Cited by 288Amyotrophic Lateral Sclerosis ResearchNeuroinflammation and Neurodegeneration MechanismsAlzheimer's disease research and treatments

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Extracellular mutant SOD1 induces microglial‐mediated motoneuron injury

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Zhao, Weihua, Beers, David R., Henkel, Jenny S., Zhang, Wei, Urushitani, Makoto, Julien, Jean‐Pierre, Appel, Stanley H.·2010·Glia

DOI 10.1002/glia.20919PMC PMC2784168

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Abstract

Through undefined mechanisms, dominant mutations in (Cu/Zn) superoxide dismutase‐1 (mSOD1) cause the non‐cell‐autonomous death of motoneurons in inherited amyotrophic lateral sclerosis (ALS). Microgliosis at sites of motoneuron injury is a neuropathological hallmark of ALS. Extracellular mutant SOD1 (mSOD1) causes motoneuron injury and triggers microgliosis in spinal cord cultures, but it is unclear whether the injury results from extracellular mSOD1 directly interacting with motoneurons or is mediated through mSOD1‐activated microglia. To dissociate these potential mSOD1‐mediated neurotoxic mechanisms, the effects of extracellular human mSOD1 G93A or mSOD1 G85R were assayed using primary cultures of motoneurons and microglia. The data demonstrate that exogenous mSOD1 G93A did not cause detectable direct killing of motoneurons. In contrast, mSOD1 G93A or mSOD1 G85R did induce the morphological and functional activation of microglia, increasing their release of pro‐inflammatory cytokines and free radicals. Furthermore, only when microglia was co‐cultured with motoneurons did extracellular mSOD1 G93A injure motoneurons. The microglial activation mediated by mSOD1 G93A was attenuated using toll‐like receptors (TLR) 2, TLR4 and CD14 blocking antibodies, or when microglia lacked CD14 expression. These data suggest that extracellular mSOD1 G93A is not directly toxic to motoneurons but requires microglial activation for toxicity, utilizing CD14 and TLR pathways. This link between mSOD1 and innate immunity may offer novel therapeutic targets in ALS. © 2009 Wiley‐Liss, Inc.

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Motor Neuron Degeneration in Mice that Express a Human Cu,Zn Superoxide Dismutase Mutation
Gurney, M. E., Pu, H., Chiu, A. Y., Dal Canto, M. C., Polchow, C. Y., Alexander, D. D., Caliendo, J., Hentati, A., Kwon, Y. W., Deng, H.-X., et al. (1994) · Science · doi:10.1126/science.8209258 · Cited by 4,143
Onset and Progression in Inherited ALS Determined by Motor Neurons and Microglia
Boillée, S., Yamanaka, K., Lobsiger, C. S., Copeland, N. G., Jenkins, N. A., Kassiotis, G., Kollias, G., & Cleveland, D. W. (2006) · Science · doi:10.1126/science.1123511 · Cited by 1,623
An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria
Wong, P. C., Pardo, C. A., Borchelt, D., Lee, M. K., Copeland, N. G., Jenkins, N. A., Sisodia, S. S., Cleveland, D. W., & Price, D. L. (1995) · Neuron · doi:10.1016/0896-6273(95)90259-7 · Cited by 1,439
From charcot to lou gehrig: deciphering selective motor neuron death in als
Cleveland, D. W., & Rothstein, J. D. (2001) · Nature reviews. Neuroscience · doi:10.1038/35097565 · Cited by 1,389
Motor neurons in Cu/Zn superoxide dismutase-deficient mice develop normally but exhibit enhanced cell death after axonal injury
Reaume, A. G., Elliott, J. L., Hoffman, E. K., Kowall, N. W., Ferrante, R. J., Siwek, D. F., Wilcox, H. M., Flood, D. G., Beal, M. F., Brown, R. H., et al. (1996) · Nature Genetics · doi:10.1038/ng0596-43 · Cited by 1,285
Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons
Nagai, M., Re, D. B., Nagata, T., Chalazonitis, A., Jessell, T. M., Wichterle, H., & Przedborski, S. (2007) · Nature Neuroscience · doi:10.1038/nn1876 · Cited by 1,220
Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs
Olson, J. K., & Miller, S. D. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.173.6.3916 · Cited by 1,215
Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis
Yamanaka, K., Chun, S. J., Boillee, S., Fujimori-Tonou, N., Yamashita, H., Gutmann, D. H., Takahashi, R., Misawa, H., & Cleveland, D. W. (2008) · Nature Neuroscience · doi:10.1038/nn2047 · Cited by 1,140 · cited 2×
“Several studies support the importance of both microglia and astroglia in mediating motoneuron injury (Beers et al., 2006; Boillee et al., 2006; Nagai et al., 2007; Yamanaka et al., 2008b; Zhao et al., 2004).”
BackgroundResult
Pivotal role for neuronal Toll-like receptors in ischemic brain injury and functional deficits
Tang, S.-C., Arumugam, T. V., Xu, X., Cheng, A., Mughal, M. R., Jo, D. G., Lathia, J. D., Siler, D. A., Chigurupati, S., Ouyang, X., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0702553104 · Cited by 779
TLR signaling tailors innate immune responses in human microglia and astrocytes
Jack, C. S., Arbour, N., Manusow, J., Montgrain, V., Blain, M., McCrea, E., Shapiro, A., & Antel, J. P. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.175.7.4320 · Cited by 734 · cited 1×
“Other lines of evidence indeed suggest that CD14/TLRs may contribute to the inflammatory responses initiated by microglia (Jack et al., 2005; Olson and Miller, 2004).”
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Authors: Zhao, W., Beers, D. R., Henkel, J. S., Zhang, W., Urushitani, M., Julien, J., & Appel, S. H.
Affiliations: Houston Methodist (US)
Shiga University of Medical Science (JP)
Université Laval (CA)
Corresponding author: Appel, Stanley H.
ORCID: Zhao, Weihua
Beers, David R.
Zhang, Wei
Urushitani, Makoto
Julien, Jean‐Pierre
Appel, Stanley H.
Venue: Glia
Publisher: Wiley
Published: 2009-08-11
Volume: 58
Issue: 2
Pages: 231-243
ISSN: 0894-1491 (ISSN-L)
1098-1136
DOI: 10.1002/glia.20919
PMC: PMC2784168
OpenAlex: W2066874059
Cited by: 288
References: 51
Citations by year: 2026: 8 · 2025: 16 · 2024: 15 · 2023: 12 · 2022: 13 · 2021: 19 · 2020: 21 · 2019: 13 · 2018: 15 · 2017: 19 · 2016: 18 · 2015: 16 · 2014: 16 · 2013: 23 · 2012: 24
FWCI: 13.61
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Glia (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Neurological Disorders and Stroke (NS048950, R01NS048950)
Topics: Health Sciences › Medicine › Clinical Neurology › Amyotrophic Lateral Sclerosis Research
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Alzheimer's disease research and treatments
Keywords: amyotrophic lateral sclerosis, SOD1 mutations, microglial activation, non-cell autonomous neurodegeneration, CD14, Toll-like receptors, TLR2, TLR4, inflammatory cytokines, free radicals, innate immunity, SOD1 G93A
MeSH terms: Superoxide Dismutase-1, Animals, Cells, Cultured, Extracellular Space, Humans, Mice, Inbred C57BL, Mice, Transgenic, Motor Neurons, Recombinant Proteins, Spinal Cord, Superoxide Dismutase, Signal Transduction, Cell Death, Microglia, Mice, Knockout, Coculture Techniques, Lipopolysaccharide Receptors, Mutation, Missense, Toll-Like Receptor 2, Toll-Like Receptor 4, Mice

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