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PreprintCited by 34Endoplasmic Reticulum Stress and DiseaseRNA and protein synthesis mechanismsCellular transport and secretion

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SAYSD1 senses UFMylated ribosome to safeguard co-translational protein translocation at the endoplasmic reticulum

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Wang, Lihui, Xu, Yue, Yun, Sijung, Yuan, Quan, Satpute-Krishnan, Prasanna, Ye, Yihong·2022·Cell Reports
DOI 10.1101/2022.12.05.519155PMC PMC10010011

Preprint — published as 10.1016/j.celrep.2023.112028 · Paper page

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Abstract

Translocon clogging at the endoplasmic reticulum (ER) as a result of translation stalling triggers ribosome UFMylation, activating a T ranslocation- A ssociated Q uality C ontrol (TAQC) mechanism that degrades clogged substrates. How cells sense ribosome UFMylation to initiate TAQC is unclear. Here we use a genome-wide CRISPR/Cas9 screen to identify an uncharacterized membrane protein named SAYSD1 that facilitates TAQC. SAYSD1 associates with the Sec61 translocon, and also recognizes both ribosome and UFM1 directly, engaging a stalled nascent chain to ensure its transport via the TRAPP complex to lysosomes for degradation. Like UFM1 deficiency, SAYSD1 depletion causes the accumulation of translocation-stalled proteins at the ER and triggers ER stress. Importantly, disrupting UFM1- and SAYSD1-dependent TAQC in Drosophila leads to intracellular accumulation of translocation-stalled collagens, defective collagen deposition, abnormal basement membranes, and reduced stress tolerance. Together, our data support a model that SAYSD1 acts as a UFM1 sensor that collaborates with ribosome UFMylation at the site of clogged translocon, safeguarding ER homeostasis during animal development.

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Metadata

Authors
Wang, L., Xu, Y., Yun, S., Yuan, Q., Satpute-Krishnan, P., & Ye, Y.
Affiliations
National Institutes of Health (US)
Corresponding author
Ye, Yihong
ORCID
Venue
Cell Reports
Publisher
openRxiv
Published
2022-12-07
Volume
42
Issue
1
Pages
112028-112028
ISSN
2211-1247 (ISSN-L)
DOI
10.1101/2022.12.05.519155
PMC
PMC10010011
OpenAlex
W4317756907
Cited by
34
References
1
Citations by year
2026: 10 · 2025: 8 · 2024: 9 · 2023: 7
FWCI
4.90
Type
journal article
Language
en
Open access
Licence
cc-by-nc-nd
Locations
  • Cell Reports (publishedVersion, cc-by-nc-nd)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion, cc-by-nc-nd)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • New York University
  • York University
  • National Institutes of Health
  • National Heart, Lung, and Blood Institute
  • National Institute of General Medical Sciences (GM134327, R01GM134327)
  • National Institute of Allergy and Infectious Diseases
  • National Institute of Diabetes and Digestive and Kidney Diseases (ZIADK033008)
  • National Institute of Neurological Disorders and Stroke
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Endoplasmic Reticulum Stress and Disease
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
Keywords
UFM1, Sec61 translocon, endoplasmic reticulum stress, nascent chain, TRAPP complex, lysosomal degradation, collagen deposition, basement membrane, Drosophila, ER homeostasis
MeSH terms
Animals, Basement Membrane, Drosophila, Endoplasmic Reticulum, Fenbendazole, Membrane Proteins, Ribosomes, Protein Transport, Drosophila Proteins

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