Exploring the origins of grey matter damage in multiple sclerosis

Calabrese, Massimiliano; Magliozzi, Roberta; Ciccarelli, Olga; Geurts, Jeroen J. G.; Reynolds, Richard; Martin, Roland

doi:10.1038/nrn3900

Cited by 414Multiple Sclerosis Research StudiesNeuroinflammation and Neurodegeneration MechanismsPsoriasis: Treatment and Pathogenesis

Exploring the origins of grey matter damage in multiple sclerosis

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Calabrese, Massimiliano, Magliozzi, Roberta, Ciccarelli, Olga, Geurts, Jeroen J. G., Reynolds, Richard, Martin, Roland·2015·Nature Reviews Neuroscience

DOI 10.1038/nrn3900

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Abstract

Multiple sclerosis is characterized at the gross pathological level by the presence of widespread focal demyelinating lesions of the myelin-rich white matter. However, it is becoming clear that grey matter is not spared, even during the earliest phases of the disease. Furthermore, grey matter damage may have an important role both in physical and cognitive disability. Grey matter pathology involves both inflammatory and neurodegenerative mechanisms, but the relationship between the two is unclear. Histological, immunological and neuroimaging studies have provided new insight in this rapidly expanding field, and form the basis of the most recent hypotheses on the pathogenesis of grey matter damage.

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Spinal cord pathology is an important determinant of permanent neurological disability in multiple sclerosis, with cardinal characteristics being inflammatory demyelination, synaptic, neuronal and axonal loss.
“Spinal cord pathology is an important determinant of permanent neurological disability with cardinal characteristics being inflammatory demyelination, synaptic, neuronal and axonal loss.6, 7, 8, 9, 10, 11”
From Neurite dispersion: a new marker of multiple sclerosis spinal cord pathology? (2017) · cites this paper as [7]
The introduction (p. 2) describes multiple sclerosis pathology as involving inflammation, demyelination, and axonal and neuronal damage. The discussion of spinal-cord cases (p. 8) links inflammation with diffuse axonal loss. But the paper does not establish spinal-cord pathology as an important determinant of permanent disability or identify synaptic loss as a cardinal feature of spinal-cord pathology. (LLM, conf=0.84)
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Most EAE models do not recapitulate the extensive grey matter pathology observed in patients, which show a demyelination pattern often characterized by chronic microglia activation, absence of leukocyte infiltration and pronounced meningeal inflammation.
“Furthermore, most EAE models do not recapitulate the extensive grey matter pathology observed in patients, which show a demyelination pattern often characterized by chronic microglia activation, absence of leukocyte infiltration [46] and pronounced meningeal inflammation [156].”
From Microglia and monocytes in inflammatory CNS disease: integrating phenotype and function (2022) · cites this paper as [46]
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Increased CD8+ T Cell Response to Epstein-Barr Virus Lytic Antigens in the Active Phase of Multiple Sclerosis
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Wallerian Degeneration: A Major Component of Early Axonal Pathology in Multiple Sclerosis
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MHC class I-restricted killing of neurons by virus-specific CD8+ T lymphocytes is effected through the Fas/FasL, but not the perforin pathway
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Gray and white matter volume changes in early RRMS
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Atrophy mainly affects the limbic system and the deep grey matter at the first stage of multiple sclerosis
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Myelin-specific T cells also recognize neuronal autoantigen in a transgenic mouse model of multiple sclerosis
Krishnamoorthy, G., Saxena, A., Mars, L. T., Domingues, H. S., Mentele, R., Ben‐Nun, A., Lassmann, H., Dornmair, K., Kurschus, F. C., Liblau, R., et al. (2009) · Nature Medicine · doi:10.1038/nm.1975 · Cited by 155 · see citing works
Cortical grey matter demyelination can be induced by elevated pro-inflammatory cytokines in the subarachnoid space of MOG-immunized rats.
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White matter hemodynamic abnormalities precede sub-cortical gray matter changes in multiple sclerosis
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Meningeal T cells associate with diffuse axonal loss in multiple sclerosis spinal cords
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B-Cell Enrichment and Epstein-Barr Virus Infection in Inflammatory Cortical Lesions in Secondary Progressive Multiple Sclerosis
Magliozzi, R., Serafini, B., Rosicarelli, B., Chiappetta, G., Veroni, C., Reynolds, R., & Aloisi, F. (2013) · Journal of Neuropathology and Experimental Neurology · doi:10.1097/nen.0b013e31827bfc62 · Cited by 140 · see citing works
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Connecting white matter injury and thalamic atrophy in clinically isolated syndromes.
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Genetic variation influences glutamate concentrations in brains of patients with multiple sclerosis
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High‐throughput sequencing of TCR repertoires in multiple sclerosis reveals intrathecal enrichment of EBV‐reactive CD8+ T cells
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Granzyme A released upon stimulation of cytotoxic T lymphocytes activates the thrombin receptor on neuronal cells and astrocytes.
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Imaging the tip of the iceberg: visualization of cortical lesions in multiple sclerosis
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Localization of grey matter atrophy in early RRMS
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Meningeal Inflammation is not Associated With Cortical Demyelination in Chronic Multiple Sclerosis
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The significance of perivascular infiltrations in multiple sclerosis
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Contribution of White Matter Lesions to Gray Matter Atrophy in Multiple Sclerosis
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Assessing the Correlation between Grey and White Matter Damage with Motor and Cognitive Impairment in Multiple Sclerosis Patients
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Grey matter pathology in clinically early multiple sclerosis: evidence from magnetic resonance imaging.
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Neurons as targets for T cells in the nervous system
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Imaging distribution and frequency of cortical lesions in patients with multiple sclerosis
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Spinal Cord Neuronal Pathology in Multiple Sclerosis
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Human autoreactive CD4+ T cell clones use perforin- or Fas/Fas ligand-mediated pathways for target cell lysis
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Cytotoxic CD8+T Cell–Neuron Interactions: Perforin-Dependent Electrical Silencing Precedes But Is Not Causally Linked to Neuronal Cell Death
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Magnetic resonance evidence of cortical onset of multiple sclerosis
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Cytotoxic NKG2C+ CD4 T Cells Target Oligodendrocytes in Multiple Sclerosis
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The changing clinical course of multiple sclerosis: A matter of gray matter
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Recognition of Conserved Amino Acid Motifs of Common Viruses and Its Role in Autoimmunity
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Association of regional gray matter volume loss and progression of white matter lesions in multiple sclerosis — A longitudinal voxel-based morphometry study
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HLA class II molecules (HLA-DR, -DP, -DQ) on cells in the human CNS studied in situ and in vitro.
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Mycovirus-Like DNA Virus Sequences from Cattle Serum and Human Brain and Serum Samples from Multiple Sclerosis Patients
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Molecules affecting myelin stability: A novel hypothesis regarding the pathogenesis of multiple sclerosis
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What Explains Gray Matter Atrophy in Long-standing Multiple Sclerosis?
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Cortical lesions in radiologically isolated syndrome
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The role of mitochondria in axonal degeneration and tissue repair in MS
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Voxel-wise assessment of progression of regional brain atrophy in relapsing-remitting multiple sclerosis.
Battaglini, M., Giorgio, A., Stromillo, M., Bartolozzi, M. L., Guidi, L., Federico, A., & de Stefano, N. (2009) · Journal of Neurological Sciences · doi:10.1016/j.jns.2009.02.322 · Cited by 76 · see citing works
Detection of Epstein–Barr virus and B-cell follicles in the multiple sclerosis brain: what you find depends on how and where you look
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MANBA, CXCR5, SOX8, RPS6KB1 and ZBTB46 are genetic risk loci for multiple sclerosis
Lill, C. M., Schjeide, B. M., Graetz, C., Ban, M., Alcina, A., Ortiz, M. A., Pérez‐Boza, J., Damotte, V., Booth, D. R., de Lapuente, A. L., et al. (2013) · Brain · doi:10.1093/brain/awt101 · Cited by 69 · see citing works
Low prevalence of TT virus in the cerebrospinal fluid of viremic patients with central nervous system disorders
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In vivo evidence of disseminated subpial T2* signal changes in multiple sclerosis at 7T: a surface-based analysis
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A novel population of CD4+CD56+ myelin-reactive T cells lyses target cells expressing CD56/neural cell adhesion molecule
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Epstein-Barr Virus Stimulates Torque Teno Virus Replication: A Possible Relationship to Multiple Sclerosis
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Heterogeneity of cortical lesions in multiple sclerosis
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Elevated matrix metalloproteinase-9 and degradation of perineuronal nets in cerebrocortical multiple sclerosis plaques
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Radioactive in situ hybridization for Epstein–Barr virus–encoded small RNA supports presence of Epstein–Barr virus in the multiple sclerosis brain
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Spatiotemporal distribution pattern of white matter lesion volumes and their association with regional grey matter volume reductions in relapsing‐remitting multiple sclerosis
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The influence of HLA‐DRB1*15 on motor cortical pathology in multiple sclerosis
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Increased Meningeal T and Plasma Cell Infiltration is Associated with Early Subpial Cortical Demyelination in Common Marmosets with Experimental Autoimmune Encephalomyelitis
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Different white matter lesion characteristics correlate with distinct grey matter abnormalities on magnetic resonance imaging in secondary progressive multiple sclerosis
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An updated histological classification system for multiple sclerosis lesions
Kuhlmann, T., Ludwin, S., Prat, A., Antel, J., Brück, W., & Lassmann, H. (2017) · Acta Neuropathologica · doi:10.1007/s00401-016-1653-y · Cited by 692 · see citing works
A Quarter Century of APOE and Alzheimer’s Disease: Progress to Date and the Path Forward
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Association of Chronic Active Multiple Sclerosis Lesions With Disability In Vivo
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Monitoring disease activity in multiple sclerosis using serum neurofilament light protein
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Progression of regional grey matter atrophy in multiple sclerosis
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Pathophysiological and cognitive mechanisms of fatigue in multiple sclerosis
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Autophagy and Microglia: Novel Partners in Neurodegeneration and Aging
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Epidemiology and treatment of multiple sclerosis in elderly populations
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Inflammatory intrathecal profiles and cortical damage in multiple sclerosis
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Self-citation
Neurite dispersion: a new marker of multiple sclerosis spinal cord pathology?
Grussu, F., Schneider, T., Tur, C., Yates, R. L., Tachrount, M., Ianuş, A., Yiannakas, M. C., Newcombe, J., Zhang, H., Alexander, D. C., et al. (2017) · Annals of Clinical and Translational Neurology · doi:10.1002/acn3.445 · Cited by 291 · see citing works
Synaptopathy connects inflammation and neurodegeneration in multiple sclerosis
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Cortical atrophy patterns in multiple sclerosis are non-random and clinically relevant
Steenwijk, M. D., Geurts, J. J. G., Daams, M., Tijms, B. M., Wink, A. M., Balk, L. J., Tewarie, P. K. B., Uitdehaag, B. M. J., Barkhof, F., Vrenken, H., et al. (2015) · Brain · doi:10.1093/brain/awv337 · Cited by 280 · see citing works
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A large fraction of neocortical myelin ensheathes axons of local inhibitory neurons
Micheva, K. D., Wolman, D. N., Mensh, B. D., Pax, E., Buchanan, J., Smith, S. J., & Bock, D. D. (2016) · eLife · doi:10.7554/elife.15784 · Cited by 271 · see citing works
Identifying multiple sclerosis subtypes using unsupervised machine learning and MRI data
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Environmental Control of Astrocyte Pathogenic Activities in CNS Inflammation
Wheeler, M. A., Jaronen, M., Covacu, R., Zandee, S., Scalisi, G., Rothhammer, V., Tjon, E. C., Chao, C., Kenison, J. E., Blain, M., et al. (2019) · Cell · doi:10.1016/j.cell.2018.12.012 · Cited by 250 · see citing works
TNF-mediated neuroinflammation is linked to neuronal necroptosis in Alzheimer's disease hippocampus
Jayaraman, A., Htike, T. T., James, R., Picón, C., & Reynolds, R. (2021) · Acta Neuropathologica Communications · doi:10.1186/s40478-021-01264-w · Cited by 239 · see citing works
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Outdoor Ambient Air Pollution and Neurodegenerative Diseases: the Neuroinflammation Hypothesis
Jayaraj, R. L., Rodriguez, E. A., Wang, Y., & Block, M. L. (2017) · Current Environmental Health Reports · doi:10.1007/s40572-017-0142-3 · Cited by 233 · see citing works
Microglia and monocytes in inflammatory CNS disease: integrating phenotype and function
Spiteri, A. G., Wishart, C. L., Pamphlett, R., Locatelli, G., & King, N. J. C. (2022) · Acta Neuropathologica · doi:10.1007/s00401-021-02384-2 · Cited by 216 · see citing works
“Furthermore, most EAE models do not recapitulate the extensive grey matter pathology observed in patients, which show a demyelination pattern often characterized by chronic microglia activation, absence of leukocyte infiltration [46] and pronounced meningeal inflammation [156].”
Background
Tumor Necrosis Factor and Interleukin-1β Modulate Synaptic Plasticity during Neuroinflammation
Rizzo, F. R., Musella, A., Vito, F. D., Fresegna, D., Bullitta, S., Vanni, V., Guadalupi, L., Bassi, M. S., Buttari, F., Mandolesi, G., et al. (2018) · Neural Plasticity · doi:10.1155/2018/8430123 · Cited by 213 · see citing works
Interleukin-12: Functional activities and implications for disease
Zundler, S., & Neurath, M. F. (2015) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2015.07.003 · Cited by 211 · see citing works
Multiple sclerosis and cognition: synaptic failure and network dysfunction
Filippo, M. D., Portaccio, E., Mancini, A., & Calabresi, P. (2018) · Nature reviews. Neuroscience · doi:10.1038/s41583-018-0053-9 · Cited by 209 · see citing works
The neuropathobiology of multiple sclerosis
Woo, M. S., Engler, J. B., & Friese, M. A. (2024) · Nature reviews. Neuroscience · doi:10.1038/s41583-024-00823-z · Cited by 194 · see citing works
Plasma neurofilament light chain levels in patients with MS switching from injectable therapies to fingolimod
Piehl, F., Kockum, I. S., Khademi, M., Blennow, K., Lycke, J., Zetterberg, H., & Olsson, T. P. (2017) · Multiple Sclerosis Journal · doi:10.1177/1352458517715132 · Cited by 184 · see citing works
Reconstruction of single cortical projection neurons reveals primary spine loss in multiple sclerosis
Jürgens, T., Jafari, M., Kreutzfeldt, M., Bahn, E., Brück, W., Kerschensteiner, M., & Merkler, D. (2016) · Brain · doi:10.1093/brain/awv353 · Cited by 175 · see citing works
Spinal cord involvement in multiple sclerosis and neuromyelitis optica spectrum disorders
Ciccarelli, O., Cohen, J. A., Reingold, S. C., Weinshenker, B. G., Amato, M. P., Banwell, B., Barkhof, F., Bebo, B. F., Becher, B., Béthoux, F., et al. (2019) · The Lancet Neurology · doi:10.1016/s1474-4422(18)30460-5 · Cited by 170 · see citing works
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Mechanism-based criteria to improve therapeutic outcomes in progressive multiple sclerosis
Yong, H. Y. F., & Yong, V. W. (2021) · Nature Reviews Neurology · doi:10.1038/s41582-021-00581-x · Cited by 170 · see citing works
Management of neurogenic bladder in patients with multiple sclerosis
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Authors: Calabrese, M., Magliozzi, R., Ciccarelli, O., Geurts, J. J. G., Reynolds, R., & Martin, R.
Affiliations: University of Verona (IT)
Istituto Superiore di Sanità (IT)
University College London Hospitals NHS Foundation Trust (GB)
Amsterdam UMC Location Vrije Universiteit Amsterdam (NL)
Hammersmith Hospital (GB)
Corresponding author: Calabrese, Massimiliano
ORCID: Calabrese, Massimiliano
Magliozzi, Roberta
Ciccarelli, Olga
Geurts, Jeroen J. G.
Reynolds, Richard
Venue: Nature Reviews Neuroscience
Publisher: Springer Science and Business Media LLC
Published: 2015-02-20
Volume: 16
Issue: 3
Pages: 147-158
ISSN: 1471-003X (ISSN-L)
1471-0048
DOI: 10.1038/nrn3900
OpenAlex: W1972438508
Cited by: 414
References: 131
Citations by year: 2026: 24 · 2025: 30 · 2024: 33 · 2023: 22 · 2022: 31 · 2021: 58 · 2020: 45 · 2019: 47 · 2018: 40 · 2017: 39 · 2016: 29 · 2015: 16
FWCI: 6.06
Type: journal article
Language: en
Open access: green
pure.amsterdamumc.nl
Licence: other-oa
www.springer.com/tdm (tdm)
Locations: Nature reviews. Neuroscience (publishedVersion)
PubMed (publishedVersion)
Pure Amsterdam UMC (publishedVersion, other-oa)
Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, other-oa)
UCL Discovery (University College London) (submittedVersion)
Zurich Open Repository and Archive (University of Zurich) (submittedVersion, other-oa)
Data Archiving and Networked Services (DANS) (submittedVersion)
Zurich Open Repository and Archive (University of Zurich)
Funders: National Science Foundation (2313255)
Fondazione Italiana Sclerosi Multipla
International Progressive MS Alliance
Multiple Sclerosis Society
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
Ministero della Salute (GR-2010-2313255, GR-2010)
Universität Zürich
Schweizerische Multiple Sklerose Gesellschaft
Medical Research Council
Topics: Health Sciences › Medicine › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Life Sciences › Immunology and Microbiology › Immunology › Psoriasis: Treatment and Pathogenesis
Keywords: multiple sclerosis, demyelination, neurodegeneration, neuroinflammation, white matter injury, cognitive disability, pathogenesis
MeSH terms: Animals, Cerebral Cortex, Humans, Inflammation, Multiple Sclerosis, White Matter, Gray Matter

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Exploring the origins of grey matter damage in multiple sclerosis

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