Regulation of Phosphoribosyl-Linked Serine Ubiquitination by Deubiquitinases DupA and DupB.

A549 Cells Bacterial Proteins / metabolism Catalytic Domain / physiology Cell Line Cell Line, Tumor Deubiquitinating Enzymes / metabolism Endoplasmic Reticulum / metabolism HEK293 Cells HeLa Cells Host-Pathogen Interactions / physiology Humans Legionella pneumophila / pathogenicity Legionnaires' Disease / metabolism Serine / metabolism Ubiquitin / metabolism Ubiquitination / physiology Vacuoles / metabolism
ADP-ribosylation ER-fragmentation Legionella pneumophila SdeA deubiquitinase deubiquitination endoplasmic reticulum phosphodiesterase phosphoribosyl serine ubiquitination

Journal

Molecular cell
ISSN: 1097-4164
Titre abrégé: Mol Cell
Pays: United States
ID NLM: 9802571

Informations de publication

Date de publication:
02 01 2020
Historique:
received: 06 06 2019
revised: 07 09 2019
accepted: 11 10 2019
pubmed: 17 11 2019
medline: 28 3 2020
entrez: 17 11 2019
Statut: ppublish

Résumé

The family of bacterial SidE enzymes catalyzes non-canonical phosphoribosyl-linked (PR) serine ubiquitination and promotes infectivity of Legionella pneumophila. Here, we describe identification of two bacterial effectors that reverse PR ubiquitination and are thus named deubiquitinases for PR ubiquitination (DUPs; DupA and DupB). Structural analyses revealed that DupA and SidE ubiquitin ligases harbor a highly homologous catalytic phosphodiesterase (PDE) domain. However, unlike SidE ubiquitin ligases, DupA displays increased affinity to PR-ubiquitinated substrates, which allows DupA to cleave PR ubiquitin from substrates. Interfering with DupA-ubiquitin binding switches its activity toward SidE-type ligase. Given the high affinity of DupA to PR-ubiquitinated substrates, we exploited a catalytically inactive DupA mutant to trap and identify more than 180 PR-ubiquitinated host proteins in Legionella-infected cells. Proteins involved in endoplasmic reticulum (ER) fragmentation and membrane recruitment to Legionella-containing vacuoles (LCV) emerged as major SidE targets. The global map of PR-ubiquitinated substrates provides critical insights into host-pathogen interactions during Legionella infection.

Identifiants

DOI: 10.1016/j.molcel.2019.10.019 PMID: 31732457 PMC: PMC6941232
pubmed: 31732457
pii: S1097-2765(19)30797-X
doi: 10.1016/j.molcel.2019.10.019
pmc: PMC6941232
pii:
doi:

Substances chimiques

Bacterial Proteins 0
Ubiquitin 0
Serine 452VLY9402
Deubiquitinating Enzymes EC 3.4.19.12

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

Pagination

164-179.e6

Subventions

Organisme : European Research Council
ID : 742720
Pays : International
Organisme : NIAID NIH HHS
ID : R01 AI127465
Pays : United States

Informations de copyright

Copyright © 2019 The Authors. Published by Elsevier Inc. All rights reserved.

Références

Autophagy. 2016 Jun 2;12(6):1053-4
pubmed: 27191778
EMBO Rep. 2017 Oct;18(10):1817-1836
pubmed: 28835546
EMBO Rep. 2010 Oct;11(10):791-7
pubmed: 20798673
Biophys J. 2007 Jun 1;92(11):3817-29
pubmed: 17351000
PLoS One. 2011;6(7):e21800
pubmed: 21789182
Cell. 2018 May 17;173(5):1231-1243.e16
pubmed: 29731171
Nat Cell Biol. 2016 May 27;18(6):579-86
pubmed: 27230526
Nat Commun. 2017 May 15;8:15406
pubmed: 28504273
Mol Cell. 2019 Jun 6;74(5):909-921.e6
pubmed: 31006538
Nat Genet. 2016 Feb;48(2):167-75
pubmed: 26752266
Nature. 2019 Aug;572(7769):382-386
pubmed: 31330532
Elife. 2016 Sep 13;5:
pubmed: 27619977
Mol Microbiol. 2009 Jul;73(2):141-51
pubmed: 19508287
Phys Chem Chem Phys. 2010 Jul 28;12(28):7821-39
pubmed: 20574571
Acta Crystallogr D Biol Crystallogr. 2011 Apr;67(Pt 4):235-42
pubmed: 21460441
Nature. 2019 Aug;572(7769):387-391
pubmed: 31330531
J Mol Graph. 1996 Feb;14(1):33-8, 27-8
pubmed: 8744570
J Mol Model. 2006 Feb;12(3):281-9
pubmed: 16240095
BMC Bioinformatics. 2006 Aug 16;7:382
pubmed: 16914055
Nat Commun. 2019 May 30;10(1):2370
pubmed: 31147549
J Chem Theory Comput. 2015 Aug 11;11(8):3696-713
pubmed: 26574453
Mol Microbiol. 2018 Feb;107(4):455-471
pubmed: 29235173
Proteins. 2015 Dec;83(12):2319-25
pubmed: 26426142
Cell Microbiol. 2006 May;8(5):793-805
pubmed: 16611228
J Biomed Biotechnol. 2009;2009:591923
pubmed: 20182554
Cell. 2016 Dec 1;167(6):1636-1649.e13
pubmed: 27912065
Infect Immun. 2010 Sep;78(9):3905-19
pubmed: 20547746
J Chem Theory Comput. 2011 Sep 13;7(9):2886-2902
pubmed: 21921995
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
Nat Rev Microbiol. 2013 May;11(5):316-26
pubmed: 23588250
Cell Res. 2016 Apr;26(4):499-510
pubmed: 26964724
Science. 2008 Nov 14;322(5904):1104-7
pubmed: 18832610
Mol Cell. 2019 Jun 6;74(5):891-908.e10
pubmed: 31006537
Structure. 2015 Aug 4;23(8):1459-1469
pubmed: 26146184
Nature. 2018 May;557(7707):734-738
pubmed: 29795347
Nature. 2018 May;557(7707):729-733
pubmed: 29795346
Proc Natl Acad Sci U S A. 2004 Jan 20;101(3):841-6
pubmed: 14715899
Cell Rep. 2017 Nov 21;21(8):2031-2038
pubmed: 29166595
Methods Mol Biol. 2017;1654:39-54
pubmed: 28986782
Cell Res. 2017 Jul;27(7):865-881
pubmed: 28497808
Acta Crystallogr D Biol Crystallogr. 2010 Apr;66(Pt 4):486-501
pubmed: 20383002
Mol Microbiol. 2005 Apr;56(1):90-103
pubmed: 15773981
Nat Commun. 2012;3:1014
pubmed: 22910360
Protein Expr Purif. 1999 Feb;15(1):34-9
pubmed: 10024467
Acta Crystallogr D Biol Crystallogr. 2012 Apr;68(Pt 4):352-67
pubmed: 22505256
Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2126-32
pubmed: 15572765
Science. 2019 May 24;364(6442):787-792
pubmed: 31123136
Int J Med Microbiol. 2018 Jan;308(1):49-57
pubmed: 28865995
Acta Crystallogr D Biol Crystallogr. 2010 Feb;66(Pt 2):213-21
pubmed: 20124702
Nat Protoc. 2019 Mar;14(3):703-721
pubmed: 30804569
Nature. 2018 May;557(7707):674-678
pubmed: 29795342
Acta Crystallogr D Biol Crystallogr. 2010 Feb;66(Pt 2):125-32
pubmed: 20124692
Annu Rev Biochem. 2017 Jun 20;86:193-224
pubmed: 28460188
Elife. 2017 Jun 15;6:
pubmed: 28617241
Trends Biochem Sci. 1998 Dec;23(12):469-72
pubmed: 9868367
Nucleic Acids Res. 2016 Jul 8;44(W1):W410-5
pubmed: 27131380
Cell Host Microbe. 2017 Feb 8;21(2):169-181
pubmed: 28041930
BMC Biol. 2018 Nov 1;16(1):131
pubmed: 30382915
Elife. 2017 Oct 02;6:
pubmed: 28968219
Science. 2012 Nov 23;338(6110):1072-6
pubmed: 23112293
Mol Microbiol. 2008 Mar;67(6):1307-19
pubmed: 18284575
Nature. 2015 Jun 18;522(7556):354-8
pubmed: 26040720
J Appl Crystallogr. 2007 Aug 1;40(Pt 4):658-674
pubmed: 19461840
Nat Rev Microbiol. 2017 Oct;15(10):591-605
pubmed: 28713154
Nat Rev Mol Cell Biol. 2019 Jun;20(6):338-352
pubmed: 30733604
Nature. 2009 Mar 26;458(7237):422-9
pubmed: 19325621
Infect Immun. 1995 Sep;63(9):3609-20
pubmed: 7642298
Nature. 2016 May 5;533(7601):120-4
pubmed: 27049943

Auteurs

Donghyuk Shin (D)

Institute of Biochemistry II, Faculty of Medicine, Goethe University Frankfurt, Theodor-Stern-Kai 7, 60590 Frankfurt am Main, Germany; Buchmann Institute for Molecular Life Sciences, Goethe University Frankfurt, Max-von-Laue-Str. 15, 60438 Frankfurt am Main, Germany; Max Planck Institute of Biophysics, Max-von-Laue-Str. 3, 60438 Frankfurt am Main, Germany.

Rukmini Mukherjee (R)

Institute of Biochemistry II, Faculty of Medicine, Goethe University Frankfurt, Theodor-Stern-Kai 7, 60590 Frankfurt am Main, Germany; Buchmann Institute for Molecular Life Sciences, Goethe University Frankfurt, Max-von-Laue-Str. 15, 60438 Frankfurt am Main, Germany.

Yaobin Liu (Y)

Institute of Biochemistry II, Faculty of Medicine, Goethe University Frankfurt, Theodor-Stern-Kai 7, 60590 Frankfurt am Main, Germany; Buchmann Institute for Molecular Life Sciences, Goethe University Frankfurt, Max-von-Laue-Str. 15, 60438 Frankfurt am Main, Germany.

Alexis Gonzalez (A)

Institute of Biochemistry II, Faculty of Medicine, Goethe University Frankfurt, Theodor-Stern-Kai 7, 60590 Frankfurt am Main, Germany; Buchmann Institute for Molecular Life Sciences, Goethe University Frankfurt, Max-von-Laue-Str. 15, 60438 Frankfurt am Main, Germany.

Florian Bonn (F)

Institute of Biochemistry II, Faculty of Medicine, Goethe University Frankfurt, Theodor-Stern-Kai 7, 60590 Frankfurt am Main, Germany.

Yan Liu (Y)

Purdue Institute of Immunology, Inflammation, and Infectious Diseases and Department of Biological Sciences, Purdue University, West Lafayette, IN 47907, USA.

Vladimir V Rogov (VV)

Institute of Biophysical Chemistry and Center for Biomolecular Magnetic Resonance and Cluster of Excellence Macromolecular Complexes (CEF), Goethe University, Frankfurt, Germany.

Marcel Heinz (M)

Max Planck Institute of Biophysics, Max-von-Laue-Str. 3, 60438 Frankfurt am Main, Germany; Institute of Biophysics, Goethe University Frankfurt, 60438 Frankfurt am Main, Germany.

Alexandra Stolz (A)

Institute of Biochemistry II, Faculty of Medicine, Goethe University Frankfurt, Theodor-Stern-Kai 7, 60590 Frankfurt am Main, Germany; Buchmann Institute for Molecular Life Sciences, Goethe University Frankfurt, Max-von-Laue-Str. 15, 60438 Frankfurt am Main, Germany.

Gerhard Hummer (G)

Max Planck Institute of Biophysics, Max-von-Laue-Str. 3, 60438 Frankfurt am Main, Germany; Institute of Biophysics, Goethe University Frankfurt, 60438 Frankfurt am Main, Germany.

Volker Dötsch (V)

Institute of Biophysical Chemistry and Center for Biomolecular Magnetic Resonance and Cluster of Excellence Macromolecular Complexes (CEF), Goethe University, Frankfurt, Germany.

Zhao-Qing Luo (ZQ)

Purdue Institute of Immunology, Inflammation, and Infectious Diseases and Department of Biological Sciences, Purdue University, West Lafayette, IN 47907, USA.

Sagar Bhogaraju (S)

Institute of Biochemistry II, Faculty of Medicine, Goethe University Frankfurt, Theodor-Stern-Kai 7, 60590 Frankfurt am Main, Germany; Buchmann Institute for Molecular Life Sciences, Goethe University Frankfurt, Max-von-Laue-Str. 15, 60438 Frankfurt am Main, Germany; European Molecular Biology Laboratory, 71 Avenue des Martyrs, 38000 Grenoble, France.

Ivan Dikic (I)

Institute of Biochemistry II, Faculty of Medicine, Goethe University Frankfurt, Theodor-Stern-Kai 7, 60590 Frankfurt am Main, Germany; Buchmann Institute for Molecular Life Sciences, Goethe University Frankfurt, Max-von-Laue-Str. 15, 60438 Frankfurt am Main, Germany; Max Planck Institute of Biophysics, Max-von-Laue-Str. 3, 60438 Frankfurt am Main, Germany. Electronic address: dikic@biochem2.uni-frankfurt.de.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female

Evaluation of Low-Value Services Across Major Medicare Advantage Insurers and Traditional Medicare.

Ciara Duggan, Adam L Beckman, Ishani Ganguli et al.
1.00
Humans United States Aged Cross-Sectional Studies Medicare Part C

Effectiveness of Virtual Yoga for Chronic Low Back Pain: A Randomized Clinical Trial.

Hallie Tankha, Devyn Gaskins, Amanda Shallcross et al.
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH

questionsmedicales.fr › Cellules › Cellules épithéliales › Cellules A549 › Regulation of Phosphoribosyl-Linked Serine...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines bactériennes › Regulation of Phosphoribosyl-Linked Serine...
questionsmedicales.fr › Phénomènes chimiques › Phénomènes biochimiques › Conformation moléculaire › Conformation des protéines › Éléments structuraux des protéines › Domaine catalytique › Regulation of Phosphoribosyl-Linked Serine...
questionsmedicales.fr › Cellules › Cellules cultivées › Lignée cellulaire › Regulation of Phosphoribosyl-Linked Serine...
questionsmedicales.fr › Cellules › Cellules cultivées › Cellules cancéreuses en culture › Lignée cellulaire tumorale › Regulation of Phosphoribosyl-Linked Serine...
questionsmedicales.fr › Enzymes et coenzymes › Enzymes › Enzymes de désubiquitinylation › Regulation of Phosphoribosyl-Linked Serine...
questionsmedicales.fr › Cellules › Structures cellulaires › Espace intracellulaire › Cytoplasme › Structures cytoplasmiques › Organites › Réticulum endoplasmique › Regulation of Phosphoribosyl-Linked Serine...
questionsmedicales.fr › Cellules › Cellules épithéliales › Cellules HEK293 › Regulation of Phosphoribosyl-Linked Serine...
questionsmedicales.fr › Cellules › Cellules épithéliales › Cellules HeLa › Regulation of Phosphoribosyl-Linked Serine...
questionsmedicales.fr › Phénomènes biologiques › Interactions hôte-microbes › Interactions hôte-pathogène › Regulation of Phosphoribosyl-Linked Serine...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Regulation of Phosphoribosyl-Linked Serine...
questionsmedicales.fr › Bactéries › Proteobacteria › Gammaproteobacteria › Legionellaceae › Legionella › Legionella pneumophila › Regulation of Phosphoribosyl-Linked Serine...
questionsmedicales.fr › Maladies de l'appareil respiratoire › Infections de l'appareil respiratoire › Légionellose › Maladie des légionnaires › Regulation of Phosphoribosyl-Linked Serine...
questionsmedicales.fr › Acides aminés, peptides et protéines › Acides aminés › Acides aminés neutres › Sérine › Regulation of Phosphoribosyl-Linked Serine...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Ubiquitines › Ubiquitine › Regulation of Phosphoribosyl-Linked Serine...
questionsmedicales.fr › Phénomènes génétiques › Régulation de l'expression des gènes › Modification traductionnelle des protéines › Maturation post-traductionnelle des protéines › Ubiquitination › Regulation of Phosphoribosyl-Linked Serine...
questionsmedicales.fr › Cellules › Structures cellulaires › Espace intracellulaire › Cytoplasme › Structures cytoplasmiques › Organites › Vésicules cytoplasmiques › Vacuoles › Regulation of Phosphoribosyl-Linked Serine...