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PreprintCited by 41RNA Research and SplicingRNA and protein synthesis mechanismsMicrotubule and mitosis dynamics

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Mechanism of ribosome-associated mRNA degradation during tubulin autoregulation

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Höpfler, Markus, Absmeier, Eva, Peak-Chew, Sew-Yeu, Vartholomaiou, Evangelia, Passmore, Lori A., Gasic, Ivana, Hegde, Ramanujan S.·2023·Molecular Cell
DOI 10.1101/2023.01.12.523749PMC PMC10403363

Preprint — published as 10.1016/j.molcel.2023.05.020 · Paper page

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Abstract

SUMMARY: Microtubules play crucial roles in cellular architecture, intracellular transport, and mitosis. The availability of free tubulin subunits impacts polymerization dynamics and microtubule function. When cells sense excess free tubulin, they trigger degradation of the encoding mRNAs, which requires recognition of the nascent polypeptide by the tubulin-specific ribosome-binding factor TTC5. How TTC5 initiates decay of tubulin mRNAs is unknown. Here, our biochemical and structural analysis reveals that TTC5 recruits the poorly studied protein SCAPER to the ribosome. SCAPER in turn engages the CCR4-NOT deadenylase complex through its CNOT11 subunit to trigger tubulin mRNA decay. SCAPER mutants that cause intellectual disability and retinitis pigmentosa in humans are impaired in CCR4-NOT recruitment, tubulin mRNA degradation, and microtubule-dependent chromosome segregation. Our findings demonstrate how recognition of a nascent polypeptide on the ribosome is physically linked to mRNA decay factors via a relay of protein-protein interactions, providing a paradigm for specificity in cytoplasmic gene regulation.

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Metadata

Authors
Höpfler, M., Absmeier, E., Peak-Chew, S.-Y., Vartholomaiou, E., Passmore, L. A., Gasic, I., & Hegde, R. S.
Affiliations
  • MRC Laboratory of Molecular Biology (GB)
  • University of Geneva (CH)
Corresponding author
Hegde, Ramanujan S.
ORCID
Venue
Molecular Cell
Publisher
openRxiv
Published
2023-01-12
Volume
83
Issue
13
Pages
2290-2302.e13
ISSN
1097-2765 (ISSN-L)
DOI
10.1101/2023.01.12.523749
PMC
PMC10403363
OpenAlex
W4380048200
Cited by
41
References
1
Citations by year
2026: 8 · 2025: 18 · 2024: 8 · 2023: 7
FWCI
3.64
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Molecular Cell (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Archive ouverte UNIGE (University of Geneva) (submittedVersion, cc-by)
Funders
  • National Science Foundation
  • Damon Runyon Cancer Research Foundation (DRG:227916)
  • Wellcome Trust
  • Diamond Light Source
  • European Commission (HORIZON2020, 101029853)
  • Deutsche Forschungsgemeinschaft (429892960)
  • Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (194312)
  • Université de Genève
  • Directorate for Biological Sciences
  • Medical Research Council (MC_ UP_A022_1007, MC_U105192715)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
Keywords
CCR4-NOT complex, microtubule assembly, intellectual disability, retinitis pigmentosa, chromosome segregation, protein-protein interaction
MeSH terms
Carrier Proteins, Homeostasis, Humans, Microtubules, Ribosomes, RNA, Messenger, Transcription Factors, Tubulin, RNA Stability

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