Combinatorial selective ER-phagy remodels the ER during neurogenesis.
Journal
Nature cell biology
ISSN: 1476-4679
Titre abrégé: Nat Cell Biol
Pays: England
ID NLM: 100890575
Informations de publication
Date de publication:
Mar 2024
Mar 2024
Historique:
received:
24
04
2023
accepted:
11
01
2024
medline:
18
3
2024
pubmed:
2
3
2024
entrez:
1
3
2024
Statut:
ppublish
Résumé
The endoplasmic reticulum (ER) employs a diverse proteome landscape to orchestrate many cellular functions, ranging from protein and lipid synthesis to calcium ion flux and inter-organelle communication. A case in point concerns the process of neurogenesis, where a refined tubular ER network is assembled via ER shaping proteins into the newly formed neuronal projections to create highly polarized dendrites and axons. Previous studies have suggested a role for autophagy in ER remodelling, as autophagy-deficient neurons in vivo display axonal ER accumulation within synaptic boutons, and the membrane-embedded ER-phagy receptor FAM134B has been genetically linked with human sensory and autonomic neuropathy. However, our understanding of the mechanisms underlying selective removal of the ER and the role of individual ER-phagy receptors is limited. Here we combine a genetically tractable induced neuron (iNeuron) system for monitoring ER remodelling during in vitro differentiation with proteomic and computational tools to create a quantitative landscape of ER proteome remodelling via selective autophagy. Through analysis of single and combinatorial ER-phagy receptor mutants, we delineate the extent to which each receptor contributes to both the magnitude and selectivity of ER protein clearance. We define specific subsets of ER membrane or lumenal proteins as preferred clients for distinct receptors. Using spatial sensors and flux reporters, we demonstrate receptor-specific autophagic capture of ER in axons, and directly visualize tubular ER membranes within autophagosomes in neuronal projections by cryo-electron tomography. This molecular inventory of ER proteome remodelling and versatile genetic toolkit provide a quantitative framework for understanding the contributions of individual ER-phagy receptors for reshaping ER during cell state transitions.
Identifiants
pubmed: 38429475
doi: 10.1038/s41556-024-01356-4
pii: 10.1038/s41556-024-01356-4
pmc: PMC10940164
doi:
Substances chimiques
Proteome
0
Carrier Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
378-392Subventions
Organisme : NINDS NIH HHS
ID : R01 NS083524
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS110395
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM132129
Pays : United States
Commentaires et corrections
Type : UpdateOf
Informations de copyright
© 2024. The Author(s).
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