Complement 3(+)-astrocytes are highly abundant in prion diseases, but their abolishment led to an accelerated disease course and early dysregulation of microglia
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Astrogliosis and activation of microglia are hallmarks of prion diseases in humans and animals. Both were viewed to be rather independent events in disease pathophysiology, with proinflammatory microglia considered to be the potential neurotoxic species at late disease stages. Recent investigations have provided substantial evidence that a proinflammatory microglial cytokine cocktail containing TNF-α, IL-1α and C1qa reprograms a subset of astrocytes to change their expression profile and phenotype, thus becoming neurotoxic (designated as A1-astrocytes). Knockout or antibody blockage of the three cytokines abolish formation of A1-astrocytes, therefore, this pathway is of high therapeutic interest in neurodegenerative diseases. Since astrocyte polarization profiles have never been investigated in prion diseases, we performed several analyses and could show that C3 + -PrP Sc -reactive-astrocytes, which may represent a subtype of A1-astrocytes, are highly abundant in prion disease mouse models and human prion diseases. To investigate their impact on prion disease pathophysiology and to evaluate their potential therapeutic targeting, we infected TNF-α, IL-1α, and C1qa Triple-KO mice (TKO-mice), which do not transit astrocytes into A1, with prions. Although formation of C3 + -astrocytes was significantly reduced in prion infected Triple-KO-mice, this did not affect the amount of PrP Sc deposition or titers of infectious prions. Detailed characterization of the astrocyte activation signature in thalamus tissue showed that astrocytes in prion diseases are highly activated, showing a mixed phenotype that is distinct from other neurodegenerative diseases and were therefore termed C3 + -PrP Sc -reactive-astrocytes. Unexpectedly, Triple-KO led to a significant acceleration of prion disease course. While pan-astrocyte and -microglia marker upregulation was unchanged compared to WT-brains, microglial homeostatic markers were lost early in disease in TKO-mice, pointing towards important functions of different glia cell types in prion diseases.
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Several proinflammatory cytokines, including TNF α, IL 1α, and C1qa, are upregulated in the brain during the prion disease course.
“Several proinflammatory cytokines are upregulated in the brain during the prion disease course including TNF α, IL 1α, and C1qa [46,69,70,71,72,73].”
From Loss of Homeostatic Microglia Signature in Prion Diseases (2022) · cites this paper as [73]
Microglia and astrocytes keep close contacts in the healthy brain but also in terminal prion disease, although both cell types are considerably dysregulated.
“Microglia and astrocytes keep close contacts in the healthy brain but also in terminal prion disease, although both cell types are considerably dysregulated (Figure 5B) [73].”
From Loss of Homeostatic Microglia Signature in Prion Diseases (2022) · cites this paper as [73]
Astrocytes in murine and human prion diseases express the A1-signature proteins complement 3 and GBP2.
“We recently showed that astrocytes in murine and human prion diseases express the A1-signature proteins complement 3 and GBP2 [73].”
From Loss of Homeostatic Microglia Signature in Prion Diseases (2022) · cites this paper as [73]
TMEM119-positive processes are highly reduced at the terminal stage of prion disease in the hippocampus, and almost completely lost in the thalamus.
“As previously shown, TMEM119-positive processes are highly reduced at the terminal stage of prion disease in the hippocampus, and almost completely lost in the thalamus during terminal prion disease (Figure 5) [73].”
From Loss of Homeostatic Microglia Signature in Prion Diseases (2022) · cites this paper as [73]
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 reciprocal regulation of both proteins in prion disease.
“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 [73]
In terminal prion disease, while homeostatic markers are still abundant in the hippocampus, the homeostatic signature is almost completely lost in the thalamus, an effect especially severe for P2RY12.
“While the homeostatic markers are still abundant in the hippocampus, this signature is almost completely lost in the thalamus, an effect which is especially severe for P2RY12 (Figure 4) [47,73,97].”
From Loss of Homeostatic Microglia Signature in Prion Diseases (2022) · cites this paper as [73]
Astrocytes in prion disease show a mixed phenotype with expression of both A1 and A2 proteins that is unique in prion disorders and differs from other neurodegenerative diseases.
“In contrast, astrocytes in prion disease showed a mixed phenotype with an expression of both A1 and A2 proteins that is unique in prion disorders and differs from other neurodegenerative diseases [73].”
From Loss of Homeostatic Microglia Signature in Prion Diseases (2022) · cites this paper as [73]
Prion disease-associated astrogliosis is prominent in human prion diseases as shown by upregulation of GFAP and YKL-40 (CHI3L1).
“Prion disease-associated astrogliosis is also prominent in human prion diseases as shown by the upregulation of GFAP and YKL-40 (or Chitinase-3-like protein 1; CHI3L1) (Figure 6B) [73,107].”
From Loss of Homeostatic Microglia Signature in Prion Diseases (2022) · cites this paper as [73]
GFAP is highly upregulated in astrocytes upon disease.
“GFAP is highly upregulated in astrocytes upon disease [73,75,107].”
From Loss of Homeostatic Microglia Signature in Prion Diseases (2022) · cites this paper as [73]
The abundance of homeostatic microglia proteins such as TMEM119 and P2RY12 is significantly reduced in terminal prion disease.
“We recently showed that the abundance of homeostatic microglia proteins such as TMEM119 and P2RY12 is significantly reduced in terminal prion disease (Figure 4) [47,73,97].”
From Loss of Homeostatic Microglia Signature in Prion Diseases (2022) · cites this paper as [73]
In recent experiments, the extensive loss of the homeostatic signature in prion diseases stands out remarkably.
“Moreover, in our recent experiments, the extensive loss of the homeostatic signature in prion diseases stands out remarkably [47,73,97].”
From Loss of Homeostatic Microglia Signature in Prion Diseases (2022) · cites this paper as [73]
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- Authors
- Hartmann, K., Sepulveda-Falla, D., Rose, I. V. L., Madore, C., Muth, C., Matschke, J., Butovsky, O., Liddelow, S., Glatzel, M., & Krasemann, S.
- Affiliations
- University Medical Center Hamburg-Eppendorf (DE)
- NYU Langone Health (US)
- Brigham and Women's Hospital (US)
- The University of Melbourne (AU)
- Corresponding author
- Krasemann, Susanne
- ORCID
- Venue
- Acta Neuropathologica Communications
- Published
- 2019-05-22
- Volume
- 7
- Issue
- 1
- Pages
- 83-83
- ISSN
- 2051-5960 (ISSN-L)
- PMC
- PMC6530067
- OpenAlex
- W2947673562
- Cited by
- 141
- References
- 66
- Citations by year
- 2026: 9 · 2025: 17 · 2024: 25 · 2023: 20 · 2022: 18 · 2021: 25 · 2020: 24 · 2019: 3
- FWCI
- 5.79
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Acta Neuropathologica Communications (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Minerva Access (University of Melbourne) (submittedVersion, cc-by)
- Funders
- Werner Otto Stiftung (9/91)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Prion Diseases and Protein Misfolding
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Keywords
- prion disease, A1 astrocytes, astrocyte polarization, microglial activation, TNF-α, IL-1α, C1QA, triple knockout mice, prion pathogenesis, neuroinflammation, glial interactions, thalamus, neurodegeneration
- MeSH terms
- Aged, Animals, Astrocytes, Complement C3, Female, Humans, Creutzfeldt-Jakob Syndrome, Male, Mice, Inbred C57BL, Middle Aged, Cytokines, Prion Diseases, Microglia, Mice, Knockout, Disease Progression, PrPSc Proteins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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