The genetic signature of perineuronal oligodendrocytes reveals their unique phenotype
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Oligodendrocytes – best known for assembling central nervous system myelin – can be categorized as precursors, myelin‐forming cells and non‐myelinating perineuronal cells. Perineuronal oligodendrocytes have been well characterized morphologically and ultrastructurally, but knowledge about their function remains scanty. It has been proposed that perineuronal oligodendrocytes support neurons and, following injury, transform into myelin‐synthesizing cells. Recent findings implicating perineuronal oligodendrocytes in cytoarchitectural abnormalities in the prefrontal cortex of schizophrenia and other psychiatric disorders shed new light on these cells. We have obtained the genetic signature of perineuronal oligodendrocytes by identifying gene expression differences between oligodendrocyte subpopulations using cell‐specific tags, microarray technology, quantitative time‐resolved polymerase chain reaction and bioinformatics tools. We show that perineuronal cells are the progeny of oligodendrocyte progenitors and, hence, are members of the oligodendrocyte lineage. Physiologically they exhibit a novel phenotype. Their expression of PDGFR‐αβ and its growth factor ligand PDGF‐CC sets them apart from members of their lineage as this receptor precludes their response to the same growth factors that act on myelinating cells. Their coordinate expression and context‐specific usage of transcription factors Olig2, Ascl1 and Pax6, together with the prominent presence of transcription factors Pea3, Lhx2 and Otx2 – not hitherto linked to the oligodendrocyte lineage – suggested a cell with features that blur the boundary between a neuron and a glial cell. But they also maintain a reservoir of untranslated transcripts encoding major myelin proteins presumably for a demyelinating episode. This first molecular characterization of perineuronal oligodendrocytes revealed the striking difference between the myelinating and non‐myelinating phenotypes.
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Satellite oligodendrocytes are largely considered non-myelinating and may fulfil specific functions in neuronal support.
“Satellite oligodendrocytes are largely considered non-myelinating and may fulfil specific functions in neuronal support.51-54”
From BCAS1-positive oligodendrocytes enable efficient cortical remyelination in multiple sclerosis (2025) · cites this paper as [52]
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- Authors
- Szuchet, S., Nielsen, J. A., Lovas, G., Domowicz, M. S., de Velasco, J. M., Maric, D., & Hudson, L. D.
- Affiliations
- University of Chicago (US)
- National Institutes of Health (US)
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2011-12
- Volume
- 34
- Issue
- 12
- Pages
- 1906-1922
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- PMC
- PMC4286392
- OpenAlex
- W1602694202
- Cited by
- 53
- References
- 84
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 6 · 2023: 5 · 2022: 3 · 2021: 4 · 2020: 1 · 2019: 4 · 2018: 3 · 2017: 1 · 2016: 1 · 2015: 2 · 2014: 4 · 2013: 8 · 2012: 1
- FWCI
- 1.37
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Multiple Sclerosis Society
- Georgia Clinical and Translational Science Alliance
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (Z01NS002528)
- National Center for Research Resources (UL1RR024999)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Health Sciences › Medicine › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- oligodendrocyte lineage, gene expression signatures, PDGFRA, PDGF-CC, transcription factors, Olig2, ASCL1, Pax6, PEA3, Lhx2, Otx2, myelination, demyelination, oligodendrocyte progenitors, prefrontal cortex, schizophrenia
- MeSH terms
- Animals, Cells, Cultured, Mice, Inbred C57BL, Mice, Transgenic, Myelin Proteins, Myelin Sheath, Neurons, Oligodendroglia, Phenotype, Transcription Factors, Signal Transduction, Biomarkers, Gene Expression, Rats, Sprague-Dawley, Cell Lineage, Gene Expression Profiling, Microarray Analysis, Mice, Rats
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