TNFα promotes proliferation of oligodendrocyte progenitors and remyelination

Arnett, Heather A.; Mason, Jeff; Marino, Mike; Suzuki, Kinuko; Matsushima, Glenn K.; Ting, Jenny P.-Y.

doi:10.1038/nn738

Cited by 1,012Neurogenesis and neuroplasticity mechanismsMultiple Sclerosis Research StudiesNeuroinflammation and Neurodegeneration Mechanisms

TNFα promotes proliferation of oligodendrocyte progenitors and remyelination

Arnett, Heather A., Mason, Jeff, Marino, Mike, Suzuki, Kinuko, Matsushima, Glenn K., Ting, Jenny P.-Y.·2001·Nature Neuroscience

DOI 10.1038/nn738

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Abstract

Here we used mice lacking tumor necrosis factor-alpha (TNF alpha) and its associated receptors to study a model of demyelination and remyelination in which these events could be carefully controlled using a toxin, cuprizone. Unexpectedly, the lack of TNF alpha led to a significant delay in remyelination as assessed by histology, immunohistochemistry for myelin proteins and electron microscopy coupled with morphometric analysis. Failure of repair correlated with a reduction in the pool of proliferating oligodendrocyte progenitors (bromodeoxyuridine-labeled NG2(+) cells) followed by a reduction in the number of mature oligodendrocytes. Analysis of mice lacking TNF receptor 1 (TNFR1) or TNFR2 indicated that TNFR2, not TNFR1, is critical to oligodendrocyte regeneration. This unexpected reparative role for TNF alpha in the CNS is important for understanding oligodendrocyte regeneration/proliferation, nerve remyelination and the design of new therapeutics for demyelinating diseases.

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The debris-clearing function of myeloid cells and mediators released from innate immune cells stimulate remyelination.
“This aligns with the notion that the debris-clearing function of myeloid cells and mediators released from innate immune cells stimulate remyelination.61-63”
From BCAS1-positive oligodendrocytes enable efficient cortical remyelination in multiple sclerosis (2025) · cites this paper as [61]
SJL mice demyelinate partially at midline, whereas C57BL/6 mice show robust demyelination, particularly at week 5.
“We found SJL mice demyelinate partially at midline (Figure 2A), whereas C57BL/6 mice show robust demyelination, particularly at week 5 2, 23, 35.”
From SJL Mice Exposed to Cuprizone Intoxication Reveal Strain and Gender Pattern Differences in Demyelination (2009) · cites this paper as [2]
C57BL/6 mice showed greater than 50% remyelination within 2 weeks of discontinuation of cuprizone.
“C57BL/6 mice showed greater than 50% remyelination within 2 weeks of discontinuation of cuprizone 2, 42, which is in stark contrast to the reduced remyelination reported here for SJL.”
From SJL Mice Exposed to Cuprizone Intoxication Reveal Strain and Gender Pattern Differences in Demyelination (2009) · cites this paper as [2]
The increased severity in EAE may be because of T-cell immune mechanisms that are not induced by cuprizone intoxication.
“The increased severity in EAE may be because of T‐cell immune mechanisms that are not induced by cuprizone intoxication 2, 24.”
From SJL Mice Exposed to Cuprizone Intoxication Reveal Strain and Gender Pattern Differences in Demyelination (2009) · cites this paper as [2]
Unlike microglia and astrocytes in C57BL/6 mice that respond vigorously to demyelination, these cell types in SJL mice have a guarded response at midline and in the lateral region, which correlates with subdued demyelination.
“Thus, unlike microglia and astrocytes in C57BL/6 mice that respond vigorously to demyelination 2, 23, 39, these cell types in SJL mice have a guarded response at midline and in the lateral region, which correlates with subdued demyelination.”
From SJL Mice Exposed to Cuprizone Intoxication Reveal Strain and Gender Pattern Differences in Demyelination (2009) · cites this paper as [2]

TNF expression levels are increased after one week of cuprizone-induced demyelination in vivo, and TNFα−/− mice showed a delay in demyelination, consistent with a role for TNF to exacerbate cuprizone-induced demyelination.
“TNF expression levels are increased after one week of cuprizone-induced demyelination in vivo [224] and TNFα−/− mice showed a delay in demyelination in the cuprizone model [56], consistent with a role for TNF to exacerbate cuprizone-induced demyelination.”
From Oligodendrocyte death and myelin loss in the cuprizone model: an updated overview of the intrinsic and extrinsic causes of cuprizone demyelination (2022) · cites this paper as [224]
TNF is also required for remyelination.
“However, TNF is also required for remyelination [224].”
From Oligodendrocyte death and myelin loss in the cuprizone model: an updated overview of the intrinsic and extrinsic causes of cuprizone demyelination (2022) · cites this paper as [224]
Cuprizone-induced de- and remyelination are not mediated by B or T cells.
“Overall, cuprizone-induced de- and remyelination are not mediated by B or T cells, as shown by the use of RAG −/− mice that lack lymphocytes (Arnett et al., 2001; Hiremath et al., 2008).”
From Glial response during cuprizone-induced de- and remyelination in the CNS: lessons learned (2014) · cites this paper as Arnett et al., 2001
In the cuprizone model, TNF-α acts in a bivalent manner, since TNF-α−/− mice displayed reduced loss of oligodendrocytes during the first 3.5 weeks of cuprizone feeding but also a significantly diminished ability to remyelinate.
“In the cuprizone model, TNF-α was demonstrated to act as well in a bivalent manner since TNF-α −/− mice displayed a reduced loss of oligodendrocytes during the first 3.5 weeks of cuprizone feeding but also a significantly diminished ability to remyelinate (Arnett et al., 2001).”
From Glial response during cuprizone-induced de- and remyelination in the CNS: lessons learned (2014) · cites this paper as Arnett et al., 2001
TNFR2−/− mice displayed diminished/delayed regeneration of myelin.
“Furthermore, similar to TNF-α-deficient mice TNFR2 −/− mice displayed diminished/delayed regeneration of myelin”
From Glial response during cuprizone-induced de- and remyelination in the CNS: lessons learned (2014) · cites this paper as Arnett et al., 2001
TNFR2 but not TNFR1 was gradually up-regulated during de- and remyelination.
“In this study TNFR2 but not TNFR1 has been shown to be gradually up-regulated during de- and remyelination (Arnett et al., 2001).”
From Glial response during cuprizone-induced de- and remyelination in the CNS: lessons learned (2014) · cites this paper as Arnett et al., 2001
An adequate and controlled inflammatory response is required for successful myelin regeneration, promoting clearance of myelin debris and stimulating proliferation/regeneration of myelin-forming oligodendrocytes.
“However, a growing body of evidence corroborates the assumption that an adequate and controlled inflammatory response is required for a successful myelin regeneration promoting the clearance of myelin debris and stimulating proliferation/regeneration of myelin-forming oligodendrocytes (Diemel et al., 1998; Robinson and Miller, 1999; Arnett et al., 2001; Kotter et al., 2001, 2005, 2006; Setzu et al”
From Glial response during cuprizone-induced de- and remyelination in the CNS: lessons learned (2014) · cites this paper as Arnett et al., 2001
Beneficial effects of TNF-α on proliferation of OPC and subsequent remyelination are promoted through the TNFR2 pathway.
“suggesting that beneficial effects of TNF-α on proliferation of OPC and subsequent remyelination are promoted through the TNFR2 pathway (Arnett et al., 2001).”
From Glial response during cuprizone-induced de- and remyelination in the CNS: lessons learned (2014) · cites this paper as Arnett et al., 2001
Functional studies using RAG-1-/- mice suggest that recruited CD3+ lymphocytes do not play a major role during cuprizone-induced demyelination and subsequent endogenous remyelination.
“Functional studies using recombinase activating gene-1 knockout (RAG-1 -/-) mice suggest that the recruited CD3 + lymphocytes do not play a major role during cuprizone-induced demyelination and the subsequent endogenous remyelination process (Arnett et al., 2001;Bieber et al., 2003;Hiremath et al., 2008).”
From Cuprizone‐induced demyelination triggers a <scp>CD8</scp>‐pronounced T cell recruitment (2021) · cites this paper as Arnett et al., 2001
IL-1beta and TNF-alpha can be harmful for cerebral elements but also play beneficial roles in the inflammatory response.
“Such cytokines can thus be harmful for the cerebral elements (138) but they also play beneficial roles in the inflammatory response (161–163).”
From The HPA â€“ Immune Axis and the Immunomodulatory Actions of Glucocorticoids in the Brain (2014) · cites this paper as [161]

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The effects of TNF-α on the development of oligodendrocyte and myelination and the intervention of Trental in vitro
Xin, Q. (2004)
The Research Progress of Tumor Necrosis Factor Alpha in Multiple Sclerosis and Remyelination
Xuda, L. (2014) · Tianjin yiyao

Authors: Arnett, H. A., Mason, J., Marino, M., Suzuki, K., Matsushima, G. K., & Ting, J. P.-Y.
Affiliations: University of North Carolina at Chapel Hill (US)
Memorial Sloan Kettering Cancer Center (US)
Corresponding author: Ting, Jenny P.-Y.
ORCID: Arnett, Heather A.
Ting, Jenny P.-Y.
Venue: Nature Neuroscience
Publisher: Springer Science and Business Media LLC
Published: 2001-10-15
Volume: 4
Issue: 11
Pages: 1116-1122
ISSN: 1097-6256 (ISSN-L)
1546-1726
DOI: 10.1038/nn738
OpenAlex: W1509596990
Cited by: 1,012
References: 48
Citations by year: 2026: 26 · 2025: 30 · 2024: 37 · 2023: 39 · 2022: 40 · 2021: 43 · 2020: 46 · 2019: 43 · 2018: 34 · 2017: 40 · 2016: 36 · 2015: 45 · 2014: 46 · 2013: 45 · 2012: 51
FWCI: 7.40
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature Neuroscience (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of Neurological Disorders and Stroke (NS34190, R01NS034190)
Topics: Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Health Sciences › Medicine › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Keywords: TNF-α, remyelination, demyelination, oligodendrocyte progenitors, oligodendrocyte proliferation, TNF receptor 1, TNF receptor 2, cuprizone, oligodendrocyte precursor cells, demyelinating disease, central nervous system regeneration
MeSH terms: Animals, B-Lymphocytes, Brain Chemistry, Corpus Callosum, Cuprizone, Demyelinating Diseases, Disease Models, Animal, Humans, Immunohistochemistry, Macrophages, Male, Monoamine Oxidase Inhibitors, Myelin Sheath, Oligodendroglia, Stem Cells, Tumor Necrosis Factor-alpha, Antigens, CD, Up-Regulation, Apoptosis, Microglia, Receptors, Tumor Necrosis Factor, Mice, Knockout, In Situ Nick-End Labeling, Receptors, Tumor Necrosis Factor, Type I, Receptors, Tumor Necrosis Factor, Type II, Mice

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TNFα promotes proliferation of oligodendrocyte progenitors and remyelination

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