · doi:10.1038/s41423-021-00751-3 · Cited by 178
Tansley, S. N., Uttam, S., Guzmán, A. U., Yaqubi, M., Pacis, A., Parisien, M., Deamond, H., Wong, C., Rabau, O., Brown, N., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-28473-8 · Cited by 194
Developmental mechanisms underlying the evolution of human cortical circuits
Vanderhaeghen, P., & Polleux, F. (2023) · Nature Reviews Neuroscience · doi:10.1038/s41583-023-00675-z · Cited by 173
Dolan, M.-J., Therrien, M., Jereb, S., Kamath, T., Gazestani, V., Atkeson, T., Marsh, S. E., Goeva, A., Lojek, N. M., Murphy, S., et al. (2023) · Nature Immunology · doi:10.1038/s41590-023-01558-2 · Cited by 185
CNS remyelination and inflammation: From basic mechanisms to therapeutic opportunities
Franklin, R. J. M., & Simons, M. (2022) · Neuron · doi:10.1016/j.neuron.2022.09.023 · Cited by 184
He, D., Xu, H., Zhang, H., Tang, R., Lan, Y., Xing, R., Li, S., Christian, E., Hou, Y., Lorello, P. J., et al. (2022) · Immunity · doi:10.1016/j.immuni.2021.12.001 · Cited by 174
CNS-Native Myeloid Cells Drive Immune Suppression in the Brain Metastatic Niche through Cxcl10
Guldner, I. H., Wang, Q., Yang, L., Golomb, S. M., Zhao, Z., Lopez, J. A., Brunory, A., Howe, E. N., Zhang, Y., Palakurthi, B., et al. (2020) · Cell · doi:10.1016/j.cell.2020.09.064 · Cited by 176
Vlaminck, K. D., Hove, H. V., Kancheva, D., Scheyltjens, I., Antunes, A. R. P., Bastos, J., Vara‐Pérez, M., Ali, L., Mampay, M., Deneyer, L., et al. (2021) · Immunity · doi:10.1016/j.immuni.2022.09.005 · Cited by 169
When encephalitogenic T cells collaborate with microglia in multiple sclerosis
Dong, Y., & Yong, V. W. (2019) · Nature Reviews Neurology · doi:10.1038/s41582-019-0253-6 · Cited by 169
Sen, M. K., Mahns, D. A., Coorssen, J. R., & Shortland, P. J. (2022) · Glia · doi:10.1002/glia.24148 · Cited by 172
MAPK signaling determines lysophosphatidic acid (LPA)-induced inflammation in microglia
Plastira, I., Bernhart, E. M., Joshi, L., Koyani, C. N., Strohmaier, H. M., Reicher, H., Malle, E., & Sattler, W. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-01809-1 · Cited by 157
Yim, A., Smith, C., & Brown, A. M. (2022) · Immunological Reviews · doi:10.1111/imr.13081 · Cited by 161
Microglia-mediated neuroinflammation and neuroplasticity after stroke
Wang, Y., Leak, R. K., & Cao, G. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.980722 · Cited by 164
Multiomic spatial landscape of innate immune cells at human central nervous system borders
Sankowski, R., Süß, P., Benkendorff, A., Böttcher, C., Fernandez-Zapata, C., Chhatbar, C., Cahueau, J., Monaco, G., Gasull, A. D., Khavaran, A., et al. (2024) · Nature Medicine · doi:10.1038/s41591-023-02673-1 · Cited by 156
Self-citationDysregulated phosphoinositide 3-kinase signaling in microglia: shaping chronic neuroinflammation
Chu, E., Mychasiuk, R., Hibbs, M. L., & Semple, B. D. (2021) · Journal of Neuroinflammation · doi:10.1186/s12974-021-02325-6 · Cited by 152
The role of glial cells in multiple sclerosis disease progression
Healy, L. M., Stratton, J. A., Kuhlmann, T., & Antel, J. (2022) · Nature Reviews Neurology · doi:10.1038/s41582-022-00624-x · Cited by 152
The Role of TGFβ Signaling in Microglia Maturation and Activation
Spittau, B., Dokalis, N., & Prinz, M. (2020) · Trends in Immunology · doi:10.1016/j.it.2020.07.003 · Cited by 157
Self-citationMicroglial autophagy–associated phagocytosis is essential for recovery from neuroinflammation
Berglund, R., Guerreiro-Cacais, A. O., Adzemovic, M. Z., Zeitelhofer, M., Lund, H., Ewing, E., Ruhrmann, S., Nutma, E., Parsa, R., Thessen-Hedreul, M., et al. (2020) · Science Immunology · doi:10.1126/sciimmunol.abb5077 · Cited by 149
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
Self-citationPro-inflammatory and proliferative microglia drive progression of glioblastoma
Liu, H., Sun, Y., Zhang, Q., Jin, W., Gordon, R. E., Zhang, Y., Wang, J., Sun, C., Wang, Z., Qi, X., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109718 · Cited by 144
What Do Microglia Really Do in Healthy Adult Brain?
Augusto‐Oliveira, M., Arrifano, G. D. P., Lopes-Araújo, A., Santos-Sacramento, L., Takeda, P. Y., Anthony, D. C., Malva, J. O., & Lopez, M. E. C. (2019) · Cells · doi:10.3390/cells8101293 · Cited by 158
Endocannabinoid Modulation of Microglial Phenotypes in Neuropathology
Tanaka, M., Sackett, S., & Zhang, Y. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.00087 · Cited by 151
Kamma, E., Lasisi, W. O., Libner, C. D., Ng, H. S., & Plemel, J. R. (2022) · Journal of Neuroinflammation · doi:10.1186/s12974-022-02408-y · Cited by 157
Kumar, P., Lim, A., Hazirah, S. N., Chua, C. J. H., Ngoh, A., Poh, S. L., Yeo, T. H., Lim, J., Ling, S., Sutamam, N. B., et al. (2022) · Nature Neuroscience · doi:10.1038/s41593-022-01095-5 · Cited by 142
Han, B., Zhou, S., Zhang, Y., Chen, S., Xi, W., Liu, C., Zhou, X., Yuan, M., Yu, X., Li, L., et al. (2024) · Science Translational Medicine · doi:10.1126/scitranslmed.adg1323 · Cited by 143
Emerging role of senescent microglia in brain aging-related neurodegenerative diseases
Rim, C., You, M., Nahm, M., & Kwon, M. (2024) · Translational Neurodegeneration · doi:10.1186/s40035-024-00402-3 · Cited by 158
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
Malhotra, S., Costa, C., Eixarch, H., Keller, C. W., Amann, L., Martínez‐Banaclocha, H., Midaglia, L. S., Sarró, E., Machín-Díaz, I., Villar, L. M., et al. (2020) · Brain · doi:10.1093/brain/awaa084 · Cited by 138
Self-citationTNF Production and Release from Microglia via Extracellular Vesicles: Impact on Brain Functions
Raffaele, S., Lombardi, M., Verderio, C., & Fumagalli, M. (2020) · Cells · doi:10.3390/cells9102145 · Cited by 147
Protective Microglial Subset in Development, Aging, and Disease: Lessons From Transcriptomic Studies
Benmamar-Badel, A., Owens, T., & Wlodarczyk, A. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00430 · Cited by 124
Brain macrophage development, diversity and dysregulation in health and disease
Silvin, A., Qian, J., & Ginhoux, F. (2023) · Cellular & Molecular Immunology · doi:10.1038/s41423-023-01053-6 · Cited by 137
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
Wieghofer, P., Hagemeyer, N., Sankowski, R., Schlecht, A., Staszewski, O., Amann, L., Gruber, M., Koch, J., Hausmann, A., Zhang, P., et al. (2021) · The EMBO Journal · doi:10.15252/embj.2020105123 · Cited by 130
Self-citationPlanas, A. M. (2024) · Glia · doi:10.1002/glia.24501 · Cited by 144
Soluble α-synuclein–antibody complexes activate the NLRP3 inflammasome in hiPSC-derived microglia
Trudler, D., Nazor, K. L., Eisele, Y. S., Grabauskas, T., Dolatabadi, N., Parker, J., Sultan, A., Zhong, Z., Goodwin, M. S., Levites, Y., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2025847118 · Cited by 137
Prenatal immune stress blunts microglia reactivity, impairing neurocircuitry
Hayes, L. N., An, K., Carloni, E., Li, F., Vincent, E., Trippaers, C., Paranjpe, M. D., Dölen, G., Goff, L. A., Ramos, A., et al. (2022) · Nature · doi:10.1038/s41586-022-05274-z · Cited by 138
The Link between Gut Dysbiosis and Neuroinflammation in Parkinson’s Disease
Baizabal-Carvallo, J. F., & Alonso-Juarez, M. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2020.02.030 · Cited by 130
Molecular and metabolic heterogeneity of astrocytes and microglia
Hasel, P., Aisenberg, W. H., Bennett, F. C., & Liddelow, S. A. (2023) · Cell Metabolism · doi:10.1016/j.cmet.2023.03.006 · Cited by 135
Villabona-Rueda, A. F., Erice, C., Pardo, C. A., & Stins, M. F. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00405 · Cited by 130
Clonal relations in the mouse brain revealed by single-cell and spatial transcriptomics
Ratz, M., von Berlin, L., Larsson, L., Martin, M., Westholm, J. O., La Manno, G., Lundeberg, J., & Frisén, J. (2022) · Nature Neuroscience · doi:10.1038/s41593-022-01011-x · Cited by 127
Neuroinflammation in Alzheimer’s disease: microglial signature and their relevance to disease
Sobue, A., Komine, O., & Yamanaka, K. (2023) · Inflammation and Regeneration · doi:10.1186/s41232-023-00277-3 · Cited by 134
Zhou, T. G., Li, Y., Li, X., Zeng, F., Rao, Y., He, Y., Wang, Y., Liu, M., Li, D., Xu, Z., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-33932-3 · Cited by 124
Pyramidal neuron subtype diversity governs microglia states in the neocortex
Stogsdill, J. A., Kim, K., Binan, L., Farhi, S. L., Levin, J. Z., & Arlotta, P. (2022) · Nature · doi:10.1038/s41586-022-05056-7 · Cited by 121
Miao, Y., Zhao, G., Cheng, S., Wang, Z., & Yang, X.-L. (2023) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2023.101169 · Cited by 126
Cellular architecture of evolving neuroinflammatory lesions and multiple sclerosis pathology
Kukanja, P., Langseth, C. M., Rubio Rodríguez-Kirby, L. A., Agirre, E., Zheng, C., Raman, A., Yokota, C., Avenel, C., Tiklová, K., Guerreiro-Cacais, A. O., et al. (2024) · Cell · doi:10.1016/j.cell.2024.02.030 · Cited by 124
Microglia in Alzheimer’s Disease in the Context of Tau Pathology
Perea, J. R., Bolós, M., & Ávila, J. (2020) · Biomolecules · doi:10.3390/biom10101439 · Cited by 134
Martins-Ferreira, R., Calafell-Segura, J., Leal, B., Rodríguez-Ubreva, J., Martínez-Saez, E., Mereu, E., Pinho E Costa, P., Laguna, A., & Ballestar, E. (2025) · Nature Communications · doi:10.1038/s41467-025-56124-1 · Cited by 123
Microglia in neurodegenerative diseases
Xu, Y., Jin, M.-Z., Yang, Z., & Jin, M.-Z. (2020) · Neural Regeneration Research · doi:10.4103/1673-5374.290881 · Cited by 121
Microglia maintain structural integrity during fetal brain morphogenesis
Lawrence, A. R., Canzi, A., Bridlance, C., Olivié, N., Lansonneur, C., Catale, C., Pizzamiglio, L., Kloeckner, B., Silvin, A., Munro, D. A. D., et al. (2024) · Cell · doi:10.1016/j.cell.2024.01.012 · Cited by 126
Self-citationDroplet-based forward genetic screening of astrocyte–microglia cross-talk
Wheeler, M. A., Clark, I. C., Lee, H., Li, Z., Linnerbauer, M., Rone, J. M., Blain, M., Akl, C. F., Piester, G., Giovannoni, F., et al. (2023) · Science · doi:10.1126/science.abq4822 · Cited by 125
Self-citationMicroglia: A Central Player in Depression
Deng, S.-L., Chen, J.-G., & Wang, F. (2020) · Current Medical Science · doi:10.1007/s11596-020-2193-1 · Cited by 119
Grassivaro, F., Menon, R., Acquaviva, M., Ottoboni, L., Ruffini, F., Bergamaschi, A., Muzio, L., Farina, C., & Martino, G. (2020) · The Journal of Neuroscience · doi:10.1523/jneurosci.1523-19.2019 · Cited by 127
Ronzano, R., Roux, T., Thétiot, M., Aigrot, M., Richard, L., Lejeune, F., Mazuir, E., Vallat, J., Lubetzki, C., & Desmazières, A. (2021) · Nature Communications · doi:10.1038/s41467-021-25486-7 · Cited by 122
Inflammation in multiple sclerosis: consequences for remyelination and disease progression
Klotz, L., Antel, J. P., & Kuhlmann, T. (2023) · Nature Reviews Neurology · doi:10.1038/s41582-023-00801-6 · Cited by 125
Tuning neural circuits and behaviors by microglia in the adult brain
Zhao, S., Umpierre, A. D., & Wu, L. (2024) · Trends in Neurosciences · doi:10.1016/j.tins.2023.12.003 · Cited by 122
Circadian Regulator CLOCK Drives Immunosuppression in Glioblastoma
Xuan, W., Hsu, W.-H., Khan, F., Dunterman, M., Pang, L., Wainwright, D. A., Ahmed, A. U., Heimberger, A. B., Lesniak, M. S., & Chen, P. (2022) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-21-0559 · Cited by 124
Diversity of transcriptomic microglial phenotypes in aging and Alzheimer's disease
Boche, D., & Gordon, M. N. (2021) · Alzheimer s & Dementia · doi:10.1002/alz.12389 · Cited by 122
Lau, S.-F., Chen, C., Fu, W.-Y., Qu, J. Y., Cheung, T. H., Fu, A. K. Y., & Ip, N. Y. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107530 · Cited by 114
Communication, Cross Talk, and Signal Integration in the Adult Hippocampal Neurogenic Niche
Vicidomini, C., Guo, N., & Sahay, A. (2020) · Neuron · doi:10.1016/j.neuron.2019.11.029 · Cited by 108
Roles and regulation of microglia activity in multiple sclerosis: insights from animal models
Distéfano‐Gagné, F., Bitarafan, S., Lacroix, S., & Gosselin, D. (2023) · Nature reviews. Neuroscience · doi:10.1038/s41583-023-00709-6 · Cited by 115
Microglial deletion and inhibition alleviate behavior of post-traumatic stress disorder in mice
Li, S., Liao, Y., Dong, Y., Li, X., Li, J., Cheng, Y., Cheng, J., & Yuan, Z. (2021) · Journal of Neuroinflammation · doi:10.1186/s12974-020-02069-9 · Cited by 118
Jiao, W., Lin, J., Deng, Y., Ji, Y., Liang, C., Wei, S., Xi, J., & Yan, F. (2025) · Journal of Neuroinflammation · doi:10.1186/s12974-024-03312-3 · Cited by 132
Matsudaira, T., Nakano, S., Konishi, Y., Kawamoto, S., Uemura, K., Kondo, T., Sakurai, K., Ozawa, T., Hikida, T., Komine, O., et al. (2023) · Communications Biology · doi:10.1038/s42003-023-05027-2 · Cited by 98
Stem-cell-derived human microglia transplanted into mouse brain to study human disease
Fattorelli, N., Martínez‐Muriana, A., Wolfs, L., Geric, I., Strooper, B. D., & Mancuso, R. (2021) · Nature Protocols · doi:10.1038/s41596-020-00447-4 · Cited by 114
Oligodendrocytes and Microglia: Key Players in Myelin Development, Damage and Repair
Kalafatakis, I., & Karagogeos, D. (2021) · Biomolecules · doi:10.3390/biom11071058 · Cited by 126
Lan, Y., Zhang, X., Liu, S., Guo, C., Jin, Y., Li, H., Wang, L., Zhao, J., Hao, Y., Li, Z., et al. (2024) · Immunity · doi:10.1016/j.immuni.2024.01.008 · Cited by 108
The gut microbiome modulates the transformation of microglial subtypes
Huang, Y., Wu, J., Zhang, H., Li, Y., Wen, L., Tan, X., Cheng, K., Liu, Y., Pu, J., Liu, L., et al. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02017-y · Cited by 111
Targeting microglia in brain disorders
Priller, J., & Prinz, M. (2019) · Science · doi:10.1126/science.aau9100 · Cited by 112
Self-citationAugusto‐Oliveira, M., Arrifano, G. D. P., Delage, C. I., Tremblay, M., Lopez, M. E. C., & Verkhratsky, A. (2021) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12797 · Cited by 114
Prenatal environmental stressors impair postnatal microglia function and adult behavior in males
Block, C. L., Eroglu, O., Mague, S. D., Smith, C. J. W., Ceasrine, A. M., Sriworarat, C., Blount, C., Beben, K. A., Malacon, K. E., Ndubuizu, N., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111161 · Cited by 108
Single-cell transcriptomics reveals functionally specialized vascular endothelium in brain
Jeong, H., Diéguez‐Hurtado, R., Arf, H., Song, J., Park, H., Kruse, K., Sorokin, L. M., & Adams, R. H. (2022) · eLife · doi:10.7554/elife.57520 · Cited by 110
Single-cell RNA-seq analysis of human CSF microglia and myeloid cells in neuroinflammation
Esaulova, E., Cantoni, C., Shchukina, I., Zaitsev, K., Bucelli, R. C., Wu, G. F., Artyomov, M. N., Cross, A. H., & Edelson, B. T. (2020) · Neurology Neuroimmunology & Neuroinflammation · doi:10.1212/nxi.0000000000000732 · Cited by 107
Microglia in brain development and regeneration
Mehl, L. C., Manjally, A. V., Bouadi, O., Gibson, E. M., & Tay, T. L. (2022) · Development · doi:10.1242/dev.200425 · Cited by 113
Border-associated macrophages in the central nervous system
Sun, R., & Jiang, H. (2024) · Journal of Neuroinflammation · doi:10.1186/s12974-024-03059-x · Cited by 120
Molecular signature of slowly expanding lesions in progressive multiple sclerosis
Jäckle, K., Zeis, T., Schaeren‐Wiemers, N., Junker, A., van der Meer, F., Kramann, N., Stadelmann, C., & Brück, W. (2020) · Brain · doi:10.1093/brain/awaa158 · Cited by 102
Self-citationNormalization of cholesterol metabolism in spinal microglia alleviates neuropathic pain
Pelaez, J. M. N., Choi, S., Capettini, L. D. S. A., Xia, Y., Gonen, A., Agatisa-Boyle, C., Delay, L., dos Santos, G. G., Catroli, G. F., Kim, J., et al. (2021) · The Journal of Experimental Medicine · doi:10.1084/jem.20202059 · Cited by 104
Microglial Function in the Effects of Early-Life Stress on Brain and Behavioral Development
Catale, C., Gironda, S. C., Iacono, L. L., & Carola, V. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9020468 · Cited by 108
Fitzgerald, K. C., Smith, M. D., Kim, S., Sotirchos, E. S., Kornberg, M. D., Douglas, M., Nourbakhsh, B., Graves, J., Rattan, R., Poisson, L., et al. (2021) · Cell Reports Medicine · doi:10.1016/j.xcrm.2021.100424 · Cited by 102
Wang, M., Song, W., Chen, M., Wang, Q., Zhou, X., Xu, P., Krek, A., Yoon, Y., Ho, L., Orr, M. E., et al. (2022) · Molecular Neurodegeneration · doi:10.1186/s13024-022-00517-z · Cited by 104
The microbiota–microglia axis in central nervous system disorders
Mossad, O., & Erny, D. (2020) · Brain Pathology · doi:10.1111/bpa.12908 · Cited by 98
Activity Shapes Neural Circuit Form and Function: A Historical Perspective
Pan, Y., & Monje, M. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.0740-19.2019 · Cited by 98
Microglia and astrocyte involvement in neurodegeneration and brain cancer
Vandenbark, A. A., Offner, H., Matejuk, S., & Matejuk, A. (2021) · Journal of Neuroinflammation · doi:10.1186/s12974-021-02355-0 · Cited by 101
The cannabinoid system and microglia in health and disease
Duffy, S. S., Hayes, J. P., Fiore, N. T., & Moalem‐Taylor, G. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108555 · Cited by 103
Microglia heterogeneity, modeling and cell-state annotation in development and neurodegeneration
Fumagalli, L., Nazlie Mohebiany, A., Premereur, J., Polanco Miquel, P., Bijnens, B., Van de Walle, P., Fattorelli, N., & Mancuso, R. (2025) · Nature Neuroscience · doi:10.1038/s41593-025-01931-4 · Cited by 90
Stratoulias, V., Ruiz, R., Kanatani, S., Osman, A. M., Keane, L., Armengol, J. A., Rodríguez-Moreno, A., Murgoci, A.-N., García-Domínguez, I., Alonso-Bellido, I., et al. (2023) · Nature Neuroscience · doi:10.1038/s41593-023-01326-3 · Cited by 96
Post-Ischaemic Immunological Response in the Brain: Targeting Microglia in Ischaemic Stroke Therapy
Rawlinson, C., Jenkins, S. I., Thei, L., Dallas, M. L., & Chen, R. (2020) · Brain Sciences · doi:10.3390/brainsci10030159 · Cited by 99
Microglia-mediated synaptic pruning as a key deficit in neurodevelopmental disorders: Hype or hope?
Mordelt, A., & de Witte, L. D. (2023) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2022.102674 · Cited by 100
Boleti, A. P. D. A., Flores, T. M. D. O., Moreno, S. E., dos Anjos, L. C., Mortari, M. R., & Migliolo, L. (2020) · Neurochemistry International · doi:10.1016/j.neuint.2020.104714 · Cited by 94
Aged lipid‐laden microglia display impaired responses to stroke
Arbaizar‐Rovirosa, M., Pedragosa, J., Lozano, J. J., Casal, C., Pol, A., Gallizioli, M., & Planas, A. M. (2023) · EMBO Molecular Medicine · doi:10.15252/emmm.202217175 · Cited by 94
Microglia‐dependent remodeling of neuronal circuits
Guedes, J. R., Ferreira, P. A., Costa, J. M., Cardoso, A. L., & Peça, J. (2022) · Journal of Neurochemistry · doi:10.1111/jnc.15689 · Cited by 93
Two phenotypically and functionally distinct microglial populations in adult zebrafish
Wu, S., Nguyen, L. T. M., Pan, H., Hassan, S., Dai, Y., Xu, J., & Wen, Z. (2020) · Science Advances · doi:10.1126/sciadv.abd1160 · Cited by 98
Böttcher, C., Fernández‐Zapata, C., Snijders, G. J. L., Schlickeiser, S., Sneeboer, M. A. M., Kunkel, D., de Witte, L. D., & Priller, J. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-00992-2 · Cited by 92
Self-citationChen, H., Chen, C., Kuo, Y.-M., Chen, B., Kuan, I. S., Huang, H., Lee, J., Anthony, N. R., Kuan, C.-Y., & Sun, Y. (2021) · Theranostics · doi:10.7150/thno.64033 · Cited by 96
Ostkamp, P., Deffner, M., Schulte‐Mecklenbeck, A., Wünsch, C., Lu, I., Wu, G. F., Goelz, S. E., Jager, P. L. D., Kuhlmann, T., Groß, C. C., et al. (2022) · Science Translational Medicine · doi:10.1126/scitranslmed.adc9778 · Cited by 93
Gene expression profiling reveals a conserved microglia signature in larval zebrafish
Mazzolini, J., Clerc, S. L., Morisse, G., Coulonges, C., Kuil, L. E., van Ham, T. J., Zagury, J., & Sieger, D. (2019) · Glia · doi:10.1002/glia.23717 · Cited by 94
Microglia Diversity in Healthy and Diseased Brain: Insights from Single-Cell Omics
Ochocka, N., & Kaminska, B. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22063027 · Cited by 97
Diversity of Reactive Astrogliosis in CNS Pathology: Heterogeneity or Plasticity?
Moulson, A. J., Squair, J. W., Franklin, R. J. M., Tetzlaff, W., & Assinck, P. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.703810 · Cited by 97
Metadata
- Authors
- Masuda, T., Sankowski, R., Staszewski, O., Böttcher, C., Amann, L., Sagar, Scheiwe, C., Nessler, S., Kunz, P., van Loo, G., Coenen, V. A., Reinacher, P. C., Michel, A., Sure, U., Gold, R., Grün, D., Priller, J., Stadelmann, C., & Prinz, M.
- Affiliations
- University of Freiburg (DE)
- Charité – Universitätsmedizin Berlin (DE)
- Max Planck Institute of Immunobiology and Epigenetics (DE)
- Universitätsmedizin Göttingen (DE)
- Essen University Hospital (DE)
- St. Josef-Hospital (DE)
- German Center for Neurodegenerative Diseases (DE)
- Corresponding author
- Prinz, Marco
- ORCID
- Venue
- Nature
- Published
- 2019-02
- Volume
- 566
- Issue
- 7744
- Pages
- 388-392
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2914756534
- Cited by
- 1,310
- References
- 37
- Citations by year
- 2026: 136 · 2025: 145 · 2024: 187 · 2023: 184 · 2022: 207 · 2021: 209 · 2020: 169 · 2019: 71
- FWCI
- 72.26
- Type
- journal article
- Language
- en
- Update notices
- correction (2019-03-27)
- Open access
- Licence
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Ghent University Academic Bibliography (Ghent University) (submittedVersion)
- DZNE Pub (submittedVersion)
- GoeScholar The Publication Server of the Georg-August-Universität Göttingen (Georg-August-Universität Göttingen) (submittedVersion, cc-by)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, other-oa)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- Funders
- National Multiple Sclerosis Society
- Deutsche Forschungsgemeinschaft (SFB-1160, SFB 992, SFB/ TRR 167, TRR 167)
- Bundesministerium für Bildung und Forschung
- Karolinska Institutet
- Deutschen Multiple Sklerose Gesellschaft
- Kanae Foundation for the Promotion of Medical Science
- Roman, Marga und Mareille Sobek Stiftung
- Medical Research Council (MC_PC_16031)
- Japan Society for the Promotion of Science
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
- Health Sciences › Medicine › Clinical Neurology › Multiple Sclerosis Research Studies
- Keywords
- microglia, microglial heterogeneity, microglial subtypes, central nervous system development, neuroinflammation, neurodegenerative diseases, demyelination, multiple sclerosis, mouse brain, human brain, single-cell transcriptomics, single-molecule fluorescence in situ hybridization, brain homeostasis
- MeSH terms
- Animals, Brain, Cell Separation, Demyelinating Diseases, Female, Humans, Kinetics, Male, Multiple Sclerosis, Case-Control Studies, Microglia, Neurodegenerative Diseases, Mice, Single-Cell Analysis, Spatio-Temporal Analysis
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