Evidence map›Paper›PMID 31123703›Full record

ArticleScience advances2019

Autophagy induction in atrophic muscle cells requires ULK1 activation by TRIM32 through unanchored K63-linked polyubiquitin chains.

M Di Rienzo, M Antonioli, C Fusco, Y Liu, M Mari, I Orhon, G Refolo, F Germani, M Corazzari, A Romagnoli and 13 more

Open access · goldAbstract read
In one paragraph

Article in Science advances, 2019. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 67 papers, 1 of them a synthesis that pooled it.

0numbers the graph read from it
0cells of the map it votes in
67citing papers in PubMed, 1 pooled it
10.5field-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

67 citing papers in PubMed, 1 synthesis or guideline pooled it, 111 citations in OpenAlex.

  1. Guideline
  2. Article
  3. Article
  4. Review
  5. Article
  6. Mitophagy in kidney transplantation ischemia-reperfusion injury.International urology and nephrology · 2026
    Review
  7. Article
  8. Article
  9. Review
  10. Review
  11. Article
  12. Article
  13. Muscle Disuse Atrophy.Advances in experimental medicine and biology · 2025
    Review
  14. Cancer Cachexia.Advances in experimental medicine and biology · 2025
    Review
  15. Review
  16. Review
  17. Article
  18. Review
  19. Review
  20. Article

7 more citing papers are in PubMed but not listed here.

4 · The record

Corrections and comments

5 · Who and what money

Authors and funding

23 authors at 10 institutions in 4 countries.

M Di RienzoNational Institute for Infectious Diseases IRCCS, Lazzaro Spallanzani, 00149 Rome, Italy.ORCID 0000-0002-1520-479X
M AntonioliNational Institute for Infectious Diseases IRCCS, Lazzaro Spallanzani, 00149 Rome, Italy.ORCID 0000-0002-7568-4713
C FuscoDivision of Medical Genetics, IRCCS, Casa Sollievo della Sofferenza, 71013 San Giovanni Rotondo, Italy.
Y LiuDepartment of Dermatology, Oregon Health and Science University, Portland, OR 97239, USA.ORCID 0000-0002-4179-6629
M MariDepartment of Biomedical Sciences of Cells and Systems, University of Groningen, University Medical Center Groningen, 9713 AV Groningen, Netherlands.
I OrhonDepartment of Biomedical Sciences of Cells and Systems, University of Groningen, University Medical Center Groningen, 9713 AV Groningen, Netherlands.ORCID 0000-0002-0779-8719
G RefoloNational Institute for Infectious Diseases IRCCS, Lazzaro Spallanzani, 00149 Rome, Italy.ORCID 0000-0002-5519-7395
F GermaniNational Institute for Infectious Diseases IRCCS, Lazzaro Spallanzani, 00149 Rome, Italy.ORCID 0000-0003-4825-6702
M CorazzariDepartment of Health Sciences, University of Piemonte Orientale "A. Avogadro", Novara, Novara, Italy.
A RomagnoliNational Institute for Infectious Diseases IRCCS, Lazzaro Spallanzani, 00149 Rome, Italy.ORCID 0000-0003-4946-6138
F CiccosantiNational Institute for Infectious Diseases IRCCS, Lazzaro Spallanzani, 00149 Rome, Italy.ORCID 0000-0003-0481-6878
B MandrianiDivision of Medical Genetics, IRCCS, Casa Sollievo della Sofferenza, 71013 San Giovanni Rotondo, Italy.
M T PellicoDivision of Medical Genetics, IRCCS, Casa Sollievo della Sofferenza, 71013 San Giovanni Rotondo, Italy.ORCID 0000-0002-4551-2160
R De La TorreDepartment of Dermatology, Oregon Health and Science University, Portland, OR 97239, USA.
H DingDepartment of Biochemistry and Medical Genetics, University of Manitoba, Winnipeg, Manitoba, Canada.ORCID 0000-0003-1608-7000
M DenticeDepartment of Clinical Medicine and Surgery, University of Naples Federico II, 80131 Naples, Italy.
M NeriSection of Medical Genetics, Department of Medical Sciences, University of Ferrara, 44121 Ferrara, Italy.
A FerliniSection of Medical Genetics, Department of Medical Sciences, University of Ferrara, 44121 Ferrara, Italy.
F ReggioriDepartment of Biomedical Sciences of Cells and Systems, University of Groningen, University Medical Center Groningen, 9713 AV Groningen, Netherlands.
M Kulesz-MartinDepartment of Dermatology, Oregon Health and Science University, Portland, OR 97239, USA.ORCID 0000-0001-7642-4051
M PiacentiniNational Institute for Infectious Diseases IRCCS, Lazzaro Spallanzani, 00149 Rome, Italy.ORCID 0000-0003-2919-1296
G MerlaDivision of Medical Genetics, IRCCS, Casa Sollievo della Sofferenza, 71013 San Giovanni Rotondo, Italy.ORCID 0000-0001-5078-928X
G M FimiaNational Institute for Infectious Diseases IRCCS, Lazzaro Spallanzani, 00149 Rome, Italy.ORCID 0000-0003-4438-3325
Istituto Nazionale per le Malattie Infettive Lazzaro Spallanzani · ITCasa Sollievo della Sofferenza · ITOregon Health & Science University · USUniversity Medical Center Groningen · NLUniversity of Ferrara · ITUniversity of Rome Tor Vergata · ITUniversità degli Studi del Piemonte Orientale “Amedeo Avogadro” · ITUniversity of Manitoba · CAUniversity of Naples Federico II · ITUniversity of Salento · IT

Funding

Trim32 regulation of PKC-zeta in atopic dermatitisR01AR070645 · NIAMS · OREGON HEALTH & SCIENCE UNIVERSITY · PI LIU, YUANGANG · 2017 to 2021
$1.9M
NIAMS NIH HHS R01 AR070645
6 · The paper itself

Abstract

Optimal autophagic activity is crucial to maintain muscle integrity, with either reduced or excessive levels leading to specific myopathies. LGMD2H is a muscle dystrophy caused by mutations in the ubiquitin ligase TRIM32, whose function in muscles remains not fully understood. Here, we show that TRIM32 is required for the induction of muscle autophagy in atrophic conditions using both in vitro and in vivo mouse models. Trim32 inhibition results in a defective autophagy response to muscle atrophy, associated with increased ROS and MuRF1 levels. The proautophagic function of TRIM32 relies on its ability to bind the autophagy proteins AMBRA1 and ULK1 and stimulate ULK1 activity via unanchored K63-linked polyubiquitin. LGMD2H-causative mutations impair TRIM32's ability to bind ULK1 and induce autophagy. Collectively, our study revealed a role for TRIM32 in the regulation of muscle autophagy in response to atrophic stimuli, uncovering a previously unidentified mechanism by which ubiquitin ligases activate autophagy regulators.

Indexed as

AutophagyAdaptor Proteins, Signal TransducingAnimalsAutophagy-Related Protein-1 HomologCell LineCell TransdifferentiationHumansLysineMiceMice, KnockoutMuscular Dystrophies, Limb-GirdleMyoblastsProtein BindingRNA InterferenceRNA, Small InterferingUbiquitinationAdaptor Proteins, Signal TransducingAmbra1 protein, mouseAutophagy-Related Protein-1 HomologLysineRNA, Small InterferingTRIM32 protein, mouseUbiquitin-Protein Ligases

Identifiers

PMID31123703
PMCPMC6527439
OpenAlexW2944528098

What OpenQuestion holds

Textmetadata
LicenceCC BY-NC
Read underepoch 390

Registered trials

None linked

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.