The ubiquitin-like modifier FAT10 interferes with SUMO activation.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
01 10 2019
Historique:
received: 11 04 2019
accepted: 10 09 2019
entrez: 3 10 2019
pubmed: 3 10 2019
medline: 7 1 2020
Statut: epublish

Résumé

The covalent attachment of the cytokine-inducible ubiquitin-like modifier HLA-F adjacent transcript 10 (FAT10) to hundreds of substrate proteins leads to their rapid degradation by the 26 S proteasome independently of ubiquitylation. Here, we identify another function of FAT10, showing that it interferes with the activation of SUMO1/2/3 in vitro and down-regulates SUMO conjugation and the SUMO-dependent formation of promyelocytic leukemia protein (PML) bodies in cells. Mechanistically, we show that FAT10 directly binds to and impedes the activity of the heterodimeric SUMO E1 activating enzyme AOS1/UBA2 by competing very efficiently with SUMO for activation and thioester formation. Nevertheless, activation of FAT10 by AOS1/UBA2 does not lead to covalent conjugation of FAT10 with substrate proteins which relies on its cognate E1 enzyme UBA6. Hence, we report that one ubiquitin-like modifier (FAT10) inhibits the conjugation and function of another ubiquitin-like modifier (SUMO) by impairing its activation.

Identifiants

pubmed: 31575873
doi: 10.1038/s41467-019-12430-z
pii: 10.1038/s41467-019-12430-z
pmc: PMC6773726
doi:

Substances chimiques

JunB protein, human 0
Promyelocytic Leukemia Protein 0
Recombinant Proteins 0
SUMO-1 Protein 0
SUMO1 protein, human 0
SUMO2 protein, human 0
SUMO3 protein, human 0
Small Ubiquitin-Related Modifier Proteins 0
Transcription Factors 0
UBA2 protein, human 0
UBA6 protein, human 0
UBD protein, human 0
Ubiquitins 0
PML protein, human 143220-95-5
Proteasome Endopeptidase Complex EC 3.4.25.1
ATP dependent 26S protease EC 3.4.99.-
SAE1 protein, human EC 6.2.1.45
Ubiquitin-Activating Enzymes EC 6.2.1.45

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

4452

Références

Nat Rev Cancer. 2017 Mar;17(3):184-197
pubmed: 28134258
Sci Signal. 2009 May 26;2(72):ra24
pubmed: 19471022
Nature. 2007 Jun 28;447(7148):1135-8
pubmed: 17597759
Nat Methods. 2012 Sep;9(9):901-3
pubmed: 22772729
EMBO J. 2005 Feb 9;24(3):439-51
pubmed: 15660128
Mol Med Rep. 2018 Jun;17(6):7487-7496
pubmed: 29620277
J Immunol. 2015 Nov 1;195(9):4106-16
pubmed: 26401002
Methods Enzymol. 2005;398:20-32
pubmed: 16275316
Int J Biochem Cell Biol. 2016 Oct;79:451-461
pubmed: 27393295
Nucleic Acids Res. 2016 Jan 4;44(D1):D447-56
pubmed: 26527722
Mol Cell. 2007 Sep 21;27(6):1014-23
pubmed: 17889673
Mol Aspects Med. 2018 Oct;63:3-17
pubmed: 30059710
Nat Commun. 2010 May 04;1:13
pubmed: 20975683
Mol Cell Biol. 2005 May;25(9):3483-91
pubmed: 15831455
J Biol Chem. 2004 Apr 16;279(16):16503-10
pubmed: 14757770
Immunogenetics. 1996;44(2):97-103
pubmed: 8662070
Cell. 2002 Jan 11;108(1):109-20
pubmed: 11792325
J Biol Chem. 2019 Mar 22;294(12):4315-4330
pubmed: 30718280
J Cell Sci. 2012 Oct 1;125(Pt 19):4576-85
pubmed: 22797925
PLoS One. 2015 Apr 10;10(4):e0123882
pubmed: 25860128
Nat Methods. 2015 Dec;12(12):1185-90
pubmed: 26501516
Oncogene. 2008 Oct 9;27(46):6068-74
pubmed: 18574467
Proc Natl Acad Sci U S A. 1999 Apr 13;96(8):4313-8
pubmed: 10200259
J Biol Chem. 1999 Apr 9;274(15):10618-24
pubmed: 10187858
J Exp Med. 2001 Jun 18;193(12):1361-71
pubmed: 11413191
Annu Rev Cell Dev Biol. 2006;22:159-80
pubmed: 16753028
J Biol Chem. 2000 Mar 3;275(9):6252-8
pubmed: 10692421
Annu Rev Biochem. 2013;82:357-85
pubmed: 23746258
FEBS Lett. 2009 Feb 4;583(3):591-4
pubmed: 19166848
Exp Mol Pathol. 2011 Feb;90(1):51-4
pubmed: 20888811
J Biol Chem. 2007 Aug 10;282(32):23010-4
pubmed: 17580310
Mol Cell. 2005 Apr 1;18(1):1-12
pubmed: 15808504
Nat Commun. 2018 Oct 25;9(1):4441
pubmed: 30361475
EMBO J. 1999 Jan 15;18(2):420-32
pubmed: 9889198
Mol Cell Biol. 2006 Jul;26(13):5180-9
pubmed: 16782901
Oncogene. 2003 May 1;22(17):2592-603
pubmed: 12730673
PLoS One. 2015 Mar 13;10(3):e0120329
pubmed: 25768649
Nat Commun. 2018 Aug 20;9(1):3321
pubmed: 30127417
PLoS One. 2012;7(8):e43270
pubmed: 22912842
Nat Rev Cancer. 2003 Nov;3(11):859-68
pubmed: 14668816
J Biol Chem. 2012 May 4;287(19):15154-63
pubmed: 22403398
Eur J Immunol. 1999 Dec;29(12):4030-6
pubmed: 10602013
J Immunol. 2008 May 1;180(9):5983-90
pubmed: 18424718
FEBS J. 2014 Apr;281(7):1848-59
pubmed: 24528925
Nature. 2010 Feb 18;463(7283):906-12
pubmed: 20164921
Oncogene. 2013 Apr 25;32(17):2189-99
pubmed: 22710716
Tumour Biol. 2014 Jun;35(6):5167-71
pubmed: 24492942
J Cell Biochem. 2018 Aug;119(8):6914-6925
pubmed: 29744931
Curr Opin Cell Biol. 2018 Jun;52:154-161
pubmed: 29723661
J Cell Biol. 1996 Dec;135(6 Pt 1):1457-70
pubmed: 8978815
Methods Mol Biol. 2012;832:125-32
pubmed: 22350880
Methods Enzymol. 2019;618:229-256
pubmed: 30850054
J Cell Sci. 2014 Nov 15;127(Pt 22):4883-93
pubmed: 25271057
Nat Protoc. 2014 Jan;9(1):120-37
pubmed: 24356771
Proc Natl Acad Sci U S A. 2014 Dec 9;111(49):E5282-91
pubmed: 25422469
Biotechnol Bioeng. 2015 Apr;112(4):652-8
pubmed: 25333792
J Biol Chem. 2012 Dec 14;287(51):42611-9
pubmed: 23095757
Mol Cell Proteomics. 2015 Apr;14(4):1137-47
pubmed: 25648531
Carcinogenesis. 2014 Apr;35(4):923-34
pubmed: 24325913
Methods Mol Biol. 2012;832:93-110
pubmed: 22350878
Arch Biochem Biophys. 2011 May 15;509(2):164-9
pubmed: 21396347

Auteurs

Annette Aichem (A)

Biotechnology Institute Thurgau at the University of Konstanz, CH-8280, Kreuzlingen, Switzerland. Annette.Aichem@bitg.ch.
Department of Biology, Division of Immunology, University of Konstanz, D-78457, Konstanz, Germany. Annette.Aichem@bitg.ch.

Carolin Sailer (C)

Department of Biology, University of Konstanz, D-78457, Konstanz, Germany.

Stella Ryu (S)

Biotechnology Institute Thurgau at the University of Konstanz, CH-8280, Kreuzlingen, Switzerland.
Department of Biology, Division of Immunology, University of Konstanz, D-78457, Konstanz, Germany.

Nicola Catone (N)

Biotechnology Institute Thurgau at the University of Konstanz, CH-8280, Kreuzlingen, Switzerland.

Nicolas Stankovic-Valentin (N)

Zentrum für Molekulare Biologie der Universität Heidelberg, DKFZ-ZMBH Alliance, D-69120, Heidelberg, Germany.

Gunter Schmidtke (G)

Department of Biology, Division of Immunology, University of Konstanz, D-78457, Konstanz, Germany.

Frauke Melchior (F)

Zentrum für Molekulare Biologie der Universität Heidelberg, DKFZ-ZMBH Alliance, D-69120, Heidelberg, Germany.

Florian Stengel (F)

Department of Biology, University of Konstanz, D-78457, Konstanz, Germany.

Marcus Groettrup (M)

Biotechnology Institute Thurgau at the University of Konstanz, CH-8280, Kreuzlingen, Switzerland.
Department of Biology, Division of Immunology, University of Konstanz, D-78457, Konstanz, Germany.

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Classifications MeSH