Experimental autoimmune encephalomyelitis (EAE) as a model for multiple sclerosis (MS)

Constantinescu, Cris S; Farooqi, Nasr; O'Brien, Kate; Gran, Bruno

doi:10.1111/j.1476-5381.2011.01302.x

Cited by 1,523Multiple Sclerosis Research StudiesNeuroinflammation and Neurodegeneration MechanismsPeripheral Neuropathies and Disorders

Experimental autoimmune encephalomyelitis (EAE) as a model for multiple sclerosis (MS)

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Constantinescu, Cris S, Farooqi, Nasr, O'Brien, Kate, Gran, Bruno·2011·British Journal of Pharmacology

DOI 10.1111/j.1476-5381.2011.01302.xPMC PMC3229753

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Abstract

Experimental autoimmune encephalomyelitis (EAE) is the most commonly used experimental model for the human inflammatory demyelinating disease, multiple sclerosis (MS). EAE is a complex condition in which the interaction between a variety of immunopathological and neuropathological mechanisms leads to an approximation of the key pathological features of MS: inflammation, demyelination, axonal loss and gliosis. The counter-regulatory mechanisms of resolution of inflammation and remyelination also occur in EAE, which, therefore can also serve as a model for these processes. Moreover, EAE is often used as a model of cell-mediated organ-specific autoimmune conditions in general. EAE has a complex neuropharmacology, and many of the drugs that are in current or imminent use in MS have been developed, tested or validated on the basis of EAE studies. There is great heterogeneity in the susceptibility to the induction, the method of induction and the response to various immunological or neuropharmacological interventions, many of which are reviewed here. This makes EAE a very versatile system to use in translational neuro- and immunopharmacology, but the model needs to be tailored to the scientific question being asked. While creating difficulties and underscoring the inherent weaknesses of this model of MS in straightforward translation from EAE to the human disease, this variability also creates an opportunity to explore multiple facets of the immune and neural mechanisms of immune-mediated neuroinflammation and demyelination as well as intrinsic protective mechanisms. This allows the eventual development and preclinical testing of a wide range of potential therapeutic interventions.

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C-Phycocyanin protects axons from demyelination in rats suffering from multiple sclerosis.
“Studies on rats suffering from MS were treated with C-Phycocyanin. The authors noted that the experimental animals have firm, albeit crumpled, myelin sheaths with no signs of axonal disintegration, so they concluded that C-Phycocyanin protects axons from demyelination [98,99].”
From Application of Arthrospira platensis for Medicinal Purposes and the Food Industry: A Review of the Literature (2023) · cites this paper as [99]
The section on induction of EAE in rodents describes rat models and demyelination, but not C-Phycocyanin treatment. A search for C-Phycocyanin found no passage reporting the claimed myelin or axonal findings; the References section mentions axonal protection with phenytoin, a different substance. (LLM, conf=0.74)
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Experimental Autoimmune Encephalomyelitis is the most used experimental model for multiple sclerosis and is capable of reproducing the main neuroimmunological and histopathological aspects of multiple sclerosis.
“The most used experimental model for the study of this disease is the Experimental Autoimmune Encephalomyelitis (EAE), capable of reproducing the main neuroimmunological and histopathological aspects of MS [155,156].”
From Beneficial Effects of Spirulina Consumption on Brain Health (2022) · cites this paper as [155]

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The CB2 Cannabinoid Receptor Controls Myeloid Progenitor Trafficking
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Transplanted neural precursor cells reduce brain inflammation to attenuate chronic experimental autoimmune encephalomyelitis
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Induction of Antigen-Specific Tolerance in Multiple Sclerosis After Immunization With DNA Encoding Myelin Basic Protein in a Randomized, Placebo-Controlled Phase 1/2 Trial
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The new orally active immunoregulator laquinimod (ABR-215062) effectively inhibits development and relapses of experimental autoimmune encephalomyelitis
Brunmark, C., Runström, A., Ohlsson, L., Sparre, B., Brodin, T., Åström, M., & Hedlund, G. (2002) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(02)00225-4 · Cited by 164 · see citing works
Experimental autoimmune encephalomyelitis in NF-kappa B-deficient mice:roles of NF-kappa B in the activation and differentiation of autoreactive T cells.
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Mechanisms of immunomodulation by glatiramer acetate
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FTY720 sustains and restores neuronal function in the DA rat model of MOG-induced experimental autoimmune encephalomyelitis
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Mitoxantrone for multiple sclerosis
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Minocycline attenuates T cell and microglia activity to impair cytokine production in T cell-microglia interaction
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Copolymer 1 inhibits chronic relapsing experimental allergic encephalomyelitis induced by proteolipid protein (PLP) peptides in mice and interferes with PLP-specific T cell responses
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Oral tolerance, an active immunologic process mediated by multiple mechanisms
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Interferon-β inhibits progression of relapsing-remitting experimental autoimmune encephalomyelitis
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Antigen Presentation in the CNS by Myeloid Dendritic Cells Drives Progression of Relapsing Experimental Autoimmune Encephalomyelitis
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Antibodies Against IL-12 Prevent Superantigen-Induced and Spontaneous Relapses of Experimental Autoimmune Encephalomyelitis
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FTY720 Rescue Therapy in the Dark Agouti Rat Model of Experimental Autoimmune Encephalomyelitis: Expression of Central Nervous System Genes and Reversal of Blood‐Brain‐Barrier Damage
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Experimental Autoimmune Encephalomyelitis in NF-κB- Deficient Mice: Roles of NF-κB in the Activation and Differentiation of Autoreactive T Cells
Hilliard, B. A., Samoilova, E. B., Liu, T.-S. T., Rostami, A. M., & Chen, Y. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.163.5.2937 · Cited by 142 · see citing works
Oral Tolerance in Experimental Autoimmune Encephalomyelitis
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Cutting Edge: TLR3 Stimulation Suppresses Experimental Autoimmune Encephalomyelitis by Inducing Endogenous IFN-β
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Swift Entry of Myelin-Specific T Lymphocytes into the Central Nervous System in Spontaneous Autoimmune Encephalomyelitis
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Transcriptional analysis of targets in multiple sclerosis
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The macrophage in MS: just a scavenger after all? Pathology and pathogenesis of the acute MS lesion
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Protective effect of the interleukin-1 receptor antagonist (IL-1ra) on experimental allergic encephalomyelitis in rats
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Axonal protection achieved in a model of multiple sclerosis using lamotrigine
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IL-4, IL-10, IL-13, and TGF-β from an Altered Peptide Ligand-Specific Th2 Cell Clone Down-Regulate Adoptive Transfer of Experimental Autoimmune Encephalomyelitis
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Suppression of experimental allergic encephalomyelitis in rhesus monkeys by a synthetic basic copolymer
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Assessment: The use of natalizumab (Tysabri) for the treatment of multiple sclerosis (an evidence-based review)
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Phase 1 trial of transforming growth factor beta 2 in chronic progressive MS
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Suppression by several synthetic polypeptides of experimental allergic encephalomyelitis induced in guinea pigs and rabbits with bovine and human basic encephalitogen
Teitelbaum, D., Webb, C., Meshorer, A., Arnon, R., & Sela, M. (1973) · European Journal of Immunology · doi:10.1002/eji.1830030505 · Cited by 122 · see citing works
Laquinimod interferes with migratory capacity of T cells and reduces IL-17 levels, inflammatory demyelination and acute axonal damage in mice with experimental autoimmune encephalomyelitis
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The clinical response to minocycline in multiple sclerosis is accompanied by beneficial immune changes: a pilot study
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Humanization of a mouse antibody against human alpha-4 integrin: A potential therapeutic for the treatment of multiple sclerosis
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Prevention and reversal of adoptively transferred, chronic relapsing experimental autoimmune encephalomyelitis with a single high dose cytoreductive treatment followed by syngeneic bone marrow transplantation.
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Dual roles of PGE 2 -EP4 signaling in mouse experimental autoimmune encephalomyelitis
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Animal Models of Multiple Sclerosis
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Estriol treatment ameliorates disease in males with experimental autoimmune encephalomyelitis: implications for multiple sclerosis
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Long-term protection of central axons with phenytoin in monophasic and chronic-relapsing EAE
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Genetic Analysis of Disease Subtypes and Sexual Dimorphisms in Mouse Experimental Allergic Encephalomyelitis (EAE): Relapsing/Remitting and Monophasic Remitting/Nonrelapsing EAE Are Immunogenetically Distinct
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Win 55212-2, a cannabinoid receptor agonist, attenuates leukocyte/endothelial interactions in an experimental autoimmune encephalomyelitis model
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Mixed results with modulation of TH-17 cells in human autoimmune diseases
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Discordant effects of anti–VLA-4 treatment before and after onset of relapsing experimental autoimmune encephalomyelitis
Theien, B. E., Vanderlugt, C. L., Eagar, T. N., Nickerson‐Nutter, C. L., Nazareno, R., Kuchroo, V. K., & Miller, S. D. (2001) · Journal of Clinical Investigation · doi:10.1172/jci11717 · Cited by 112 · see citing works
Intravenous immunoglobulin treatment of experimental T cell-mediated autoimmune disease. Upregulation of T cell proliferation and downregulation of tumor necrosis factor alpha secretion.
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Memantine abrogates neurological deficits, but not CNS inflammation, in Lewis rat experimental autoimmune encephalomyelitis
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Treatment of chronic-relapsing experimental autoimmune encephalomyelitis with the synthetic immunomodulator linomide (quinoline-3-carboxamide).
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Demyelinated neocortical lesions in marmoset autoimmune encephalomyelitis mimic those in multiple sclerosis.
Pomeroy, I., Matthews, P., Frank, J., Jordan, E., & Esiri, M. (2005) · Brain : a journal of neurology · doi:10.1093/brain/awh626 · Cited by 111 · see citing works

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BJP EAE as model for MS British Journal of Pharmacology (2011) 164 1079-1106 1095
BJP EAE as model for MS British Journal of Pharmacology (2011) 164 1079-1106 1097
BJP EAE as model for MS British Journal of Pharmacology (2011) 164 1079-1106 1101
BJP EAE as model for MS British Journal of Pharmacology (2011) 164 1079-1106 1105

Sorted by citations

Microglia in Neuroinflammation and Neurodegeneration: From Understanding to Therapy
Muzio, L., Viotti, A., & Martino, G. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.742065 · Cited by 581 · see citing works
Stem Cell-Derived Exosomes as Nanotherapeutics for Autoimmune and Neurodegenerative Disorders
Riazifar, M., Mohammadi, M. R., Pone, E. J., Yeri, A., Lässer, C., Segaliny, A. I., McIntyre, L. L., Shelke, G. V., Hutchins, E., Hamamoto, A., et al. (2019) · ACS Nano · doi:10.1021/acsnano.9b01004 · Cited by 551 · see citing works
Single-cell analysis reveals T cell infiltration in old neurogenic niches
Dulken, B. W., Buckley, M. T., Navarro Negredo, P., Saligrama, N., Cayrol, R., Leeman, D. S., George, B. M., Boutet, S. C., Hebestreit, K., Pluvinage, J. V., et al. (2019) · Nature · doi:10.1038/s41586-019-1362-5 · Cited by 521 · see citing works
NADPH oxidase in brain injury and neurodegenerative disorders
Ma, M. W., Wang, J., Zhang, Q., Wang, R., Dhandapani, K. M., Vadlamudi, R. K., & Brann, D. W. (2017) · Molecular Neurodegeneration · doi:10.1186/s13024-017-0150-7 · Cited by 432 · see citing works
Glial response during cuprizone-induced de- and remyelination in the CNS: lessons learned
Gudi, V., Gingele, S., Skripuletz, T., & Stangel, M. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00073 · Cited by 375 · see citing works
“EAE reflects the autoimmune origin of MS and is probably the most frequently used model that already has been proven as extremely useful to develop/establish/test some of the currently available immunomodulating MS therapeutics (Gold et al., 2000, 2006; Constantinescu et al., 2011).”
Method
Target identification among known drugs by deep learning from heterogeneous networks
Zeng, X., Zhu, S., Lu, W., Liu, Z., Huang, J., Zhou, Y., Fang, J., Huang, Y., Guo, H., Li, L., et al. (2020) · Chemical Science · doi:10.1039/c9sc04336e · Cited by 357 · see citing works
SYK coordinates neuroprotective microglial responses in neurodegenerative disease
Ennerfelt, H., Frost, E. L., Shapiro, D. A., Holliday, C., Zengeler, K. E., Voithofer, G., Bolte, A. C., Lammert, C. R., Kulas, J. A., Ulland, T. K., et al. (2022) · Cell · doi:10.1016/j.cell.2022.09.030 · Cited by 329 · see citing works
The contribution of astrocytes to the neuroinflammatory response in multiple sclerosis and experimental autoimmune encephalomyelitis
Brambilla, R. (2019) · Acta Neuropathologica · doi:10.1007/s00401-019-01980-7 · Cited by 246 · see citing works
Xist ribonucleoproteins promote female sex-biased autoimmunity
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A shared disease-associated oligodendrocyte signature among multiple CNS pathologies
Kenigsbuch, M., Bost, P., Halevi, S., Chang, Y., Chen, S., Ma, Q., Hajbi, R., Schwikowski, B., Bodenmiller, B., Fu, H., et al. (2022) · Nature Neuroscience · doi:10.1038/s41593-022-01104-7 · 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
“APCs play an important role in the activation of peripherally-primed T cells, resulting in an inflammatory cascade that leads to oligodendrocyte death, chronic demyelination, and neuronal loss [64, 77].”
Background
Aging and Neurodegenerative Disease: Is the Adaptive Immune System a Friend or Foe?
Mayne, K., White, J. A., McMurran, C. E., Rivera, F. J., & de la Fuente, A. G. (2020) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2020.572090 · Cited by 167 · 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
Where are we? The anatomy of the murine cortical meninges revisited for intravital imaging, immunology, and clearance of waste from the brain
Coles, J. A., Myburgh, E., Brewer, J. M., & McMenamin, P. G. (2017) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2017.05.002 · Cited by 123 · see citing works
Cellular senescence in white matter microglia is induced during ageing in mice and exacerbates the neuroinflammatory phenotype
Matsudaira, T., Nakano, S., Konishi, Y., Kawamoto, S., Uemura, K., Kondo, T., Sakurai, K., Ozawa, T., Hikida, T., Komine, O., et al. (2023) · Communications Biology · doi:10.1038/s42003-023-05027-2 · Cited by 98 · see citing works
Application of Arthrospira platensis for Medicinal Purposes and the Food Industry: A Review of the Literature
Gentscheva, G., Nikolova, K., Panayotova, V., Peycheva, K., Makedonski, L., Slavov, P., Radusheva, P., Petrova, P., & Yotkovska, I. (2023) · Life · doi:10.3390/life13030845 · Cited by 106 · 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
Microglial NLRP3 inflammasome activation in multiple sclerosis
(2020) · Advances in Protein Chemistry and Structural Biology · doi:10.1016/bs.apcsb.2019.08.007 · Cited by 83 · see citing works
An overall view of the most common experimental models for multiple sclerosis
Dedoni, S., Scherma, M., Camoglio, C., Siddi, C., Dazzi, L., Puliga, R., Frau, J., Cocco, E., & Fadda, P. (2023) · Neurobiology of Disease · doi:10.1016/j.nbd.2023.106230 · Cited by 79 · see citing works
Emerging pathogenic role of peripheral blood factors following BBB disruption in neurodegenerative disease
Jeon, M.-T., Kim, K.-S., Kim, E. S., Lee, S., Kim, J., Hoe, H.-S., & Kim, D.-G. (2021) · Ageing Research Reviews · doi:10.1016/j.arr.2021.101333 · Cited by 76 · see citing works
Mice deficient in NRROS show abnormal microglial development and neurological disorders
Wong, K., Noubade, R., Manzanillo, P., Ota, N., Foreman, O., Hackney, J. A., Friedman, B. A., Pappu, R., Scearce-Levie, K., & Ouyang, W. (2017) · Nature Immunology · doi:10.1038/ni.3743 · Cited by 71 · see citing works
The gut microbiome regulates astrocyte reaction to Aβ amyloidosis through microglial dependent and independent mechanisms
Chandra, S., Di Meco, A., Dodiya, H. B., Popovic, J., Cuddy, L. K., Weigle, I. Q., Zhang, X., Sadleir, K., Sisodia, S. S., & Vassar, R. (2023) · Molecular Neurodegeneration · doi:10.1186/s13024-023-00635-2 · Cited by 58 · see citing works
Sex differences in EAE reveal common and distinct cellular and molecular components
Wiedrick, J., Meza-Romero, R., Gerstner, G., Seifert, H., Chaudhary, P., Headrick, A., Kent, G., Maestas, A., Offner, H., & Vandenbark, A. A. (2021) · Cellular Immunology · doi:10.1016/j.cellimm.2020.104242 · Cited by 55 · see citing works
Purinergic Receptors in Neurological Diseases With Motor Symptoms: Targets for Therapy
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Suppression of the Peripheral Immune System Limits the Central Immune Response Following Cuprizone-Feeding: Relevance to Modelling Multiple Sclerosis
Sen, M. K., Almuslehi, M. S. M., Gyengesi, E., Myers, S. J., Shortland, P. J., Mahns, D. A., & Coorssen, J. R. (2019) · Cells · doi:10.3390/cells8111314 · Cited by 35 · see citing works
Emerging roles of leptin in Parkinson’s disease: Chronic inflammation, neuroprotection and more?
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“This approach bypasses the peripheral priming phase, hereby allowing for direct assessment of how effector T cell populations mediate disease [91, 92].”

Schwann cell remyelination and recurrent demyelination in the central nervous system of mice infected with attenuated Theiler's virus.
Canto, M. C. D., & Lipton, H. L. (1980) · PubMed · Cited by 54 · see citing works
An experimental model of secondary progressive multiple sclerosis that shows regional variation in gliosis, remyelination, axonal and neuronal loss
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Authors: Constantinescu, C. S., Farooqi, N., O'Brien, K., & Gran, B.
Affiliations: University of Nottingham (GB)
Corresponding author: Constantinescu, Cris S
ORCID: Constantinescu, Cris S
Farooqi, Nasr
Gran, Bruno
Venue: British Journal of Pharmacology
Publisher: Wiley
Published: 2011-10
Volume: 164
Issue: 4
Pages: 1079-1106
ISSN: 0007-1188 (ISSN-L)
1476-5381
DOI: 10.1111/j.1476-5381.2011.01302.x
PMC: PMC3229753
OpenAlex: W1607206274
Cited by: 1,523
References: 395
Citations by year: 2026: 102 · 2025: 120 · 2024: 165 · 2023: 147 · 2022: 178 · 2021: 159 · 2020: 131 · 2019: 111 · 2018: 89 · 2017: 80 · 2016: 71 · 2015: 57 · 2014: 49 · 2013: 50 · 2012: 11
FWCI: 4.53
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 131 d)
Locations: British Journal of Pharmacology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Multiple Sclerosis Society
European Commission
University of Nottingham
China Scholarship Council
Topics: Health Sciences › Medicine › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Health Sciences › Medicine › Neurology › Peripheral Neuropathies and Disorders
Keywords: experimental autoimmune encephalomyelitis, multiple sclerosis, animal models of disease, demyelination, neuroinflammation, axonal loss, gliosis, remyelination, anti-inflammatory mechanism, neuropharmacology, immunopharmacology, cell-mediated autoimmunity, translational research, preclinical drug testing
MeSH terms: Animals, Haplorhini, Disease Models, Animal, Drug Evaluation, Preclinical, Encephalomyelitis, Autoimmune, Experimental, Female, Humans, Male, Multiple Sclerosis, Drug Design, Mice, Rats

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Experimental autoimmune encephalomyelitis (EAE) as a model for multiple sclerosis (MS)

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