Functional genomic analyses highlight a shift in Gpr17 ‐regulated cellular processes in oligodendrocyte progenitor cells and underlying myelin dysregulation in the aged mouse cerebrum
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Abstract
Brain ageing is characterised by a decline in neuronal function and associated cognitive deficits. There is increasing evidence that myelin disruption is an important factor that contributes to the age-related loss of brain plasticity and repair responses. In the brain, myelin is produced by oligodendrocytes, which are generated throughout life by oligodendrocyte progenitor cells (OPCs). Currently, a leading hypothesis points to ageing as a major reason for the ultimate breakdown of remyelination in Multiple Sclerosis (MS). However, an incomplete understanding of the cellular and molecular processes underlying brain ageing hinders the development of regenerative strategies. Here, our combined systems biology and neurobiological approach demonstrate that oligodendroglial and myelin genes are amongst the most altered in the ageing mouse cerebrum. This was underscored by the identification of causal links between signalling pathways and their downstream transcriptional networks that define oligodendroglial disruption in ageing. The results highlighted that the G-protein coupled receptor Gpr17 is central to the disruption of OPCs in ageing and this was confirmed by genetic fate-mapping and cellular analyses. Finally, we used systems biology strategies to identify therapeutic agents that rejuvenate OPCs and restore myelination in age-related neuropathological contexts.
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The strong activation of immune- and inflammation-related genes, as well as differential expression of remyelination regulators like Gpr17, suggest that the homeostasis of white matter is compromised at old age.
“The strong activation of immune- and inflammation-related genes, as well as differential expression of remyelination regulators like Gpr17 (Dziedzic et al., 2020; Rivera et al., 2021), suggest that the homeostasis of this region is compromised at old age.”
From Atlas of the aging mouse brain reveals white matter as vulnerable foci (2023) · cites this paper as Rivera et al., 2021
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Rocha, I. C. D. L., Fryatt, G. L., Rivera, A. D., Restani, L., Caleo, M., Raineteau, O., Gómez‐Nicola, D., & Butt, A. M. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.09.23.309682 · Cited by 4 · see citing works
Self-citationAzim, K., Calzolari, F., Cantone, M., Akkermann, R., Vera, J., Hartung, H., Başak, O., Butt, A. M., & Küry, P. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.12.18.423285 · Cited by 2 · see citing works
Self-citationNolte (2001) · doi:10.1002/1098-1136(20010101)33:1
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Atlas of the aging mouse brain reveals white matter as vulnerable foci
Hahn, O., Foltz, A. G., Atkins, M., Kedir, B., Moran-Losada, P., Guldner, I. H., Munson, C., Kern, F., Pálovics, R., Lu, N., et al. (2023) · Cell · doi:10.1016/j.cell.2023.07.027 · Cited by 213 · see citing works
- Authors
- Rivera, A. D., Pieropan, F., Chacon‐De‐La‐Rocha, I., Lecca, D., Abbracchio, M. P., Azim, K., & Butt, A. M.
- Affiliations
- University of Padua (IT)
- University of Portsmouth (GB)
- School of Pharmacy and Biomedical Science University of Portsmouth Portsmouth UK
- University of Milan (IT)
- Heinrich Heine University Düsseldorf (DE)
- Corresponding author
- Azim, Kasum
- Butt, Arthur M.
- ORCID
- Venue
- Aging Cell
- Publisher
- Wiley
- Published
- 2021-03-05
- Volume
- 20
- Issue
- 4
- Pages
- e13335-e13335
- ISSN
- 1474-9718 (ISSN-L)
- 1474-9726
- PMC
- PMC8045941
- OpenAlex
- W3135398361
- Cited by
- 61
- References
- 87
- Citations by year
- 2026: 3 · 2025: 15 · 2024: 8 · 2023: 14 · 2022: 13 · 2021: 8
- FWCI
- 3.88
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Aging Cell (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Archivio Istituzionale della Ricerca (Universita Degli Studi Di Milano) (submittedVersion, other-oa)
- Funders
- Deutsche Forschungsgemeinschaft (AZ115/1‐1)
- Egészségügyi Tudományos Tanács (MR/P025811/1)
- Biotechnology and Biological Sciences Research Council (BB/M029379/1)
- Anatomical Society
- Multiple Sclerosis Society
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Health Sciences › Medicine › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- GPR17, oligodendrocyte precursor cells, brain aging, myelin damage, G protein-coupled receptors, remyelination, multiple sclerosis, transcriptional regulatory networks, signaling pathways, fate mapping, myelination, therapeutic agents
- MeSH terms
- Oligodendrocyte Precursor Cells, RNA-Seq, Aging, Animals, Cell Differentiation, Mice, Inbred C57BL, Mice, Transgenic, Myelin Sheath, Nerve Tissue Proteins, Neurons, Signal Transduction, Genomics, Receptors, G-Protein-Coupled, Mice, Cerebrum, Transcriptome
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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