A DNM2 Centronuclear Myopathy Mutation Reveals a Link between Recycling Endosome Scission and Autophagy.


Journal

Developmental cell
ISSN: 1878-1551
Titre abrégé: Dev Cell
Pays: United States
ID NLM: 101120028

Informations de publication

Date de publication:
20 04 2020
Historique:
received: 21 08 2019
revised: 24 01 2020
accepted: 23 03 2020
entrez: 22 4 2020
pubmed: 22 4 2020
medline: 15 12 2020
Statut: ppublish

Résumé

Autophagy involves engulfment of cytoplasmic contents by double-membraned autophagosomes, which ultimately fuse with lysosomes to enable degradation of their substrates. We recently proposed that the tubular-vesicular recycling endosome membranes were a core platform on which the critical early events of autophagosome formation occurred, including LC3-membrane conjugation to autophagic precursors. Here, we report that the release of autophagosome precursors from recycling endosomes is mediated by DNM2-dependent scission of these tubules. This process is regulated by DNM2 binding to LC3 and is increased by autophagy-inducing stimuli. This scission is defective in cells expressing a centronuclear-myopathy-causing DNM2 mutant. This mutant has an unusual mechanism as it depletes normal-functioning DNM2 from autophagosome formation sites on recycling endosomes by causing increased binding to an alternative plasma membrane partner, ITSN1. This "scission" step is, thus, critical for autophagosome formation, is defective in a human disease, and influences the way we consider how autophagosomes are formed.

Identifiants

pubmed: 32315611
pii: S1534-5807(20)30230-6
doi: 10.1016/j.devcel.2020.03.018
pii:
doi:

Substances chimiques

Adaptor Proteins, Vesicular Transport 0
ITSN1 protein, human 0
MAP1LC3A protein, human 0
Microtubule-Associated Proteins 0
DNM2 protein, human EC 3.6.5.5
Dynamin II EC 3.6.5.5

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

154-168.e6

Subventions

Organisme : Medical Research Council
ID : MC_U105161083
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/T012412/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : UKDRI-2002
Pays : United Kingdom

Informations de copyright

Copyright © 2020 Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Interests F.M.M. is employed by Eli Lilly, and D.C.R. is CSO of Aladdin Healthcare Technologies.

Auteurs

Claudia Puri (C)

Department of Medical Genetics, Cambridge Biomedical Campus, Hills Road, Cambridge CB2 0XY, UK; Cambridge Institute for Medical Research, The Keith Peters Building, Cambridge Biomedical Campus, Hills Road, Cambridge CB2 0XY, UK; UK Dementia Research Institute, Cambridge BioMedical Campus, The Keith Peters Building, Hills Road, Cambridge CB2 0XY, UK.

Marco M Manni (MM)

Department of Medical Genetics, Cambridge Biomedical Campus, Hills Road, Cambridge CB2 0XY, UK; Cambridge Institute for Medical Research, The Keith Peters Building, Cambridge Biomedical Campus, Hills Road, Cambridge CB2 0XY, UK.

Mariella Vicinanza (M)

Department of Medical Genetics, Cambridge Biomedical Campus, Hills Road, Cambridge CB2 0XY, UK; Cambridge Institute for Medical Research, The Keith Peters Building, Cambridge Biomedical Campus, Hills Road, Cambridge CB2 0XY, UK; UK Dementia Research Institute, Cambridge BioMedical Campus, The Keith Peters Building, Hills Road, Cambridge CB2 0XY, UK.

Christine Hilcenko (C)

Cambridge Institute for Medical Research, The Keith Peters Building, Cambridge Biomedical Campus, Hills Road, Cambridge CB2 0XY, UK; Department of Haematology, University of Cambridge, Cambridge CB2 0XY, UK; Wellcome Trust-Medical Research Council Stem Cell Institute, University of Cambridge, Jeffrey Cheah Biomedical Centre Puddicombe Way, Cambridge Biomedical Campus, Cambridge CB2 0AW, UK.

Ye Zhu (Y)

Department of Medical Genetics, Cambridge Biomedical Campus, Hills Road, Cambridge CB2 0XY, UK; Cambridge Institute for Medical Research, The Keith Peters Building, Cambridge Biomedical Campus, Hills Road, Cambridge CB2 0XY, UK.

Gautam Runwal (G)

Department of Medical Genetics, Cambridge Biomedical Campus, Hills Road, Cambridge CB2 0XY, UK; Cambridge Institute for Medical Research, The Keith Peters Building, Cambridge Biomedical Campus, Hills Road, Cambridge CB2 0XY, UK.

Eleanna Stamatakou (E)

Department of Medical Genetics, Cambridge Biomedical Campus, Hills Road, Cambridge CB2 0XY, UK; Cambridge Institute for Medical Research, The Keith Peters Building, Cambridge Biomedical Campus, Hills Road, Cambridge CB2 0XY, UK; UK Dementia Research Institute, Cambridge BioMedical Campus, The Keith Peters Building, Hills Road, Cambridge CB2 0XY, UK.

Fiona M Menzies (FM)

Department of Medical Genetics, Cambridge Biomedical Campus, Hills Road, Cambridge CB2 0XY, UK; Cambridge Institute for Medical Research, The Keith Peters Building, Cambridge Biomedical Campus, Hills Road, Cambridge CB2 0XY, UK.

Kamel Mamchaoui (K)

Myology Center for Research, U974, Sorbonne Université - INSERM - American Institute of Mathematics, GH Pitie Salpetrière, Paris 75013, France.

Marc Bitoun (M)

Myology Center for Research, U974, Sorbonne Université - INSERM - American Institute of Mathematics, GH Pitie Salpetrière, Paris 75013, France.

David C Rubinsztein (DC)

Department of Medical Genetics, Cambridge Biomedical Campus, Hills Road, Cambridge CB2 0XY, UK; Cambridge Institute for Medical Research, The Keith Peters Building, Cambridge Biomedical Campus, Hills Road, Cambridge CB2 0XY, UK; UK Dementia Research Institute, Cambridge BioMedical Campus, The Keith Peters Building, Hills Road, Cambridge CB2 0XY, UK. Electronic address: dcr1000@cam.ac.uk.

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Classifications MeSH