Evidence map›Paper›PMID 33217318›Full record

ArticleMolecular cell2020

Spatiotemporal Proteomic Analysis of Stress Granule Disassembly Using APEX Reveals Regulation by SUMOylation and Links to ALS Pathogenesis.

Hagai Marmor-Kollet, Aviad Siany, Nancy Kedersha, Naama Knafo, Natalia Rivkin, Yehuda M Danino, Thomas G Moens, Tsviya Olender, Daoud Sheban, Nir Cohen and 17 more

Open access · bronzeAbstract read
In one paragraph

Article in Molecular cell, 2020. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 167 papers.

0numbers the graph read from it
0cells of the map it votes in
167citing papers in PubMed
12.7field-weighted citation impact, top 1% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

167 citing papers in PubMed, 253 citations in OpenAlex.

  1. Review
  2. Article
  3. Review
  4. BOULE is Essential for the Dynamic Disassembly of Heat Shock Granules in Male Germ Cells.Advanced science (Weinheim, Baden-Wurttemberg, Germany) · 2026
    Article
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  13. The Role of Stress Granules in Cardiovascular Diseases.Reviews in cardiovascular medicine · 2026
    Review
  14. Article
  15. BAG2 Condensates Couple Proteostasis to CD8bioRxiv : the preprint server for biology · 2026
    Article
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107 more citing papers are in PubMed but not listed here.

4 · The record

Corrections and comments

PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.

5 · Who and what money

Authors and funding

27 authors at 7 institutions in 4 countries.

Hagai Marmor-KolletDepartment of Molecular Genetics, Weizmann Institute of Science, Rehovot 7610001, Israel.
Aviad SianyDepartment of Molecular Genetics, Weizmann Institute of Science, Rehovot 7610001, Israel.
Nancy KedershaDivision of Rheumatology, Immunity, and Inflammation, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA; Harvard Medical School Initiative for RNA Medicine, Harvard Medical School, Boston, MA 02115, USA.
Naama KnafoDepartment of Human Molecular Genetics and Biochemistry, Sackler School of Medicine, Tel Aviv University, Tel Aviv 6997801, Israel.
Natalia RivkinDepartment of Molecular Genetics, Weizmann Institute of Science, Rehovot 7610001, Israel.
Yehuda M DaninoDepartment of Molecular Genetics, Weizmann Institute of Science, Rehovot 7610001, Israel.
Thomas G MoensKU Leuven - University of Leuven, Department of Neurosciences, Experimental Neurology and Leuven Brain Institute (LBI), Leuven, Belgium; VIB, Center for Brain & Disease Research, Laboratory of Neurobiology, Leuven, Belgium.
Tsviya OlenderDepartment of Molecular Genetics, Weizmann Institute of Science, Rehovot 7610001, Israel.
Daoud ShebanDepartment of Molecular Genetics, Weizmann Institute of Science, Rehovot 7610001, Israel; Department of Immunology, Weizmann Institute of Science, Rehovot 7610001, Israel.
Nir CohenDepartment of Molecular Genetics, Weizmann Institute of Science, Rehovot 7610001, Israel.
Tali DadoshDepartment of Chemical Research Support, Weizmann Institute of Science, Rehovot 7610001, Israel.
Yoseph AddadiDepartment of Life Sciences Core Facilities, Weizmann Institute of Science, Rehovot 7610001, Israel.
Revital RavidDepartment of Molecular Genetics, Weizmann Institute of Science, Rehovot 7610001, Israel.
Chen EitanDepartment of Molecular Genetics, Weizmann Institute of Science, Rehovot 7610001, Israel.
Beata Toth CohenDepartment of Molecular Genetics, Weizmann Institute of Science, Rehovot 7610001, Israel.
Sarah HofmannDivision of Rheumatology, Immunity, and Inflammation, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA; Harvard Medical School Initiative for RNA Medicine, Harvard Medical School, Boston, MA 02115, USA.
Claire L RiggsDivision of Rheumatology, Immunity, and Inflammation, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA; Harvard Medical School Initiative for RNA Medicine, Harvard Medical School, Boston, MA 02115, USA.
Vivek M AdvaniDivision of Rheumatology, Immunity, and Inflammation, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA; Harvard Medical School Initiative for RNA Medicine, Harvard Medical School, Boston, MA 02115, USA.
Adrian HigginbottomSheffield Institute for Translational Neuroscience (SITraN), University of Sheffield, Sheffield S10 2HQ, UK.
Johnathan Cooper-KnockSheffield Institute for Translational Neuroscience (SITraN), University of Sheffield, Sheffield S10 2HQ, UK.
Jacob H HannaDepartment of Molecular Genetics, Weizmann Institute of Science, Rehovot 7610001, Israel.
Yifat MerblDepartment of Immunology, Weizmann Institute of Science, Rehovot 7610001, Israel.
Ludo Van Den BoschKU Leuven - University of Leuven, Department of Neurosciences, Experimental Neurology and Leuven Brain Institute (LBI), Leuven, Belgium; VIB, Center for Brain & Disease Research, Laboratory of Neurobiology, Leuven, Belgium.
Paul AndersonDivision of Rheumatology, Immunity, and Inflammation, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA; Harvard Medical School Initiative for RNA Medicine, Harvard Medical School, Boston, MA 02115, USA.
Pavel IvanovDivision of Rheumatology, Immunity, and Inflammation, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA; Harvard Medical School Initiative for RNA Medicine, Harvard Medical School, Boston, MA 02115, USA.
Tamar GeigerHarvard Medical School Initiative for RNA Medicine, Harvard Medical School, Boston, MA 02115, USA; Department of Human Molecular Genetics and Biochemistry, Sackler School of Medicine, Tel Aviv University, Tel Aviv 6997801, Israel. Electronic address: geiger@tauex.tau.ac.il.
Eran HornsteinDepartment of Molecular Genetics, Weizmann Institute of Science, Rehovot 7610001, Israel. Electronic address: eran.hornstein@weizmann.ac.il.
Weizmann Institute of Science · ILHarvard University · USBrigham and Women's Hospital · USUniversity of Sheffield · GBKU Leuven · BETel Aviv University · ILVIB-KU Leuven Center for Brain & Disease Research · BE

Funding

Resource Component: Acquisition, maintenance and distribution of Drosophila stocksP40OD018537 · OD · TRUSTEES OF INDIANA UNIVERSITY · PI Annette L. Parks · 2014 to 2026
$13.5M
Cellular Stress Response MechanismsR35GM126901 · NIGMS · BRIGHAM AND WOMEN'S HOSPITAL · PI ANDERSON, PAUL J. · 2018 to 2022
$2.9M
Biology of RNA G-quadruplexesR01GM126150 · NIGMS · BRIGHAM AND WOMEN'S HOSPITAL · PI IVANOV, PAVEL · 2019 to 2023
$1.9M
tRNA-derived stress-induced RNAs and translational controlR01GM146997 · NIGMS · BRIGHAM AND WOMEN'S HOSPITAL · PI IVANOV, PAVEL · 2022 to 2025
$1.6M
NIGMS NIH HHS R01 GM126150NIGMS NIH HHS R01 GM146997NIGMS NIH HHS R35 GM126901NIH HHS P40 OD018537
6 · The paper itself

Abstract

Stress granules (SGs) are cytoplasmic assemblies of proteins and non-translating mRNAs. Whereas much has been learned about SG formation, a major gap remains in understanding the compositional changes SGs undergo during normal disassembly and under disease conditions. Here, we address this gap by proteomic dissection of the SG temporal disassembly sequence using multi-bait APEX proximity proteomics. We discover 109 novel SG proteins and characterize distinct SG substructures. We reveal dozens of disassembly-engaged proteins (DEPs), some of which play functional roles in SG disassembly, including small ubiquitin-like modifier (SUMO) conjugating enzymes. We further demonstrate that SUMOylation regulates SG disassembly and SG formation. Parallel proteomics with amyotrophic lateral sclerosis (ALS)-associated C9ORF72 dipeptides uncovered attenuated DEP recruitment during SG disassembly and impaired SUMOylation. Accordingly, SUMO activity ameliorated C9ORF72-ALS-related neurodegeneration in Drosophila. By dissecting the SG spatiotemporal proteomic landscape, we provide an in-depth resource for future work on SG function and reveal basic and disease-relevant mechanisms of SG disassembly.

Indexed as

SumoylationAmyotrophic Lateral SclerosisAnimalsC9orf72 ProteinCell Line, TumorCytoplasmic GranulesDipeptidesDrosophila melanogasterDrosophila ProteinsHumansMiceProteomicsSmall Ubiquitin-Related Modifier ProteinsC9orf72 ProteinC9orf72 protein, humanC9orf72 protein, mouseDipeptidesDrosophila ProteinsSmall Ubiquitin-Related Modifier ProteinsALSamyotrophic lateral sclerosisAPEXcondensatesmembraneless organellesneurodegenerationphase separationRNA binding proteinsstress granulessumoylation

Identifiers

PMID33217318
PMCPMC7816607
OpenAlexW3106401261

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Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.