TFG binds LC3C to regulate ULK1 localization and autophagosome formation.


Journal

The EMBO journal
ISSN: 1460-2075
Titre abrégé: EMBO J
Pays: England
ID NLM: 8208664

Informations de publication

Date de publication:
17 05 2021
Historique:
revised: 17 02 2021
received: 26 09 2019
accepted: 01 03 2021
pubmed: 2 5 2021
medline: 16 11 2021
entrez: 1 5 2021
Statut: ppublish

Résumé

The early secretory pathway and autophagy are two essential and evolutionarily conserved endomembrane processes that are finely interlinked. Although growing evidence suggests that intracellular trafficking is important for autophagosome biogenesis, the molecular regulatory network involved is still not fully defined. In this study, we demonstrate a crucial effect of the COPII vesicle-related protein TFG (Trk-fused gene) on ULK1 puncta number and localization during autophagy induction. This, in turn, affects formation of the isolation membrane, as well as the correct dynamics of association between LC3B and early ATG proteins, leading to the proper formation of both omegasomes and autophagosomes. Consistently, fibroblasts derived from a hereditary spastic paraparesis (HSP) patient carrying mutated TFG (R106C) show defects in both autophagy and ULK1 puncta accumulation. In addition, we demonstrate that TFG activity in autophagy depends on its interaction with the ATG8 protein LC3C through a canonical LIR motif, thereby favouring LC3C-ULK1 binding. Altogether, our results uncover a link between TFG and autophagy and identify TFG as a molecular scaffold linking the early secretion pathway to autophagy.

Identifiants

pubmed: 33932238
doi: 10.15252/embj.2019103563
pmc: PMC8126910
doi:

Substances chimiques

Intracellular Signaling Peptides and Proteins 0
MAP1LC3C protein, human 0
Microtubule-Associated Proteins 0
Proteins 0
TFG protein, human 0
Autophagy-Related Protein-1 Homolog EC 2.7.11.1
ULK1 protein, human EC 2.7.11.1

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e103563

Subventions

Organisme : Biotechnology and Biological Sciences Research Council
ID : BBS/E/B/000C0413
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BBS/E/B/000C0417
Pays : United Kingdom

Informations de copyright

© 2021 The Authors. Published under the terms of the CC BY NC ND 4.0 license.

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Auteurs

Marianna Carinci (M)

Department of Pediatric Hemato-Oncology and Cell and Gene Therapy, IRCCS Bambino Gesù Children's Hospital, Rome, Italy.
Department of Medical Sciences, University of Ferrara, Laboratory of Technologies for Advanced Therapy (LTTA), Technopole of Ferrara, Ferrara, Italy.

Beatrice Testa (B)

Department of Biology, University of Rome Tor Vergata, Rome, Italy.

Matteo Bordi (M)

Department of Pediatric Hemato-Oncology and Cell and Gene Therapy, IRCCS Bambino Gesù Children's Hospital, Rome, Italy.
Department of Biology, University of Rome Tor Vergata, Rome, Italy.

Giacomo Milletti (G)

Department of Pediatric Hemato-Oncology and Cell and Gene Therapy, IRCCS Bambino Gesù Children's Hospital, Rome, Italy.
Department of Biology, University of Rome Tor Vergata, Rome, Italy.

Massimo Bonora (M)

Department of Medical Sciences, University of Ferrara, Laboratory of Technologies for Advanced Therapy (LTTA), Technopole of Ferrara, Ferrara, Italy.

Laura Antonucci (L)

Department of Pediatric Hemato-Oncology and Cell and Gene Therapy, IRCCS Bambino Gesù Children's Hospital, Rome, Italy.

Caterina Ferraina (C)

Department of Pediatric Hemato-Oncology and Cell and Gene Therapy, IRCCS Bambino Gesù Children's Hospital, Rome, Italy.

Marta Carro (M)

Department of Biology, University of Padua, Padua, Italy.

Mukesh Kumar (M)

Computational Biology Laboratory, Danish Cancer Society Research Center, Copenhagen, Denmark.

Donatella Ceglie (D)

Department of Pediatric Hemato-Oncology and Cell and Gene Therapy, IRCCS Bambino Gesù Children's Hospital, Rome, Italy.

Franziska Eck (F)

Munich Cluster for Systems Neurology (SyNergy), Ludwig-Maximilians-Universität (LMU), München, Germany.

Roberta Nardacci (R)

Department of Epidemiology and Preclinical Research, National Institute for Infectious Diseases IRCCS "L. Spallanzani", Rome, Italy.

Francois le Guerroué (F)

Munich Cluster for Systems Neurology (SyNergy), Ludwig-Maximilians-Universität (LMU), München, Germany.

Stefania Petrini (S)

Confocal Microscopy Core Facility, Research Laboratories, IRCCS Bambino Gesù Children's Hospital, Rome, Italy.

Maria E Soriano (ME)

Department of Biology, University of Padua, Padua, Italy.

Ignazio Caruana (I)

Department of Pediatric Hemato-Oncology and Cell and Gene Therapy, IRCCS Bambino Gesù Children's Hospital, Rome, Italy.

Valentina Doria (V)

Confocal Microscopy Core Facility, Research Laboratories, IRCCS Bambino Gesù Children's Hospital, Rome, Italy.

Maria Manifava (M)

The Babraham Institute, Cambridge, UK.

Camille Peron (C)

UO Medical Genetics and Neurogenetics, Fondazione IRCCS Istituto Neurologico C. Besta, Milan, Italy.

Matteo Lambrughi (M)

Computational Biology Laboratory, Danish Cancer Society Research Center, Copenhagen, Denmark.

Valeria Tiranti (V)

UO Medical Genetics and Neurogenetics, Fondazione IRCCS Istituto Neurologico C. Besta, Milan, Italy.

Christian Behrends (C)

Munich Cluster for Systems Neurology (SyNergy), Ludwig-Maximilians-Universität (LMU), München, Germany.

Elena Papaleo (E)

Computational Biology Laboratory, Danish Cancer Society Research Center, Copenhagen, Denmark.
Translational Disease Systems Biology, Faculty of Health and Medical Sciences, Novo Nordisk Foundation Center for Protein Research University of Copenhagen, Copenhagen, Denmark.

Paolo Pinton (P)

Department of Medical Sciences, University of Ferrara, Laboratory of Technologies for Advanced Therapy (LTTA), Technopole of Ferrara, Ferrara, Italy.

Carlotta Giorgi (C)

Department of Medical Sciences, University of Ferrara, Laboratory of Technologies for Advanced Therapy (LTTA), Technopole of Ferrara, Ferrara, Italy.

Nicholas T Ktistakis (NT)

The Babraham Institute, Cambridge, UK.

Franco Locatelli (F)

Department of Pediatric Hemato-Oncology and Cell and Gene Therapy, IRCCS Bambino Gesù Children's Hospital, Rome, Italy.
Department of Gynecology/Obstetrics and Pediatrics, Sapienza University, Rome, Italy.

Francesca Nazio (F)

Department of Pediatric Hemato-Oncology and Cell and Gene Therapy, IRCCS Bambino Gesù Children's Hospital, Rome, Italy.

Francesco Cecconi (F)

Department of Pediatric Hemato-Oncology and Cell and Gene Therapy, IRCCS Bambino Gesù Children's Hospital, Rome, Italy.
Department of Biology, University of Rome Tor Vergata, Rome, Italy.
Unit of Cell Stress and Survival, Danish Cancer Society Research Center, Copenhagen, Denmark.

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Classifications MeSH