Colony-Stimulating Factor 1 Receptor (CSF1R) Regulates Microglia Density and Distribution, but Not Microglia Differentiation In Vivo

Oosterhof, Nynke; Kuil, Laura E.; van der Linde, Herma C.; Burm, Saskia M.; Berdowski, Woutje; van Ijcken, Wilfred F.J.; van Swieten, John C.; Hol, Elly M.; Verheijen, Mark H.G.; van Ham, Tjakko J.

doi:10.1016/j.celrep.2018.06.113

Cited by 182Neuroinflammation and Neurodegeneration MechanismsMultiple Sclerosis Research StudiesZebrafish Biomedical Research Applications

Colony-Stimulating Factor 1 Receptor (CSF1R) Regulates Microglia Density and Distribution, but Not Microglia Differentiation In Vivo

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Oosterhof, Nynke, Kuil, Laura E., van der Linde, Herma C., Burm, Saskia M., Berdowski, Woutje, van Ijcken, Wilfred F.J., van Swieten, John C., Hol, Elly M. +2 more·2018·Cell Reports

DOI 10.1016/j.celrep.2018.06.113

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Abstract

Microglia are brain-resident macrophages with trophic and phagocytic functions. Dominant loss-of-function mutations in a key microglia regulator, colony-stimulating factor 1 receptor (CSF1R), cause adult-onset leukoencephalopathy with axonal spheroids and pigmented glia (ALSP), a progressive white matter disorder. Because it remains unclear precisely how CSF1R mutations affect microglia, we generated an allelic series of csf1r mutants in zebrafish to identify csf1r-dependent microglia changes. We found that csf1r mutations led to aberrant microglia density and distribution and regional loss of microglia. The remaining microglia still had a microglia-specific gene expression signature, indicating that they had differentiated normally. Strikingly, we also observed lower microglia numbers and widespread microglia depletion in postmortem brain tissue of ALSP patients. Both in zebrafish and in human disease, local microglia loss also presented in regions without obvious pathology. Together, this implies that CSF1R mainly regulates microglia density and that early loss of microglia may contribute to ALSP pathogenesis.

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Csf1r is required for development, maintenance, and proliferation of microglia.
“The colony stimulating factor 1 receptor (Csf1r) is required for the development, maintenance, and proliferation of microglia”
From Microglia specific deletion of miR-155 in Alzheimer’s disease mouse models reduces amyloid-β pathology but causes hyperexcitability and seizures (2023) · cites this paper as [51]
The Introduction (page unavailable) reports that Csf1r loss in mice produces an almost complete absence of microglia and describes a homeostatic role in microglial viability and proliferation. This supports a role in development and maintenance, but “required” for proliferation is too absolute: the Discussion (page unavailable) says that loss of three csf1r alleles did not severely impede microglia’s proliferative response to dying neurons. (LLM, conf=0.85)
Experimental — accuracy not yet measured
Dysregulation of CSF1R/IL-34 signaling contributes to changes in density and distribution of microglia populations in mouse brain.
“dysregulation of CSF1R/IL-34 signaling contributes to changes in density and distribution of microglia populations in the mouse brain [51].”
From Microglia specific deletion of miR-155 in Alzheimer’s disease mouse models reduces amyloid-β pathology but causes hyperexcitability and seizures (2023) · cites this paper as [51]
The Discussion reports reduced microglia density and altered distribution with CSF1R haploinsufficiency in zebrafish and humans. It also notes regional differences in microglia numbers in mutant mice, but says it is unclear whether density falls elsewhere in the mouse brain. The Introduction identifies IL-34 as a CSF1R ligand; the cited findings do not establish that dysregulation of IL-34 signaling causes the stated changes in mice. Page numbers were not provided for these passages. (LLM, conf=0.86)
Experimental — accuracy not yet measured
CSF1R regulates microglial density and distribution in zebrafish.
“It has recently been reported that CSF1R regulates microglial density and distribution in zebrafish [37], supporting our finding of altered microglial distribution in CSF1R-related leukoencephalopathy.”
From Loss of homeostatic microglial phenotype in CSF1R-related Leukoencephalopathy (2020) · cites this paper as [37]

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Monies, D., Maddirevula, S., Kurdi, W., Alanazy, M. H., Alkhalidi, H., Al‐Owain, M. A., Sulaiman, R. A., Faqeih, E., Goljan, E., Ibrahim, N., et al. (2017) · Genetics in Medicine · doi:10.1038/gim.2017.22 · Cited by 91 · see citing works
Identification of a conserved and acute neurodegeneration‐specific microglial transcriptome in the zebrafish
Oosterhof, N., Holtman, I. R., Kuil, L. E., van der Linde, H. C., Boddeke, E., Eggen, B. J. L., & van Ham, T. J. (2016) · Glia · doi:10.1002/glia.23083 · Cited by 85 · see citing works
Self-citation
Claudin k is specifically expressed in cells that form myelin during development of the nervous system and regeneration of the optic nerve in adult zebrafish
Muenzel, E. J., Schaefer, K., Obirei, B., Kremmer, E., Burton, E. A., Kuscha, V., Becker, C. G., Brösamle, C., Williams, A., & Becker, T. (2011) · Glia · doi:10.1002/glia.21260 · Cited by 76 · see citing works
Apoptotic Cells Are Cleared by Directional Migration and elmo1- Dependent Macrophage Engulfment
van Ham, T. J., Kokel, D., & Peterson, R. T. (2012) · Current Biology · doi:10.1016/j.cub.2012.03.027 · Cited by 72 · see citing works
Characteristic microglial features in patients with hereditary diffuse leukoencephalopathy with spheroids
Tada, M., Konno, T., Tada, M., Tezuka, T., Miura, T., Mezaki, N., Okazaki, K., Arakawa, M., Itoh, K., Yamamoto, T., et al. (2016) · Annals of Neurology · doi:10.1002/ana.24754 · Cited by 70 · see citing works
A Founder Mutation in VPS11 Causes an Autosomal Recessive Leukoencephalopathy Linked to Autophagic Defects
Zhang, J., Lachance, V., Schaffner, A., Li, X., Fedick, A., Kaye, L. E., Liao, J., Rosenfeld, J. A., Yachelevich, N., Chu, M.-L., et al. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1005848 · Cited by 70 · see citing works
Immune cell dynamics in the CNS: Learning from the zebrafish
Oosterhof, N., Boddeke, E., & van Ham, T. J. (2014) · Glia · doi:10.1002/glia.22780 · Cited by 53 · see citing works
Self-citation
Adult onset leukoencephalopathy with axonal spheroids and pigmented glia (ALSP) and N asu– H akola disease: lesion staging and dynamic changes of axons and microglial subsets
Oyanagi, K., Kinoshita, M., Suzuki‐Kouyama, E., Inoue, T., Nakahara, A., Tokiwai, M., Arai, N., Satoh, J., Aoki, N., Jinnai, K., et al. (2016) · Brain Pathology · doi:10.1111/bpa.12443 · Cited by 53 · see citing works
Intravital correlated microscopy reveals differential macrophage and microglial dynamics during resolution of neuroinflammation
van Ham, T. J., Brady, C. A., Kalicharan, R. D., Oosterhof, N., Kuipers, J., Veenstra-Algra, A., Sjollema, K. A., Peterson, R. T., Kampinga, H. H., & Giepmans, B. N. G. (2014) · Disease Models & Mechanisms · doi:10.1242/dmm.014886 · Cited by 52 · see citing works
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Stimulation of macrophage phagocytic but not bactericidal activity by colony-stimulating factor 1
Cheers, C., Hill, M. A., Haigh, A. M., & Stanley, E. R. (1989) · Infection and Immunity · doi:10.1128/iai.57.5.1512-1516.1989 · Cited by 48 · see citing works
Effects of macrophage‐colony‐stimulating factor deficiency on the maturation of microglia and brain macrophages and on their expression of scavenger receptor
Sasaki, A., Yokoo, H., Naito, M., Kaizu, C., Shultz, L. D., & Nakazato, Y. (2000) · Neuropathology · doi:10.1046/j.1440-1789.2000.00286.x · Cited by 44 · see citing works
Absence of neurological abnormalities in mice homozygous for the Polr3a G672E hypomyelinating leukodystrophy mutation
Choquet, K., Yang, S., Moir, R. D., Forget, D., Larivière, R., Bouchard, A., Poitras, C., Sgarioto, N., Dicaire, M., Noohi, F., et al. (2017) · Molecular Brain · doi:10.1186/s13041-017-0294-y · Cited by 37 · see citing works
CSF-1–induced Src signaling can instruct monocytic lineage choice
Endele, M., Loeffler, D., Kokkaliaris, K. D., Hilsenbeck, O., Skylaki, S., Hoppe, P. S., Schambach, A., Stanley, E. R., & Schroeder, T. (2017) · Blood · doi:10.1182/blood-2016-05-714329 · Cited by 31 · see citing works
Neonatal changes of osteoclasts in osteopetrosis (op/op) mice defective in production of functional macrophage colony-stimulating factor (M-CSF) protein and effects of M-CSF on osteoclast development and differentiation.
Umeda, S., Takahashi, K., Naito, M., Shultz, L. D., & Takagi, K. (1996) · PubMed · Cited by 31 · see citing works
Rapid and recoverable in vivo magnetic resonance imaging of the adult zebrafish at 7T
Merrifield, G. D., Mullin, J., Gallagher, L., Tucker, C. S., Jansen, M. A., Denvir, M. A., & Holmes, W. M. (2016) · Magnetic Resonance Imaging · doi:10.1016/j.mri.2016.10.013 · Cited by 29 · see citing works
Adult onset leukoencephalopathy with axonal spheroids and pigmented glia (ALSP) and Nasu-Hakola disease: Lesion staging and dynamic changes of axons and microglial subsets
Oyanagi, K., Kinoshita, M., Nakahara, A., Satoh, J., Aoki, N., Jinnai, K., Yazawa, I., Arai, K., Ishiihara, K., Kawamura, M., et al. (2017) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2017.08.235 · Cited by 6 · see citing works

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Microglia regulate central nervous system myelin growth and integrity
McNamara, N. B., Munro, D. A. D., Bestard-Cuche, N., Uyeda, A., Bogie, J. F. J., Hoffmann, A., Holloway, R. K., Molina-Gonzalez, I., Askew, K. E., Mitchell, S., et al. (2023) · Nature · doi:10.1038/s41586-022-05534-y · Cited by 507 · see citing works
Dynamic control of proinflammatory cytokines Il-1β and Tnf-α by macrophages in zebrafish spinal cord regeneration
Tsarouchas, T. M., Wehner, D., Cavone, L., Munir, T., Keatinge, M., Lambertus, M., Underhill, A., Barrett, T., Kassapis, E., Ogryzko, N. V., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-07036-w · Cited by 294 · see citing works
Homozygous Mutations in CSF1R Cause a Pediatric-Onset Leukoencephalopathy and Can Result in Congenital Absence of Microglia
Oosterhof, N., Chang, I. J., Karimiani, E. G., Kuil, L. E., Jensen, D. M., Daza, R., Young, E., Astle, L., van der Linde, H. C., Shivaram, G. M., et al. (2019) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2019.03.010 · Cited by 247 · see citing works
Self-citation
Origins, Biology, and Diseases of Tissue Macrophages
Cox, N., Pokrovskii, M. V., Vicario, R., & Geissmann, F. (2021) · Annual Review of Immunology · doi:10.1146/annurev-immunol-093019-111748 · Cited by 162 · see citing works
Pro-inflammatory activation following demyelination is required for myelin clearance and oligodendrogenesis
Cunha, M. I., Su, M., Cantuti-Castelvetri, L., Müller, S. A., Schifferer, M., Djannatian, M., Alexopoulos, I., van der Meer, F., Winkler, A., van Ham, T. J., et al. (2020) · Journal of Experimental Medicine · doi:10.1084/jem.20191390 · Cited by 160 · see citing works
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 157 · see citing works
Phenotypic impacts of CSF1R deficiencies in humans and model organisms
Hume, D. A., Caruso, M., Ferrari-Cestari, M., SUMMERS, K. M., Pridans, C., & Irvine, K. M. (2019) · Journal of Leukocyte Biology · doi:10.1002/jlb.mr0519-143r · Cited by 121 · see citing works
Microglial Corpse Clearance: Lessons From Macrophages
Márquez-Ropero, M., Benito, E., Plaza‐Zabala, A., & Sierra, A. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00506 · Cited by 112 · see citing works
Insights Into the Role of CSF1R in the Central Nervous System and Neurological Disorders
Hu, B., Duan, S., Wang, Z., Li, X., Zhou, Y., Zhang, X., Zhang, Y., Xu, H., & Zheng, H. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.789834 · Cited by 105 · see citing works
TREM2 is required for microglial instruction of astrocytic synaptic engulfment in neurodevelopment
Jay, T. R., von Saucken, V. E., Muñoz, B., Codocedo, J. F., Atwood, B. K., Lamb, B. T., & Landreth, G. E. (2019) · Glia · doi:10.1002/glia.23664 · Cited by 97 · see citing works
Microglial dyshomeostasis drives perineuronal net and synaptic loss in a CSF1R +/− mouse model of ALSP, which can be rescued via CSF1R inhibitors
Arreola, M. A., Soni, N., Crapser, J. D., Hohsfield, L. A., Elmore, M. R. P., Matheos, D. P., Wood, M. A., Swarup, V., Mortazavi, A., & Green, K. N. (2021) · Science Advances · doi:10.1126/sciadv.abg1601 · Cited by 89 · see citing works
White matter microglia heterogeneity in the CNS
Amor, S., McNamara, N. B., Gerrits, E., Marzin, M. C., Kooistra, S. M., Miron, V. E., & Nutma, E. (2022) · Acta Neuropathologica · doi:10.1007/s00401-021-02389-x · Cited by 89 · see citing works
Hematopoietic stem cell transplantation chemotherapy causes microglia senescence and peripheral macrophage engraftment in the brain
Sailor, K. A., Agoranos, G., López-Manzaneda, S., Tada, S., Gillet-Legrand, B., Guérinot, C., Masson, J., Vestergaard, C. L., Bonner, M. A., Gagnidze, K., et al. (2022) · Nature Medicine · doi:10.1038/s41591-022-01691-9 · Cited by 87 · see citing works
Adult-Onset Leukoencephalopathy With Axonal Spheroids and Pigmented Glia: Review of Clinical Manifestations as Foundations for Therapeutic Development
Papapetropoulos, S., Pontius, A., Finger, E. C., Karrenbauer, V. D., Lynch, D. S., Brennan, M. J., Zappia, S., Koehler, W., Schöls, L. J., Hayer, S. N., et al. (2022) · Frontiers in Neurology · doi:10.3389/fneur.2021.788168 · Cited by 80 · see citing works
Myelination generates aberrant ultrastructure that is resolved by microglia
Djannatian, M., Radha, S., Weikert, U., Safaiyan, S., Wrede, C., Deichsel, C., Kislinger, G., Rhomberg, A., Ruhwedel, T., Campbell, D. S., et al. (2022) · The Journal of Cell Biology · doi:10.1083/jcb.202204010 · Cited by 81 · see citing works
CSF1R-dependent macrophages control postnatal somatic growth and organ maturation
Keshvari, S., Caruso, M., Teakle, N., Batoon, L., Sehgal, A., Patkar, O. L., Ferrari-Cestari, M., Snell, C., Chen, C., Stevenson, A. J., et al. (2020) · bioRxiv · doi:10.1371/journal.pgen.1009605 · Cited by 64 · see citing works
Regeneration associated transcriptional signature of retinal microglia and macrophages
Mitchell, D. M., Sun, C. C., Hunter, S. S., New, D. D., & Stenkamp, D. L. (2019) · Scientific Reports · doi:10.1038/s41598-019-41298-8 · Cited by 78 · see citing works
Inflammation induces zebrafish regeneration
Iribarne, M. (2021) · Neural Regeneration Research · doi:10.4103/1673-5374.306059 · Cited by 73 · see citing works
Loss of homeostatic microglial phenotype in CSF1R-related Leukoencephalopathy
Kempthorne, L., Yoon, H., Madore, C., Smith, S., Wszolek, Z. K., Rademakers, R., Kim, J., Butovsky, O., & Dickson, D. W. (2020) · Acta Neuropathologica Communications · doi:10.1186/s40478-020-00947-0 · Cited by 77 · see citing works
“It has recently been reported that CSF1R regulates microglial density and distribution in zebrafish [37], supporting our finding of altered microglial distribution in CSF1R-related leukoencephalopathy.”
Background
Flow-cytometric microglial sorting coupled with quantitative proteomics identifies moesin as a highly-abundant microglial protein with relevance to Alzheimer’s disease
Rayaprolu, S., Gao, T., Xiao, H., Ramesha, S., Weinstock, L. D., Shah, J., Duong, D. M., Dammer, E. B., Webster, J. A., Lah, J. J., et al. (2019) · doi:10.1101/802694 · Cited by 71 · see citing works
Inhibited CSF1R Alleviates Ischemia Injury via Inhibition of Microglia M1 Polarization and NLRP3 Pathway
Du, X., Xu, Y., Chen, S., & Fang, M. (2020) · Neural Plasticity · doi:10.1155/2020/8825954 · Cited by 69 · see citing works
Zebrafish macrophage developmental arrest underlies depletion of microglia and reveals Csf1r-independent metaphocytes
Kuil, L. E., Oosterhof, N., Ferrero, G., Mikulášová, T., Hason, M., Dekker, J., Rovira, M., van der Linde, H. C., van Strien, P. M. H., de Pater, E., et al. (2020) · eLife · doi:10.7554/elife.53403 · Cited by 68 · see citing works
Self-citation
Dietary fat exacerbates postprandial hypothalamic inflammation involving glial fibrillary acidic protein‐positive cells and microglia in male mice
Cansell, C., Stobbe, K., Sanchez, C., Thuc, O. L., Mosser, C., Fradj, S. B., Leredde, J., Lebeaupin, C., Debayle, D., Fleuriot, L., et al. (2020) · Glia · doi:10.1002/glia.23882 · Cited by 69 · see citing works
Allogeneic HSCT for adult-onset leukoencephalopathy with spheroids and pigmented glia
Gelfand, J. M., Greenfield, A. L., Barkovich, M. J., Mendelsohn, B. A., van Haren, K. P., Hess, C. P., & Mannis, G. N. (2019) · Brain · doi:10.1093/brain/awz390 · Cited by 61 · see citing works
In situ and transcriptomic identification of microglia in synapse-rich regions of the developing zebrafish brain
Silva, N. J., Dorman, L. C., Vainchtein, I. D., Horneck, N. C., & Molofsky, A. V. (2021) · Nature Communications · doi:10.1038/s41467-021-26206-x · Cited by 67 · see citing works
Microglial replacement therapy: a potential therapeutic strategy for incurable CSF1R-related leukoencephalopathy
Han, J., Sarlus, H., Wszolek, Z. K., Karrenbauer, V. D., & Harris, R. A. (2020) · Acta Neuropathologica Communications · doi:10.1186/s40478-020-01093-3 · Cited by 65 · see citing works
Aged Microglia in Neurodegenerative Diseases: Microglia Lifespan and Culture Methods
Yoo, H.-J., & Kwon, M. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.766267 · Cited by 63 · see citing works
Glial Cells Promote Myelin Formation and Elimination
Hughes, A. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.661486 · Cited by 58 · see citing works
Role of Glia in the Regulation of Sleep in Health and Disease
Garofalo, S., Picard, K., Limatola, C., Nadjar, A., Pascual, O., & Tremblay, M. (2020) · Comprehensive physiology · doi:10.1002/cphy.c190022 · Cited by 63 · see citing works
Genome editing reveals fitness effects of a gene for sexual dichromatism in Sulawesian fishes
Ansai, S., Mochida, K., Fujimoto, S., Mokodongan, D. F., Sumarto, B. K. A., Masengi, K. W. A., Hadiaty, R. K., Nagano, A. J., Toyoda, A., Naruse, K., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-21697-0 · Cited by 53 · see citing works
Effect of the CSF1R inhibitor PLX3397 on remyelination of corpus callosum in a cuprizone‐induced demyelination mouse model
Tahmasebi, F., Pasbakhsh, P., Mortezaee, K., Madadi, S., Barati, S., & Kashani, I. R. (2019) · Journal of Cellular Biochemistry · doi:10.1002/jcb.28344 · Cited by 55 · see citing works
Reverse genetic screen reveals that Il34 facilitates yolk sac macrophage distribution and seeding of the brain
Kuil, L. E., Oosterhof, N., Geurts, S. N., van der Linde, H. C., Meijering, E. H. W., & van Ham, T. J. (2019) · Disease Models & Mechanisms · doi:10.1242/dmm.037762 · Cited by 49 · see citing works
Self-citation
Dominant-acting CSF1R variants cause microglial depletion and altered astrocytic phenotype in zebrafish and adult-onset leukodystrophy
Berdowski, W. M., van der Linde, H. C., Breur, M., Oosterhof, N., Beerepoot, S., Sanderson, L. E., Wijnands, L. I., de Jong, P., Tsai-Meu-Chong, E., de Valk, W. G., et al. (2022) · Acta Neuropathologica · doi:10.1007/s00401-022-02440-5 · Cited by 49 · see citing works
Self-citation
Molecular Actors of Inflammation and Their Signaling Pathways: Mechanistic Insights from Zebrafish
Leiba, J., Özbilgiç, R., Hernández, L., Demou, M., Lutfalla, G., Yatime, L., & Chi, M. N. (2023) · Biology · doi:10.3390/biology12020153 · Cited by 51 · see citing works
CNS-wide repopulation by hematopoietic-derived microglia-like cells corrects progranulin deficiency in mice
Colella, P., Sayana, R., Suárez-Nieto, M. V., Sarno, J., Nyame, K., Xiong, J., Vera, L. N. P., Basurto, J. A., Corbo, M., Limaye, A., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-49908-4 · Cited by 48 · see citing works
Modeling CSF‐1 receptor deficiency diseases – how close are we?
Chiţu, V., Gökhan, Ş., & Stanley, E. R. (2021) · FEBS Journal · doi:10.1111/febs.16085 · Cited by 50 · see citing works
Hexb enzyme deficiency leads to lysosomal abnormalities in radial glia and microglia in zebrafish brain development
Kuil, L. E., Martí, A. L., Mascaro, A. C., van den Bosch, J. C., van den Berg, P., van der Linde, H. C., Schoonderwoerd, K. C., Ruijter, G. J. G., & van Ham, T. J. (2019) · Glia · doi:10.1002/glia.23641 · Cited by 44 · see citing works
Self-citation
Zebrafish Galectin 3 binding protein is the target antigen of the microglial 4C4 monoclonal antibody
Rovira, M., Miserocchi, M., Montanari, A., Hammou, L., Chomette, L., Pozo, J., Imbault, V., Bisteau, X., & Wittamer, V. (2022) · Developmental Dynamics · doi:10.1002/dvdy.549 · Cited by 43 · see citing works
Microglia specific deletion of miR-155 in Alzheimer’s disease mouse models reduces amyloid-β pathology but causes hyperexcitability and seizures
Aloi, M. S., Prater, K. E., Sánchez, R. E. A., Beck, A., Pathan, J. L., Davidson, S., Wilson, A., Keene, C. D., de la Iglesia, H., Jayadev, S., et al. (2023) · Journal of Neuroinflammation · doi:10.1186/s12974-023-02745-6 · Cited by 43 · see citing works
Microglia control small vessel calcification via TREM2
Zarb, Y., Sridhar, S., Nassiri, S., Utz, S. G., Schaffenrath, J., Maheshwari, U., Rushing, E. J., Nilsson, K. P. R., Delorenzi, M., Colonna, M., et al. (2021) · Science Advances · doi:10.1126/sciadv.abc4898 · Cited by 44 · see citing works
Müller glia–myeloid cell crosstalk accelerates optic nerve regeneration in the adult zebrafish
Dyck, A. V., Bollaerts, I., Beckers, A., Vanhunsel, S., Glorian, N., houcke, J. V., van Ham, T. J., Groef, L. D., Andries, L., & Moons, L. (2021) · Glia · doi:10.1002/glia.23972 · Cited by 37 · see citing works
Clinicopathologic characterization and abnormal autophagy of CSF1R-related leukoencephalopathy
Tian, W., Zhan, F., Liu, Q. F., Luan, X., Zhang, C., Shang, L., Zhang, B., Pan, S., Miao, F., Hu, J., et al. (2019) · Translational Neurodegeneration · doi:10.1186/s40035-019-0171-y · Cited by 36 · see citing works
Aged-Related Changes in Microglia and Neurodegenerative Diseases: Exploring the Connection
Borrajo, A. (2024) · Biomedicines · doi:10.3390/biomedicines12081737 · Cited by 36 · see citing works
Rh‐CSF1 attenuates neuroinflammation via the CSF1R/PLCG2/PKCε pathway in a rat model of neonatal HIE
Hu, X., Li, S., Doycheva, D. M., Huang, L., Lenahan, C., Liu, R., Huang, J., Xie, S., Tang, J., Zuo, G., et al. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-01862-w · Cited by 35 · see citing works
The Primary Microglial Leukodystrophies: A Review
Ferrer, I. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23116341 · Cited by 34 · see citing works
Glial cells in the driver seat of leukodystrophy pathogenesis
Garcia, L., Hacker, J. L., Sase, S., Adang, L. A., & Almad, A. (2020) · Neurobiology of Disease · doi:10.1016/j.nbd.2020.105087 · Cited by 33 · see citing works
A c sf1rb mutation uncouples two waves of microglia development in zebrafish
Ferrero, G., Miserocchi, M., Ruggiero, E. D., & Wittamer, V. (2020) · Development · doi:10.1242/dev.194241 · Cited by 33 · see citing works
Vegf signaling between Müller glia and vascular endothelial cells is regulated by immune cells and stimulates retina regeneration
Mitra, S., Devi, S., Lee, M., Jui, J., Sahu, A., & Goldman, D. J. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2211690119 · Cited by 30 · see citing works
Pediatric PK/PD Phase I Trial of Pexidartinib in Relapsed and Refractory Leukemias and Solid Tumors Including Neurofibromatosis Type I–Related Plexiform Neurofibromas
Boal, L. H., Glod, J. W., Spencer, M., Kasai, M., Derdak, J., Dombi, E., Ahlman, M., Beury, D. W., Merchant, M. S., Persenaire, C., et al. (2020) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-20-1696 · Cited by 31 · see citing works
Therapeutic Targeting of Retinal Immune Microenvironment With CSF-1 Receptor Antibody Promotes Visual Function Recovery After Ischemic Optic Neuropathy
Tang, Y., Xiao, Z., Pan, L., Zhuang, D., Cho, K., Robert, K., Chen, X., Shu, L., Tang, G., Wu, J., et al. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.585918 · Cited by 31 · see citing works
Epigenetics and Neuroinflammation Associated With Neurodevelopmental Disorders: A Microglial Perspective
Komada, M., & Nishimura, Y. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.852752 · Cited by 32 · see citing works
Advanced therapeutic strategies targeting microglia: beyond neuroinflammation
Kwon, M. (2022) · Archives of Pharmacal Research · doi:10.1007/s12272-022-01406-1 · Cited by 29 · see citing works
Macrophages in tissue repair and regeneration: insights from zebrafish
Zhao, C., Yang, Z., Li, Y., & Wen, Z. (2024) · Cell Regeneration · doi:10.1186/s13619-024-00195-w · Cited by 30 · see citing works
Unique and non-redundant function of csf1r paralogues in regulation and evolution of post-embryonic development of the zebrafish
Caetano‐Lopes, J., Henke, K., Urso, K., Duryea, J. W., Charles, J. F., Warman, M. L., & Harris, M. P. (2020) · Development · doi:10.1242/dev.181834 · Cited by 29 · see citing works
M-CSFR/CSF1R signaling regulates myeloid fates in zebrafish via distinct action of its receptors and ligands
Hason, M., Mikulášová, T., Machoňová, O., Pombinho, A. R., van Ham, T. J., Irion, U., Nüsslein‐Volhard, C., Bartůněk, P., & Svoboda, O. (2022) · Blood Advances · doi:10.1182/bloodadvances.2021005459 · Cited by 29 · see citing works
Rotenone exposure causes features of Parkinson`s disease pathology linked with muscle atrophy in developing zebrafish embryo
Ranasinghe, T., Seo, Y., Park, H., Choe, S., & Cha, S. (2024) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2024.136215 · Cited by 28 · see citing works
Time Course of Inflammation in Dorsal Root Ganglia Correlates with Differential Reversibility of Mechanical Allodynia
Noh, M., Mikler, B., Joy, T., & Smith, P. A. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2019.12.040 · Cited by 28 · see citing works
Suppression of Microgliosis With the Colony-Stimulating Factor 1 Receptor Inhibitor PLX3397 Does Not Attenuate Memory Defects During Epileptogenesis in the Rat
Wyatt‐Johnson, S. K., Sommer, A. L., Shim, K., & Brewster, A. L. (2021) · Frontiers in Neurology · doi:10.3389/fneur.2021.651096 · Cited by 26 · see citing works
CNS Resident Innate Immune Cells: Guardians of CNS Homeostasis
Muzio, L., & Perego, J. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25094865 · Cited by 26 · see citing works
Macrophage activation drives ovarian failure and masculinization in zebrafish
Bravo, P., Liu, Y., Draper, B. W., & Marlow, F. L. (2023) · Science Advances · doi:10.1126/sciadv.adg7488 · Cited by 23 · see citing works
Mutations in the human CSF1R gene impact microglia’s maintenance of brain white matter integrity
Du, S., Zhou, Y., Li, D., Lier, J., Cella, M., Tada, M., Hamasaki, H., Wu, J., Cai, Z., Orthmann‐Murphy, J. L., et al. (2025) · Nature Immunology · doi:10.1038/s41590-025-02195-7 · Cited by 26 · see citing works
Microglia across evolution: from conserved origins to functional divergence
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Understanding the Role of Glia-Neuron Communication in the Pathophysiology of Epilepsy: A Review
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Authors: 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.
Affiliations: Erasmus MC (NL)
Utrecht University (NL)
Netherlands Institute for Neuroscience (NL)
Amsterdam Neuroscience (NL)
ORCID: Oosterhof, Nynke
Kuil, Laura E.
Burm, Saskia M.
Berdowski, Woutje
Hol, Elly M.
Verheijen, Mark H.G.
Venue: Cell Reports
Publisher: Elsevier BV
Published: 2018-07
Volume: 24
Issue: 5
Pages: 1203-1217.e6
ISSN: 2211-1247 (ISSN-L)
DOI: 10.1016/j.celrep.2018.06.113
OpenAlex: W2886114630
Cited by: 178
References: 80
Citations by year: 2026: 13 · 2025: 19 · 2024: 34 · 2023: 20 · 2022: 29 · 2021: 24 · 2020: 25 · 2019: 12 · 2018: 2
FWCI: 7.10
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by-nc-nd
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
creativecommons.org/licenses/by-nc-nd/4.0/ (vor)
Locations: Cell Reports (publishedVersion, cc-by-nc-nd)
PubMed (publishedVersion)
Pure Amsterdam UMC (publishedVersion, other-oa)
Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion, other-oa)
KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (publishedVersion, cc-by-nc-nd)
KNAW research portal (Royal Academy of Art and Sciences (KNAW)) (publishedVersion, cc-by-nc-nd)
VU Research Portal (publishedVersion, other-oa)
EUR Research Repository (Erasmus University Rotterdam) (submittedVersion, other-oa)
RePub (Erasmus University Rotterdam) (submittedVersion, other-oa)
Data Archiving and Networked Services (DANS) (submittedVersion, cc-by-nc-nd)
Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, other-oa)
Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
Funders: ZonMw
Marie Curie (322368, WE.15-2012-01)
Erasmus Universiteit Rotterdam (016.136.150)
Topics: Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Health Sciences › Medicine › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Zebrafish Biomedical Research Applications
Keywords: CSF1R, microglia, adult-onset leukoencephalopathy with axonal spheroids and pigmented glia, ALSP, microglial density, microglial differentiation, microglial depletion, white matter disease, CSF1R mutation
MeSH terms: Animals, Cell Differentiation, Humans, Mutation, Protein-Tyrosine Kinases, Zebrafish, Receptor, Macrophage Colony-Stimulating Factor, Receptors, Granulocyte-Macrophage Colony-Stimulating Factor, Microglia, Receptor Protein-Tyrosine Kinases, Zebrafish Proteins, Leukoencephalopathies

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Colony-Stimulating Factor 1 Receptor (CSF1R) Regulates Microglia Density and Distribution, but Not Microglia Differentiation In Vivo

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