Transcriptional profiling of CD11c-positive microglia accumulating around amyloid plaques in a mouse model for Alzheimer’s disease
Open accessAbstract
Amyloid plaques in Alzheimer's disease (AD) mice are surrounded by activated microglia. The functional role of microglia activation in AD is not well understood; both detrimental and beneficial effects on AD progression have been reported. Here we show that the population of activated microglia in the cortex of the APPswe/PS1dE9 mouse AD model is divided into a CD11c-positive and a CD11c-negative subpopulation. Cd11c transcript levels and number of CD11c-positive microglia increase sharply when plaques start to occur and both parameters continue to rise in parallel with the age-related increasing plaque load. CD11c cells are localized near plaques at all stages of the disease development and constitute 23% of all activated microglia. No differences between these two populations were found in terms of proliferation, immunostaining intensity of Iba1, MHC class II, CD45, or immunoproteasome subunit LMP7/β5i. Comparison of the transcriptome of isolated CD11c-positive and CD11c-negative microglia from the cortex of aged APPswe/PS1dE9 with WT microglia showed that gene expression changes had a similar general pattern. However, a differential expression was found for genes involved in immune signaling (Il6, S100a8/Mrp8, S100a9/Mrp14, Spp1, Igf1), lysosome activation, and carbohydrate- and cholesterol/lipid-metabolism (Apoe). In addition, the increased expression of Gpnmb/DC-HIL, Tm7sf4/DC-STAMP, and Gp49a/Lilrb4, suggests a suppressive/tolerizing influence of CD11c cells. We show that amyloid plaques in the APP/PS1 model are associated with two distinct populations of activated microglia: CD11c-positive and CD11c-negative cells. Our findings imply that CD11c-positive microglia can potentially counteract amyloid deposition via increased Aβ-uptake and degradation, and by containing the inflammatory response.
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Twenty-one core genes associated with the XO4+/XO4− phenotype were identified as altered in several studies of neurodegenerative disease-associated microglia (DAM).
“Twenty one core genes associated with XO4+/XO4− phenotype were identified as altered in several studies of neurodegenerative disease-associated microglia (DAM)13,14,32”
From Transcriptional signature in microglia associated with Aβ plaque phagocytosis (2021) · cites this paper as [32]
Section 3.4 reports a cluster of genes consistently upregulated across several mouse models of chronic microglial activation. Section 3.6 reports increased expression for 21 tested genes in CD11c versus CD11b cells, but those are not presented as 21 core genes of an XO4+/XO4− phenotype. The copy does not establish the claimed XO4-based, cross-study set. (LLM, conf=0.86)
Experimental — accuracy not yet measuredThe XO4+-associated gene expression signature identified here partially overlaps with other microglia signatures obtained from aged, APP/PS1, 5xFAD or tau model mice.
“The XO4+-associated gene expression signature identified here partially overlaps with other microglia signatures obtained from aged, APP/PS1, 5xFAD or tau model mice13,14,31–33”
From Transcriptional signature in microglia associated with Aβ plaque phagocytosis (2021) · cites this paper as [32]
Activated microglia in Alzheimer's disease show increased proliferation and increased expression of inflammatory markers such as CD36, CD14, CD11c, MHC-II, and iNOS.
“activated microglia in AD show increased proliferation (63,64) and increased expression of inflammatory markers such as CD36, CD14, CD11c, MHC-II, and iNOS (65,66)”
From Microglia in Alzheimer's disease (2017) · cites this paper as [65]
Analyzing activated microglia as a separate population or by single-cell RNA-sequencing reveals subtle (two- to threefold) increases in Trem2 and Tyrobp mRNAs.
“Analyzing activated microglia as a separate population or by single-cell RNA-sequencing also reveals subtle (two- to threefold) increases in Trem2 and Tyrobp mRNAs (Kamphuis et al., 2016; Keren-Shaul et al., 2017; Yin et al., 2017).”
From Microglia in Alzheimer’s disease (2018) · cites this paper as Kamphuis et al., 2016
Transcriptomic studies of microglia in an Alzheimer disease mouse model and in human Alzheimer disease found a proinflammatory signature in microglia associated with Aβ plaques.
“Transcriptomic analysis of microglia in an AD mouse model and in human AD has revealed a proinflammatory signature present in Aβ-plaque-associated microglia52,111,139,140 (FIG. 2a).”
From Microglial signatures and their role in health and disease (2018) · cites this paper as [139]
Upregulated genes in Aβ-plaque-associated microglia, called disease-associated microglia or DAM microglia, include Axl, Apoe, Clec7a, Itgax, Lgals3 and Cst7.
“The upregulated genes in Aβ-plaque-associated microglia, also known as disease-associated microglia (‘DAM microglia’), included Axl, Apoe, Clec7a, Itgax, Lgals3 and Cst7”
From Microglial signatures and their role in health and disease (2018) · cites this paper as [139]
The proinflammatory phenotype was not seen in microglia located outside plaque areas.
“This phenotype was not observed in microglia in non-plaque areas, suggesting that the neuroinflammation associated with AD predominantly occurs in plaque-associated microglia.”
From Microglial signatures and their role in health and disease (2018) · cites this paper as [139]
The DAM microglia identified in these studies are associated with Aβ plaques.
“Although it is clear that the DAM microglia identified in these studies are associated with Aβ plaques, it is not clear whether they have a protective or disease-inducing function (FIG. 2b).”
From Microglial signatures and their role in health and disease (2018) · cites this paper as [139]
ITGAM/CD11b is a cell surface receptor involved in activation, migration and phagocytosis of immune cells, and is used as a marker of activated microglia.
“ITGAM/CD11b (or CR3A), is a cell surface receptor involved in activation, migration and phagocytosis of immune cells, so much so that ITGAM/CD11b is used as a marker of activated microglia (Matsuoka et al., 2001; Heneka et al., 2013; Kamphuis et al., 2016).”
From Genetic variability in response to amyloid beta deposition influences Alzheimer’s disease risk (2019) · cites this paper as Kamphuis et al., 2016
LILRB4 orthologues are increased with amyloid deposition and specifically associated with amyloid plaques.
“LILRB4 (leukocyte immunoglobulin-like receptor, subfamily B, member 4), orthologues have also been shown to be increased with amyloid deposition and specifically associated with amyloid plaques (Wirz et al., 2013; Kamphuis et al., 2016; Castillo et al., 2017).”
From Genetic variability in response to amyloid beta deposition influences Alzheimer’s disease risk (2019) · cites this paper as Kamphuis et al., 2016
Increased proliferation has been associated with 'activated' pro-inflammatory microglia in animal models.
“In contrast, increased proliferation has been associated with ‘activated’ pro-inflammatory microglia in animal models [84,153–155].”
From Untangling senescent and damage‐associated microglia in the aging and diseased brain (2023) · cites this paper as [84]
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- Authors
- Kamphuis, W., Kooijman, L., Schetters, S., Orre, M., & Hol, E. M.
- Affiliations
- Netherlands Institute for Neuroscience (NL)
- Corresponding author
- Kamphuis, Willem
- Venue
- Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease
- Publisher
- Elsevier BV
- Published
- 2016-10
- Volume
- 1862
- Issue
- 10
- Pages
- 1847-1860
- ISSN
- 0925-4439 (ISSN-L)
- OpenAlex
- W2504925882
- Cited by
- 209
- References
- 98
- Citations by year
- 2026: 10 · 2025: 22 · 2024: 28 · 2023: 20 · 2022: 17 · 2021: 28 · 2020: 33 · 2019: 19 · 2018: 21 · 2017: 10 · 2012: 1
- FWCI
- 9.09
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease (publishedVersion)
- PubMed (publishedVersion)
- KNAW research portal (Royal Academy of Art and Sciences (KNAW)) (publishedVersion, other-oa)
- KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (publishedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
- Utrecht University Repository (Utrecht University) (submittedVersion)
- Funders
- Internationale Stichting Alzheimer Onderzoek (ISAO 08504/12,509)
- Netherlands Organization for Scientific Research (865.09.003)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Life Sciences › Neuroscience › Neurology › Neurological Disease Mechanisms and Treatments
- Keywords
- Alzheimer's disease, microglia, CD11c, amyloid plaques, microglial activation, microglial transcriptome, immunosuppression, immune signaling, apolipoprotein E, GPNMB, amyloid-beta clearance, neuroinflammation
- MeSH terms
- Alzheimer Disease, Animals, Disease Models, Animal, Gene Expression Regulation, Mice, Transgenic, Nerve Tissue Proteins, Amyloid beta-Peptides, Microglia, Gene Expression Profiling, CD11c Antigen, Mice
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