RNA-seq and network analysis reveal unique glial gene expression signatures during prion infection
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Background: Prion diseases and prion-like disorders, including Alzheimer’s disease and Parkinson’s disease, are characterized by gliosis and accumulation of misfolded aggregated host proteins. Ablating microglia in prion-infected brain by treatment with the colony-stimulating factor-1 receptor (CSF-1R) inhibitor, PLX5622, increased accumulation of misfolded prion protein and decreased survival time. Methods: To better understand the role of glia during neurodegeneration, we used RNA-seq technology, network analysis, and hierarchical cluster analysis to compare gene expression in brains of prion-infected versus mock-inoculated mice. Comparisons were also made between PLX5622-treated prion-infected mice and untreated prion-infected mice to assess mechanisms involved in disease acceleration in the absence of microglia. Results: RNA-seq and network analysis suggested that microglia responded to prion infection through activation of integrin CD11c/18 and did not adopt the expression signature associated with other neurodegenerative disease models. Instead, microglia acquired an alternative molecular signature late in the disease process. Furthermore, astrocytes expressed a signature pattern of genes which appeared to be specific for prion diseases. Comparisons were also made with prion-infected mice treated with PLX5622 to assess the impact of microglia ablation on astrocyte gene expression during prion infection. In the presence of microglia, a unique mix of transcripts associated with A1- and A2-reactive astrocytes was increased in brains of prion-infected mice. After ablation of microglia, this reactive astrocyte expression pattern was enhanced. Thus, after prion infection, microglia appeared to decrease the overall A1/A2-astrocyte responses which might contribute to increased survival after infection. Conclusions: RNA-seq analysis indicated dysregulation of over 300 biological processes within the CNS during prion disease. Distinctive microglia- and astrocyte-associated expression signatures were identified during prion infection. Furthermore, astrogliosis and the unique astrocyte-associated expression signature were independent of microglial influences. Astrogliosis and the unique astrocyte-associated gene expression pattern were increased when microglia were ablated. Our findings emphasize the potential existence of alternative pathways for activating the A1/A2 paradigm in astrocytes during neurodegenerative disease.
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This prion disease-specific astrocyte signature develops without the proinflammatory stimulation provided by microglia.
“Interestingly, novel investigations in mouse models after microglia depletion have shown that this prion disease-specific astrocyte signature develops without the proinflammatory stimulation provided by microglia [98].”
From Loss of Homeostatic Microglia Signature in Prion Diseases (2022) · cites this paper as [98]
Findings on the loss of homeostatic microglial proteins in terminal prion disease contrast with findings on RNA expression of the corresponding genes, since P2ry12 RNA expression has been shown to be relatively upregulated.
“Interestingly, these findings on the loss of homeostatic microglial proteins in terminal prion disease are in contrast to findings on the RNA expression of the corresponding genes, since P2ry12 RNA expression has been shown to be relatively upregulated [98,99].”
From Loss of Homeostatic Microglia Signature in Prion Diseases (2022) · cites this paper as [98]
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Kim, T., Lee, I., Cho, J.-H., Canine, B., Keller, A., Price, N. D., Hwang, D., Carlson, G. A., & Hood, L. (2020) · Molecular Brain · doi:10.1186/s13041-020-0551-3 · Cited by 20 · see citing works
Neuronal loss and apoptosis in experimental Creutzfeldt-Jakob disease in mice.
Jesionek‐Kupnicka, D., Buczyński, J., Kordek, R., et al. (1999) · PubMed · Cited by 17 · see citing works
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Microglia deficiency accelerates prion disease but does not enhance prion accumulation in the brain
Bradford, B. M., McGuire, L. I., Hume, D. A., Pridans, C., & Mabbott, N. A. (2022) · Glia · doi:10.1002/glia.24244 · Cited by 44 · see citing works
Sinha, A., Kushwaha, R., Molesworth, K., Mychko, O., Makarava, N., & Baskakov, I. V. (2021) · Cells · doi:10.3390/cells10071728 · Cited by 42 · see citing works
Slota, J. A., Medina, S. J., Frost, K. L., & Booth, S. A. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.918811 · Cited by 16 · see citing works
Pankiewicz, J. E., Lizińczyk, A. M., Franco, L. A., Diaz, J. R., Martá-Ariza, M., & Sadowski, M. J. (2021) · Acta Neuropathologica Communications · doi:10.1186/s40478-021-01261-z · Cited by 15 · see citing works
Loss of Homeostatic Microglia Signature in Prion Diseases
Wang, Y., Hartmann, K., Thies, E., Mohammadi, B., Altmeppen, H., Sepulveda-Falla, D., Glatzel, M., & Krasemann, S. (2022) · Cells · doi:10.3390/cells11192948 · Cited by 12 · see citing works
“Interestingly, novel investigations in mouse models after microglia depletion have shown that this prion disease-specific astrocyte signature develops without the proinflammatory stimulation provided by microglia [98].”
BackgroundResult
- Authors
- Carroll, J. A., Race, B., Williams, K., Striebel, J., & Chesebro, B.
- Affiliations
- National Institutes of Health (US)
- Corresponding author
- Carroll, James A.
- Venue
- Molecular Brain
- Published
- 2020-05-07
- Volume
- 13
- Issue
- 1
- Pages
- 71-71
- ISSN
- 1756-6606 (ISSN-L)
- PMC
- PMC7206698
- OpenAlex
- W3021619272
- Cited by
- 66
- References
- 92
- Citations by year
- 2026: 5 · 2025: 8 · 2024: 18 · 2023: 8 · 2022: 13 · 2021: 12 · 2020: 2
- FWCI
- 2.84
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Molecular Brain (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Division of Intramural Research, National Institute of Allergy and Infectious Diseases
- 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, glial gene expression, microglia, astrocytes, astrocyte activation, microglial ablation, PLX5622, CSF1R inhibition, reactive astrocytes, neurodegeneration, prion aggregation, gliosis
- MeSH terms
- RNA-Seq, Animals, Astrocytes, Brain, Female, Gene Expression Regulation, Gliosis, Immunohistochemistry, Male, Mice, Inbred C57BL, Neuroglia, Organic Chemicals, Prions, Scrapie, Signal Transduction, Cluster Analysis, Prion Diseases, Apoptosis, In Situ Hybridization, Microglia, CD18 Antigens, Neurodegenerative Diseases, CD11c Antigen, Mice, Transcriptome, Gene Ontology
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.
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