The DOI matches its Crossref record; 67 of the 68 references it cites were found in a registry or an index.
Loss of ‘homeostatic’ microglia and patterns of their activation in active multiple sclerosis
Open accessAbstract
Microglia and macrophages accumulate at the sites of active demyelination and neurodegeneration in the multiple sclerosis brain and are thought to play a central role in the disease process. We used recently described markers to characterize the origin and functional states of microglia/macrophages in acute, relapsing and progressive multiple sclerosis. We found microglia activation in normal white matter of controls and that the degree of activation increased with age. This microglia activation was more pronounced in the normal-appearing white matter of patients in comparison to controls and increased with disease duration. In contrast to controls, the normal-appearing white matter of patients with multiple sclerosis showed a significant reduction of P2RY12, a marker expressed in homeostatic microglia in rodents, which was completely lost in active and slowly expanding lesions. Early stages of demyelination and neurodegeneration in active lesions contained microglia with a pro-inflammatory phenotype, which expressed molecules involved in phagocytosis, oxidative injury, antigen presentation and T cell co-stimulation. In later stages, the microglia and macrophages in active lesions changed to a phenotype that was intermediate between pro- and anti-inflammatory activation. In inactive lesions, the density of microglia/macrophages was significantly reduced and microglia in part converted to a P2RY12+ phenotype. Analysis of TMEM119, which is expressed on microglia but not on recruited macrophages, demonstrated that on average 45% of the macrophage-like cells in active lesions were derived from the resident microglia pool. Our study demonstrates the loss of the homeostatic microglial signature in active multiple sclerosis with restoration associated with disease inactivity.
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In the citing paper
“Similarly, microglia in active MS lesions lack Tmem119 (Satoh et al., 2016; Zrzavy et al., 2017).”
From Activated microglia drive demyelination via CSF1R signaling (2021) · cites this paper as Zrzavy et al., 2017
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In the citing paper
“Microglial cells within active white matter lesions are characterized by the absence of homeostatic markers such as P2RY12 and an upregulation of CXCR4, indicating a shift to a disease-associated state (31, 41, 42).”
From The role of microglia in multiple sclerosis: implications for treatment with Bruton’s tyrosine kinase inhibitors (2025) · cites this paper as [41]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“TMEM119 is one of the main homeostatic microglia markers that is not expressed on monocyte-derived macrophages and has been shown to be downregulated in active MS lesions and other inflammatory conditions of the brain47–49.”
From CHIT1 at diagnosis predicts faster disability progression and reflects early microglial activation in multiple sclerosis (2024) · cites this paper as [47]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Interestingly, the phenotype of microglia we observed in HDLS is similar to that found in an SOD1 ALS mouse model and in multiple sclerosis patients, in which the molecules associated with the homeostatic microglial phenotype (e.g., P2RY12, CSF-1R) are down-regulated and inflammatory markers are up-regulated [24, 57].”
From Loss of homeostatic microglial phenotype in CSF1R-related Leukoencephalopathy (2020) · cites this paper as [57]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“As reported previously (Zrzavy et al., 2017), P2RY12+ cells expressing TSPO were substantially reduced in active lesions (Fig. 2E–H).”
From A quantitative neuropathological assessment of translocator protein expression in multiple sclerosis (2019) · cites this paper as Zrzavy et al., 2017
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In the citing paper
“Thus, in contrast to the pattern of TSPO expression in rodent models, it may not be so specifically associated with pro-inflammatory microglia in multiple sclerosis (Zrzavy et al., 2017).”
From A quantitative neuropathological assessment of translocator protein expression in multiple sclerosis (2019) · cites this paper as Zrzavy et al., 2017
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“Indeed, most phagocytes initially present in active MS lesions are microglia, and with lesion maturation, more macrophages will infiltrate from the blood47.”
From CHIT1 at diagnosis predicts faster disability progression and reflects early microglial activation in multiple sclerosis (2024) · cites this paper as [47]
The cited source says what the claim attributes to it.
In the citing paper
“TMEM119 is one of the main homeostatic microglia markers that is not expressed on monocyte-derived macrophages and has been shown to be downregulated in active MS lesions and other inflammatory conditions of the brain47–49.”
From CHIT1 at diagnosis predicts faster disability progression and reflects early microglial activation in multiple sclerosis (2024) · cites this paper as [47]
In the citing paper
“The loss of homeostatic microglial proteins is visible in immunofluorescence double-staining of IBA1 and TMEM119 in terminally sick mice and mock-infected healthy control brains, and shows the reciprocal regulation of both proteins in prion disease (Figure 5A) [55,73,88,89,90,91].”
From Loss of Homeostatic Microglia Signature in Prion Diseases (2022) · cites this paper as [90]
In the citing paper
“since its expression is maintained by resident human microglia in MS lesions and is not expressed by infiltrating immune cells (Zrzavy et al., 2017).”
From Complex cell-state changes revealed by single cell RNA sequencing of 76,149 microglia throughout the mouse lifespan and in the injured brain (2018) · cites this paper as Zrzavy et al., 2017
In the citing paper
“Several of these microglial genes were also observed in human microglia, including P2RY12 and TMEM119 (REFs25,33–36).”
From Microglial signatures and their role in health and disease (2018) · cites this paper as [36]
In the citing paper
“In human MS, microglia lose the expression of the P2RY12 homeostatic microglial marker and adopt a pro-inflammatory phenotype that includes the expression of phagocytic-related markers (macrosialin (also known as CD68)), antigen presentation markers (MHC class I and II molecules and T lymphocyte activation antigen CD86) and proteins involved in the production of reactive oxygen species (cytochrome”
From Microglial signatures and their role in health and disease (2018) · cites this paper as [36]
In the citing paper
“and appears to exhibit stable expression even in response to a variety of inflammatory conditions (9, 96).”
From The Transcriptional Landscape of Microglial Genes in Aging and Neurodegenerative Disease (2019) · cites this paper as [96]
In the citing paper
“Studies have shown that microglial migration, proliferation, and activation are involved in the onset and progression of disease in acute, relapsing, and progressive forms of MS in humans (Zrzavy et al. 2017).”
From MiR-124 and MiR-155 as Therapeutic Targets in Microglia-Mediated Inflammation in Multiple Sclerosis (2025) · cites this paper as Zrzavy et al. 2017
In the citing paper
“However, activation conditions are variable and microglial phenotype changes with disease progression (Zrzavy et al. 2017).”
From MiR-124 and MiR-155 as Therapeutic Targets in Microglia-Mediated Inflammation in Multiple Sclerosis (2025) · cites this paper as Zrzavy et al. 2017
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Citations
Cites
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BackgroundNew tools for studying microglia in the mouse and human CNS
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Flagged first, then by citations
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Additional file 1 of Epigenetic regulation of innate immune memory in microglia
Zhang, X., Kracht, L., Lerário, A. M., Dubbelaar, M. L., Brouwer, N., Wesseling, E. M., Boddeke, E., Eggen, B. J. L., & Kooistra, S. M. (2022) · Figshare · doi:10.6084/m9.figshare.19768078
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Li, S., Sakurai, K., Ohgidani, M., Kato, T. A., & Hikida, T. (2023) · Figshare · doi:10.6084/m9.figshare.23672675
Additional file 2 of Epigenetic regulation of innate immune memory in microglia
Zhang, X., Kracht, L., Lerário, A. M., Dubbelaar, M. L., Brouwer, N., Wesseling, E. M., Boddeke, E., Eggen, B. J. L., & Kooistra, S. M. (2022) · Figshare · doi:10.6084/m9.figshare.19768081
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Additional file 3 of Epigenetic regulation of innate immune memory in microglia
Zhang, X., Kracht, L., Lerário, A. M., Dubbelaar, M. L., Brouwer, N., Wesseling, E. M., Boddeke, E., Eggen, B. J. L., & Kooistra, S. M. (2022) · Figshare · doi:10.6084/m9.figshare.19768084
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Additional file 4 of Epigenetic regulation of innate immune memory in microglia
Zhang, X., Kracht, L., Lerário, A. M., Dubbelaar, M. L., Brouwer, N., Wesseling, E. M., Boddeke, E., Eggen, B. J. L., & Kooistra, S. M. (2022) · Figshare · doi:10.6084/m9.figshare.19768087
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Metadata
- Authors
- Zrzavy, T., Hametner, S., Wimmer, I., Butovsky, O., Weiner, H. L., & Lassmann, H.
- Affiliations
- Medical University of Vienna (AT)
- Brigham and Women's Hospital (US)
- Corresponding author
- Lassmann, Hans
- Venue
- Brain
- Publisher
- Oxford University Press (OUP)
- Published
- 2017-05-24
- Volume
- 140
- Issue
- 7
- Pages
- 1900-1913
- ISSN
- 0006-8950 (ISSN-L)
- 1460-2156
- PMC
- PMC6057548
- OpenAlex
- W2620266814
- Cited by
- 684
- References
- 68
- Citations by year
- 2026: 62 · 2025: 65 · 2024: 78 · 2023: 87 · 2022: 92 · 2021: 116 · 2020: 71 · 2019: 60 · 2018: 43 · 2017: 10
- FWCI
- 39.52
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Brain (publishedVersion, cc-by-nc)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Funders
- NIH (R01NS088137)
- National Multiple Sclerosis Society (5092A1)
- Topics
- Health Sciences › Medicine › Clinical Neurology › Multiple Sclerosis Research Studies
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Inflammasome and immune disorders
- Keywords
- multiple sclerosis, microglia, macrophages, homeostatic microglia, microglial activation, P2Y12 receptor, TMEM119, normal-appearing white matter, demyelination, neurodegeneration, lesion activity, disease duration, pro-inflammatory phenotype, anti-inflammatory phenotype, phagocytosis, oxidative damage, antigen presentation, T cell costimulation, microglial origin
- MeSH terms
- Adult, Aged, Aged, 80 and over, Aging, Demyelinating Diseases, Female, Homeostasis, Humans, Macrophage Activation, Male, Membrane Proteins, Middle Aged, Multiple Sclerosis, Nerve Degeneration, Case-Control Studies, Microglia, Receptors, Purinergic P2Y12, White Matter
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