Ataxin-3 Links NOD2 and TLR2 Mediated Innate Immune Sensing and Metabolism in Myeloid Cells.


Journal

Frontiers in immunology
ISSN: 1664-3224
Titre abrégé: Front Immunol
Pays: Switzerland
ID NLM: 101560960

Informations de publication

Date de publication:
2019
Historique:
received: 02 04 2019
accepted: 14 06 2019
entrez: 6 8 2019
pubmed: 6 8 2019
medline: 23 10 2020
Statut: epublish

Résumé

The interplay between NOD2 and TLR2 following recognition of components of the bacterial cell wall peptidoglycan is well-established, however their role in redirecting metabolic pathways in myeloid cells to degrade pathogens and mount antigen presentation remains unclear. We show NOD2 and TLR2 mediate phosphorylation of the deubiquitinase ataxin-3 via RIPK2 and TBK1. In myeloid cells ataxin-3 associates with the mitochondrial cristae protein MIC60, and is required for oxidative phosphorylation. Depletion of ataxin-3 leads to impaired induction of mitochondrial reactive oxygen species (mROS) and defective bacterial killing. A mass spectrometry analysis of NOD2/TLR2 triggered ataxin-3 deubiquitination targets revealed immunometabolic regulators, including HIF-1α and LAMTOR1 that may contribute to these effects. Thus, we define how ataxin-3 plays an essential role in NOD2 and TLR2 sensing and effector functions in myeloid cells.

Identifiants

pubmed: 31379806
doi: 10.3389/fimmu.2019.01495
pmc: PMC6659470
doi:

Substances chimiques

NOD2 protein, human 0
Nod2 Signaling Adaptor Protein 0
Reactive Oxygen Species 0
TLR2 protein, human 0
Toll-Like Receptor 2 0
Protein Serine-Threonine Kinases EC 2.7.11.1
RIPK2 protein, human EC 2.7.11.1
Receptor-Interacting Protein Serine-Threonine Kinase 2 EC 2.7.11.1
TBK1 protein, human EC 2.7.11.1
Ataxin-3 EC 3.4.19.12

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

1495

Subventions

Organisme : Department of Health
ID : NIHR-RP-R3-12-026
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_UU_00008/7
Pays : United Kingdom
Organisme : Medical Research Council
ID : G0501068
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_UU_12010/7
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/S036377/1
Pays : United Kingdom

Références

Immunity. 1999 Jan;10(1):29-38
pubmed: 10023768
Nature. 2001 May 31;411(6837):599-603
pubmed: 11385576
Nature. 2001 May 31;411(6837):603-6
pubmed: 11385577
Nature. 2002 Mar 14;416(6877):194-9
pubmed: 11894098
J Biol Chem. 2002 Nov 22;277(47):45004-12
pubmed: 12297501
J Biol Chem. 2003 Mar 14;278(11):8869-72
pubmed: 12527755
Cell. 2003 Mar 7;112(5):645-57
pubmed: 12628185
Cell Cycle. 2003 May-Jun;2(3):192-3
pubmed: 12734422
Proc Natl Acad Sci U S A. 2005 Mar 22;102(12):4330-5
pubmed: 15767577
J Immunol. 2005 May 15;174(10):6518-23
pubmed: 15879155
Lancet. 2005 May 21-27;365(9473):1794-6
pubmed: 15910952
J Clin Invest. 2005 Jul;115(7):1806-15
pubmed: 16007254
Proc Natl Acad Sci U S A. 2005 Jul 26;102(30):10493-8
pubmed: 16020535
Proc Natl Acad Sci U S A. 2005 Sep 6;102(36):12700-5
pubmed: 16118278
Hum Mol Genet. 2006 Aug 15;15(16):2409-20
pubmed: 16822850
J Immunol. 2007 Jun 15;178(12):7516-9
pubmed: 17548584
J Neurosci. 2007 Jul 4;27(27):7310-7
pubmed: 17611283
EMBO J. 2008 Jan 23;27(2):373-83
pubmed: 18079694
Drug Discov Today. 2008 Mar;13(5-6):268-74
pubmed: 18342804
J Biol Chem. 2008 Sep 26;283(39):26436-43
pubmed: 18599482
Biochem J. 2009 Jan 1;417(1):1-13
pubmed: 19061483
EMBO J. 2009 Mar 4;28(5):477-89
pubmed: 19177150
Biopolymers. 2009 Dec;91(12):1203-14
pubmed: 19382171
Annu Rev Biochem. 2009;78:363-97
pubmed: 19489724
EMBO Rep. 2009 Nov;10(11):1250-8
pubmed: 19798103
Genome Biol. 2009;10(11):R130
pubmed: 19919682
Nat Med. 2010 Jan;16(1):90-7
pubmed: 19966812
Cell. 2010 Mar 19;140(6):805-20
pubmed: 20303872
Blood. 2010 Jun 10;115(23):4742-9
pubmed: 20351312
Cell. 2010 Apr 16;141(2):290-303
pubmed: 20381137
PLoS One. 2010 Jun 08;5(6):e10977
pubmed: 20544018
Nature. 2011 Apr 28;472(7344):476-80
pubmed: 21525932
J Inherit Metab Dis. 2011 Aug;34(4):941-51
pubmed: 21541724
Science. 2011 Jul 8;333(6039):228-33
pubmed: 21617041
Handb Clin Neurol. 2012;103:437-49
pubmed: 21827905
Mol Cell. 2011 Oct 21;44(2):325-40
pubmed: 21906983
Dev Cell. 2011 Oct 18;21(4):694-707
pubmed: 21944719
EMBO J. 2011 Oct 18;30(21):4356-70
pubmed: 22009199
Science. 2011 Nov 4;334(6056):678-83
pubmed: 22053050
Immunity. 2012 Jan 27;36(1):68-78
pubmed: 22206904
Biochem Biophys Res Commun. 2012 Jan 27;417(4):1151-7
pubmed: 22227194
Protein Cell. 2012 Sep;3(9):675-90
pubmed: 22802047
Mol Biol Cell. 2012 Oct;23(20):3948-56
pubmed: 22918945
Cell. 2012 Sep 14;150(6):1196-208
pubmed: 22980980
Immunity. 2013 Sep 19;39(3):521-36
pubmed: 24054330
Mol Neurobiol. 2014 Jun;49(3):1513-31
pubmed: 24293103
Nat Rev Immunol. 2014 Jan;14(1):9-23
pubmed: 24336102
Nature. 2014 Jan 23;505(7484):550-554
pubmed: 24336208
Gut Microbes. 2014 May-Jun;5(3):340-4
pubmed: 24637801
Nat Rev Immunol. 2014 Jul;14(7):463-77
pubmed: 24962261
Cell Metab. 2014 Sep 2;20(3):526-40
pubmed: 25002183
Front Immunol. 2014 Jul 10;5:317
pubmed: 25071778
Nat Immunol. 2014 Sep;15(9):846-55
pubmed: 25086775
Front Immunol. 2014 Sep 25;5:461
pubmed: 25309543
Immunity. 2014 Oct 16;41(4):518-28
pubmed: 25367569
Nucleic Acids Res. 2015 Jan;43(Database issue):D512-20
pubmed: 25514926
PLoS Genet. 2015 Jan 15;11(1):e1004834
pubmed: 25590633
Sci Rep. 2015 Jan 23;5:7990
pubmed: 25612828
Science. 2015 Jan 23;347(6220):1260419
pubmed: 25613900
PLoS Genet. 2015 Jan 29;11(1):e1004749
pubmed: 25633985
Osteoarthritis Cartilage. 2015 Sep;23(9):1575-85
pubmed: 25917637
Hum Mol Genet. 2015 Aug 1;24(15):4429-42
pubmed: 25972374
Cell Death Differ. 2016 Mar;23(3):380-92
pubmed: 26250910
Chem Biol. 2015 Sep 17;22(9):1174-84
pubmed: 26320862
J Exp Med. 2016 Jan 11;213(1):15-23
pubmed: 26694970
Nat Rev Immunol. 2016 Jan;16(1):35-50
pubmed: 26711677
Sci Rep. 2016 Feb 02;6:20295
pubmed: 26830977
Cell Res. 2016 Apr;26(4):399-422
pubmed: 27012465
Cell Res. 2016 Apr;26(4):457-83
pubmed: 27012466
Nat Immunol. 2016 Sep;17(9):1037-1045
pubmed: 27348412
Nat Rev Immunol. 2016 Sep;16(9):553-65
pubmed: 27396447
Methods Mol Biol. 2016;1449:161-75
pubmed: 27613034
Methods Mol Biol. 2016;1449:177-92
pubmed: 27613035
Semin Immunol. 2016 Oct;28(5):469-477
pubmed: 27717536
Nat Commun. 2016 Oct 12;7:13130
pubmed: 27731330
J Proteome Res. 2017 Mar 3;16(3):1288-1299
pubmed: 28164708
Nature. 2017 May 4;545(7652):108-111
pubmed: 28445460
Brain. 2017 Nov 1;140(11):2860-2878
pubmed: 29053796
Mol Immunol. 2017 Nov 29;:null
pubmed: 29198621
Front Med (Lausanne). 2018 Feb 19;5:32
pubmed: 29515999
J Immunol. 2018 Jul 15;201(2):675-687
pubmed: 29802126
Nat Immunol. 2018 Sep;19(9):942-953
pubmed: 30111894
Nat Genet. 1994 Nov;8(3):221-8
pubmed: 7874163

Auteurs

Thomas P Chapman (TP)

MRC Human Immunology Unit, MRC Weatherall Institute of Molecular Medicine, John Radcliffe Hospital, University of Oxford, Oxford, United Kingdom.

Daniele Corridoni (D)

MRC Human Immunology Unit, MRC Weatherall Institute of Molecular Medicine, John Radcliffe Hospital, University of Oxford, Oxford, United Kingdom.

Seiji Shiraishi (S)

MRC Human Immunology Unit, MRC Weatherall Institute of Molecular Medicine, John Radcliffe Hospital, University of Oxford, Oxford, United Kingdom.

Sumeet Pandey (S)

Translational Gastroenterology Unit, John Radcliffe Hospital, University of Oxford, Oxford, United Kingdom.

Anna Aulicino (A)

MRC Human Immunology Unit, MRC Weatherall Institute of Molecular Medicine, John Radcliffe Hospital, University of Oxford, Oxford, United Kingdom.

Simon Wigfield (S)

Department of Oncology, University of Oxford, Oxford, United Kingdom.

Maria do Carmo Costa (M)

Department of Neurology, University of Michigan, Ann Arbor, MI, United States.

Marie-Laëtitia Thézénas (ML)

Nuffield Department of Medicine, Target Discovery Institute, University of Oxford, Oxford, United Kingdom.

Henry Paulson (H)

Department of Neurology, University of Michigan, Ann Arbor, MI, United States.

Roman Fischer (R)

Nuffield Department of Medicine, Target Discovery Institute, University of Oxford, Oxford, United Kingdom.

Benedikt M Kessler (BM)

Nuffield Department of Medicine, Target Discovery Institute, University of Oxford, Oxford, United Kingdom.

Alison Simmons (A)

MRC Human Immunology Unit, MRC Weatherall Institute of Molecular Medicine, John Radcliffe Hospital, University of Oxford, Oxford, United Kingdom.

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