Interferon-β acts directly on T cells to prolong allograft survival by enhancing regulatory T cell induction through Foxp3 acetylation.


Journal

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

Informations de publication

Date de publication:
08 03 2022
Historique:
received: 29 07 2020
revised: 18 06 2021
accepted: 13 01 2022
pubmed: 13 2 2022
medline: 6 5 2022
entrez: 12 2 2022
Statut: ppublish

Résumé

Type I interferons (IFNs) are pleiotropic cytokines with potent antiviral properties that also promote protective T cell and humoral immunity. Paradoxically, type I IFNs, including the widely expressed IFNβ, also have immunosuppressive properties, including promoting persistent viral infections and treating T-cell-driven, remitting-relapsing multiple sclerosis. Although associative evidence suggests that IFNβ mediates these immunosuppressive effects by impacting regulatory T (Treg) cells, mechanistic links remain elusive. Here, we found that IFNβ enhanced graft survival in a Treg-cell-dependent murine transplant model. Genetic conditional deletion models revealed that the extended allograft survival was Treg cell-mediated and required IFNβ signaling on T cells. Using an in silico computational model and analysis of human immune cells, we found that IFNβ directly promoted Treg cell induction via STAT1- and P300-dependent Foxp3 acetylation. These findings identify a mechanistic connection between the immunosuppressive effects of IFNβ and Treg cells, with therapeutic implications for transplantation, autoimmunity, and malignancy.

Identifiants

pubmed: 35148827
pii: S1074-7613(22)00040-1
doi: 10.1016/j.immuni.2022.01.011
pmc: PMC8917088
mid: NIHMS1781177
pii:
doi:

Substances chimiques

FOXP3 protein, human 0
Forkhead Transcription Factors 0
Foxp3 protein, mouse 0
Interferon-beta 77238-31-4

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

459-474.e7

Subventions

Organisme : NIAID NIH HHS
ID : R01 AI141710
Pays : United States

Informations de copyright

Copyright © 2022 Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Références

J Neuroimmunol. 2010 Jan 25;218(1-2):120-4
pubmed: 19932513
Front Immunol. 2018 May 15;9:1048
pubmed: 29868011
J Am Soc Nephrol. 2017 Aug;28(8):2377-2392
pubmed: 28302753
PLoS Genet. 2015 Jun 24;11(6):e1005251
pubmed: 26107960
J Exp Med. 2014 Aug 25;211(9):1905-18
pubmed: 25113973
Nat Rev Immunol. 2013 Jul;13(7):535-42
pubmed: 23743475
J Clin Invest. 2006 Dec;116(12):3252-7
pubmed: 17099776
J Interferon Cytokine Res. 2010 Oct;30(10):759-66
pubmed: 20874253
PLoS One. 2012;7(1):e29035
pubmed: 22247766
J Virol. 2006 Aug;80(16):8271-3
pubmed: 16873284
J Exp Med. 2012 Sep 24;209(10):1713-22, S1-19
pubmed: 22966003
Nat Med. 2010 Apr;16(4):406-12
pubmed: 20348925
Proc Natl Acad Sci U S A. 2007 Apr 17;104(16):6758-63
pubmed: 17412832
Trends Immunol. 2017 Aug;38(8):542-557
pubmed: 28579323
Am J Transplant. 2017 Dec;17(12):3199-3209
pubmed: 28805342
Immunity. 2011 Apr 22;34(4):479-91
pubmed: 21458306
Arthritis Rheum. 2007 Nov;56(11):3784-92
pubmed: 17968926
Nature. 2007 Feb 22;445(7130):936-40
pubmed: 17237761
J Immunol. 2008 Nov 15;181(10):6872-6881
pubmed: 18981106
Proc Natl Acad Sci U S A. 2003 Mar 4;100(5):2610-5
pubmed: 12604793
Science. 2013 Apr 12;340(6129):207-11
pubmed: 23580529
Cell Rep. 2014 Jun 12;7(5):1471-1480
pubmed: 24835996
Nat Med. 2007 Nov;13(11):1299-307
pubmed: 17922010
Annu Rev Pathol. 2006;1:23-61
pubmed: 18039107
Bioinformatics. 2006 Dec 15;22(24):3067-74
pubmed: 17032683
Transplantation. 2016 Dec;100(12):2533-2547
pubmed: 27861285
Immunity. 2013 Aug 22;39(2):259-71
pubmed: 23973222
J Immunol. 2011 Aug 1;187(3):1113-9
pubmed: 21697455
Am J Transplant. 2012 Feb;12(2):313-21
pubmed: 22070565
J Neurol. 2013 Jul;260(7):1838-45
pubmed: 23504050
J Immunol. 2017 May 15;198(10):4046-4053
pubmed: 28373583
J Immunol. 2016 Oct 15;197(8):2992-3007
pubmed: 27619998
J Neurovirol. 2007;13(1):73-7
pubmed: 17454451
PLoS One. 2013;8(2):e56527
pubmed: 23437155
Immunity. 2006 Sep;25(3):361-72
pubmed: 16979568
Am J Transplant. 2010 Jan;10(1):162-7
pubmed: 19951284
J Immunol. 1999 Dec 1;163(11):6306-13
pubmed: 10570325
J Immunol. 2007 Jul 15;179(2):854-68
pubmed: 17617576
Dig Dis Sci. 1999 Mar;44(3):608-17
pubmed: 10080158
J Immunol. 2006 Sep 15;177(6):3542-53
pubmed: 16951313
PLoS Comput Biol. 2013 Apr;9(4):e1003027
pubmed: 23592971
J Viral Hepat. 1995;2(2):103-6
pubmed: 7493297
J Immunol. 2002 Jul 1;169(1):522-30
pubmed: 12077284
Immunity. 2015 Jun 16;42(6):1143-58
pubmed: 26070485
Adv Virus Res. 2016;96:219-243
pubmed: 27712625
J Neuroimmunol. 2002 Jun;127(1-2):69-79
pubmed: 12044977
Blood. 2010 Feb 4;115(5):965-74
pubmed: 19996091
Cell. 2016 Jan 28;164(3):349-52
pubmed: 26824652
Nature. 2007 Feb 22;445(7130):931-5
pubmed: 17237765
Cell Host Microbe. 2015 May 13;17(5):653-61
pubmed: 25974304
PLoS Pathog. 2014 Feb 20;10(2):e1003962
pubmed: 24586165
Cell Rep. 2012 Jun 28;1(6):665-75
pubmed: 22813742
Nat Genet. 2006 May;38(5):550-5
pubmed: 16642019
J Virol. 2004 Dec;78(23):13082-9
pubmed: 15542660
Nat Immunol. 2007 Feb;8(2):191-7
pubmed: 17136045
J Immunol. 2010 Apr 1;184(7):3377-85
pubmed: 20181889
Am J Transplant. 2019 Mar;19(3):633-645
pubmed: 30106232
J Hepatol. 2007 Sep;47(3):316-24
pubmed: 17475362
J Immunol. 2013 Jun 15;190(12):5921-5
pubmed: 23690475
Proc Natl Acad Sci U S A. 2002 Nov 26;99(24):15669-74
pubmed: 12441396
Clin Exp Immunol. 2000 Mar;119(3):479-85
pubmed: 10691920
J Exp Med. 2012 Sep 24;209(10):1723-42, S1
pubmed: 22966001
J Clin Invest. 2013 Nov;123(11):4859-74
pubmed: 24216477
J Virol. 2016 Apr 29;90(10):5187-99
pubmed: 26984726
J Biol Chem. 2009 Feb 27;284(9):5709-16
pubmed: 19117830
Nat Rev Immunol. 2015 Apr;15(4):231-42
pubmed: 25790790
Annu Rev Virol. 2019 Sep 29;6(1):567-584
pubmed: 31283436
J Immunol. 2004 Dec 15;173(12):7115-9
pubmed: 15585830
Cell Host Microbe. 2012 Jun 14;11(6):631-42
pubmed: 22704623
Nat Immunol. 2002 Feb;3(2):135-42
pubmed: 11812990
Nat Rev Immunol. 2010 Dec;10(12):849-59
pubmed: 21107346
Arch Neurol. 2008 Nov;65(11):1434-9
pubmed: 19001161
Cochrane Database Syst Rev. 2016 Nov 24;11:CD009333
pubmed: 27880972
Methods Mol Biol. 2017;1510:287-293
pubmed: 27761829
J Neuroimmunol. 2007 Jan;182(1-2):204-11
pubmed: 17157927
Nat Rev Immunol. 2014 Jan;14(1):36-49
pubmed: 24362405
J Virol. 2015 Oct;89(19):9886-95
pubmed: 26202227
J Clin Invest. 2018 Jun 1;128(6):2487-2499
pubmed: 29558366
Arthritis Rheum. 2005 Apr;52(4):1185-95
pubmed: 15818675
Ann Neurol. 1996 Oct;40(4):618-27
pubmed: 8871582
JCI Insight. 2019 Apr 23;5:
pubmed: 31013255
Cell. 2020 May 28;181(5):1036-1045.e9
pubmed: 32416070
Virus Res. 2008 Mar;132(1-2):97-103
pubmed: 18093678
Curr Opin Organ Transplant. 2015 Aug;20(4):376-84
pubmed: 26126193
Nat Rev Rheumatol. 2010 Jan;6(1):40-9
pubmed: 20046205
J Immunol. 2011 Jan 15;186(2):675-84
pubmed: 21160051
J Neuroimmunol. 2009 Oct 30;215(1-2):125-8
pubmed: 19758707
Nat Med. 2020 Oct;26(10):1636-1643
pubmed: 32839624
Sci Rep. 2020 Jan 16;10(1):424
pubmed: 31949209
Trends Immunol. 2014 Aug;35(8):368-78
pubmed: 25047417

Auteurs

Francisco Fueyo-González (F)

Division of Nephrology, Department of Medicine, Translational Transplant Research Center, Icahn School of Medicine at Mount Sinai, New York City, NY, USA; Immunology Institute Icahn School of Medicine at Mount Sinai, New York City, NY, USA.

Mitchell McGinty (M)

Carter Immunology Center, University of Virginia, Charlottesville, VA 22903, USA.

Mehek Ningoo (M)

Division of Nephrology, Department of Medicine, Translational Transplant Research Center, Icahn School of Medicine at Mount Sinai, New York City, NY, USA; Immunology Institute Icahn School of Medicine at Mount Sinai, New York City, NY, USA.

Lisa Anderson (L)

Division of Nephrology, Department of Medicine, Translational Transplant Research Center, Icahn School of Medicine at Mount Sinai, New York City, NY, USA; Immunology Institute Icahn School of Medicine at Mount Sinai, New York City, NY, USA.

Chiara Cantarelli (C)

UO Nefrologia, Azienda Ospedaliero-Universitaria Parma, Parma, Italy.
Division of Nephrology, Dialysis, Transplantation, IRCCS Giannina Gaslini, Genoa, Italy.

Markus Demir (M)

Department of Anesthesiology, University of Cologne, Cologne, Germany.

Inés Llaudó (I)

Division of Nephrology, Department of Medicine, Translational Transplant Research Center, Icahn School of Medicine at Mount Sinai, New York City, NY, USA; Immunology Institute Icahn School of Medicine at Mount Sinai, New York City, NY, USA.

Carolina Purroy (C)

Department of Nephrology, Complejo Hospitalario de Navarra, Navarra, Spain.

Nada Marjanovic (N)

Immunology Institute Icahn School of Medicine at Mount Sinai, New York City, NY, USA; Department of Neurology, Icahn School of Medicine at Mount Sinai, New York City, NY, USA.

David Heja (D)

Division of Nephrology, Department of Medicine, Translational Transplant Research Center, Icahn School of Medicine at Mount Sinai, New York City, NY, USA; Immunology Institute Icahn School of Medicine at Mount Sinai, New York City, NY, USA.

Stuart C Sealfon (SC)

Immunology Institute Icahn School of Medicine at Mount Sinai, New York City, NY, USA; Department of Neurology, Icahn School of Medicine at Mount Sinai, New York City, NY, USA.

Peter S Heeger (PS)

Division of Nephrology, Department of Medicine, Translational Transplant Research Center, Icahn School of Medicine at Mount Sinai, New York City, NY, USA; Immunology Institute Icahn School of Medicine at Mount Sinai, New York City, NY, USA.

Paolo Cravedi (P)

Division of Nephrology, Department of Medicine, Translational Transplant Research Center, Icahn School of Medicine at Mount Sinai, New York City, NY, USA; Immunology Institute Icahn School of Medicine at Mount Sinai, New York City, NY, USA.

Miguel Fribourg (M)

Division of Nephrology, Department of Medicine, Translational Transplant Research Center, Icahn School of Medicine at Mount Sinai, New York City, NY, USA; Immunology Institute Icahn School of Medicine at Mount Sinai, New York City, NY, USA. Electronic address: miguel.fribourg@mssm.edu.

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