Immunology of multiple sclerosis

Sospedra, Mireia; Martin, Roland

doi:10.1146/annurev.immunol.23.021704.115707

Cited by 2,149Multiple Sclerosis Research StudiesT-cell and B-cell ImmunologyPsoriasis: Treatment and Pathogenesis

Immunology of multiple sclerosis

Sospedra, Mireia, Martin, Roland·2005·Annual Review of Immunology

DOI 10.1146/annurev.immunol.23.021704.115707

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Abstract

Multiple sclerosis (MS) develops in young adults with a complex predisposing genetic trait and probably requires an inciting environmental insult such as a viral infection to trigger the disease. The activation of CD4+ autoreactive T cells and their differentiation into a Th1 phenotype are a crucial events in the initial steps, and these cells are probably also important players in the long-term evolution of the disease. Damage of the target tissue, the central nervous system, is, however, most likely mediated by other components of the immune system, such as antibodies, complement, CD8+ T cells, and factors produced by innate immune cells. Perturbations in immunomodulatory networks that include Th2 cells, regulatory CD4+ T cells, NK cells, and others may in part be responsible for the relapsing-remitting or chronic progressive nature of the disease. However, an important paradigmatic shift in the study of MS has occurred in the past decade. It is now clear that MS is not just a disease of the immune system, but that factors contributed by the central nervous system are equally important and must be considered in the future.

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“Neurological deficits in MS patients result from two pathogenic events: acute inflammatory demyelination and axonal injury [150,151].”
From Beneficial Effects of Spirulina Consumption on Brain Health (2022) · cites this paper as [150]

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The pathology of primary progressive multiple sclerosis
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CD1-restricted T-cell responses and microbial infection
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Nitric Oxide and Peroxynitrite in Health and Disease
Pacher, P., Beckman, J. S., & Liaudet, L. (2007) · Physiological Reviews · doi:10.1152/physrev.00029.2006 · Cited by 6,390 · see citing works
Mechanisms underlying inflammation in neurodegeneration
Glass, C. K., Saijo, K., Winner, B., Marchetto, M. C., & Gage, F. H. (2010) · Cell · doi:10.1016/j.cell.2010.02.016 · Cited by 3,580 · see citing works
The Endocannabinoid System as an Emerging Target of Pharmacotherapy
Pacher, P., Bátkai, S., & Kunos, G. (2006) · Pharmacological Reviews · doi:10.1124/pr.58.3.2 · Cited by 2,077 · see citing works
The complex role of estrogens in inflammation
Straub, R. H. (2007) · Endocrine Reviews · doi:10.1210/er.2007-0001 · Cited by 1,950 · see citing works
Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation
Kebir, H., Kreymborg, K., Ifergan, I., Dodelet-Devillers, A., Cayrol, R., Bernard, M., Giuliani, F., Arbour, N., Becher, B., & Prat, A. (2007) · Nature Medicine · doi:10.1038/nm1651 · Cited by 1,759 · see citing works
Experimental autoimmune encephalomyelitis (EAE) as a model for multiple sclerosis (MS)
Constantinescu, C. S., Farooqi, N., O'Brien, K., & Gran, B. (2011) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2011.01302.x · Cited by 1,523 · see citing works
Heritability enrichment of specifically expressed genes identifies disease-relevant tissues and cell types
Finucane, H. K., Reshef, Y. A., Anttila, V., Slowikowski, K., Gusev, A., Byrnes, A., Gazal, S., Loh, P.-R., Lareau, C., Shoresh, N., et al. (2018) · Nature Genetics · doi:10.1038/s41588-018-0081-4 · Cited by 1,097 · see citing works
Multiple sclerosis: a complicated picture of autoimmunity
McFarland, H. F., & Martin, R. (2007) · Nature Immunology · doi:10.1038/ni1507 · Cited by 985 · see citing works
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Revisiting the Mechanisms of CNS Immune Privilege
Louveau, A., Harris, T. H., & Kipnis, J. (2015) · Trends in Immunology · doi:10.1016/j.it.2015.08.006 · Cited by 682 · see citing works
Molecular mimicry and autoimmunity
Rojas, M., Restrepo-Jiménez, P., Monsalve, D. M., Pacheco, Y., Acosta-Ampudia, Y., Ramírez-Santana, C., Leung, P. S. C., Ansari, A. A., Gershwin, M. E., & Anaya, J.-M. (2018) · Journal of Autoimmunity · doi:10.1016/j.jaut.2018.10.012 · Cited by 627 · see citing works
Preferential recruitment of interferon‐γ–expressing T <sub>H</sub> 17 cells in multiple sclerosis
Kebir, H., Ifergan, I., Alvarez, J. I., Bernard, M., Poirier, J., Arbour, N., Duquette, P., & Prat, A. (2009) · Annals of Neurology · doi:10.1002/ana.21748 · Cited by 551 · see citing works
Systemic inflammation and the brain: novel roles of genetic, molecular, and environmental cues as drivers of neurodegeneration
Sankowski, R., Mader, S., & ValdÃ©s-Ferrer, S. I. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00028 · Cited by 351 · see citing works
Myelin-laden macrophages are anti-inflammatory, consistent with foam cells in multiple sclerosis
Boven, L. A., Van Meurs, M., Van Zwam, M., Wierenga-Wolf, A., Hintzen, R. Q., Boot, R. G., Aerts, J. M., Amor, S., Nieuwenhuis, E. E., & Laman, J. D. (2006) · Brain · doi:10.1093/brain/awh707 · Cited by 353 · see citing works
The resolution of neuroinflammation in neurodegeneration: leukocyte recruitment via the choroid plexus
Schwartz, M., & Baruch, K. (2014) · The EMBO Journal · doi:10.1002/embj.201386609 · Cited by 349 · see citing works
Melatonin Contributes to the Seasonality of Multiple Sclerosis Relapses
Farez, M. F., Mascanfroni, I. D., Méndez-Huergo, S. P., Yeste, A., Murugaiyan, G., Garo, L. P., Balbuena Aguirre, M. E., Patel, B., Ysrraelit, M. C., Zhu, C., et al. (2015) · Cell · doi:10.1016/j.cell.2015.08.025 · Cited by 318 · see citing works
The Inflammasome Sensor, NLRP3, Regulates CNS Inflammation and Demyelination via Caspase-1 and Interleukin-18
Jha, S., Srivastava, S. Y., Brickey, W. J., Iocca, H., Toews, A., Morrison, J. P., Chen, V. S., Gris, D., Matsushima, G. K., & Ting, J. P.-Y. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4088-10.2010 · Cited by 310 · see citing works
Astrocyte-restricted ablation of interleukin-17-induced ACT1-mediated signaling ameliorates autoimmune encephalomyelitis
Kang, Z., Altuntas, C. Z., Gulen, M. F., Liu, C., Giltiay, N., Qin, H., Liu, L., Qian, W., Ransohoff, R. M., Bergmann, C., et al. (2010) · Immunity · doi:10.1016/j.immuni.2010.03.004 · Cited by 297 · see citing works
Immune cell trafficking across the barriers of the central nervous system in multiple sclerosis and stroke
Lopes Pinheiro, M. A., Kooij, G., Mizee, M. R., Kamermans, A., Enzmann, G., Lyck, R., Schwaninger, M., Engelhardt, B., & de Vries, H. E. (2016) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2015.10.018 · Cited by 247 · see citing works
Butyrate suppresses demyelination and enhances remyelination
Chen, T., Noto, D., Hoshino, Y., Mizuno, M., & Miyake, S. (2019) · Journal of Neuroinflammation · doi:10.1186/s12974-019-1552-y · Cited by 229 · see citing works
Act1 mediates IL-17-induced EAE pathogenesis selectively in NG2+ glial cells
Kang, Z., Wang, C., Zepp, J., Wu, L., Sun, K., Zhao, J., Chandrasekharan, U., DiCorleto, P. E., Trapp, B. D., Ransohoff, R. M., et al. (2013) · Nature Neuroscience · doi:10.1038/nn.3505 · Cited by 218 · see citing works
Sex: A Significant Risk Factor for Neurodevelopmental and Neurodegenerative Disorders
Pinares-Garcia, P., Stratikopoulos, M., Zagato, A., Loke, H., & Lee, J. (2018) · Brain Sciences · doi:10.3390/brainsci8080154 · Cited by 200 · see citing works
Amelioration of experimental autoimmune encephalomyelitis by probiotic mixture is mediated by a shift in T helper cell immune response
Kwon, H.-K., Kim, G.-C., Kim, Y., Hwang, W., Jash, A., Sahoo, A., Kim, J.-E., Nam, J. H., & Im, S.-H. (2013) · Clinical Immunology · doi:10.1016/j.clim.2013.01.001 · Cited by 212 · see citing works
Virgin Olive Oil and Health: Summary of the III International Conference on Virgin Olive Oil and Health Consensus Report, JAEN (Spain) 2018
Gaforio, J. J., Visioli, F., Alarcón-de-la-Lastra, C., Castañer, O., Delgado-Rodríguez, M., Fitó, M., Hernández, A. F., Huertas, J. R., Martínez-González, M. A., Menendez, J. A., et al. (2019) · Nutrients · doi:10.3390/nu11092039 · Cited by 187 · see citing works
Microglial autophagy–associated phagocytosis is essential for recovery from neuroinflammation
Berglund, R., Guerreiro-Cacais, A. O., Adzemovic, M. Z., Zeitelhofer, M., Lund, H., Ewing, E., Ruhrmann, S., Nutma, E., Parsa, R., Thessen-Hedreul, M., et al. (2020) · Science Immunology · doi:10.1126/sciimmunol.abb5077 · Cited by 149 · see citing works
Melanoma cell adhesion molecule identifies encephalitogenic T lymphocytes and promotes their recruitment to the central nervous system
Larochelle, C., Cayrol, R., Kebir, H., Alvarez, J. I., Lécuyer, M.-A., Ifergan, I., Viel, É., Bourbonnière, L., Beauseigle, D., Terouz, S., et al. (2012) · Brain · doi:10.1093/brain/aws212 · Cited by 145 · see citing works
The role of chemokines and chemokine receptors in multiple sclerosis
Cui, L.-Y., Chu, S.-F., & Chen, N.-H. (2020) · International Immunopharmacology · doi:10.1016/j.intimp.2020.106314 · Cited by 135 · see citing works
Nutrition and fasting mimicking diets in the prevention and treatment of autoimmune diseases and immunosenescence
Choi, I. Y., Lee, C., & Longo, V. D. (2017) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2017.01.042 · Cited by 133 · see citing works
CNS: Not an immunoprivilaged site anymore but a virtual secondary lymphoid organ
Negi, N., & Das, B. K. (2018) · International Reviews of Immunology · doi:10.1080/08830185.2017.1357719 · Cited by 123 · see citing works
Immunomodulation mechanism of antidepressants: interactions between serotonin/norepinephrine balance and Th1/Th2 balance
Martino, M., Rocchi, G., Escelsior, A., & Fornaro, M. (2012) · Current Neuropharmacology · doi:10.2174/157015912800604542 · Cited by 111 · see citing works
Identification of a Novel Risk Locus for Multiple Sclerosis at 13q31.3 by a Pooled Genome-Wide Scan of 500,000 Single Nucleotide Polymorphisms
Comabella, M., Craig, D. W., Camiña-Tato, M., Morcillo, C., Lopez, C., Navarro, A., Rio, J., BiomarkerMS Study Group, Montalban, X., & Martin, R. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003490 · Cited by 105 · see citing works
Self-citation
Contribution of Astrocyte-Derived IL-15 to CD8 T Cell Effector Functions in Multiple Sclerosis
Saikali, P., Antel, J. P., Pittet, C. L., Newcombe, J., & Arbour, N. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.1002188 · Cited by 101 · see citing works
Mechanisms of oligodendrocyte regeneration from ventricular-subventricular zone-derived progenitor cells in white matter diseases
Maki, T., Liang, A. C., Miyamoto, N., Lo, E. H., & Arai, K. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00275 · Cited by 99 · see citing works
Beneficial Effects of Spirulina Consumption on Brain Health
Trotta, T., Porro, C., Cianciulli, A., & Panaro, M. A. (2022) · Nutrients · doi:10.3390/nu14030676 · Cited by 98 · see citing works
Allopregnanolone and neuroinflammation: a focus on multiple sclerosis
Noorbakhsh, F., Baker, G. B., & Power, C. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00134 · Cited by 95 · see citing works
Immunology of neuromyelitis optica: a T cell-B cell collaboration
Mitsdoerffer, M., Kuchroo, V., & Korn, T. (2013) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12118 · Cited by 91 · see citing works
IL-17-Induced Act1-Mediated Signaling Is Critical for Cuprizone-Induced Demyelination
Kang, Z., Liu, L., Spangler, R., Spear, C., Wang, C., Gulen, M. F., Veenstra, M., Ouyang, W., Ransohoff, R. M., & Li, X. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0841-12.2012 · Cited by 78 · see citing works
Estrogen protection against EAE modulates the microbiota and mucosal-associated regulatory cells
Benedek, G., Zhang, J., Nguyen, H., Kent, G., Seifert, H. A., Davin, S., Stauffer, P., Vandenbark, A. A., Karstens, L., Asquith, M., et al. (2017) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2017.06.007 · Cited by 64 · see citing works
The GPR17 receptor-A promising goal for therapy and a potential marker of the neurodegenerative process in multiple sclerosis
Dziedzic, A., Miller, E., Saluk-Bijak, J., & Bijak, M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21051852 · Cited by 38 · see citing works
Comparative Neuroregenerative Effects of C-Phycocyanin and IFN-Beta in a Model of Multiple Sclerosis in Mice
Pentón-Rol, G., Lagumersindez-Denis, N., Muzio, L., Bergami, A., Furlan, R., Fernández-Massó, J. R., Nazabal-Galvez, M., Llópiz-Arzuaga, A., Herrera-Rolo, T., Veliz-Rodriguez, T., et al. (2016) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-015-9642-9 · Cited by 36 · see citing works
Epstein-Barr Virus and Multiple Sclerosis
Lünemann, J. D., & Münz, C. (2007) · Current Neurology and Neuroscience Reports · doi:10.1007/s11910-007-0038-y · Cited by 36 · see citing works
Methylprednisolone inhibits IFN-γ and IL-17 expression and production by cells infiltrating central nervous system in experimental autoimmune encephalomyelitis
Miljković, Ž., Momčilović, M., Miljković, D., & Mostarica-Stojković, M. (2009) · Journal of Neuroinflammation · doi:10.1186/1742-2094-6-37 · Cited by 35 · see citing works
The potential role of T cell migration and chemotaxis as targets of glucocorticoids in multiple sclerosis and experimental autoimmune encephalomyelitis
Fischer, H. J., Schweingruber, N., Lühder, F., & Reichardt, H. M. (2013) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2013.04.001 · Cited by 34 · see citing works
Comparative Analysis of T-Cell Responses to Aquaporin-4 and Myelin Oligodendrocyte Glycoprotein in Inflammatory Demyelinating Central Nervous System Diseases
Hofer, L. S., Ramberger, M., Gredler, V., Pescoller, A. S., Rostásy, K., Sospedra, M., Hegen, H., Berger, T., Lutterotti, A., & Reindl, M. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01188 · Cited by 30 · see citing works
Self-citation
PBMCs protein expression profile in relapsing IFN-treated multiple sclerosis: A pilot study on relation to clinical findings and brain atrophy
De Masi, R., Vergara, D., Pasca, S., Acierno, R., Greco, M., Spagnolo, L., Blasi, E., Sanapo, F., Trianni, G., & Maffia, M. (2009) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2009.03.002 · Cited by 26 · see citing works
Role for antibodies in altering behavior and movement
Libbey, J. E., & Fujinami, R. S. (2010) · Autism Research · doi:10.1002/aur.144 · Cited by 25 · see citing works
The role of the adaptive immune system in the initiation and persistence of multiple sclerosis
Afzali, A. M., & Korn, T. (2025) · Seminars in Immunology · doi:10.1016/j.smim.2025.101947 · Cited by 25 · see citing works
Astrocyte‐specific expression of a soluble form of the murine complement control protein Crry confers demyelination protection in the cuprizone model
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Authors: Sospedra, M., & Martin, R.
Affiliations: National Institutes of Health (US)
Cellular Immunology Section, Neuroimmunology Branch, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland 20892-1400;
ORCID: Sospedra, Mireia
Venue: Annual Review of Immunology
Publisher: Annual Reviews
Published: 2005-04-01
Volume: 23
Issue: 1
Pages: 683-747
ISSN: 0732-0582 (ISSN-L)
1545-3278
DOI: 10.1146/annurev.immunol.23.021704.115707
OpenAlex: W2113291839
Cited by: 2,149
References: 362
Citations by year: 2026: 27 · 2025: 43 · 2024: 62 · 2023: 64 · 2022: 69 · 2021: 72 · 2020: 78 · 2019: 84 · 2018: 71 · 2017: 110 · 2016: 107 · 2015: 149 · 2014: 133 · 2013: 144 · 2012: 120
FWCI: 19.06
Type: journal article
Language: en
Open access: closed
Locations: Annual Review of Immunology (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Life Sciences › Immunology and Microbiology › Immunology › Psoriasis: Treatment and Pathogenesis
Keywords: multiple sclerosis, autoimmunity, CD4+ T cells, Th1 cells, Th2 cells, regulatory T cells, natural killer cells, CD8+ T cells, complement system, autoantibodies, innate immunity, viral triggers, genetic susceptibility, relapsing-remitting disease, chronic progressive disease, central nervous system, neuroimmune interactions
MeSH terms: Autoantibodies, Autoantigens, Central Nervous System, HLA Antigens, Humans, Immunity, Innate, Immunogenetics, Infections, Multiple Sclerosis, Myelin Proteins, T-Lymphocyte Subsets, Cytokines, Models, Immunological, Molecular Mimicry, Chemokines, Genomics

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