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Coupling of terminal differentiation deficit with neurodegenerative pathology in Vps35-deficient pyramidal neurons

Tang, Fu-Lei, Zhao, Lu, Zhao, Yang, Sun, Dong, Zhu, Xiao-Juan, Mei, Lin, Xiong, Wen-Cheng·2020·Cell Death & Differentiation
DOI 10.1038/s41418-019-0487-2PMC PMC7308361
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Abstract

Vps35 (vacuolar protein sorting 35) is a key component of retromer that regulates transmembrane protein trafficking. Dysfunctional Vps35 is a risk factor for neurodegenerative diseases, including Parkinson’s and Alzheimer’s diseases. Vps35 is highly expressed in developing pyramidal neurons, and its physiological role in developing neurons remains to be explored. Here, we provide evidence that Vps35 in embryonic neurons is necessary for axonal and dendritic terminal differentiation. Loss of Vps35 in embryonic neurons results in not only terminal differentiation deficits, but also neurodegenerative pathology, such as cortical brain atrophy and reactive glial responses. The atrophy of neocortex appears to be in association with increases in neuronal death, autophagosome proteins (LC3-II and P62), and neurodegeneration associated proteins (TDP43 and ubiquitin-conjugated proteins). Further studies reveal an increase of retromer cargo protein, sortilin1 (Sort1), in lysosomes of Vps35-KO neurons, and lysosomal dysfunction. Suppression of Sort1 diminishes Vps35-KO-induced dendritic defects. Expression of lysosomal Sort1 recapitulates Vps35-KO-induced phenotypes. Together, these results demonstrate embryonic neuronal Vps35’s function in terminal axonal and dendritic differentiation, reveal an association of terminal differentiation deficit with neurodegenerative pathology, and uncover an important lysosomal contribution to both events.

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  • Retromer depletion in neurons has been shown to increase gliosis and lead to dysmorphic microglial morphology in mice, phenotypic of the microglial morphology observed in AD patients.

    “Retromer depletion in neurons has been shown to increase gliosis [82,131], and lead to dysmorphic microglial morphology in mice, phenotypic of the microglial morphology observed in AD patients [82].”

    From Global identification of neuronal and astrocytic integral membrane proteins that require Retromer for their endosomal recycling (2026) · cites this paper as [131]

    The Results section (‘Concurrence of neurodegenerative and reactive glial responses’) reports increased reactive astrogliosis and altered microglial morphology in mice with neuronal Vps35 deficiency. It describes larger microglial cell bodies and shorter processes, but does not compare that morphology with microglia in AD patients. No page number is available in our copy. (LLM, conf=0.87)

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  • Increased SLC7A11 lysosomal levels upon SNX3-Retromer deficiency may contribute to the lysosomal acidification defects observed upon loss of VPS35 expression.

    “Increased SLC7A11 lysosomal levels upon SNX3-Retromer deficiency may therefore contribute to the lysosomal acidification defects observed upon loss of VPS35 expression [131, 132].”

    From Global identification of neuronal and astrocytic integral membrane proteins that require Retromer for their endosomal recycling (2026) · cites this paper as [131]

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Metadata

Authors
Tang, F.-L., Zhao, L., Zhao, Y., Sun, D., Zhu, X.-J., Mei, L., & Xiong, W.-C.
ORCID
Xiong, Wen-Cheng
Venue
Cell Death & Differentiation
Publisher
Springer Science and Business Media LLC
Published
2020-01-06
Volume
27
Issue
7
Pages
2099-2116
ISSN
  • 1350-9047
  • 1476-5403
DOI
10.1038/s41418-019-0487-2
PMC
PMC7308361
Cited by
47
References
10
Language
en
Licence
Funders
Foundation for the National Institutes of Health (AG045781)

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