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Localized molecular chaperone synthesis maintains neuronal dendrite proteostasis.

Nature communications · 2024 · Vol. 15 (1) · pp. 10796

Abstract

Proteostasis is maintained through regulated protein synthesis and degradation and chaperone-assisted protein folding. However, this is challenging in neuronal projections because of their polarized morphology and constant synaptic proteome remodeling. Using high-resolution fluorescence microscopy, we discover that hippocampal and spinal cord motor neurons of mouse and human origin localize a subset of chaperone mRNAs to their dendrites and use microtubule-based transport to increase this asymmetric localization following proteotoxic stress. The most abundant dendritic chaperone mRNA encodes a constitutive heat shock protein 70 family member (HSPA8). Proteotoxic stress also enhances HSPA8 mRNA translation efficiency in dendrites. Stress-mediated HSPA8 mRNA localization to the dendrites is impaired by depleting fused in sarcoma-an amyotrophic lateral sclerosis-related protein-in cultured spinal cord mouse motor neurons or by expressing a pathogenic variant of heterogenous nuclear ribonucleoprotein A2/B1 in neurons derived from human induced pluripotent stem cells. These results reveal a neuronal stress response in which RNA-binding proteins increase the dendritic localization of HSPA8 mRNA to maintain proteostasis and prevent neurodegeneration.

Publication Types

["Journal Article", "Research Support, U.S. Gov't, P.H.S.", "Research Support, Non-U.S. Gov't", "Research Support, N.I.H., Extramural"]

Keywords

[]

MeSH Terms

["Dendrites", "Proteostasis", "Animals", "Humans", "Mice", "RNA-Binding Protein FUS", "RNA, Messenger", "Motor Neurons", "HSC70 Heat-Shock Proteins", "Hippocampus", "Spinal Cord", "Induced Pluripotent Stem Cells", "Protein Biosynthesis", "Molecular Chaperones", "HSP70 Heat-Shock Proteins", "Microtubules"]

Funding

U24 HG009889 NHGRI NIH HHS (United States)
R01 HG004659 NHGRI NIH HHS (United States)
RF1 MH126719 NIMH NIH HHS (United States)
R01 HG011864 NHGRI NIH HHS (United States)
R01 NS103172 NINDS NIH HHS (United States)
U41 HG009889 NHGRI NIH HHS (United States)
300232 Fonds de Recherche du Québec - Santé (Fonds de la recherche en sante du Quebec)
MH126719 U.S. Department of Health & Human Services | National Institutes of Health (NIH)
HG009889 U.S. Department of Health & Human Services | National Institutes of Health (NIH)
HG011864 U.S. Department of Health & Human Services | National Institutes of Health (NIH)
PJT-186141 Gouvernement du Canada | Canadian Institutes of Health Research (Instituts de Recherche en Santé du Canada)
HG004659 U.S. Department of Health & Human Services | National Institutes of Health (NIH)
Hudson Translational Team Grant ALS Society of Canada (ALS Canada)
2022-ALS Discovery Grant ALS Society of Canada (ALS Canada)
P30 CA008748 NCI NIH HHS (United States)

Linked Datasets (1)

GSE202202 GSE via ncbi_elink
GEO

RNA-seq in neurites and soma of primary hippocampal neurons isolated from P0 or P1 mice

Mus musculus
24 data files
FileTypeSize
211012DIV18DendCtrl_S3_R1_001.fastq.gz RNA-Seq 320.2 MB
211012DIV18DendCtrl_S3_R1_001.fastq.gz RNA-Seq 320.2 MB
211012DIV18DendMG132_S4_R1_001.fastq.gz RNA-Seq 351.4 MB
211012DIV18DendMG132_S4_R1_001.fastq.gz RNA-Seq 351.4 MB
211012DIV18SomaCtrl_S1_R1_001.fastq.gz RNA-Seq 476.2 MB
211012DIV18SomaCtrl_S1_R1_001.fastq.gz RNA-Seq 476.2 MB
211012DIV18SomaMG132_S2_R1_001.fastq.gz RNA-Seq 385.4 MB
211012DIV18SomaMG132_S2_R1_001.fastq.gz RNA-Seq 385.4 MB
211115DIV17DendCtrl_S7_R1_001.fastq.gz RNA-Seq 496.1 MB
211115DIV17DendCtrl_S7_R1_001.fastq.gz RNA-Seq 496.1 MB
211115DIV17DendMG132_S8_R1_001.fastq.gz RNA-Seq 1.1 GB
211115DIV17DendMG132_S8_R1_001.fastq.gz RNA-Seq 1.1 GB
211115DIV17SomaCtrl_S5_R1_001.fastq.gz RNA-Seq 338.5 MB
211115DIV17SomaCtrl_S5_R1_001.fastq.gz RNA-Seq 338.5 MB
211115DIV17SomaMG132_S6_R1_001.fastq.gz RNA-Seq 229.8 MB
211115DIV17SomaMG132_S6_R1_001.fastq.gz RNA-Seq 229.8 MB
211122DIV17DendCtrl_S11_R1_001.fastq.gz RNA-Seq 368.7 MB
211122DIV17DendCtrl_S11_R1_001.fastq.gz RNA-Seq 368.7 MB
211122DIV17DendMG132_S12_R1_001.fastq.gz RNA-Seq 569.3 MB
211122DIV17DendMG132_S12_R1_001.fastq.gz RNA-Seq 569.3 MB
211122DIV17SomaCtrl_S9_R1_001.fastq.gz RNA-Seq 405.6 MB
211122DIV17SomaCtrl_S9_R1_001.fastq.gz RNA-Seq 405.6 MB
211122DIV17SomaMG132_S10_R1_001.fastq.gz RNA-Seq 926.3 MB
211122DIV17SomaMG132_S10_R1_001.fastq.gz RNA-Seq 926.3 MB

Potentially Related Datasets (2)

These accessions were text-mined from the PMC full text. They may be referenced for comparison, cited from other studies, or otherwise mentioned without being primary data for this paper.

RNA-seq in neurites and soma of primary hippocampal neurons isolated from P0 or P1 mice

PXD046036 PXD PRIDE

Analysis Pipelines (1)

RNA-seq geo_data_processing GSE202202