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Cited by 118Multiple Sclerosis Research StudiesPeripheral Neuropathies and DisordersNeuroinflammation and Neurodegeneration Mechanisms

Relationship of acute axonal damage, Wallerian degeneration, and clinical disability in multiple sclerosis

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Singh, Shailender, Dallenga, Tobias, Winkler, Anne, Roemer, Shanu, Maruschak, Brigitte, Siebert, Heike, Brück, Wolfgang, Stadelmann, Christine·2017·Journal of Neuroinflammation
DOI 10.1186/s12974-017-0831-8PMC PMC5356322
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Abstract

Axonal damage and loss substantially contribute to the incremental accumulation of clinical disability in progressive multiple sclerosis. Here, we assessed the amount of Wallerian degeneration in brain tissue of multiple sclerosis patients in relation to demyelinating lesion activity and asked whether a transient blockade of Wallerian degeneration decreases axonal loss and clinical disability in a mouse model of inflammatory demyelination. Wallerian degeneration and acute axonal damage were determined immunohistochemically in the periplaque white matter of multiple sclerosis patients with early actively demyelinating lesions, chronic active lesions, and inactive lesions. Furthermore, we studied the effects of Wallerian degeneration blockage on clinical severity, inflammatory pathology, acute axonal damage, and long-term axonal loss in experimental autoimmune encephalomyelitis using Wallerian degeneration slow (Wld S ) mutant mice. The highest numbers of axons undergoing Wallerian degeneration were found in the perilesional white matter of multiple sclerosis patients early in the disease course and with actively demyelinating lesions. Furthermore, Wallerian degeneration was more abundant in patients harboring chronic active as compared to chronic inactive lesions. No co-localization of neuropeptide Y-Y1 receptor, a bona fide immunohistochemical marker of Wallerian degeneration, with amyloid precursor protein, frequently used as an indicator of acute axonal transport disturbance, was observed in human and mouse tissue, indicating distinct axon-degenerative processes. Experimentally, a delay of Wallerian degeneration, as observed in Wld S mice, did not result in a reduction of clinical disability or acute axonal damage in experimental autoimmune encephalomyelitis, further supporting that acute axonal damage as reflected by axonal transport disturbances does not share common molecular mechanisms with Wallerian degeneration. Furthermore, delaying Wallerian degeneration did not result in a net rescue of axons in late lesion stages of experimental autoimmune encephalomyelitis. Our data indicate that in multiple sclerosis, ongoing demyelination in focal lesions is associated with axonal degeneration in the perilesional white matter, supporting a role for focal pathology in diffuse white matter damage. Also, our results suggest that interfering with Wallerian degeneration in inflammatory demyelination does not suffice to prevent acute axonal damage and finally axonal loss.

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  • Reductions in AxD are observed in human WM during acute injury settings, such as optic neuritis.

    “Reductions in AxD is observed in human WM during acute injury settings, as in optic neuritis (inflammation/neurodegeneration of the ON) 56”

    From Amyloid-beta induced retrograde axonal degeneration in a mouse tauopathy model (2019) · cites this paper as [56]

    The Results sections describe histological measures of axonal damage in multiple sclerosis tissue and mouse EAE lesions, not reductions in AxD in human white matter during optic neuritis. Searches for axial diffusivity, AxD, and optic neuritis found no passage addressing the cited claim. (LLM, conf=0.76)

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  • The reduction in AxD during acute axonal degeneration is transient and eventually increases relative to control subjects.

    “This reduction is transient, though and eventually increases relative to control subjects 56, 58.”

    From Amyloid-beta induced retrograde axonal degeneration in a mouse tauopathy model (2019) · cites this paper as [56]

    The Results sections on acute axonal damage and chronic axonal loss compare histological markers in WldS and wild-type mice, not AxD in subjects versus controls. Searches for AxD and axial diffusivity found no passage describing a transient reduction followed by an increase relative to controls; page numbers were not available in our copy. (LLM, conf=0.74)

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Authors
Singh, S., Dallenga, T., Winkler, A., Roemer, S., Maruschak, B., Siebert, H., Brück, W., & Stadelmann, C.
Affiliations
  • Universitätsmedizin Göttingen (DE)
  • Rigshospitalet (DK)
Corresponding author
Stadelmann, Christine
ORCID
Venue
Journal of Neuroinflammation
Publisher
Springer Science and Business Media LLC
Published
2017-03-17
Volume
14
Issue
1
Pages
57-57
ISSN
1742-2094 (ISSN-L)
DOI
10.1186/s12974-017-0831-8
PMC
PMC5356322
OpenAlex
W2596538588
Cited by
118
References
3
Citations by year
2026: 6 · 2025: 8 · 2024: 13 · 2023: 15 · 2022: 18 · 2021: 21 · 2020: 15 · 2019: 14 · 2018: 3 · 2017: 5
FWCI
7.95
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Journal of Neuroinflammation (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • GoeScholar The Publication Server of the Georg-August-Universität Göttingen (Georg-August-Universität Göttingen) (submittedVersion, cc-by)
  • GRO (submittedVersion, cc-by)
Funders
  • Deutsche Forschungsgemeinschaft (DFG) transregional collaborative research group (TRR-SFB) 43
  • ENC Network - European Commission
Topics
  • Health Sciences › Medicine › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
  • Health Sciences › Medicine › Neurology › Peripheral Neuropathies and Disorders
  • Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Keywords
multiple sclerosis, Wallerian degeneration, axonal injury, axonal loss, clinical disability, demyelinating lesions, chronic active lesions, experimental autoimmune encephalomyelitis, axonal transport, Y1 receptor, amyloid precursor protein, inflammatory demyelination, axonal degeneration
MeSH terms
Adult, Aged, Animals, Axons, Brain, Disease Models, Animal, Encephalomyelitis, Autoimmune, Experimental, Female, Disabled Persons, Persons with Disabilities, Humans, Male, Mice, Inbred C57BL, Mice, Mutant Strains, Middle Aged, Multiple Sclerosis, Myelin Proteins, Nerve Tissue Proteins, Sciatica, Wallerian Degeneration, Amyloid beta-Protein Precursor, Stroke, Mice

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