TORC1 regulates vacuole membrane composition through ubiquitin- and ESCRT-dependent microautophagy.


Journal

The Journal of cell biology
ISSN: 1540-8140
Titre abrégé: J Cell Biol
Pays: United States
ID NLM: 0375356

Informations de publication

Date de publication:
02 03 2020
Historique:
received: 20 02 2019
revised: 22 11 2019
accepted: 07 01 2020
entrez: 12 2 2020
pubmed: 12 2 2020
medline: 21 10 2020
Statut: ppublish

Résumé

Cellular adaptation in response to nutrient limitation requires the induction of autophagy and lysosome biogenesis for the efficient recycling of macromolecules. Here, we discovered that starvation and TORC1 inactivation not only lead to the up-regulation of autophagy and vacuole proteins involved in recycling but also result in the down-regulation of many vacuole membrane proteins to supply amino acids as part of a vacuole remodeling process. Down-regulation of vacuole membrane proteins is initiated by ubiquitination, which is accomplished by the coordination of multiple E3 ubiquitin ligases, including Rsp5, the Dsc complex, and a newly characterized E3 ligase, Pib1. The Dsc complex is negatively regulated by TORC1 through the Rim15-Ume6 signaling cascade. After ubiquitination, vacuole membrane proteins are sorted into the lumen for degradation by ESCRT-dependent microautophagy. Thus, our study uncovered a complex relationship between TORC1 inactivation and vacuole biogenesis.

Identifiants

pubmed: 32045480
pii: 133713
doi: 10.1083/jcb.201902127
pmc: PMC7055007
pii:
doi:

Substances chimiques

Endosomal Sorting Complexes Required for Transport 0
Repressor Proteins 0
Saccharomyces cerevisiae Proteins 0
TORC1 protein complex, S cerevisiae 0
Transcription Factors 0
UME6 protein, S cerevisiae 0
Ubiquitin 0
Ubiquitin-Protein Ligase Complexes EC 2.3.2.23
Protein Kinases EC 2.7.-
Rim15 protein, S cerevisiae EC 2.7.1.-
PIB1 protein, S cerevisiae EC 6.3.2.-
RSP5 protein, S cerevisiae EC 6.3.2.-

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Austrian Science Fund FWF
ID : P 30263
Pays : Austria
Organisme : NIGMS NIH HHS
ID : R01 GM133873
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35 GM131919
Pays : United States

Informations de copyright

© 2020 Yang et al.

Références

J Cell Biol. 2016 Sep 12;214(6):653-64
pubmed: 27621362
Autophagy. 2012 Dec;8(12):1835-6
pubmed: 22960621
Proc Natl Acad Sci U S A. 2006 Aug 29;103(35):13004-9
pubmed: 16916930
Mol Cell Biol. 1986 Jul;6(7):2500-10
pubmed: 3537721
Nat Commun. 2017 Nov 17;8(1):1580
pubmed: 29146937
Traffic. 2012 Apr;13(4):586-98
pubmed: 22212814
Proc Natl Acad Sci U S A. 2002 Oct 15;99(21):13431-6
pubmed: 12370439
Cell. 2005 Nov 18;123(4):569-80
pubmed: 16286006
Annu Rev Biochem. 1986;55:663-700
pubmed: 2874766
Mol Cell. 1998 Jul;2(1):157-62
pubmed: 9702203
Eukaryot Cell. 2007 Jul;6(7):1166-77
pubmed: 17526722
Elife. 2017 Oct 11;6:
pubmed: 29019322
Mol Cell. 2003 Dec;12(6):1607-13
pubmed: 14690612
Yeast. 1997 Jul;13(9):837-48
pubmed: 9234672
Mol Biol Cell. 2014 Apr;25(7):1171-85
pubmed: 24478451
Science. 2009 Jul 24;325(5939):473-7
pubmed: 19556463
Autophagy. 2019 May;15(5):915-916
pubmed: 30732525
Genomics. 1999 Feb 15;56(1):111-20
pubmed: 10036191
Proc Natl Acad Sci U S A. 2012 Jul 10;109(28):11206-10
pubmed: 22733735
Curr Protoc Mol Biol. 2005 Feb;Chapter 21:Unit 21.3
pubmed: 18265358
Mol Cell. 2015 Feb 5;57(3):467-78
pubmed: 25620559
Cell Logist. 2014 Jan 1;4(1):e28023
pubmed: 24843828
J Biol Chem. 2001 Nov 2;276(44):41388-93
pubmed: 11526110
EMBO J. 2012 Mar 7;31(5):1095-108
pubmed: 22343943
Mol Cell Biol. 1986 Jul;6(7):2490-9
pubmed: 3023936
EMBO J. 1997 Apr 15;16(8):1820-31
pubmed: 9155008
Biomolecules. 2017 Jul 07;7(3):
pubmed: 28686223
Mol Biol Cell. 2010 Oct 1;21(19):3475-86
pubmed: 20702584
Mol Cell. 2007 Jun 8;26(5):663-74
pubmed: 17560372
Biochim Biophys Acta. 2009 Apr;1793(4):650-63
pubmed: 18786576
EMBO J. 2005 Dec 21;24(24):4271-8
pubmed: 16308562
J Cell Biol. 2015 Nov 9;211(3):639-52
pubmed: 26527740
Sci Signal. 2014 Jan 21;7(309):ra9
pubmed: 24448649
Microsc Res Tech. 2000 Dec 15;51(6):496-510
pubmed: 11169854
Mol Microbiol. 2008 Jul;69(1):277-85
pubmed: 18513215
J Cell Biol. 2019 Apr 1;218(4):1319-1334
pubmed: 30808705
FEMS Yeast Res. 2013 Aug;13(5):471-84
pubmed: 23679341
EMBO J. 2007 May 16;26(10):2454-64
pubmed: 17446860
Biosci Biotechnol Biochem. 2014;78(7):1199-202
pubmed: 25229858
Elife. 2018 Jan 22;7:
pubmed: 29355480
Mol Biol Cell. 2006 Dec;17(12):5094-104
pubmed: 17021250
Annu Rev Cell Dev Biol. 2016 Oct 6;32:223-253
pubmed: 27501449
J Cell Sci. 2009 Oct 15;122(Pt 20):3589-94
pubmed: 19812304
Mol Cell Proteomics. 2014 Nov;13(11):2871-82
pubmed: 25078903
Mol Cell. 2019 Jan 17;73(2):325-338.e8
pubmed: 30527664
Dev Cell. 2017 Jan 23;40(2):151-167
pubmed: 28017618
Science. 2011 Jun 17;332(6036):1429-33
pubmed: 21617040
Elife. 2017 Jun 29;6:
pubmed: 28661397
J Cell Biol. 2017 Oct 2;216(10):3263-3274
pubmed: 28838958
J Biol Chem. 1992 Jul 15;267(20):14294-303
pubmed: 1385813
J Biol Chem. 1995 Jul 14;270(28):17025-32
pubmed: 7622524
Nat Rev Mol Cell Biol. 2013 May;14(5):283-96
pubmed: 23609508
Nat Struct Mol Biol. 2014 Jun;21(6):513-21
pubmed: 24793651
EMBO J. 2018 Jun 1;37(11):
pubmed: 29764979
Autophagy. 2019 Feb;15(2):212-227
pubmed: 30422029
Elife. 2015 Apr 22;4:e07736
pubmed: 25902403
EMBO J. 2012 Sep 12;31(18):3691-703
pubmed: 22885598

Auteurs

Xi Yang (X)

Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI.

Weichao Zhang (W)

Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI.

Xin Wen (X)

Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI.
Life Sciences Institute, University of Michigan, Ann Arbor, MI.

Patrick J Bulinski (PJ)

Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI.

Dominic A Chomchai (DA)

Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI.

Felichi Mae Arines (FM)

Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI.

Yun-Yu Liu (YY)

Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI.

Simon Sprenger (S)

Institute for Cell Biology, Biocenter, Medical University of Innsbruck, Innsbruck, Austria.

David Teis (D)

Institute for Cell Biology, Biocenter, Medical University of Innsbruck, Innsbruck, Austria.

Daniel J Klionsky (DJ)

Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI.
Life Sciences Institute, University of Michigan, Ann Arbor, MI.

Ming Li (M)

Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI.

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Classifications MeSH