Ribosome-Targeting Antibiotics Impair T Cell Effector Function and Ameliorate Autoimmunity by Blocking Mitochondrial Protein Synthesis.


Journal

Immunity
ISSN: 1097-4180
Titre abrégé: Immunity
Pays: United States
ID NLM: 9432918

Informations de publication

Date de publication:
12 01 2021
Historique:
received: 10 11 2019
revised: 16 09 2020
accepted: 03 11 2020
pubmed: 26 11 2020
medline: 10 9 2021
entrez: 25 11 2020
Statut: ppublish

Résumé

While antibiotics are intended to specifically target bacteria, most are known to affect host cell physiology. In addition, some antibiotic classes are reported as immunosuppressive for reasons that remain unclear. Here, we show that Linezolid, a ribosomal-targeting antibiotic (RAbo), effectively blocked the course of a T cell-mediated autoimmune disease. Linezolid and other RAbos were strong inhibitors of T helper-17 cell effector function in vitro, showing that this effect was independent of their antibiotic activity. Perturbing mitochondrial translation in differentiating T cells, either with RAbos or through the inhibition of mitochondrial elongation factor G1 (mEF-G1) progressively compromised the integrity of the electron transport chain. Ultimately, this led to deficient oxidative phosphorylation, diminishing nicotinamide adenine dinucleotide concentrations and impairing cytokine production in differentiating T cells. In accordance, mice lacking mEF-G1 in T cells were protected from experimental autoimmune encephalomyelitis, demonstrating that this pathway is crucial in maintaining T cell function and pathogenicity.

Identifiants

pubmed: 33238133
pii: S1074-7613(20)30466-0
doi: 10.1016/j.immuni.2020.11.001
pmc: PMC7837214
mid: NIHMS1668683
pii:
doi:

Substances chimiques

Anti-Bacterial Agents 0
Mitochondrial Proteins 0
Peptide Elongation Factor G 0
Peptides, Cyclic 0
argyrin c 0
NAD 0U46U6E8UK
Linezolid ISQ9I6J12J

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

68-83.e6

Subventions

Organisme : NIAID NIH HHS
ID : P01 AI056299
Pays : United States
Organisme : NCI NIH HHS
ID : P01 CA065493
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL118979
Pays : United States
Organisme : NIAID NIH HHS
ID : R37 AI034495
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL155114
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL056067
Pays : United States
Organisme : Wellcome Trust
Pays : United Kingdom

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2020 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Interests The authors declare no competing interests.

Références

J Antibiot (Tokyo). 2002 Jun;55(6):543-51
pubmed: 12195959
Nature. 2013 May 23;497(7450):451-7
pubmed: 23698443
J Am Board Fam Med. 2008 Jul-Aug;21(4):261-8
pubmed: 18612052
Clin Infect Dis. 2009 Jan 15;48(2):203-12
pubmed: 19072714
Int J Mol Sci. 2017 Dec 08;18(12):
pubmed: 29292737
Cancer Cell. 2011 Nov 15;20(5):674-88
pubmed: 22094260
Genes Dev. 2018 Oct 1;32(19-20):1285-1296
pubmed: 30275044
Cold Spring Harb Perspect Biol. 2012 May 01;4(5):
pubmed: 22550233
Cell Metab. 2015 Sep 1;22(3):485-98
pubmed: 26299452
Nat Rev Microbiol. 2010 Jun;8(6):423-35
pubmed: 20440275
Genomics. 2001 May 15;74(1):109-14
pubmed: 11374907
Nature. 2019 Jul;571(7765):403-407
pubmed: 31217581
Semin Immunol. 2016 Oct;28(5):514-524
pubmed: 27825556
Cell Rep. 2019 Jul 2;28(1):159-171.e4
pubmed: 31269437
Cell. 2019 Sep 5;178(6):1313-1328.e13
pubmed: 31491384
PLoS Biol. 2013 Oct;11(10):e1001674
pubmed: 24115907
Diagn Microbiol Infect Dis. 2002 May;43(1):65-73
pubmed: 12052631
Science. 2016 Apr 29;352(6285):535-8
pubmed: 27126035
Hum Mol Genet. 2013 Mar 15;22(6):1132-9
pubmed: 23223015
Mol Cell. 2007 May 11;26(3):393-402
pubmed: 17499045
Med Clin (Barc). 2017 Oct 23;149(8):369
pubmed: 28571952
Cold Spring Harb Perspect Biol. 2010 May;2(5):a000414
pubmed: 20452953
Cell Metab. 2017 Jun 6;25(6):1254-1268.e7
pubmed: 28591633
FEBS Lett. 2005 Nov 21;579(28):6423-7
pubmed: 16271719
Lancet. 1963 Apr 13;1(7285):785-9
pubmed: 13990765
J Immunol. 2009 Nov 15;183(10):6041-50
pubmed: 19841183
Am J Cancer Res. 2017 Dec 01;7(12):2395-2405
pubmed: 29312795
Antimicrob Agents Chemother. 2004 Jan;48(1):281-4
pubmed: 14693551
Toxicol Appl Pharmacol. 2004 Apr 1;196(1):68-79
pubmed: 15050409
Blood. 2017 Feb 9;129(6):729-739
pubmed: 27879260
Nat Immunol. 2003 Apr;4(4):330-6
pubmed: 12612578
Cell Metab. 2016 Jul 12;24(1):104-17
pubmed: 27411012
Genome Biol. 2016 May 12;17:103
pubmed: 27176874
Mitochondrion. 2007 Dec;7(6):374-85
pubmed: 17890163
Int Immunol. 2001 Jul;13(7):921-31
pubmed: 11431422
J Immunol. 2000 Nov 1;165(9):5017-26
pubmed: 11046030
Immunity. 2013 Feb 21;38(2):225-36
pubmed: 23415911
Drugs. 2001;61(4):525-51
pubmed: 11324682
Nature. 2011 Jun 15;474(7351):337-42
pubmed: 21677750
BMC Med Genet. 2015 Feb 04;16:3
pubmed: 25650108
Allergy Asthma Clin Immunol. 2015 Jan 09;11(1):1
pubmed: 25784943
Oncotarget. 2015 Mar 10;6(7):4569-84
pubmed: 25625193
Biochim Biophys Acta Mol Basis Dis. 2017 Jun;1863(6):1539-1555
pubmed: 28215579
PLoS One. 2012;7(9):e42657
pubmed: 22970117
Prim Care Companion J Clin Psychiatry. 2009;11(6):353-6
pubmed: 20098528
Cell. 2016 Jun 30;166(1):63-76
pubmed: 27293185
PLoS One. 2014 May 07;9(5):e96566
pubmed: 24804722
Eur J Hum Genet. 2012 Jun;20(6):607-12
pubmed: 22317974
Cell. 2013 Jun 6;153(6):1239-51
pubmed: 23746840
Mol Cell. 2009 Aug 28;35(4):502-10
pubmed: 19716793
Biochem Soc Trans. 2003 Dec;31(Pt 6):1143-51
pubmed: 14641014
Eukaryot Cell. 2005 Dec;4(12):2078-86
pubmed: 16339725
Nat Methods. 2008 Jul;5(7):621-8
pubmed: 18516045
Redox Biol. 2017 Oct;13:244-254
pubmed: 28600981
J Clin Invest. 2014 Jul;124(7):2836-40
pubmed: 24983424
Am J Dig Dis. 1975 Apr;20(4):295-7
pubmed: 1130357
J Lab Clin Med. 1973 May;81(5):713-8
pubmed: 4698658
Eur J Immunol. 2011 Mar;41(3):833-44
pubmed: 21287545
Front Immunol. 2018 Mar 13;9:302
pubmed: 29593707
Sci Rep. 2018 Sep 21;8(1):14190
pubmed: 30242167
Eur J Biochem. 1999 May;262(1):108-16
pubmed: 10231371
Cell. 2016 Oct 6;167(2):471-483.e10
pubmed: 27693358
Naunyn Schmiedebergs Arch Pharmacol. 1975;290(2-3):161-73
pubmed: 171591
Medicine (Baltimore). 2018 Sep;97(36):e12114
pubmed: 30200095
Chem Biol Drug Des. 2014 Jul;84(1):99-107
pubmed: 24521156
J Exp Med. 2003 Dec 15;198(12):1875-86
pubmed: 14676299
Mayo Clin Proc. 1999 Apr;74(4):420-34
pubmed: 10221472
Front Immunol. 2019 Jun 14;10:1374
pubmed: 31258540
Cancer Lett. 2017 Jul 28;399:20-28
pubmed: 28408354
Cell. 2016 Jun 30;166(1):9-10
pubmed: 27368094
Cell Rep. 2015 Mar 17;10(10):1681-1691
pubmed: 25772356
Cell. 2015 Jul 30;162(3):552-63
pubmed: 26232225
Cancer Cell. 2008 Jul 8;14(1):23-35
pubmed: 18598941
Drug Saf. 2008;31(9):753-68
pubmed: 18707190
Pharmacogenomics. 2010 Sep;11(9):1185-7
pubmed: 20860455
Drug Des Devel Ther. 2018 Jun 18;12:1759-1767
pubmed: 29950810
J Biol Chem. 1998 Sep 4;273(36):22983-9
pubmed: 9722521
Cell Metab. 2020 Apr 7;31(4):809-821.e6
pubmed: 32187526
Antimicrob Agents Chemother. 2006 Jun;50(6):2042-9
pubmed: 16723564
Immunity. 2011 Dec 23;35(6):871-82
pubmed: 22195744
Protein Expr Purif. 2004 Oct;37(2):368-76
pubmed: 15358359
Science. 2020 Jun 19;368(6497):1371-1376
pubmed: 32439659

Auteurs

Luís Almeida (L)

Institute of Infection Immunology, TWINCORE, Center for Experimental and Clinical Infection Research, Hannover Medical School and the Helmholtz Center for Infection Research, Hannover 30625, Germany; Institute of Medical Microbiology and Hygiene, University Medical Center of the Johannes Gutenberg-University, Mainz 55131, Germany.

Ayesha Dhillon-LaBrooy (A)

Institute of Infection Immunology, TWINCORE, Center for Experimental and Clinical Infection Research, Hannover Medical School and the Helmholtz Center for Infection Research, Hannover 30625, Germany; Institute of Medical Microbiology and Hygiene, University Medical Center of the Johannes Gutenberg-University, Mainz 55131, Germany.

Carla N Castro (CN)

Institute of Infection Immunology, TWINCORE, Center for Experimental and Clinical Infection Research, Hannover Medical School and the Helmholtz Center for Infection Research, Hannover 30625, Germany.

Nigatu Adossa (N)

QIAGEN, Aarhus C 8000, Denmark; University of Turku, Computational Biomedicine, Turku Center for Biotechnology, Turku 20520, Finland.

Guilhermina M Carriche (GM)

Institute of Infection Immunology, TWINCORE, Center for Experimental and Clinical Infection Research, Hannover Medical School and the Helmholtz Center for Infection Research, Hannover 30625, Germany; Institute of Medical Microbiology and Hygiene, University Medical Center of the Johannes Gutenberg-University, Mainz 55131, Germany.

Melanie Guderian (M)

Institute of Infection Immunology, TWINCORE, Center for Experimental and Clinical Infection Research, Hannover Medical School and the Helmholtz Center for Infection Research, Hannover 30625, Germany.

Saskia Lippens (S)

VIB Imaging Core Facility Gent, Gent 9052, Belgium.

Sven Dennerlein (S)

Department of Cellular Biochemistry, University Medical Center, Göttingen 37073, Germany.

Christina Hesse (C)

Fraunhofer Institute for Toxicology and Experimental Medicine (ITEM), Hannover 30625, Germany.

Bart N Lambrecht (BN)

VIB-UGent, Center for Inflammation Research, Gent 9052, Belgium.

Luciana Berod (L)

Institute of Infection Immunology, TWINCORE, Center for Experimental and Clinical Infection Research, Hannover Medical School and the Helmholtz Center for Infection Research, Hannover 30625, Germany; Institute of Molecular Medicine, University Medical Center of the Johannes Gutenberg-University Mainz, Mainz, Germany.

Leif Schauser (L)

QIAGEN, Aarhus C 8000, Denmark.

Bruce R Blazar (BR)

Department of Pediatrics, Division of Blood and Marrow Transplantation, University of Minnesota, Minneapolis, MN 55454, USA.

Markus Kalesse (M)

Institute for Organic Chemistry, Leibniz University Hannover, Hannover, Germany; Helmholtz Center for Infection Research (HZI), Braunschweig 38124, Germany.

Rolf Müller (R)

Helmholtz Institute for Pharmaceutical Research, Helmholtz Center for Infection Research and Department of Pharmaceutical Biotechnology, Saarland University, Saarbrücken 66123, Germany.

Luís F Moita (LF)

Innate Immunity and Inflammation Laboratory, Instituto Gulbenkian de Ciência, Oeiras, Portugal.

Tim Sparwasser (T)

Institute of Infection Immunology, TWINCORE, Center for Experimental and Clinical Infection Research, Hannover Medical School and the Helmholtz Center for Infection Research, Hannover 30625, Germany; Institute of Medical Microbiology and Hygiene, University Medical Center of the Johannes Gutenberg-University, Mainz 55131, Germany. Electronic address: sparwasser.office@uni-mainz.de.

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