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Induction of Autophagy in Axonal Dystrophy and Degeneration
Open accessAbstract
Autophagy is a highly regulated cellular mechanism for the bulk degradation of cytoplasmic contents. It has been implicated in a variety of physiological and pathological conditions relevant to neurological diseases. However, the regulation of autophagy in neurons and its role in neuronal and axonal pathology are not yet understood. Using transgenic mice producing green fluorescent protein-tagged autophagic marker microtubule-associated protein light chain 3 (GFP–LC3), we provide molecular evidence for the induction of autophagy in axonal dystrophy and degeneration in Purkinje cells of the Lurcher mice, a model for excitotoxic neurodegeneration. We show that the excitotoxic insult of Lurcher mutation triggers an early response of Purkinje cells involving accumulation of GFP–LC3-labeled autophagosomes in axonal dystrophic swellings (a hallmark of CNS axonopathy). In brain, LC3 interacts with high affinity with the microtubule-associated protein 1B (MAP1B). We show that MAP1B binds to LC3 of both cytosolic form (LC3I) and lipidated form (LC3II). Moreover, in cell culture, overexpression of MAP1B results in reduced LC3II levels and number of GFP–LC3-labeled autophagosomes; phosphorylated MAP1B is associated with GFP–LC3-labeled autophagosomes. Furthermore, in brain, phosphorylated MAP1B accumulates in axonal dystrophic swellings of degenerating Purkinje cells and binds to LC3 at increased level. Therefore, the MAP1B–LC3 interaction may participate in regulation of LC3-associated autophagosomes in neurons, in particular at axons, under normal and pathogenic conditions. We propose that induction of autophagy serves as an early stress response in axonal dystrophy and may participate in the remodeling of axon structures.
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“Purkinje cell degeneration models such as pcd mice display motor abnormalities that were similar to those observed in B6.Clec16aGT/GT and Clec16aCURT/CURT mice3031 and staining with the Purkinje cell marker calbindin confirmed loss of these cells in B6.Clec16aGT/GT mice (Fig. 2d) at 8 weeks of age that was dramatically increased by 47 weeks of age (Supplementary Fig. 2e).”
From Clec16a is Critical for Autolysosome Function and Purkinje Cell Survival (2016) · cites this paper as [31]
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“Although the accumulation of this protein complex can be related to the accumulation of ubiquitinated SQSTM1-bound proteins, or the dimerization/inactivation of SQSTM1 [561, 607], evaluation of the ratio between SQSTM1 aggregates/dimers and SQSTM1 monomers is likely a better measurement of changes in SQSTM1 dynamics linked to autophagy or the UPS.”
From Guidelines for the use and interpretation of assays for monitoring autophagy (4th edition) 1 (2021) · cites this paper as [561]
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“A number of stressors that impair the UPS induce the aggregation/dimerization of SQSTM1, and this can be seen by the detection of a high molecular mass (~150 kDa) protein complex by western blot, which is recognized by SQSTM1 antibodies [561, 605, 606]”
From Guidelines for the use and interpretation of assays for monitoring autophagy (4th edition) 1 (2021) · cites this paper as [561]
Experimental — accuracy not yet measuredIn the citing paper
“Autophagy is also necessary for maintaining the structural integrity of the axon [375]”
From Autophagy and ALS: mechanistic insights and therapeutic implications (2022) · cites this paper as [375]
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“but can also accentuate axon degeneration during excitotoxic stress [375].”
From Autophagy and ALS: mechanistic insights and therapeutic implications (2022) · cites this paper as [375]
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“Similarly, decreased SQSTM1 levels are associated with autophagy activation; however, similar to LC3-II, lysosomal inhibitors (such as CQ) can be used to assess increased autophagy flux based on an accumulation of SQSTM1 [87,561].”
From Guidelines for the use and interpretation of assays for monitoring autophagy (4th edition) 1 (2021) · cites this paper as [561]
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Metadata
- Authors
- Wang, Q. J., Ding, Y., Kohtz, S., Mizushima, N., Cristea, I. M., Rout, M. P., Chait, B. T., Zhong, Y., Heintz, N., & Yue, Z.
- Affiliations
- Tokyo Metropolitan Institute of Medical Science (JP)
- ORCID
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2006-08-02
- Volume
- 26
- Issue
- 31
- Pages
- 8057-8068
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6673783
- OpenAlex
- W2149332763
- Cited by
- 308
- References
- 46
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 6 · 2023: 14 · 2022: 7 · 2021: 11 · 2020: 10 · 2019: 14 · 2018: 7 · 2017: 15 · 2016: 19 · 2015: 20 · 2014: 24 · 2013: 20 · 2012: 26
- FWCI
- 15.44
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institutes of Health (RR00862, RR022220)
- U.S. Public Health Service (RNS055683A)
- National Cancer Institute (R33CA089810, CA 89810)
- National Institute of General Medical Sciences (R01GM062427, GM062427)
- National Center for Research Resources (RR00862, P41RR000862, RR 022220, U54RR022220)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Alzheimer's disease research and treatments
- Keywords
- autophagy, axonal dystrophy, axonal degeneration, axonopathy, Purkinje cells, excitotoxic neurodegeneration, MAP1B, LC3, autophagosomes, axonal swellings, neuronal stress response, axon remodeling
- MeSH terms
- Animals, Autophagy, Axons, Cells, Cultured, Mice, Neurologic Mutants, Mice, Transgenic, Nerve Degeneration, Phagosomes, Purkinje Cells, Retrograde Degeneration, Mice
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