M-CSF increases proliferation and phagocytosis while modulating receptor and transcription factor expression in adult human microglia

Smith, Amy M; Gibbons, Hannah M; Oldfield, Robyn L; Bergin, Peter M; Mee, Edward W; Curtis, Maurice A; Faull, Richard L M; Dragunow, Mike

doi:10.1186/1742-2094-10-85

Cited by 107Neuroinflammation and Neurodegeneration MechanismsNeurogenesis and neuroplasticity mechanismsNeuroscience and Neuropharmacology Research

M-CSF increases proliferation and phagocytosis while modulating receptor and transcription factor expression in adult human microglia

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Smith, Amy M, Gibbons, Hannah M, Oldfield, Robyn L, Bergin, Peter M, Mee, Edward W, Curtis, Maurice A, Faull, Richard L M, Dragunow, Mike·2013·Journal of Neuroinflammation

DOI 10.1186/1742-2094-10-85PMC PMC3729740

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Abstract

BACKGROUND: Microglia are the primary immune cells of the brain whose phenotype largely depends on their surrounding micro-environment. Microglia respond to a multitude of soluble molecules produced by a variety of brain cells. Macrophage colony-stimulating factor (M-CSF) is a cytokine found in the brain whose receptor is expressed by microglia. Previous studies suggest a critical role for M-CSF in brain development and normal functioning as well as in several disease processes involving neuroinflammation. METHODS: Using biopsy tissue from patients with intractable temporal epilepsy and autopsy tissue, we cultured primary adult human microglia to investigate their response to M-CSF. Mixed glial cultures were treated with 25 ng/ml M-CSF for 96 hours. Proliferation and phagocytosis assays, and high through-put immunocytochemistry, microscopy and image analysis were performed to investigate microglial phenotype and function. RESULTS: We found that the phenotype of primary adult human microglia was markedly changed following exposure to M-CSF. A greater number of microglia were present in the M-CSF- treated cultures as the percentage of proliferating (BrdU and Ki67-positive) microglia was greatly increased. A number of changes in protein expression occurred following M-CSF treatment, including increased transcription factors PU.1 and C/EBPβ, increased DAP12 adaptor protein, increased M-CSF receptor (CSF-1R) and IGF-1 receptor, and reduced HLA-DP, DQ, DR antigen presentation protein. Furthermore, a distinct morphological change was observed with elongation of microglial processes. These changes in phenotype were accompanied by a functional increase in phagocytosis of Aβ1-42 peptide. CONCLUSIONS: We show here that the cytokine M-CSF dramatically influences the phenotype of adult human microglia. These results pave the way for future investigation of M-CSF-related targets for human therapeutic benefit.

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Adding key maintenance factors can hinder interpretation of in vitro disease models because factors such as CSF1 promote microglia viability and increase PU.1 expression, which can affect microglial function in disease.
“However, the addition of key factors for microglial maintenance can hinder the interpretation of In vitro disease models, since factors such as CSF1 can promote microglia viability and increased PU.1 expression that can also influence microglial function in disease states [76].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [76]
Several groups have tried different culture conditions with cytokines such as CSF1, GM-CSF, TGFβ, and IL-34 to preserve homeostatic microglia signature and ramified morphology in vitro.
“Several groups have attempted different cell culture conditions to maintain homeostatic microglia signature and ramified morphology In vitro using a variety of cytokines, such as CSF1, GM-CSF, TGFβ, and IL-34 [73-76].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [76]

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Studies on Colony Stimulating Factor Receptor-1 and Ligands Colony Stimulating Factor-1 and Interleukin-34 in Alzheimer's Disease Brains and Human Microglia
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Routine culture and study of adult human brain cells from neurosurgical specimens
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New therapeutic avenues of MCSF for brain diseases and injuries
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In major dysmood disorder, physiosomatic, chronic fatigue and fibromyalgia symptoms are driven by immune activation and increased immune-associated neurotoxicity
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IGF1 enhances memory function in obese mice and stabilizes the neural structure under insulin resistance via AKT-GSK3β-BDNF signaling
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In Vitro Model to Investigate Communication between Dorsal Root Ganglion and Spinal Cord Glia
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PET Imaging of Neuroinflammation
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A modified protocol for isolation of retinal microglia from the pig
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Polarized macrophage functions are affected differentially after CSF-1R inhibition with PLX5622
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‘Unpredictable chronic mild stress does not exacerbate memory impairment or altered neuronal and glial plasticity in the hippocampus of middle‐aged vitamin D deficient mice’
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Open Access
Smith, A. M., Gibbons, H. M., Oldfield, R. L., Bergin, P. M., Mee, E. W., Curtis, M. A., Faull, R. L. M., & Dragunow, M. (2014)
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Authors: Smith, A. M., Gibbons, H. M., Oldfield, R. L., Bergin, P. M., Mee, E. W., Curtis, M. A., Faull, R. L. M., & Dragunow, M.
Affiliations: University of Auckland (NZ)
Corresponding author: Dragunow, Mike
ORCID: Smith, Amy M
Bergin, Peter M
Curtis, Maurice A
Faull, Richard L M
Dragunow, Mike
Venue: Journal of Neuroinflammation
Publisher: Springer Science and Business Media LLC
Published: 2013-07-17
Volume: 10
Issue: 1
Pages: 85-85
ISSN: 1742-2094 (ISSN-L)
DOI: 10.1186/1742-2094-10-85
PMC: PMC3729740
OpenAlex: W1973529716
Cited by: 107
References: 72
Citations by year: 2026: 2 · 2025: 14 · 2024: 10 · 2023: 7 · 2022: 7 · 2021: 10 · 2020: 7 · 2019: 8 · 2018: 10 · 2017: 6 · 2016: 7 · 2015: 7 · 2014: 9 · 2013: 3
FWCI: 4.86
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/2.0 (unspecified)
Locations: Journal of Neuroinflammation (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Funders: Tertiary Education Commission
Hugh Green Foundation
Neurological Foundation of New Zealand
Health Research Council of New Zealand
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: macrophage colony-stimulating factor, microglia, microglial proliferation, phagocytosis, CSF-1 receptor, PU.1, C/EBPβ, DAP12, IGF-1 receptor, HLA antigen expression, microglial morphology, amyloid-beta, temporal lobe epilepsy, neuroinflammation, microglial phenotype
MeSH terms: Proto-Oncogene Protein Spi-1, Antimetabolites, Autopsy, Biopsy, Bromodeoxyuridine, Cells, Cultured, HLA Antigens, Humans, Image Processing, Computer-Assisted, Immunohistochemistry, Macrophage Activation, Membrane Proteins, Phagocytosis, Proto-Oncogene Proteins, Transcription Factors, Trans-Activators, Macrophage Colony-Stimulating Factor, Receptor, Macrophage Colony-Stimulating Factor, Microglia, Ki-67 Antigen, CCAAT-Enhancer-Binding Protein-beta, Adaptor Proteins, Signal Transducing, Cell Proliferation

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M-CSF increases proliferation and phagocytosis while modulating receptor and transcription factor expression in adult human microglia

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