The DOI matches its Crossref record; 82 of the 82 references it cites were found in a registry or an index.
Microglia development follows a stepwise program to regulate brain homeostasis
Abstract
Microglia development follows a stepwise program: Microglia are cells that defend the central nervous system. However, because they migrate into the brain during development, the changes that they undergo, including those that affect gene expression, have been difficult to document. Matcovitch-Natan et al. transcriptionally profiled gene expression and analyzed epigenetic signatures of microglia at the single-cell level in the early postnatal life of mice. They identified three stages of microglia development, which are characterized by gene expression and linked with chromatin changes, occurring in sync with the developing brain. Furthermore, they showed that the proper development of microglia is affected by the microbiome. Science , this issue p. 789
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
“Gene expression studies have shown that microglial cells have distinct profiles during the embryonic, early post-natal, and adult stages (26).”
From The role of microglia in multiple sclerosis: implications for treatment with Bruton’s tyrosine kinase inhibitors (2025) · cites this paper as [26]
In the citing paper
“MAFB is known to play a key role in the final stages of microglial development from yolk sac progenitors, supporting the acquisition and maintenance of microglial identity (19).”
From Acute TREM2 inhibition depletes MAFB-high microglia and hinders remyelination (2025) · cites this paper as [19]
In the citing paper
“Additionally, it promotes the final stages of microglial development from yolk sac progenitors, facilitating the acquisition and maintenance of microglia identity (19).”
From Acute TREM2 inhibition depletes MAFB-high microglia and hinders remyelination (2025) · cites this paper as [19]
In the citing paper
“Integration of these findings with recent studies of yolk sac and embryonic microglia (56, 63) suggests a model by which intersecting developmentally determined and environment-dependent transcriptional networks establish microglia identity and function (Fig. 6E).”
From An environment-dependent transcriptional network specifies human microglia identity (2017) · cites this paper as [63]
In the citing paper
“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 [21]
In the citing paper
“To minimize the reported effect of brain region on microglial gene expression 6,23,24 , only cortical microglia were included in our comparisons.”
From Transcriptomic analysis of purified human cortical microglia reveals age-associated changes (2017) · cites this paper as [24]
In the citing paper
“An extensive overlap was observed between human and these three independent mouse microglial gene expression data sets ( Fig. 2c ). The median ∆ percentiles were 14.3, 20.4 and 9.3 for our own expression data set, that of Grabert et al. 23 and that of Matcovich-Natan et al. 24 , respectively.”
From Transcriptomic analysis of purified human cortical microglia reveals age-associated changes (2017) · cites this paper as [24]
In the citing paper
“Microglia from adult GF mice also display differential expression of genes associated with microglial maturation, including down-regulation of genes that regulate cell activation and immune system defense pathways, such as Mapk8, IL-1α, Ly86, Jak3, and Stat1, all of which are normally highly expressed in adult microglia (Fig. 1; Erny et al., 2015; Matcovitch-Natan et al., 2016).”
From Microbiome–microglia connections via the gut–brain axis (2019) · cites this paper as Matcovitch-Natan et al., 2016
In the citing paper
“However, the differences in the microglial transcriptome seen in offspring from MIA versus healthy dams decline as mice reach adulthood.”
From Microbiome–microglia connections via the gut–brain axis (2019) · cites this paper as Matcovitch-Natan et al., 2016
In the citing paper
“Microglia from young MIA offspring show increased expression of inflammation-related genes typically associated with an adult microglial phenotype and down-regulation of genes expressed during earlier developmental stages (e.g., Pu.1 and Irf8), suggesting that maternal inflammation disrupts the timeline of normal microglial maturation (Matcovitch-Natan et al., 2016).”
From Microbiome–microglia connections via the gut–brain axis (2019) · cites this paper as Matcovitch-Natan et al., 2016
In the citing paper
“While commensal symbiotic bacteria are critical for proper microglial maturation, induction of infection in pregnant dams can have disruptive effects on the progression of microglial development in offspring (Pratt et al., 2013; Matcovitch-Natan et al., 2016; Mattei et al., 2017).”
From Microbiome–microglia connections via the gut–brain axis (2019) · cites this paper as Matcovitch-Natan et al., 2016
In the citing paper
“We found that microglial diversity is highest during early development, when microglia are still differentiating (Matcovitch-Natan et al., 2016).”
From Complex cell-state changes revealed by single cell RNA sequencing of 76,149 microglia throughout the mouse lifespan and in the injured brain (2018) · cites this paper as Matcovitch-Natan et al., 2016
In the citing paper
“These signatures - cell cycle, phagocytosis, and surveillance - correspond with only three of the nine states presented here (Matcovitch-Natan et al., 2016).”
From Complex cell-state changes revealed by single cell RNA sequencing of 76,149 microglia throughout the mouse lifespan and in the injured brain (2018) · cites this paper as Matcovitch-Natan et al., 2016
In the citing paper
“our new cluster definitions highlight the greater degree of developmental complexity that were covered up by dominating signatures in bulk sequencing experiments.”
From Complex cell-state changes revealed by single cell RNA sequencing of 76,149 microglia throughout the mouse lifespan and in the injured brain (2018) · cites this paper as Matcovitch-Natan et al., 2016
In the citing paper
“This study uses single-cell RNA-sequencing and bioinformatics to describe microglial transcriptome profiles and temporal stages of development in early, pre-adult microglia, which are regulated by distinct regulatory circuits.”
From Microglial signatures and their role in health and disease (2018) · cites this paper as [82]
In the citing paper
“GF mice display marked defects in microglia structure and function and hence feature impaired CNS innate immune responses.240,241”
From Interaction between microbiota and immunity in health and disease (2020) · cites this paper as [241]
In the citing paper
“our study detected about 3 times as many genes per cell, and produced higher detection rates for over 80% of genes”
From Developmental Heterogeneity of Microglia and Brain Myeloid Cells Revealed by Deep Single-Cell RNA Sequencing (2019) · cites this paper as Matcovitch-Natan et al., 2016
In the citing paper
“which consists of three distinct temporal stages: early microglia spanning until embryonic day 14, premicroglia from embryonic day 14 to a few weeks after birth, and adult microglia from a few weeks after birth onward [13].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [13]
In the citing paper
“In mice, microglia undergo a step-wise program of maturation that is synchronized with the developmental phases of the brain [13, 14]”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [13]
In the citing paper
“ATAC-seq of isolated microglia across different developmental stages showed that accessibility of promoter regions by transcriptional complexes was largely conserved over time [13, 34].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [13]
In the citing paper
“Hippocampal microglial cells from polyI:C offspring mice showed dysregulation of genes associated with inflammatory response, cell migration and phagocytosis [13, 59, 60].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [13]
In the citing paper
“Maternal immune activation (MIA) by administration of polyinosinic:polycytidylic acid (polyI:C), which is a synthetic analog of double-stranded RNA used to simulate viral infections via interaction with TLRs, can disrupt pre-microglial development in offspring, leading to a more advanced developmental stage.”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [13]
In the citing paper
“showing dramatic differences in microglial gene expression between early postnatal periods (P3–9) and adulthood (2 months) (Matcovitch-Natan et al., 2016).”
From Local cues establish and maintain region-specific phenotypes of basal ganglia microglia (2017) · cites this paper as Matcovitch-Natan et al., 2016
In the citing paper
“The cerebellar microglia phenotype is reminiscent of microglia during early brain development9,10 as well as microglia associated with neurodegenerative disease11–13.”
From Epigenetic regulation of brain region-specific microglia clearance activity (2018) · cites this paper as [10]
In the citing paper
“Furthermore, cbMg show an increase in the expression of genes characteristic of immature microglia9,10, as well as genes that are expressed in neurodegenerative disease-associated microglia (such as primed microglia, MGnD, and DAMs)11–13 (Supplementary Fig. 5c,d, Supplementary Table 4).”
From Epigenetic regulation of brain region-specific microglia clearance activity (2018) · cites this paper as [10]
In the citing paper
“We found that the cbMg-specific clearance gene expression pattern significantly overlaps with the signature of microglia associated with neurodegeneration11–13 and early brain development9,10, two stages of life characterized by enhanced neuronal attrition and heightened microglia clearance activity.”
From Epigenetic regulation of brain region-specific microglia clearance activity (2018) · cites this paper as [10]
In the citing paper
“This is another key characteristic feature of early microglia progenitors9,10 as well as microglia exposed to dying neurons during different diseases11–13.”
From Epigenetic regulation of brain region-specific microglia clearance activity (2018) · cites this paper as [10]
In the citing paper
“iMGLs not cultured with neurons differentially expressed early microglia genes including FFAR2”
From iPSC-derived human microglia-like cells to study neurological diseases (2017) · cites this paper as Matcovitch-Natan et al., 2016
In the citing paper
“Another study with germ-free mice found functional defects in microglia and as a result observed heightened levels of proinflammatory cytokines IL-1B, IL-6, and TNF-alpha [39], indicating an impairment in immune function.”
From Role of diet and its effects on the gut microbiome in the pathophysiology of mental disorders (2022) · cites this paper as [39]
Citations
Cites
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.
Langmead, B., Trapnell, C., Pop, M., & Salzberg, S. L. (2009) · Genome Biology · doi:10.1186/gb-2009-10-3-r25 · Cited by 21,849
Learning the parts of objects by non-negative matrix factorization
Lee, D. D., & Seung, H. S. (1999) · Nature · doi:10.1038/44565 · Cited by 14,137
Heinz, S., Benner, C., Spann, N., Bertolino, E., Lin, Y. C., Laslo, P., Cheng, J. X., Murre, C., Singh, H., & Glass, C. K. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.05.004 · Cited by 13,382
TopHat: discovering splice junctions with RNA-Seq
Trapnell, C., Pachter, L. S., & Salzberg, S. L. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp120 · Cited by 11,682
High-Resolution Profiling of Histone Methylations in the Human Genome
Barski, A., Cuddapah, S., Cui, K., Roh, T.-Y., Schones, D. E., Wang, Z., Wei, G., Chepelev, I., & Zhao, K. (2007) · Cell · doi:10.1016/j.cell.2007.05.009 · Cited by 6,845
Buenrostro, J. D., Giresi, P. G., Zaba, L. C., Chang, H. Y., & Greenleaf, W. J. (2013) · Nature Methods · doi:10.1038/nmeth.2688 · Cited by 6,422
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
Genome-wide atlas of gene expression in the adult mouse brain
Lein, E. S., Hawrylycz, M. J., Ao, N., Ayres, M., Bensinger, A., Bernard, A., Boe, A. F., Boguski, M. S., Brockway, K. S., Byrnes, E. J., et al. (2007) · Nature · doi:10.1038/nature05453 · Cited by 5,572
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
Synaptic Pruning by Microglia Is Necessary for Normal Brain Development
Paolicelli, R. C., Bolasco, G., Pagani, F., Maggi, L., Scianni, M., Panzanelli, P., Giustetto, M., Ferreira, T. A., Guiducci, E., Dumas, L., et al. (2011) · Science · doi:10.1126/science.1202529 · Cited by 4,244
Flagged first, then by citations
Research works printed but not linked: 1
- 10.1016/jbbi.2015.09015; · DOI
Cited by
Sorted by citations
Items 901–1,000 of 1,002
Contribution of microglia to the epileptiform activity that results from neonatal hypoxia
Leavy, A., Phelan, J., & Jimenez-Mateos, E. M. (2024) · Neuropharmacology · doi:10.1016/j.neuropharm.2024.109968 · Cited by 4
Olasunkanmi, O. I., Aremu, J., Wong, M., Licinio, J., & Zheng, P. (2024) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2024.10.028 · Cited by 5
Single-Cell Analysis in Cerebrovascular Research: Primed for Breakthroughs and Clinical Impact
Albertson, A. J., Winkler, E. A., Yang, A. C., Buckwalter, M. S., Dingman, A., Fan, H., Herson, P. S., McCullough, L. D., Pérez‐Pinzón, M. A., Sansing, L. H., et al. (2024) · Stroke · doi:10.1161/strokeaha.124.049001 · Cited by 4
“45,46 Understanding of oligodendrocyte biology across development has been advanced in recent years by scRNA-seq.”
Building Immunocompetent Cerebral Organoids From a Developmental Perspective
Cuesta‐Puente, X., González-Domínguez, M., Pereira‐Iglesias, M., Perez‐Arriazu, N., Villegas‐Zafra, P., Ramos‐Gonzalez, P., Cavaliere, F., Bengoa‐Vergniory, N., & Sierra, A. (2025) · Glia · doi:10.1002/glia.70062 · Cited by 6
“…in mice have provided key insights into how microglial transcriptional signatures evolve over time, revealing a developmental trajectory that reflects their adaptation to environmental cues, territorial establishment, and functional maturation (Matcovitch-Natan et al. 2016; Hammond et al. 2019).”
Indigenous gut microbes modulate neural cell state and neurodegenerative disease susceptibility
Blackmer‐Raynolds, L., Lipson, L. D., Kozlov, A., Yang, A., Hill, E. J., Sampson, M. M., Hamilton, A. M., Fraccaroli, I., Kelly, S. D., Chopra, P., et al. (2026) · Cell Systems · doi:10.1016/j.cels.2025.101481 · Cited by 5
“5,6 9 In addition to—or perhaps even as a result of—microbiome contributions to neuroinflammatory tone, the microbiome also has broad impacts on neurological function in the context of both health and disease.”
Sierra, A., Navascués, J., Neubrand, V. E., Sepúlveda, M. R., Martín‐Oliva, D., Cuadros, M. Á., & Marín‐Teva, J. L. (2023) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2023.1120400 · Cited by 4
“Immature microglia in the normal developing CNS have specific traits, which are different from the ones of adult microglia (Matcovitch-Natan et al., 2016), showing mostly an amoeboid morphology with high migratory and phagocytic activities (Ling and Wong, 1993; Cuadros and Navascues, 1998; Marín-Teva et al.”
BackgroundCombined Analysis of mRNA Expression and Open Chromatin in Microglia
Scholz, R., Brösamle, D., Yuan, X., Neher, J. J., & Beyer, M. (2023) · Methods in molecular biology · doi:10.1007/978-1-0716-3437-0_35 · Cited by 4
Couch, A. C. M., Brown, A. M., Raimundo, C., Solomon, S., Taylor, M., Sichlinger, L., Matulevičiūtė, R., Srivastava, D. P., & Vernon, A. C. (2024) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2024.08.007 · Cited by 4
Neurodevelopmental and Neuropsychiatric Disorders
Traetta, M. E., Filho, A. M. C., Akinluyi, E. T., & Tremblay, M. (2024) · Advances in neurobiology · doi:10.1007/978-3-031-55529-9_26 · Cited by 4
Prasad, J. D., Steenwinckel, J. V., Gunn, A. J., Bennet, L., Korzeniewski, S. J., Gressèns, P., & Dean, J. M. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252312999 · Cited by 5
Blanchard, A. C., Maximova, A. A., Phillips-Jones, T., Bruce, M. R., Anastasiadis, P., Dionisos, C. V., Engel, K., Reinl, E. L., Pham, A. L., Malaiya, S., et al. (2024) · Developmental Cell · doi:10.1016/j.devcel.2024.11.015 · Cited by 6
da Silva, L. E., Martins, D. F., de Oliveira, M. P., Stenier, M. R., Fernandes, B. B., Willemann, S. D. S., de Souza, G., Vieira, W. F., Hewitson, A., Cidral‐Filho, F. J., et al. (2025) · Lasers in Medical Science · doi:10.1007/s10103-025-04319-9 · Cited by 5
The microbiota-microglia axis: A novel clue for diet and brain health
Song, Z., Song, R., Liu, Y., Zhu, Y., & Zhang, X. (2025) · Trends in Food Science & Technology · doi:10.1016/j.tifs.2025.104942 · Cited by 4
Generation of an Inducible Destabilized‐Domain Cre Mouse Line to Target Disease Associated Microglia
Henningfield, C. M., Ngo, M., Murray, K. M., Kwang, N. E., Tsourmas, K. I., Neumann, J. C., Pashkutz, Z. A., Kawauchi, S., Swarup, V., Lane, T. E., et al. (2025) · Glia · doi:10.1002/glia.70004 · Cited by 4
“…functions based on their RNA expression (Keren-Shaul et al. 2017; Spangenberg et al. 2019; Hammond et al. 2019; Masuda et al. 2019; Li et al. 2019; Matcovitch-Natan et al. 2016; Safaiyan et al. 2021; Deczkowska et al. 2018), and confusion about the role of microglia in AD may in part come from…”
Pecoraro, S., Verkerke, M., Sluijs, J. A., Hof, B. V. H., van der Pol, S. M. A., van Strien, M. E., van der Kant, R., de Vries, C. J. M., de Vries, H. E., van de Berg, W. D. J., et al. (2025) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2025.06.017 · Cited by 4
Microglia as critical mediators linking perinatal immune stress to mental health trajectories
Raju, R. M., & Smith, C. J. W. (2025) · Neuropsychopharmacology · doi:10.1038/s41386-025-02162-8 · Cited by 4
Neonatal microglia replacement in mice modulates seizure severity in adulthood
O’Brien, C. A., Delcy, S. A. S., Shukla, S., Levitt, E. M., Cohen, A. S., Bennett, M. L., & Bennett, F. C. (2025) · Molecular Therapy · doi:10.1016/j.ymthe.2025.08.039 · Cited by 4
“21 It is unknown how microglia depletion, re-population, or transplantation may impact this developmental programming.”
Thinking BIG rheumatology: how to make functional genomics data work for you
Winter, D. R. (2018) · Arthritis Research & Therapy · doi:10.1186/s13075-017-1504-9 · Cited by 4
“These cellular states may differ based on cell type [37], development [40], cell cycle [75], spatial niche [76], response to stimuli [77], and so forth.”
InfluentialSelf-citationThe “systems approach” to treating the brain: opportunities in developmental psychopharmacology
Bussone, S., & Iacono, L. L. (2019) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2019.21.2/lloiacono · Cited by 4
Neurodevelopment and the gut microbiome
Oliphant, K., & Lu, J. N. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-820602-7.00006-4 · Cited by 6
Pilozzi, A. R., Carro, C., Whalen, M. J., & Huang, X. (2020) · Exon Publications eBooks · doi:10.36255/exonpublications.alzheimersdisease.2020.ch8 · Cited by 5
“Microglial progenitors emerge from the yolk sac, and the development of microglia occurs in phases, with each phase being regulated by different transcription factors, and exhibiting differing gene expression profiles (19).”
BackgroundAnderson, R. C., O’Keeffe, G. W., & McDermott, K. W. G. (2022) · Journal of Anatomy · doi:10.1111/joa.13726 · Cited by 3
Not just Glia—Dissecting brain macrophages in the mouse
Frumer, G. R., Shin, S., Jung, S., & Kim, J. (2023) · Glia · doi:10.1002/glia.24445 · Cited by 3
Caesarine, A., Batorsky, R., Shook, L. L., Kışlal, S., Bordt, E. A., Devlin, B. A., Perlis, R. H., Slonim, D. K., Bilbo, S. D., & Edlow, A. G. (2021) · SSRN Electronic Journal · doi:10.2139/ssrn.3985607 · Cited by 4
Mordelt, A., Schuurmans, I. M. E., Scheefhals, N., Hommersom, M. P., Slottje, K., Mast, K., Graziani, M., González, C. O., Wingens, L. J. A., Schubert, D., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.10.24.684345 · Cited by 4
“Unraveling these processes is challenged by the following factors: 1) Microglia adopt diverse states and their function is context dependent 14–17 , we need models that recapitulate the in vivo microglia phenotypes.”
InfluentialPreterm birth: A neuroinflammatory origin for metabolic diseases?
Diao, S., Chen, C., Bénani, A., Magnan, C., Steenwinckel, J. V., Gressèns, P., Cruciani‐Guglielmacci, C., Jacquens, A., & Bokobza, C. (2024) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2024.100745 · Cited by 3
Wang, Y., Ghimire, S., Mangalam, A. K., & Kang, Z. (2025) · Journal of Neuroinflammation · doi:10.1186/s12974-025-03463-x · Cited by 4
“Detecting abundant transcripts can be challenging due to the simultaneous sequencing of numerous cell types, and the process of isolating single cells through sorting may potentially alter gene expression [21, 22].”
Chiu, T., Huang, H., Liew, H., Chang, H., Wu, H.-R., & Wang, M.-J. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26157099 · Cited by 3
“This developmental program can be controlled by both intrinsic genetic programs and extrinsic signals from their niche in the brain [3,16,18–20].”
Ye, N., Song, X., Yu, J., Bao, X., Ye, M., & Jiang, L. (2025) · Frontiers in Microbiology · doi:10.3389/fmicb.2025.1681559 · Cited by 3
Sharallah, O. A., Malakar, V. K., Salama, A. E., Elmaaz, S. M., Daba, S. A., & Poddar, N. K. (2026) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-026-01702-0 · Cited by 3
“GM regulates immune cells’ differentiation and func - tion in the intestine, periphery tissues, and brain (Erny et al. 2015; Matcovitch-Natan et al. 2016).”
Liu, C., Li, T., Ji, J.-J., Li, Z., Samsom, J., Liu, K., Lu, Q., Zhu, W., & Liu, F. (2026) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2026.106770 · Cited by 4
Lan, Z., Liu, H., Huang, C., Li, J. R., Dai, Z., Yuan, Y. Z., He, C., Qin, S., & Su, Z. (2026) · Neurochemistry International · doi:10.1016/j.neuint.2026.106170 · Cited by 4
Bizzotto, M., You, S. F., Tamborini, M., Faggiani, E., Morini, R., Borreca, A., Zhang, R., Aladyeva, E., Nallapu, A., Ferrari, C., et al. (2026) · Neuron · doi:10.1016/j.neuron.2026.04.043 · Cited by 4
Human-specific SRGAP2 paralogs synchronize neotenic microglial maturation and synaptic development
Diaz-Salazar, C., Kim, J., Krzisch, M., Yoo, J., Nano, P. R., Bhaduri, A., Jaenisch, R., Paredes, M., & Polleux, F. (2026) · Neuron · doi:10.1016/j.neuron.2026.07.007 · Cited by 5
“1,6 Although the dynamics and timing of neuronal and microglial maturation have been well characterized in the brains of rodents 1,2,6,16,20–23 and, to some extent, in non-human primates, 24–26 less is known about the timing and features of microglial maturation in the human brain.”
Microglial Phagocytosis During Embryonic and Postnatal Development
Marín‐Teva, J. L., Sepúlveda, M. R., Neubrand, V. E., & Cuadros, M. Á. (2024) · Advances in neurobiology · doi:10.1007/978-3-031-55529-9_9 · Cited by 4
Common and distinct features of diverse macrophage populations in the central nervous system
Masuda, T. (2025) · Proceedings of the Japan Academy Series B · doi:10.2183/pjab.101.013 · Cited by 3
Neuro-immune interactions in memory
Stewart, E., & Ryan, T. J. (2025) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2025.108077 · Cited by 3
Plunk, E. C., Navnith, N., Swan, H., Le, L., McCall, M. N., Sobolewski, M., & Majewska, A. K. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26168008 · Cited by 3
Spielman, B. P., Bagnall-Moreau, C., Chen, F., Balvuena, C., Cruz, C., Carrión, J., Vo, A., Arazi, A., & Brimberg, L. (2025) · Molecular Psychiatry · doi:10.1038/s41380-025-03298-1 · Cited by 4
“8A. Similar to a previous study [44], genes that were reversed by captopril treatment include genes involved in microglial homeostasis such as Csf1r, Fcrls, Tmem119 and Trem2 [39, 58, 61, 71] (Fig.”
Kudryashova, I. V., Stepanichev, M. Y., Манолова, А. О., & Gulyaeva, N. V. (2019) · Developmental Neuroscience · doi:10.1159/000507347 · Cited by 3
The Cell Culture Environment Regulates the Transcription Factor MafB in BV-2 Microglia.
Miller‐Rhodes, P., & Gelbard, H. A. (2021) · PubMed · Cited by 3
Origin and Development of Microglia
Patro, N., & Patro, I. K. (2022) · Springer eBooks · doi:10.1007/978-981-16-8313-8_7 · Cited by 3
Cheah, C. H., Ling, A. P. K., Wong, Y. P., Koh, R. Y., Hussein, S., & Agrotechnology and Biosciences Division, M. N. A. (2022) · Reports of Biochemistry and Molecular Biology · doi:10.52547/rbmb.11.1.125 · Cited by 3
Human microglia development in the embryonic brain
Li, B., Li, Y., Li, Z., Jiao, J., & Amit, I. (2022) · Life Medicine · doi:10.1093/lifemedi/lnac029 · Cited by 3
Self-citationMicroglia Heterogeneity: A Single-cell Concerto
Wang, L., Wu, H., Zhang, S., He, D., Chen, Y., Xue, J., You, L., Liu, Q., & Li, W. (2022) · Human Brain · doi:10.37819/hb.001.001.0208 · Cited by 3
MAGNET: A web-based application for gene set enrichment analysis using macrophage data sets
Chen, S.-Y., Gadhvi, G. T., & Winter, D. R. (2023) · PLoS ONE · doi:10.1371/journal.pone.0272166 · Cited by 3
“2016 [18]—Early microglia E1/E2 (2/3)–were also enriched (Fig 6D).”
BackgroundInfluentialSelf-citationArbat‐Plana, A., Bolívar, S., Navarro, X., Udina, E., & Álvarez, F. J. (2023) · eNeuro · doi:10.1523/eneuro.0436-22.2023 · Cited by 3
Sporopollenin exine capsules modulate the function of microglial cells
Li, M., Hu, B., Wu, Z., Wang, Z., Weng, J. H., Zheng, H., & Sun, L. (2023) · Biomaterials Science · doi:10.1039/d3bm01154b · Cited by 3
The metabolic journey of microglia from early development to adulthood
Das, A., Sadeghdoust, M., Templeman, E. C., & Kaushik, D. K. (2024) · Glial health research. · doi:10.1016/j.ghres.2024.100003 · Cited by 3
Targeting gut microbiota as a possible therapeutic intervention in autism
El-Ansary, A. K., & Bhat, R. S. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-818466-0.00017-4 · Cited by 3
Enteric nervous system, gut-brain connection and related neurodevelopmental disorders
Alim, E., Gülekon, N., Atalar, K., & Bahçelioğlu, M. (2020) · Anatomy (International Journal of Experimental and Clinical Anatomy) · doi:10.2399/ana.20.008 · Cited by 3
The meal Maketh the Microglia: Why studying microglial phagocytosis is critical to stroke research
Morrison, V. E., & Bix, G. J. (2023) · Neurochemistry International · doi:10.1016/j.neuint.2023.105488 · Cited by 3
Lowery, R. L., Latchney, S. E., Peer, R. P., Lamantia, C. E., Opanashuk, L. A., McCall, M. N., & Majewska, A. K. (2020) · Neuroscience Letters · doi:10.1016/j.neulet.2020.135516 · Cited by 3
“There is increasing evidence that microglia undergo a critical period of development during and shortly after gestation, prior to microglial migration into the brain and BBB formation [35,36].”
BackgroundLiu, X., Li, X., Xia, B., Jin, X., Zeng, Z., Yan, S., Li, L., Yuan, S., Zhao, S., Dai, X., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.07.16.206714 · Cited by 3
Shaul, H. K., Keren‐Shaul, H., Kenigsberg, E., Jaitin, D. A., David, E., Paul, F., Tanay, A., & Amit, I. (2019) · doi:10.17504/protocols.io.7hkhj4w · Cited by 2
Self-citationLion, M., Ibrahim, E. C., Caccomo-Garcia, E., Bourret, J., Cinquanta, G., Khalfallah, O., Glaichenhaus, N., Davidovic, L., Courtet, P., Turecki, G., et al. (2025) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2025.01.001 · Cited by 2
Postpartum Brain Reveals Repopulating Process and Long‐Lasting Proteomic Changes of Microglia
Rim, C., You, M., Shin, D., Kim, H., Sung, S., Kim, Y., Park, J., & Kwon, M. (2025) · Glia · doi:10.1002/glia.70088 · Cited by 3
“To address the character of F4/80 + microglia, we analyzed the change of Adgre1 (F4/80) expression during microglial development (Matcovitch-Natan et al. 2016) and repopulation phase by CSF1Ri cessation (Huang et al. 2018) (Figure S5F).”
Microglial Prrc2a regulates microglia-neuron interaction in cerebellum and motor functions in mice
Li, X., Yang, P., Dong, B., Jiang, L., Xiu, R., Guo, J., Li, S., Zhang, P., Gu, R.-Z., Li, A., et al. (2025) · iScience · doi:10.1016/j.isci.2025.113949 · Cited by 2
“Given that either Sall1 or Mafb deletion can cause microglia to adopt an antiviral response state, 45,46 this upregulation of IFN signaling may be due to reduced Sall1 and Mafb expression.”
Intravital observation of neuronal and immune cell dynamics in the developing mammalian brain
Long, Z., Yu, Y., He, C., Xu, L., Yan, Y., Li, Z., Guo, Z. V., & Mi, D. (2025) · Cell · doi:10.1016/j.cell.2025.11.017 · Cited by 3
Transcriptional Regulation of Macrophage Specification and Function
Vanneste, D., & Marichal, T. (2025) · European Journal of Immunology · doi:10.1002/eji.70097 · Cited by 3
“…comparing MG during embryogenesis and in neonates MafB is highly expressed in adult MG. Deletion of MafB in MG revealed a reduced expression of genes associated with the late adult stage of MG development, such as Ctsh and Pmepa1 , highlighting its role in maintaining MG homeostasis [88].”
Bokobza, C., Réda, C., Nair, S., Guenoun, D., Rocha‐Ferreira, E., Faivre, V., Charpentier, T. L., Nijboer, C. H. A., de Theije, C. G. M., Lebon, S., et al. (2025) · Journal of Neuroinflammation · doi:10.1186/s12974-025-03593-2 · Cited by 2
“Underpinning these strikingly different functions over time are distinct transcriptional profiles across development [20, 100].”
Knoop, M. S., Trak, E., Possovre, M.-L., van de Looij, Y., Schirmbeck, G. H., Ceyzériat, K., Pitetti, J.-L., Sanches, E. F., Musardo, S., Millet, P., et al. (2026) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2026.106293 · Cited by 2
Khodabakhsh, P., & Garaschuk, O. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27031185 · Cited by 3
“This observation is well supported by both human and mouse studies [8,12].”
Günther, A., Chini, M., Bitzenhofer, S. H., Marquardt, A., & Hanganu‐Opatz, I. L. (2026) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2026.106470 · Cited by 2
Liu, Z., Wang, J., Ge, Y., Wang, Y., Ling, H., Liu, Y., Zhang, J., You, Z., & Han, Y. (2026) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2026.106483 · Cited by 2
Microglial Neurotransmitter Receptors in Health and Disease
Bi, Q., Guo, C., Chen, N., Zhou, X., Zhou, Q., Liu, X., Shen, X. Z., & Shi, P. D. (2026) · Physiology · doi:10.1152/physiol.00030.2025 · Cited by 3
Gargus, M., Poyhia, L., Errico, J. P., Rogers, M. K. N., & Tremblay, M. (2026) · Frontiers in Neuroscience · doi:10.3389/fnins.2026.1827714 · Cited by 2
Mestranol induces a reversible lysosomal storage–like state in zebrafish microglia
Zhu, E., Xu, H., Sun, W., Chen, X., Li, F., Liu, W., Huang, Z., & Zhang, W. (2026) · Aquatic Toxicology · doi:10.1016/j.aquatox.2026.107880 · Cited by 2
Hyeon, S. J., Kim, S. C., Chu, J., Kim, Y., Kim, C., Park, U., Tufail, Z., Nguyen, P. T., Eom, A., Kim, S., et al. (2026) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-026-02789-z · Cited by 2
Circadian rhythms in microglia mediate early life synaptic development in a sex-specific manner
Routh, B. N., Gibson, C. R., Yang, C. C., Doan, L., Gaudet, A. D., Hofmann, H. A., Mangieri, R. A., & Fonken, L. K. (2026) · Cell Reports · doi:10.1016/j.celrep.2026.117834 · Cited by 2
“Because the functions of microglia vary across the lifespan, 60 the specific impacts of microglia dysregulation depend on life stage.”
Yan, X., Georgopoulou, C., Lee, H., Ahrari, A., Russ, J., Chandrasekar, V., Ducksch, T., Crispatzu, G., Talevi, V., Qiao, L., et al. (2026) · Nature Neuroscience · doi:10.1038/s41593-026-02404-y · Cited by 3
“30; n = 1 mouse for E14.”
InfluentialGeneration of CSF1-Independent Ramified Microglia-Like Cells from Leptomeninges In Vitro
Tanaka, J., Takahashi, H., Yano, H., & Nakanishi, H. (2020) · Cells · doi:10.3390/cells10010024 · Cited by 2
“Seeded microglial progenitors persist in the CNS and appear to continue to persist until adulthood [6].”
BackgroundRegulation of Microglia for the Treatment of Glioma
Zhou, S., & Cisse, B. (2021) · World Neurosurgery · doi:10.1016/j.wneu.2021.06.107 · Cited by 2
Role of the gut microbiome in the pathophysiology of brain disorders
Mayer, E. A., Horn, J. V., Mayer, E. D., & Chen, S. J. (2022) · Elsevier eBooks · doi:10.1016/b978-0-323-85654-6.00058-7 · Cited by 2
Link Between the Immune System and Aggression
Takahashi, A., & Russo, S. J. (2022) · Springer eBooks · doi:10.1007/978-3-030-98711-4_146-1 · Cited by 2
Microglial physiology and function
Verkhratsky, A., & Butt, A. M. (2023) · Elsevier eBooks · doi:10.1016/b978-0-12-821565-4.00002-x · Cited by 2
Abdullatef, S., & Farina, C. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1211079 · Cited by 2
Unraveling the enigma: housekeeping gene Ugt1a7c as a universal biomarker for microglia
Kim, W., Kim, M.-J., & Kim, B. (2024) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2024.1364201 · Cited by 3
“The gene P2ry12 , which encodes P2RY12, is expressed approximately 82 times more in the adult stage than in the yolk sac stage [(62), Figure 1B].”
BackgroundInfluentialAyoub, R., Yang, S., Ji, H., Fan, L., Michino, S. D. D., Mabbott, D., & Nieman, B. J. (2024) · NMR in Biomedicine · doi:10.1002/nbm.5222 · Cited by 2
“While proliferation is considered a hallmark of microglial activation in adults, 72 microglia in the postnatal and juvenile period are phenotypically distinct from adult microglia, 56 so microglial proliferation is expected in this context.”
Gilfarb, R. A., Ranade, S., Dybas, E., Biddle, A., Stewart, M., Rajesh, A., Leuner, B., & Lenz, K. M. (2025) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2025.02.016 · Cited by 2
Hall, M. B., Lemanski, E. A., & Schwarz, J. M. (2025) · Biomolecules · doi:10.3390/biom15030347 · Cited by 2
“The effects of this dysregulation may also extend beyond the fetal period and alter offspring neurodevelopment and behavior during the postnatal period [70,71].”
Zhu, Y., Wei, S., Fu, X.-T., Cheng, X., & Lin, X.-H. (2025) · Frontiers in Bioscience-Landmark · doi:10.31083/fbl36412 · Cited by 2
“Studies have found that microglia in the period of neu-rodevelopment, including the perinatal and early postnatal stage, have distinctly different morphologies and gene expression compared to the adult brain [47–49].”
Manitz, M. P., Violou, K., Hedstück, M., Bösing, K., Kottmann, M., Freund, N., & Juckel, G. (2025) · In Vitro Cellular & Developmental Biology - Animal · doi:10.1007/s11626-025-01091-6 · Cited by 2
Fructose malabsorption induces dysbiosis and increases anxiety in male human and animal models
Coursan, A., Polve, D., Leroi, A., Monnoye, M., Roussin, L., Benatar, C., Tavolacci, M., Quillard‐Muraine, M., Maccarone, M., Guérin, O., et al. (2025) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2025.106221 · Cited by 3
Regulation of development of central nervous system and related diseases by gut microflora
Yin, Y., Ren, W., HuCong, W. U., Liu, J., Zhang, D., & Zhu, G. (2020) · Scientia Sinica Vitae · doi:10.1360/ssv-2019-0111 · Cited by 2
Role of epigenetics in the brain
Matt, S. M., Roth, E. D., & Roth, T. L. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-823577-5.00007-6 · Cited by 2
Nrf2 as a Potential Therapeutic Target for Treatment of Huntington’s Disease
Saravanan, J., Krishnamurthy, P. T., Joshi, M., & Kumar, V. (2022) · IntechOpen eBooks · doi:10.5772/intechopen.103177 · Cited by 2
Microglial integrin, chemokine receptors, and inflammatory response vary with development
Chen, Y., Zhang, H., Zhao, Y. M., Zhang, Y., Yin, S., Hu, Y. P., Ma, G., Lü, D., & Sun, J. (2022) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2022.05.054 · Cited by 2
Microglia Colonization Associated with Angiogenesis and Neural Cell Development
Harry, G. J. (2024) · Advances in neurobiology · doi:10.1007/978-3-031-55529-9_10 · Cited by 2
From seed to flower: blossoming of microglia in development and brain repair
Neckles, V. N., & Feliciano, D. M. (2021) · Cell and Tissue Research · doi:10.1007/s00441-021-03486-9 · Cited by 2
“Single-cell RNA sequencing studies, for example, have highlighted various macrophage-like and microglia-like cells within the brain including the VZ-SVZ and bordering the brain including within the choroid plexus (ChP) (Matcovitch-Natan et al. 2016; Hammond et al. 2019; Li et al. 2019; Masuda et al. 2019; Mizrak et al…”
BackgroundMicroglia and Psychiatric Disorders
Couch, A. C. M., & Vernon, A. C. (2021) · Springer eBooks · doi:10.1007/978-3-030-71229-7_8 · Cited by 2
Blank-Stein, N., Mayer, M., & Mass, E. (2021) · Advances in immunology · doi:10.1016/bs.ai.2021.08.001 · Cited by 2
Microglia inhibition rescues developmental hypofrontality in a mouse model of mental illnessPreprint
Chini, M., Lindemann, C., Pöpplau, J. A., Xu, X., Ahlbeck, J., Bitzenhofer, S. H., Mulert, C., & Hanganu‐Opatz, I. L. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/254656 · Cited by 2
Hook, P. W., & McCallion, A. S. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/427484 · Cited by 3
The Brain Origin of Neonatal Microglia Determines the Content of Exosomes and Biological FunctionPreprint
Murgoci, A., Mallah, K., Aboulouard, S., Lefebvre, C., Čížek, M., Fournier, I., Cizkova, D., & Salzet, M. (2019) · Preprints.org · doi:10.20944/preprints201907.0102.v1 · Cited by 1
Iyer, H., Shen, K., Meireles, A. M., & Talbot, W. S. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.10.27.357897 · Cited by 2
Li, H., Liu, L., Bin, Y., Zeng, H., Wang, J., Zhang, R., Tong, F., Yang, N., & Dong, X. (2022) · Research Square · doi:10.21203/rs.3.rs-2259805/v1 · Cited by 2
Pesämaa, I., Müller, S. A., Robinson, S., Darcher, A., Paquet, D., Zetterberg, H., Lichtenthaler, S. F., & Haass, C. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.06.15.545187 · Cited by 2
The interactions between gut and brain in psychiatric and neurological disorders
Shin, C., & Kim, Y. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-821927-0.00010-3 · Cited by 1
Linking adhesion GPCRs to glial cell development and function
Chiou, B., & Piao, X. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-817986-4.00009-2 · Cited by 1
Metadata
- Authors
- Matcovitch-Natan, O., Winter, D. R., Giladi, A., Vargas Aguilar, S., Spinrad, A., Sarrazin, S., Ben-Yehuda, H., David, E., Zelada González, F., Perrin, P., Keren-Shaul, H., Gury, M., Lara-Astaiso, D., Thaiss, C. A., Cohen, M., Bahar Halpern, K., Baruch, K., Deczkowska, A., Lorenzo-Vivas, E., Itzkovitz, S., Elinav, E., Sieweke, M. H., Schwartz, M., & Amit, I.
- Affiliations
- Weizmann Institute of Science (IL)
- Centre d'Immunologie de Marseille-Luminy (CIML), Université Aix-Marseille, UM2, Campus de Luminy, Marseille, France.
- Centre National de la Recherche Scientifique (FR)
- Department of Immunology, Weizmann Institute of Science, Rehovot, Israel.
- Department of Cell Biology, Weizmann Institute of Science, Rehovot, Israel.
- Corresponding author
- Matcovitch-Natan, Orit
- Winter, Deborah R.
- Sieweke, Michael H.
- Schwartz, Michal
- Amit, Ido
- ORCID
- Venue
- Science
- Published
- 2016-08-19
- Volume
- 353
- Issue
- 6301
- Pages
- aad8670-aad8670
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2468501494
- Cited by
- 1,180
- References
- 82
- Citations by year
- 2026: 76 · 2025: 111 · 2024: 119 · 2023: 105 · 2022: 144 · 2021: 145 · 2020: 143 · 2019: 117 · 2018: 119 · 2017: 84 · 2016: 17
- FWCI
- 61.54
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (submittedVersion)
- Funders
- European Research Council (309788)
- Israeli Science Foundation (1782/11)
- European Commission Seventh Framework Programme (EC FP7)
- Ernest and Bonnie Beutler Research Program of Excellence in Genomic Medicine
- Minerva Stiftung
- Israeli Ministry of Science, Technology and Space
- David and Fela Shapell Family Foundation
- National Human Genome Research Institute Center for Excellence in Genome Science (1P50HG006193)
- Alan and Laraine Fischer Career Development Chair
- Advanced European Research Council (232835)
- EC FP7 HEALTH-2011 (279017)
- Agence Nationale de la Recherche (ANR BLAN07-1_205752, ANR-11-BSV3-026-01)
- Fondation pour la Recherche Medicale (20071210559, 20110421320)
- InCA (13-10/405/AB-LC-HS)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
- Keywords
- microglia development, brain homeostasis, MAFB, chromatin regulation, single-cell transcriptomics, microbiome, prenatal immune activation, neurodevelopmental disorders, immune pathways, myeloid cells
- MeSH terms
- Animals, Blood-Brain Barrier, Brain, Chromatin, Female, Homeostasis, Immunity, Mice, Inbred C57BL, Microglia, Mice, Knockout, Gene Expression Profiling, Myeloid Cells, Histone Code, Epigenesis, Genetic, MafB Transcription Factor, Mice, Neurogenesis, Gene Knockout Techniques, Single-Cell 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
