Neuronal vulnerability and multilineage diversity in multiple sclerosis
Open accessAbstract
Multiple sclerosis (MS) is a neuroinflammatory disease with a relapsing-remitting disease course at early stages, distinct lesion characteristics in cortical grey versus subcortical white matter and neurodegeneration at chronic stages. Here we used single-nucleus RNA sequencing to assess changes in expression in multiple cell lineages in MS lesions and validated the results using multiplex in situ hybridization. We found selective vulnerability and loss of excitatory CUX2-expressing projection neurons in upper-cortical layers underlying meningeal inflammation; such MS neuron populations exhibited upregulation of stress pathway genes and long non-coding RNAs. Signatures of stressed oligodendrocytes, reactive astrocytes and activated microglia mapped most strongly to the rim of MS plaques. Notably, single-nucleus RNA sequencing identified phagocytosing microglia and/or macrophages by their ingestion and perinuclear import of myelin transcripts, confirmed by functional mouse and human culture assays. Our findings indicate lineage- and region-specific transcriptomic changes associated with selective cortical neuron damage and glial activation contributing to progression of MS lesions.
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Focal lesions such as those in the brainstem result in axonal loss, and cortical demyelination is associated with selective neuronal loss; both are prominent determinants of progression.
“It is well established that focal lesions such as those in the brainstem result in axonal loss, and that cortical demyelination, which occurs independently of white matter lesions, is associated with selective neuronal loss18; both these degenerative features are prominent determinants of progression18,19.”
From Locus for severity implicates CNS resilience in progression of multiple sclerosis (2023) · cites this paper as [18]
The Abstract links focal plaques with progressive white-matter axonal damage, and the Results report selective loss of CUX2-expressing neurons in demyelinated cortical lesions (page numbers unavailable). The copy does not establish the brainstem-specific example, that cortical demyelination occurs independently of white-matter lesions, or that both degenerative features are prominent determinants of progression. (LLM, conf=0.84)
Experimental — accuracy not yet measuredHomozygous rs10191329 risk allele carriers demonstrated more severe MS-specific brainstem and cortical pathology, which result in axonal and neuronal degeneration respectively and drive progression.
“Besides these clinical differences, homozygous rs10191329 risk allele carriers also demonstrated more severe MS-specific brainstem and cortical pathology, which result in axonal and neuronal degeneration respectively and drive progression18,19.”
From Locus for severity implicates CNS resilience in progression of multiple sclerosis (2023) · cites this paper as [18]
The Results report degeneration and selective loss of upper-layer excitatory neurons in cortical MS lesions, and the Discussion links cortical neurodegeneration to regions involved in progression. The paper does not establish that homozygous rs10191329 carriers have more severe pathology, nor does it report brainstem pathology or show that these changes drive progression. (LLM, conf=0.87)
Experimental — accuracy not yet measuredIn the Schirmer et al. dataset, microglial cluster 1 was selectively enriched within acute/chronic active MS lesions.
“This cluster was selectively enriched within acute/chronic active MS lesions (Fig. 4 C and D and Dataset S7).”
From Acute TREM2 inhibition depletes MAFB-high microglia and hinders remyelination (2025) · cites this paper as [37]
The Results (page unavailable) map activated microglia to the boundaries of chronic-active MS lesions, and Extended Data Fig. 5 describes microglial subtypes associated with inflammatory lesion stages. Our copy does not identify the mapped cells as “microglial cluster 1” or establish selective enrichment in both acute and chronic-active lesions. (LLM, conf=0.83)
Experimental — accuracy not yet measuredMicroglia contribute to both the development and progression of MS.
“Together, these results suggest microglia contribute to both the development and progression of MS”
From Activated microglia drive demyelination via <scp>CSF1R</scp> signaling (2021) · cites this paper as Schirmer et al., 2019
The Results (page not available in our copy) identify activated, phagocytosing microglia at the rims of chronic-active MS lesions, and the Discussion links microglial activation there to lesion areas involved in progression. These findings support a suggested role in progression, but the paper does not establish a role for microglia in the initial development of MS. (LLM, conf=0.84)
Experimental — accuracy not yet measuredReanalysis of the human MS snRNA-seq dataset from Schirmer et al. showed that microglia coexpressed TREM2 and MAFB.
“A reanalysis of the human MS snRNA-seq dataset from Schirmer et al. (37) showed that microglia coexpressed TREM2 and MAFB (SI Appendix, Fig. S9 A–D).”
From Acute TREM2 inhibition depletes MAFB-high microglia and hinders remyelination (2025) · cites this paper as [37]
Reclustering of microglia in the Schirmer et al. dataset revealed three distinct clusters spanning three different MS conditions.
“Reclustering of microglia revealed three distinct clusters spanning three different MS conditions (Fig. 4 A and B and Dataset S7).”
From Acute TREM2 inhibition depletes MAFB-high microglia and hinders remyelination (2025) · cites this paper as [37]
MS lesions, particularly the rims of chronic active lesions, contain stressed OLs, reactive astrocytes, and activated phagocytosing microglia/macrophages.
“MS lesions, particularly the rims of chronic active lesions, contain stressed OLs, reactive astrocytes, and activated phagocytosing microglia/macrophages11,12,15.”
From A comparative transcriptomic analysis of mouse demyelination models and multiple sclerosis lesions (2026) · cites this paper as [12]
B2M has been shown to be upregulated in other MS datasets.
“Interestingly, B2M was not significantly upregulated by MOLs in any MS lesion type, however it has been shown to be upregulated in other MS datasets11–13.”
From A comparative transcriptomic analysis of mouse demyelination models and multiple sclerosis lesions (2026) · cites this paper as [12]
Numerous studies have found reactive microglia in both active and pre-active MS lesions, including evidence for their active phagocytosis of myelin and myelin transcripts.
“As tools for identifying and visualizing microglia have advanced, numerous studies have found reactive microglia in both active, and pre-active MS lesions (Lassmann, 2014; van der Valk & Amor, 2009; Zhang et al., 2011), including evidence for their active phagocytosis of myelin and myelin transcripts (Schirmer et al., 2019).”
From Activated microglia drive demyelination via <scp>CSF1R</scp> signaling (2021) · cites this paper as Schirmer et al., 2019
In the Schirmer et al. dataset, MAFB was also weakly expressed in inhibitory neurons.
“In this dataset, MAFB was also weakly expressed in inhibitory neurons.”
From Acute TREM2 inhibition depletes MAFB-high microglia and hinders remyelination (2025) · cites this paper as [37]
The Results section describes inhibitory-neuron markers and cell-type-specific expression, but does not report MAFB expression in inhibitory neurons. Searches for “MAFB” and “MAFB expression in inhibitory interneurons” found no passage addressing that claim in our copy. (LLM, conf=0.70)
Experimental — accuracy not yet measuredIn the Schirmer et al. dataset, microglial cluster 1 stood out due to its pronounced MAFB expression.
“Within these clusters, cluster 1 stood out due to its pronounced MAFB expression.”
From Acute TREM2 inhibition depletes MAFB-high microglia and hinders remyelination (2025) · cites this paper as [37]
The Results describe microglial clusters and list markers for homeostatic and activated cells, while Extended Data Fig. 5 describes clusters annotated a–f; neither identifies a MAFB-high cluster 1. Searches of our copy for “MAFB” and “microglial cluster 1 MAFB expression” found no passage establishing the claimed expression pattern. (LLM, conf=0.75)
Experimental — accuracy not yet measuredThe ground truth cell-type labels for the multiple sclerosis dataset were taken from the original publication of the data.
“The ground truth cell-type labels were taken from the original publication of the data [19].”
From A Deep Dive into Single-Cell RNA Sequencing Foundation Models (2023) · cites this paper as [19]
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- Authors
- Schirmer, L., Velmeshev, D., Holmqvist, S., Kaufmann, M., Werneburg, S., Jung, D., Vistnes, S., Stockley, J. H., Young, A., Steindel, M., Tung, B., Goyal, N., Bhaduri, A., Mayer, S., Engler, J. B., Bayraktar, O. A., Franklin, R. J. M., Haeussler, M., Reynolds, R., Schafer, D. P., Friese, M. A., Shiow, L. R., Kriegstein, A. R., & Rowitch, D. H.
- Affiliations
- University of California, San Francisco (US)
- Wellcome/MRC Cambridge Stem Cell Institute (GB)
- Universität Hamburg (DE)
- University of Massachusetts Chan Medical School (US)
- University of California, Santa Cruz (US)
- Imperial College London (GB)
- Corresponding author
- Kriegstein, Arnold R.
- Rowitch, David H.
- ORCID
- Schirmer, Lucas
- Velmeshev, Dmitry
- Holmqvist, Staffan
- Kaufmann, Max
- Werneburg, Sebastian
- Vistnes, Stephanie
- Stockley, John H.
- Steindel, Maike
- Bhaduri, Aparna
- Mayer, Simone
- Engler, Jan Broder
- Bayraktar, Omer A.
- Franklin, Robin J. M.
- Haeussler, Maximilian
- Reynolds, Richard
- Schafer, Dorothy P.
- Friese, Manuel A.
- Shiow, Lawrence R.
- Kriegstein, Arnold R.
- Rowitch, David H.
- Venue
- Nature
- Published
- 2019-07-17
- Volume
- 573
- Issue
- 7772
- Pages
- 75-82
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC6731122
- OpenAlex
- W2951560273
- Cited by
- 638
- References
- 56
- Citations by year
- 2026: 69 · 2025: 100 · 2024: 118 · 2023: 91 · 2022: 99 · 2021: 89 · 2020: 56 · 2019: 15 · 2012: 1
- FWCI
- 47.59
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship@UMassChan (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Spiral (Imperial College London) (submittedVersion)
- Apollo (University of Cambridge) (submittedVersion)
- Apollo
- Funders
- Wellcome Trust (108139, 108139/B/15/Z, 108139/Z/15/Z)
- Multiple Sclerosis Society
- Rosetrees Trust (M525-CD2)
- Cambridge University Hospitals (146281)
- Medical Research Council (MC_PC_12009, MR/K008803/1, MR/M010503/1)
- Biotechnology and Biological Sciences Research Council (1517905, BB/I013210/1)
- National Human Genome Research Institute (U41HG002371)
- National Institute of Neurological Disorders and Stroke (F32NS103266, R35NS097305, R01NS040511)
- Topics
- Health Sciences › Medicine › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
- Keywords
- multiple sclerosis, neuronal vulnerability, meningeal inflammation, reactive astrocytes, microglial activation, macrophages, MS plaques, long non-coding RNA, glial activation, single-nucleus RNA sequencing
- MeSH terms
- RNA-Seq, Adult, Animals, Astrocytes, Autopsy, Female, Humans, Macrophages, Male, Middle Aged, Multiple Sclerosis, Myelin Sheath, Neurons, Oligodendroglia, Phagocytosis, RNA, Small Nuclear, Cryopreservation, Microglia, Homeodomain Proteins, Cell Lineage, Mice, Transcriptome
About these checks
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