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Cited by 220Neuroinflammation and Neurodegeneration MechanismsNeurogenesis and neuroplasticity mechanismsNeuroscience and Neuropharmacology Research

CSF‐1 Controls Cerebellar Microglia and Is Required for Motor Function and Social Interaction

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Kana, Veronika, Desland, Fiona A., Casanova-Acebes, Maria, Ayata, Pinar, Badimon, Ana, Nabel, Elisa, Yamamuro, Kazuhiko, Sneeboer, Marjolein +23 more·2019·Journal of Experimental Medicine
DOI 10.1084/jem.20182037PMC PMC6781012

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Abstract

Microglia, the brain resident macrophages, critically shape forebrain neuronal circuits. However, their precise function in the cerebellum is unknown. Here we show that human and mouse cerebellar microglia express a unique molecular program distinct from forebrain microglia. Cerebellar microglial identity was driven by the CSF-1R ligand CSF-1, independently of the alternate CSF-1R ligand, IL-34. Accordingly, CSF-1 depletion from Nestin+ cells led to severe depletion and transcriptional alterations of cerebellar microglia, while microglia in the forebrain remained intact. Strikingly, CSF-1 deficiency and alteration of cerebellar microglia were associated with reduced Purkinje cells, altered neuronal function, and defects in motor learning and social novelty interactions. These findings reveal a novel CSF-1–CSF-1R signaling-mediated mechanism that contributes to motor function and social behavior.

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  • Irf8, Csf1, and Csf1r are critical for microglial survival and proliferation.

    “It functions both intrinsically and through the regulation of its target genes Irf8, colony stimulating Factor 1 (Csf1), and Csf1 receptor (Csf1r) [32], which are themselves known to be critical for microglial survival and proliferation [33, 34, 35].”

    From Targeting Microglial Transcriptional Reprogramming as a Therapy Strategy for Alzheimer's Disease (2026) · cites this paper as [34]

    The Results (page unavailable) report that cerebellar microglia depend on CSF-1 for maintenance and remain reduced in CSF-1-deficient mice; the paper also identifies CSF-1R as their shared signaling receptor. Our copy does not establish a role for Irf8 or specifically show that all three genes are critical for microglial proliferation. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • PU.1, IRF8, and BHLHE40/41 regulate multiple downstream targets that orchestrate microglial immune response functions, including phagocytosis, cytokine production, and inflammatory signaling.

    “PU.1, IRF8, and BHLHE40/41 regulates multiple downstream targets that orchestrate microglial immune response functions, including phagocytosis, cytokine production, and inflammatory signaling”

    From Targeting Microglial Transcriptional Reprogramming as a Therapy Strategy for Alzheimer's Disease (2026) · cites this paper as [34]

    The Results section on CSF-1–CSF-1R signaling describes changes in microglial immune-response genes, but does not connect them to regulation by PU.1, IRF8, or BHLHE40/41. Searches for those factors and for the claimed phagocytosis, cytokine-production, and inflammatory-signaling functions found no passage establishing the attributed relationship. No page numbers were available in our copy. (LLM, conf=0.76)

    Experimental — accuracy not yet measured

  • MEF2C functions as a counterbalance by suppressing excessive pro-inflammatory responses.

    “MEF2C functions as a counterbalance by suppressing excessive pro‐inflammatory responses”

    From Targeting Microglial Transcriptional Reprogramming as a Therapy Strategy for Alzheimer's Disease (2026) · cites this paper as [34]

    The Results section reports increased immune-response gene expression in CSF-1–deficient cerebellar microglia, but does not attribute suppression of pro-inflammatory responses to MEF2C. Searches for MEF2C and for suppression of pro-inflammatory microglial responses found no passage addressing MEF2C’s proposed role. (LLM, conf=0.72)

    Experimental — accuracy not yet measured

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Authors
Kana, V., Desland, F. A., Casanova-Acebes, M., Ayata, P., Badimon, A., Nabel, E., Yamamuro, K., Sneeboer, M., Tan, I.-L., Flanigan, M. E., Rose, S. A., Chang, C., Leader, A., Le Bourhis, H., Sweet, E. S., Tung, N., Wroblewska, A., Lavin, Y., See, P., Baccarini, A., Ginhoux, F., Chitu, V., Stanley, E. R., Russo, S. J., Yue, Z., Brown, B. D., Joyner, A. L., De Witte, L. D., Morishita, H., Schaefer, A., & Merad, M.
Affiliations
  • Tisch Cancer Institute (US)
  • Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 1
  • Icahn School of Medicine at Mount Sinai (US)
  • Utrecht University (NL)
  • Memorial Sloan Kettering Cancer Center (US)
  • Agency for Science, Technology and Research (SG)
  • Department of Developmental and Molecular Biology, Albert Einstein College of Medicine, Bronx, NY 14
  • Albert Einstein College of Medicine (US)
  • Department of Psychiatry, Icahn School of Medicine at Mount Sinai, New York, NY 6
ORCID
Venue
Journal of Experimental Medicine
Publisher
Rockefeller University Press
Published
2019-07-26
Volume
216
Issue
10
Pages
2265-2281
ISSN
  • 0022-1007 (ISSN-L)
  • 1540-9538
DOI
10.1084/jem.20182037
PMC
PMC6781012
OpenAlex
W2965869106
Cited by
220
References
20
Citations by year
2026: 27 · 2025: 34 · 2024: 17 · 2023: 25 · 2022: 36 · 2021: 45 · 2020: 28 · 2019: 8
FWCI
12.99
Type
journal article
Language
en
Open access
Licence
Locations
  • The Journal of Experimental Medicine (publishedVersion, cc-by-nc-sa)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
  • PubMed Central (publishedVersion, cc-by-nc-sa)
  • PubMed (publishedVersion)
Funders
  • National Institutes of Health (R01CA154947, R01MH104559, U19AI128949, DP2 MH100012-01, 1RF1 AG054011-01, T32 AG049688, R21MH106919, R01 NS091519)
  • Swiss National Foundation
  • Human Frontier Science Program Organization (LT000110/2015-L/1)
  • National Institute of Mental Health (F30MH111143)
  • National Eye Institute (R01EY024918, R01EY 026053, R21EY026702)
  • National Institute of Neurological Disorders and Stroke (R21NS105119)
  • Naito Foundation
  • Uehara Memorial Foundation
  • Seaver Foundation
  • National Research Foundation Senior Investigatorship (NFR2016NRF-NRFI001-02)
  • Singapore Immunology Network Core Funding
  • EMBO
  • Brain and Behavior Research Foundation (25065)
Topics
  • Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
CSF-1, IL-34, Purkinje cells, motor learning, social behavior, microglial depletion, cerebellum
MeSH terms
Animals, Behavior, Animal, Humans, Mice, Transgenic, Motor Activity, Purkinje Cells, Social Behavior, Signal Transduction, Macrophage Colony-Stimulating Factor, Receptor, Macrophage Colony-Stimulating Factor, Microglia, Mice

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