Mechanisms of Neurodegeneration and Axonal Dysfunction in Progressive Multiple Sclerosis

Correale, Jorge; Marrodan, Mariano; Ysrraelit, María Célica

doi:10.3390/biomedicines7010014

Cited by 167Multiple Sclerosis Research StudiesNeuroinflammation and Neurodegeneration MechanismsPeripheral Neuropathies and Disorders

Mechanisms of Neurodegeneration and Axonal Dysfunction in Progressive Multiple Sclerosis

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Correale, Jorge, Marrodan, Mariano, Ysrraelit, María Célica·2019·Biomedicines

DOI 10.3390/biomedicines7010014PMC PMC6466454

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Abstract

Multiple Sclerosis (MS) is a major cause of neurological disability, which increases predominantly during disease progression as a result of cortical and grey matter structures involvement. The gradual accumulation of disability characteristic of the disease seems to also result from a different set of mechanisms, including in particular immune reactions confined to the Central Nervous System such as: (a) B-cell dysregulation, (b) CD8+ T cells causing demyelination or axonal/neuronal damage, and (c) microglial cell activation associated with neuritic transection found in cortical demyelinating lesions. Other potential drivers of neurodegeneration are generation of oxygen and nitrogen reactive species, and mitochondrial damage, inducing impaired energy production, and intra-axonal accumulation of Ca2+, which in turn activates a variety of catabolic enzymes ultimately leading to progressive proteolytic degradation of cytoskeleton proteins. Loss of axon energy provided by oligodendrocytes determines further axonal degeneration and neuronal loss. Clearly, these different mechanisms are not mutually exclusive and could act in combination. Given the multifactorial pathophysiology of progressive MS, many potential therapeutic targets could be investigated in the future. This remains however, an objective that has yet to be undertaken.

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Neurological deficits in multiple sclerosis patients result from two pathogenic events: acute inflammatory demyelination and axonal injury.
“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 [151]

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Inflammatory Processes in Alzheimer’s Disease—Pathomechanism, Diagnosis and Treatment: A Review
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PPARγ/PGC1α signaling as a potential therapeutic target for mitochondrial biogenesis in neurodegenerative disorders
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The Role of Vitamins in Neurodegenerative Disease: An Update
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The Role of a Gut Microbial-Derived Metabolite, Trimethylamine N-Oxide (TMAO), in Neurological Disorders
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Beneficial Effects of Spirulina Consumption on Brain Health
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Mitochondrial Behavior in Axon Degeneration and Regeneration
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Monitoring the Redox Status in Multiple Sclerosis
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Microglial NLRP3 inflammasome activation in multiple sclerosis
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Epilepsy in Neurodegenerative Diseases: Related Drugs and Molecular Pathways
Cano, A. C., Fonseca, E., Ettcheto, M., Sánchez‐López, E., de Rojas, I., Alonso-Lana, S., Morató, X., Souto, E. B., Toledo, M., Boada, M., et al. (2021) · Pharmaceuticals · doi:10.3390/ph14101057 · Cited by 83 · see citing works
Chronic Demyelination and Axonal Degeneration in Multiple Sclerosis: Pathogenesis and Therapeutic Implications
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CNS Border-Associated Macrophages: Ontogeny and Potential Implication in Disease
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Approved and Emerging Disease Modifying Therapies on Neurodegeneration in Multiple Sclerosis
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MicroRNA (miRNA) as a biomarker for diagnosis, prognosis, and therapeutics molecules in neurodegenerative disease
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Functions and dysfunctions of oligodendrocytes in neurodegenerative diseases
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The SIRT-1/Nrf2/HO-1 axis: Guardians of neuronal health in neurological disorders
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Overview of Metformin and Neurodegeneration: A Comprehensive Review
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The effect of probiotics on immune responses and their therapeutic application: A new treatment option for multiple sclerosis
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Exosomes-Based Nanomedicine for Neurodegenerative Diseases: Current Insights and Future Challenges
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Exosomes as Biomarkers and Therapeutic Agents in Neurodegenerative Diseases: Current Insights and Future Directions
Dehghani, S., Ocakcı, O., Hatipoglu, P. T., Özalp, V. C., & Tevlek, A. (2025) · Molecular Neurobiology · doi:10.1007/s12035-025-04825-5 · Cited by 43 · see citing works
Piperine ameliorated memory impairment and myelin damage in lysolecethin induced hippocampal demyelination
Roshanbakhsh, H., Salmani, M. E., Dehghan, S., Nazari, A., Javan, M., & Pourabdolhossein, F. (2020) · Life Sciences · doi:10.1016/j.lfs.2020.117671 · Cited by 43 · see citing works
Relationship between inflammation and oxidative stress and its effect on multiple sclerosis
Ramos-González, E. J., Bitzer-Quintero, O. K., Ortíz, G. G., Hernández-Cruz, J. J., & Ramírez-Jirano, L. J. (2024) · Neurología (English Edition) · doi:10.1016/j.nrleng.2021.10.010 · Cited by 46 · see citing works
Tantalizing role of p53 molecular pathways and its coherent medications in neurodegenerative diseases
Talebi, M., Talebi, M., Kakouri, E., Farkhondeh, T., Pourbagher‐Shahri, A. M., Tarantilis, P. Α., & Samarghandian, S. (2021) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2021.01.042 · Cited by 39 · see citing works
Chronic inflammation is associated with neural responses to faces in bangladeshi children
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Mdivi-1 Modulates Macrophage/Microglial Polarization in Mice with EAE via the Inhibition of the TLR2/4-GSK3β-NF-κB Inflammatory Signaling Axis
Liu, X., Zhang, X., Niu, X.-J., Zhang, P., Wang, Q., Xue, X.-H., Song, G., Yu, J.-Z., Xi, G.-P., Song, L.-J., et al. (2021) · Molecular Neurobiology · doi:10.1007/s12035-021-02552-1 · Cited by 37 · see citing works
Effect of siponimod on magnetic resonance imaging measures of neurodegeneration and myelination in secondary progressive multiple sclerosis: Gray matter atrophy and magnetization transfer ratio analyses from the EXPAND phase 3 trial
Arnold, D. L., Piani-Meier, D., Bar‐Or, A., Benedict, R. H. B., Cree, B., Giovannoni, G., Gold, R., Vermersch, P., Arnould, S., Dahlke, F., et al. (2022) · Multiple Sclerosis Journal · doi:10.1177/13524585221076717 · Cited by 35 · see citing works
Time is myelin: Early cortical myelin repair prevents atrophy and clinical progression in multiple sclerosis
Lazzarotto, A., Hamzaoui, M., Tonietto, M., Dubessy, A.-L., Khalil, M., Pirpamer, L., Ropele, S., Enzinger, C., Battaglini, M., Stromillo, M. L., et al. (2024) · Brain · doi:10.1093/brain/awae024 · Cited by 33 · see citing works
Reduced TUBA1A Tubulin Causes Defects in Trafficking and Impaired Adult Motor Behavior
Buscaglia, G., Northington, K. R., Moore, J. K., & Bates, E. A. (2020) · eNeuro · doi:10.1523/eneuro.0045-20.2020 · Cited by 32 · see citing works
Effects of Palmitoylethanolamide on Neurodegenerative Diseases: A Review from Rodents to Humans
Landolfo, E., Cutuli, D., Petrosini, L., & Caltagirone, C. (2022) · Biomolecules · doi:10.3390/biom12050667 · Cited by 32 · see citing works
Spatio-temporal expression profile of NGF and the two-receptor system, TrkA and p75NTR, in experimental autoimmune encephalomyelitis
Delivanoglou, N., Boziki, M. K., Theotokis, P., Kesidou, E., Touloumi, O., Dafi, N., Nousiopoulou, E., Lagoudaki, R., Grigoriadis, N., Charalampopoulos, I., et al. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-1708-9 · Cited by 31 · see citing works
MRI biomarkers of disease progression and conversion to secondary-progressive multiple sclerosis
Tavazzi, E., Zivadinov, R., Dwyer, M. G., Jakimovski, D., Singhal, T., Weinstock‐Guttman, B., & Bergsland, N. (2020) · Expert Review of Neurotherapeutics · doi:10.1080/14737175.2020.1757435 · Cited by 32 · see citing works
Proteomics of Multiple Sclerosis: Inherent Issues in Defining the Pathoetiology and Identifying (Early) Biomarkers
Sen, M. K., Almuslehi, M. S. M., Shortland, P. J., Mahns, D. A., & Coorssen, J. R. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22147377 · Cited by 31 · see citing works
Nogo-A and LINGO-1: Two Important Targets for Remyelination and Regeneration
Kalafatakis, I., Papagianni, F., Theodorakis, Κ., & Karagogeos, D. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24054479 · Cited by 28 · see citing works
Fatty acid elongation by ELOVL6 hampers remyelination by promoting inflammatory foam cell formation during demyelination
Corrales, A. V. G., Verberk, S. G. S., Haidar, M., Grajchen, E., Dehairs, J., Vanherle, S., Loix, M., Weytjens, T., Gervois, P., Matsuzaka, T., et al. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2301030120 · Cited by 29 · see citing works
B-Cell Receptor Repertoire: Recent Advances in Autoimmune Diseases
Wang, Q., Feng, D., Jia, S., Lu, Q., & Zhao, M. (2024) · Clinical Reviews in Allergy & Immunology · doi:10.1007/s12016-024-08984-6 · Cited by 26 · see citing works
Clinical Use of Schistosoma mansoni Antigens as Novel Immunotherapies for Autoimmune Disorders
Cleenewerk, L., Garssen, J., & Hogenkamp, A. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01821 · Cited by 26 · see citing works
Direct and indirect effects of microbiota-derived metabolites on neuroinflammation in multiple sclerosis
Fettig, N. M., & Osborne, L. C. (2021) · Microbes and Infection · doi:10.1016/j.micinf.2021.104814 · Cited by 26 · see citing works
Matrine Inhibits CNS Autoimmunity Through an IFN-β-Dependent Mechanism
Chu, Y., Ma, W., Thomé, R., Ping, J.-D., Liu, F., Wang, M., Zhang, M., Zhang, G., & Zhu, L. D. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.569530 · Cited by 26 · see citing works
The Alteration of Microglial Calcium Homeostasis in Central Nervous System Disorders: A Comprehensive Review
Hasan, A. R., Tasnim, F., Aktaruzzaman, M., Islam, M. T., Rayhan, R., Brishti, A., Hur, J., Porter, J. E., & Raihan, M. O. (2024) · Neuroglia · doi:10.3390/neuroglia5040027 · Cited by 25 · see citing works
How do neurons age? A focused review on the aging of the microtubular cytoskeleton
Richardson, B., Goedert, T., Quraishe, S., Deinhardt, K., & Mudher, A. K. (2023) · Neural Regeneration Research · doi:10.4103/1673-5374.390974 · Cited by 24 · see citing works
The Na+/Ca2+ exchangers in demyelinating diseases
Boscia, F., de Rosa, V., Cammarota, M., Secondo, A., Pannaccione, A., & Annunziato, L. (2019) · Cell Calcium · doi:10.1016/j.ceca.2019.102130 · Cited by 21 · see citing works
Targeting Vascular Impairment, Neuroinflammation, and Oxidative Stress Dynamics with Whole-Body Cryotherapy in Multiple Sclerosis Treatment
Dziedzic, A., Maciak, K., Miller, E. D., Starosta, M., & Saluk, J. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25073858 · Cited by 24 · see citing works
Analysis of shared underlying mechanism in neurodegenerative disease
Butler, R., Bradford, D. R., & Rodgers, K. E. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.1006089 · Cited by 23 · see citing works
Exploring novel roles of lipid droplets and lipid metabolism in regulating inflammation and blood–brain barrier function in neurological diseases
Fu, L., Luo, T., Hao, Z., Pan, Y., Xin, W., Zhang, L., Lai, Z., Zhang, H., Liu, H., & Wei, W. (2025) · Frontiers in Neuroscience · doi:10.3389/fnins.2025.1603292 · Cited by 20 · see citing works
Enhanced mitochondrial autophagy (mitophagy) in oligodendrocytes might play a role in white matter pathology in schizophrenia
Bernstein, H., Keilhoff, G., Dobrowolny, H., & Steiner, J. H. (2019) · Medical Hypotheses · doi:10.1016/j.mehy.2019.109443 · Cited by 20 · see citing works
Using Redox Proteomics to Gain New Insights into Neurodegenerative Disease and Protein Modification
Cadenas-Garrido, P., Schonvandt-Alarcos, A., Herrera‐Quintana, L., Vázquez‐Lorente, H., Santamaría-Quiles, A., de Francisco, J. R., Moya-Escudero, M., Martín‐Oliva, D., Martín-Guerrero, S. M., Rodríguez-Santana, C., et al. (2024) · Antioxidants · doi:10.3390/antiox13010127 · Cited by 20 · see citing works
Variation of genes encoding nitric oxide synthases and antioxidant enzymes as potential risks of multiple sclerosis development: a preliminary study
Wigner, P., Dziedzic, A., Synowiec, E., Miller, E. D., Bijak, M., & Saluk, J. (2022) · Scientific Reports · doi:10.1038/s41598-022-14795-6 · Cited by 20 · see citing works
Identifying miRNAs in multiple sclerosis gray matter lesions that correlate with atrophy measures
Tripathi, A. K., Pandit, I., Perles, A., Zhou, Y., Cheng, F., & Dutta, R. (2021) · Annals of Clinical and Translational Neurology · doi:10.1002/acn3.51365 · Cited by 18 · see citing works
Transdiagnostic treatment of emotional disorders for women with multiple sclerosis: a randomized controlled trial
Nazari, N., Aligholipour, A., & Sadeghi, M. (2020) · BMC Women s Health · doi:10.1186/s12905-020-01109-z · Cited by 17 · see citing works
Cognitive Decline in Older People with Multiple Sclerosis—A Narrative Review of the Literature
Chiang, H., Khera, A., Stopschinski, B. E., Stüve, O., Hart, J., Kelley, B. J., & Nguyen, T. P. (2022) · Geriatrics · doi:10.3390/geriatrics7030061 · Cited by 16 · see citing works
Modulators of ASIC1a and its potential as a therapeutic target for age-related diseases
Zhou, R., Liang, H., Hu, W., Ding, J., Li, S., Chen, Y., Zhao, Y., Lü, C., Chen, F., & Hu, W. (2022) · Ageing Research Reviews · doi:10.1016/j.arr.2022.101785 · Cited by 16 · see citing works
Astroglial connexin 43 is a novel therapeutic target for chronic multiple sclerosis model
Takase, E. O., Yamasaki, R., Nagata, S., Watanabe, M., Masaki, K., Yamaguchi, H., Kira, J., Takeuchi, H., & Isobe, N. (2024) · Scientific Reports · doi:10.1038/s41598-024-61508-2 · Cited by 16 · see citing works
Translocator Protein Ligand PIGA1138 Reduces Disease Symptoms and Severity in Experimental Autoimmune Encephalomyelitis Model of Primary Progressive Multiple Sclerosis
Tremolanti, C., Cavallini, C., Meyer, L., Klein, C., Pozzo, E. D., Costa, B., Germelli, L., Taliani, S., Patte‐Mensah, C., & Mensah‐Nyagan, A. G. (2022) · Molecular Neurobiology · doi:10.1007/s12035-022-02737-2 · Cited by 16 · see citing works
Discovery of new macrophage M2 polarization modulators as multiple sclerosis treatment agents that enable the inflammation microenvironment remodeling
Che, J., Li, D., Hong, W., Wang, L., Guo, Y. L., Wu, M., Lu, J., Tong, L., Weng, Q., Wang, J., et al. (2022) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2022.114732 · Cited by 15 · see citing works
Protective Effects of Leukadherin1 in a Rat Model of Targeted Experimental Autoimmune Encephalomyelitis (EAE): Possible Role of P47phox and MDA Downregulation
Hemmati, S., Sadeghi, M. A., Yousefi‐Manesh, H., Eslamiyeh, M., Vafaei, A., Foroutani, L., Donyadideh, G., Dehpour, A. R., & Rezaei, N. (2020) · Journal of Inflammation Research · doi:10.2147/jir.s258991 · Cited by 15 · see citing works
The expression analyses of RMRP, DDX5, and RORC in RRMS patients treated with different drugs versus naïve patients and healthy controls
Rahmani, S., Noorolyai, S., Ayromlou, H., Khaze, V., Shanehbandi, D., Baghbani, E., Shadbad, M. A., Jigari‐Asl, F., Khamiriyan, M., Safaralizadeh, R., et al. (2020) · Gene · doi:10.1016/j.gene.2020.145236 · Cited by 15 · see citing works
Risk of secondary progressive multiple sclerosis after early worsening of disability
Dzau, W., Sharmin, S., Patti, F., Izquierdo, G., Eichau, S., Prat, A., Girard, M., Duquette, P., ONOFRJ, M. C., Lugaresi, A., et al. (2023) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp-2023-331748 · Cited by 14 · see citing works
The emerging role of the microglia triggering receptor expressed on myeloid cells (TREM) 2 in multiple sclerosis
Farzan, M., Rounkian, M. S., Rizi, A. A., Heidari, Z., Farzan, M., Fathi, M., Aghaei, A., Azadegan‐Dehkordi, F., & Bagheri, N. (2024) · Experimental Neurology · doi:10.1016/j.expneurol.2024.115071 · Cited by 14 · see citing works
Remyelination therapies for multiple sclerosis: optimizing translation from animal models into clinical trials
Sutiwisesak, R., Burns, T. C., Rodriguez, M., & Warrington, A. E. (2021) · Expert Opinion on Investigational Drugs · doi:10.1080/13543784.2021.1942840 · Cited by 14 · see citing works
Treatment with MDL 72527 Ameliorated Clinical Symptoms, Retinal Ganglion Cell Loss, Optic Nerve Inflammation, and Improved Visual Acuity in an Experimental Model of Multiple Sclerosis
Liu, F., Alfarhan, M., Baker, L., Shenoy, N., Liao, Y., Henry-Ojo, H. O., Somanath, P. R., & Narayanan, S. P. (2022) · Cells · doi:10.3390/cells11244100 · Cited by 14 · see citing works
Reactive nitrogen species as therapeutic targets for autophagy/mitophagy modulation to relieve neurodegeneration in multiple sclerosis: Potential application for drug discovery.
Li, W., Wu, M., Li, Y., & Shen, J.-G. (2023) · Free Radical Biology & Medicine · doi:10.1016/j.freeradbiomed.2023.07.032 · Cited by 13 · see citing works
Multiple Sclerosis and Related Challenges to Young women’s Health: Canadian Expert Review
Vorobeychik, G., Black, D., Cooper, P. E., & Cox, A. R. (2020) · Neurodegenerative Disease Management · doi:10.2217/nmt-2020-0010 · Cited by 14 · see citing works
An Interpretable Machine Learning Model to Predict Cortical Atrophy in Multiple Sclerosis
Conti, A., Treaba, C. A., Mehndiratta, A., Barletta, V. T., Mainero, C., & Toschi, N. (2023) · Brain Sciences · doi:10.3390/brainsci13020198 · Cited by 12 · see citing works
Extracellular vesicles from adipose mesenchymal stem cells target inflamed lymph nodes in experimental autoimmune encephalomyelitis
Turano, E., Scambi, I., Bonafede, R., Dusi, S., Angelini, G., Lopez, N., Marostica, G., Rossi, B., Furlan, R., Constantin, G., et al. (2024) · Cytotherapy · doi:10.1016/j.jcyt.2023.12.007 · Cited by 11 · see citing works
Metformin Protects Myelin from Degeneration in A Mouse Model of Iysophosphatidylcholine-Induced Demyelination in The Optic Chiasm.
Esmaeilnejad, S., Semnanian, S., & Javan, M. (2021) · PubMed Central · doi:10.22074/cellj.2021.7174 · Cited by 12 · see citing works
Neuronal and Endothelial Transglutaminase-2 Expression during Experimental Autoimmune Encephalomyelitis and Multiple Sclerosis
Pearse, D. D., Otero, P. A., Diaz, A., Pan, X., & Ghosh, M. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2020.11.034 · Cited by 10 · see citing works
Polysialic acid promotes remyelination in cerebellar slice cultures by Siglec-E-dependent modulation of microglia polarization
Schröder, L.-J., Thiesler, H., Gretenkort, L., Möllenkamp, T. M., Stangel, M., Gudi, V., & Hildebrandt, H. (2023) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2023.1207540 · Cited by 10 · see citing works
Quantitative Susceptibility Mapping Values Quantification in Deep Gray Matter Structures for Relapsing‐Remitting Multiple Sclerosis: A Systematic Review and Meta‐Analysis
Mohammadi, S., Ghaderi, S., & Fatehi, F. (2024) · Brain and Behavior · doi:10.1002/brb3.70093 · Cited by 9 · see citing works
Assessment of axonal injury in multiple sclerosis: combined analysis of serum light-chain neurofilaments and diffusion tensor imaging
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Authors: Correale, J., Marrodan, M., & Ysrraelit, M. C.
Affiliations: Fundación para la Lucha contra las Enfermedades Neurológicas de la Infancia (AR)
Department of Neurology, FLENI, Buenos Aires 1428, Argentina
Corresponding author: Correale, Jorge
ORCID: Correale, Jorge
Ysrraelit, María Célica
Venue: Biomedicines
Publisher: MDPI AG
Published: 2019-02-20
Volume: 7
Issue: 1
Pages: 14
ISSN: 2227-9059 (ISSN-L)
DOI: 10.3390/biomedicines7010014
PMC: PMC6466454
OpenAlex: W2917933180
Cited by: 167
References: 174
Citations by year: 2026: 15 · 2025: 25 · 2024: 39 · 2023: 27 · 2022: 20 · 2021: 15 · 2020: 19 · 2019: 7
FWCI: 2.27
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (vor)
Locations: Biomedicines (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders: Fleni
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: multiple sclerosis, progressive multiple sclerosis, neurodegeneration, axonal dysfunction, axonal degeneration, B cell dysregulation, CD8+ T cells, demyelination, microglial activation, reactive oxygen species, mitochondrial damage, calcium accumulation, neuronal loss, disability progression, therapeutic target

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Mechanisms of Neurodegeneration and Axonal Dysfunction in Progressive Multiple Sclerosis

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