Microglia recapitulate a hematopoietic master regulator network in the aging human frontal cortex
Open accessAbstract
Microglia form the immune system of the brain. Previous studies in cell cultures and animal models suggest altered activation states and cellular senescence in the aged brain. Instead, we analyzed 3 transcriptome data sets from the postmortem frontal cortex of 381 control individuals to show that microglia gene markers assemble into a transcriptional module in a gene coexpression network. These markers predominantly represented M1 and M1/M2b activation phenotypes. Expression of genes in this module generally declines over the adult life span. This decrease was more pronounced in microglia surface receptors for microglia and/or neuron crosstalk than in markers for activation state phenotypes. In addition to these receptors for exogenous signals, microglia are controlled by brain-expressed regulatory factors. We identified a subnetwork of transcription factors, including RUNX1, IRF8, PU.1, and TAL1, which are master regulators (MRs) for the age-dependent microglia module. The causal contributions of these MRs on the microglia module were verified using publicly available ChIP-Seq data. Interactions of these key MRs were preserved in a protein-protein interaction network. Importantly, these MRs appear to be essential for regulating microglia homeostasis in the adult human frontal cortex in addition to their crucial roles in hematopoiesis and myeloid cell-fate decisions during embryogenesis.
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This highlights age-dependent change in microglial plasticity.
“highlighting the age-dependent change in microglial plasticity [53, 55].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [53]
During maturation and aging, pro-inflammatory gene expression increases in adult microglia.
“With maturation and aging, expression of pro-inflammatory genes in adult microglia increase, suggesting their reactive state and reduced plasticity in the adult stage possibly due to repetitive exposure to infectious agents and active removal of cell debris [53, 55].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [53]
Wehrspaun et al. analyzed three transcriptome datasets from postmortem human cortical tissue spanning teens to elderly and found microglial markers assembled into a gene co-expression network regulated by an age-dependent transcriptional module consisting of RUNX1, IRF8, SPI1, and TAL1.
“Interestingly, Wehrspaun et al. analyzed three transcriptome data sets from postmortem human cortical tissue spanning teens to elderly, and found microglial markers to be assembled into a gene co-expression network regulated by an age-dependent transcriptional module consisting of RUNX1, IRF8, SPI1, and TAL1 [53].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [53]
This suggests a reactive state and reduced plasticity in adult microglia, possibly due to repeated infections and debris clearance.
“suggesting their reactive state and reduced plasticity in the adult stage possibly due to repetitive exposure to infectious agents and active removal of cell debris [53, 55].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [53]
Transcriptome analysis of aged human microglia reveals specific genes influenced by aging.
“Transcriptome analysis of aged human microglia reveal specific genes influenced by aging [52-54].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [53]
Expression of microglial surface receptors CX3CR1, P2RY12, and TREM2 and TLRs tends to negatively correlate with age.
“Further analysis revealed that microglia surface receptors for microglia-neuron crosstalk (CX3CR1, P2RY12, and TREM2) and TLRs for communication with pathogen-associated molecular patterns tended to show a negative correlation between gene expression level and age, highlighting the age-dependent change in microglial plasticity [53, 55].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [53]
These aged microglia gene changes are modulated by RUNX1, IRF8, PU.1, and TAL1.
“which are modulated by RUNX1, IRF8, PU.1 and TAL1”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [53]
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- Authors
- Wehrspaun, C. C., Haerty, W., & Ponting, C. P.
- Affiliations
- National Institutes of Health (US)
- University of Oxford (GB)
- Corresponding author
- Wehrspaun, Claudia C.
- Venue
- Neurobiology of Aging
- Publisher
- Elsevier BV
- Published
- 2015-08
- Volume
- 36
- Issue
- 8
- Pages
- 2443.e9-2443.e20
- ISSN
- 0197-4580 (ISSN-L)
- PMC
- PMC4503803
- OpenAlex
- W2001285655
- Cited by
- 64
- References
- 94
- Citations by year
- 2026: 9 · 2025: 8 · 2024: 2 · 2023: 6 · 2022: 5 · 2021: 7 · 2020: 8 · 2019: 4 · 2018: 6 · 2017: 4 · 2016: 4 · 2015: 1
- FWCI
- 2.62
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Neurobiology of Aging (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- UEA Digital Repository (University of East Anglia) (submittedVersion)
- Funders
- Wellcome Trust
- NIMH
- MRC
- ERC
- 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 › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
- Keywords
- microglia, brain aging, frontal cortex, master regulators, transcriptional modules, gene co-expression network, RUNX1, IRF8, PU.1, TAL1, microglial homeostasis, hematopoietic regulation, protein-protein interaction network
- MeSH terms
- T-Cell Acute Lymphocytic Leukemia Protein 1, Interferon Regulatory Factor-8, Proto-Oncogene Protein Spi-1, Aging, Animals, Frontal Lobe, Hematopoiesis, Homeostasis, Humans, Neurons, Proto-Oncogene Proteins, Receptors, Cell Surface, Transcription Factors, Trans-Activators, Microglia, Core Binding Factor Alpha 2 Subunit, Interferon Regulatory Factors, Basic Helix-Loop-Helix Proteins, Transcriptome, Protein Interaction Maps, Datasets as Topic
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