How persistent infection overcomes peripheral tolerance mechanisms to cause T cell-mediated autoimmune disease.


Journal

Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876

Informations de publication

Date de publication:
12 Mar 2024
Historique:
medline: 8 3 2024
pubmed: 6 3 2024
entrez: 6 3 2024
Statut: ppublish

Résumé

T cells help orchestrate immune responses to pathogens, and their aberrant regulation can trigger autoimmunity. Recent studies highlight that a threshold number of T cells (a quorum) must be activated in a tissue to mount a functional immune response. These collective effects allow the T cell repertoire to respond to pathogens while suppressing autoimmunity due to circulating autoreactive T cells. Our computational studies show that increasing numbers of pathogenic peptides targeted by T cells during persistent or severe viral infections increase the probability of activating T cells that are weakly reactive to self-antigens (molecular mimicry). These T cells are easily re-activated by the self-antigens and contribute to exceeding the quorum threshold required to mount autoimmune responses. Rare peptides that activate many T cells are sampled more readily during severe/persistent infections than in acute infections, which amplifies these effects. Experiments in mice to test predictions from these mechanistic insights are suggested.

Identifiants

pubmed: 38446856
doi: 10.1073/pnas.2318599121
doi:

Substances chimiques

Autoantigens 0
Peptides 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2318599121

Subventions

Organisme : National Science Foundation (NSF)
ID : DMR-2218849
Organisme : National Science Foundation (NSF)
ID : 2141064
Organisme : Ragon Institute of MGH, MIT and Harvard (Ragon Institute)
ID : 220568
Organisme : Massachusetts Institute of Technology (MIT)
ID : Physics of Living Systems Fellowship

Déclaration de conflit d'intérêts

Competing interests statement:A.K.C. is a consultant (titled Academic Partner) for Flagship Pioneering, serves as consultant and on the Strategic Oversight Board of its affiliated company, Apriori Bio, and is a consultant and SAB member of another affiliated company, Metaphore Bio. The other authors declare no competing interest.

Références

Nat Immunol. 2006 Nov;7(11):1191-9
pubmed: 17041605
Nature. 2015 Dec 10;528(7581):225-30
pubmed: 26605524
Diabetologia. 2017 Apr;60(4):656-667
pubmed: 28062922
Sci Immunol. 2021 Apr 14;6(58):
pubmed: 33853928
Science. 2018 Jun 15;360(6394):
pubmed: 29903938
Proc Natl Acad Sci U S A. 2002 Jul 9;99(14):9369-73
pubmed: 12077322
Nat Immunol. 2003 Jun;4(6):579-85
pubmed: 12730692
Immunol Today. 1993 May;14(5):203-8
pubmed: 7686009
Cell. 2006 Jul 28;126(2):375-87
pubmed: 16873067
Proc Natl Acad Sci U S A. 2007 Mar 20;104(12):5115-20
pubmed: 17360338
Annu Rev Immunol. 2012;30:531-64
pubmed: 22224781
Front Immunol. 2021 Jan 07;11:587380
pubmed: 33488588
Nat Immunol. 2013 Apr;14(4):356-63
pubmed: 23475183
Cell. 1989 Dec 22;59(6):1035-48
pubmed: 2598259
J Exp Med. 2001 Dec 17;194(12):1711-9
pubmed: 11748273
Phys Rev E. 2018 Mar;97(3-1):032413
pubmed: 29776088
Trends Immunol. 2009 Aug;30(8):409-14
pubmed: 19643667
Annu Rev Immunol. 2009;27:287-312
pubmed: 19302042
J Infect Dis. 2005 Nov 1;192(9):1513-24
pubmed: 16206065
J Exp Med. 2008 Aug 4;205(8):1763-73
pubmed: 18663124
J Immunol. 2009 Sep 15;183(6):3895-905
pubmed: 19717517
Phys Rev Lett. 2009 Aug 7;103(6):068103
pubmed: 19792616
J Immunol. 1996 Oct 15;157(8):3280-9
pubmed: 8871622
Cell. 1993 Jun 4;73(5):1041-9
pubmed: 8500174
J Mol Biol. 1996 Mar 1;256(3):623-44
pubmed: 8604144
Nat Rev Immunol. 2002 Feb;2(2):85-95
pubmed: 11910899
Proc Natl Acad Sci U S A. 1989 Feb;86(4):1333-7
pubmed: 2465550
Nat Immunol. 2010 Jan;11(1):7-13
pubmed: 20016504
Immunity. 2007 Jul;27(1):76-88
pubmed: 17629516
Proc Natl Acad Sci U S A. 2005 Dec 20;102(51):18425-30
pubmed: 16339897
Nucleic Acids Res. 2023 Jan 6;51(D1):D523-D531
pubmed: 36408920
Heliyon. 2022 Nov;8(11):e11328
pubmed: 36338884
Cell. 1994 Jan 14;76(1):17-27
pubmed: 8287475
Elife. 2023 Jan 20;12:
pubmed: 36661220
Annu Rev Microbiol. 2001;55:165-99
pubmed: 11544353
Clin Microbiol Rev. 2006 Jan;19(1):80-94
pubmed: 16418524
Eur J Immunol. 2000 Jan;30(1):50-8
pubmed: 10602026
Immunity. 2020 Feb 18;52(2):313-327.e7
pubmed: 32049052
Diabetes. 2012 Jul;61(7):1752-9
pubmed: 22522618
Annu Rev Med. 2022 Jan 27;73:483-499
pubmed: 34794324
Science. 2022 Jan 21;375(6578):296-301
pubmed: 35025605
Nat Immunol. 2000 Jul;1(1):47-53
pubmed: 10881174
J Clin Invest. 2008 Oct;118(10):3390-402
pubmed: 18802479
J Exp Med. 2007 Nov 26;204(12):2899-912
pubmed: 17984305
J Exp Med. 2005 Mar 21;201(6):891-902
pubmed: 15781581
Nat Rev Immunol. 2014 Jun;14(6):377-91
pubmed: 24830344
Nat Immunol. 2014 May;15(5):473-81
pubmed: 24633226
Proc Natl Acad Sci U S A. 2014 Jul 8;111(27):9875-80
pubmed: 24941953
J Immunol. 1999 Jan 1;162(1):129-35
pubmed: 9886378
Science. 2014 Dec 19;346(6216):1536-40
pubmed: 25525252
Nat Commun. 2018 Feb 8;9(1):561
pubmed: 29422654
J Immunol. 2006 Mar 1;176(5):3037-43
pubmed: 16493062
Cell. 2021 Jul 22;184(15):3981-3997.e22
pubmed: 34157301
Front Immunol. 2012 Nov 27;3:357
pubmed: 23230439
Science. 2022 Apr 15;376(6590):eabi9591
pubmed: 35258337
Nucleic Acids Res. 2020 Jul 2;48(W1):W449-W454
pubmed: 32406916
Cell. 1995 Mar 10;80(5):695-705
pubmed: 7534214
Proc Natl Acad Sci U S A. 2013 Jul 16;110(29):11833-8
pubmed: 23818603
Nat Immunol. 2023 Apr;24(4):652-663
pubmed: 36807641
Proc Natl Acad Sci U S A. 2005 Jul 26;102(30):10581-6
pubmed: 16030147
Cell. 2009 Jan 23;136(2):337-51
pubmed: 19167334
Curr Opin Pharmacol. 2018 Dec;43:11-19
pubmed: 30064099
Nat Immunol. 2016 Feb;17(2):187-95
pubmed: 26726812
Proc Natl Acad Sci U S A. 2005 Mar 29;102(13):4824-9
pubmed: 15772168
J Transl Med. 2021 Jul 5;19(1):290
pubmed: 34225749
Science. 1990 Jun 15;248(4961):1369-73
pubmed: 1972594
Hum Immunol. 2019 Nov;80(11):923-929
pubmed: 31451291
Mol Cell Biol. 1987 Dec;7(12):4472-81
pubmed: 2830495
Nature. 2010 May 20;465(7296):350-4
pubmed: 20445539
Nat Med. 2004 Mar;10(3):282-9
pubmed: 14770175
Nat Rev Endocrinol. 2022 Aug;18(8):503-516
pubmed: 35650334
Immunity. 2012 Oct 19;37(4):709-20
pubmed: 23084359
Proc Natl Acad Sci U S A. 1998 Feb 17;95(4):1721-4
pubmed: 9465083
Proc Natl Acad Sci U S A. 2017 Sep 19;114(38):E7875-E7881
pubmed: 28874554
Nature. 2006 Apr 13;440(7086):890-5
pubmed: 16612374
Nature. 1992 Jul 9;358(6382):155-7
pubmed: 1377368
Immunol Today. 1992 Jan;13(1):11-6
pubmed: 1739426
Immunity. 2015 May 19;42(5):929-41
pubmed: 25992863
Mult Scler. 2016 Mar;22(3):279-91
pubmed: 26041797
J Exp Med. 1997 Jan 6;185(1):1-11
pubmed: 8996237
Mol Immunol. 2008 Feb;45(3):599-606
pubmed: 17920446
Nature. 1990 Jul 12;346(6280):183-7
pubmed: 1694970
J Immunol. 2004 Apr 15;172(8):5120-7
pubmed: 15067096
Science. 1988 May 27;240(4856):1169-76
pubmed: 3131876
Annu Rev Immunol. 2018 Apr 26;36:411-433
pubmed: 29677473
Nat Commun. 2022 Aug 23;13(1):4951
pubmed: 35999236
Immunogenetics. 2019 Mar;71(3):171-187
pubmed: 30421030
J Exp Med. 1997 Oct 6;186(7):1149-58
pubmed: 9314563
Curr Opin Immunol. 2015 Apr;33:43-8
pubmed: 25660212
Blood. 2004 Jun 1;103(11):4222-31
pubmed: 14976054
J Immunol. 1991 Oct 15;147(8):2461-6
pubmed: 1717561
J Immunol. 1994 Jun 1;152(11):5220-5
pubmed: 7514632
Immunity. 2009 May;30(5):636-45
pubmed: 19464986
Clin Immunol. 2012 May;143(2):99-115
pubmed: 22391152
Proc Natl Acad Sci U S A. 1976 Oct;73(10):3628-32
pubmed: 824647
Immunity. 2008 Aug 15;29(2):238-48
pubmed: 18674934
J Exp Med. 2002 Jun 17;195(12):1515-22
pubmed: 12070279
Nat Med. 1998 Jul;4(7):781-5
pubmed: 9662368
Diabetologia. 2015 Jan;58(1):79-86
pubmed: 25335440
Nature. 2022 Dec;612(7941):771-777
pubmed: 36477533
Proc Natl Acad Sci U S A. 2008 Oct 28;105(43):16671-6
pubmed: 18946038
Proc Natl Acad Sci U S A. 2012 Oct 2;109(40):16161-6
pubmed: 22988065
Nat Rev Immunol. 2007 Nov;7(11):875-88
pubmed: 17948021
Cell. 2005 Jul 29;122(2):247-60
pubmed: 16051149
Nat Immunol. 2007 Sep;8(9):921-30
pubmed: 17660821
Nat Rev Mol Cell Biol. 2001 Mar;2(3):179-87
pubmed: 11265247
Nat Immunol. 2014 Sep;15(9):798-807
pubmed: 25137454
Proc Natl Acad Sci U S A. 2019 Aug 20;116(34):16955-16960
pubmed: 31375628
Immunity. 2013 Feb 21;38(2):373-83
pubmed: 23395677
Adv Immunol. 2003;81:331-71
pubmed: 14711059
Science. 1991 Jan 18;251(4991):313-6
pubmed: 1846244
Stem Cells. 2008 Sep;26(9):2444-54
pubmed: 18635871
Nature. 2022 Mar;603(7900):321-327
pubmed: 35073561
Nat Immunol. 2012 Jan 19;13(2):121-8
pubmed: 22261968
Immunity. 2001 Feb;14(2):135-43
pubmed: 11239446
Eur Respir J. 2022 Feb 3;59(2):
pubmed: 34531277
Immunity. 2015 Jan 20;42(1):95-107
pubmed: 25601203
Indian J Endocrinol Metab. 2012 Mar;16 Suppl 1:S27-36
pubmed: 22701840
Front Genet. 2023 Mar 23;14:866407
pubmed: 37035735
Nat Immunol. 2016 Aug;17(8):946-55
pubmed: 27348411
Int Immunol. 2003 Jul;15(7):885-92
pubmed: 12807827
J Virol. 2000 Nov;74(21):10153-64
pubmed: 11024144
J Immunol. 2003 Oct 1;171(7):3837-46
pubmed: 14500685
Int Immunol. 1990;2(1):83-9
pubmed: 2150922
Proteomics Clin Appl. 2015 Dec;9(11-12):1035-52
pubmed: 26768311
J Theor Biol. 2004 Jun 7;228(3):397-416
pubmed: 15135038

Auteurs

Rose Yin (R)

Department of Chemical Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139.

Samuel Melton (S)

Physics of Living Systems, Department of Physics, Massachusetts Institute of Technology, Cambridge, MA 02139.

Eric S Huseby (ES)

Basic Pathology, Department of Pathology, University of Massachusetts Medical School, Worcester, MA 01655.

Mehran Kardar (M)

Physics of Living Systems, Department of Physics, Massachusetts Institute of Technology, Cambridge, MA 02139.

Arup K Chakraborty (AK)

Department of Chemical Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139.
Physics of Living Systems, Department of Physics, Massachusetts Institute of Technology, Cambridge, MA 02139.
Ragon Institute of Massachusetts General Hospital, Massachusetts Institute of Technology and Harvard University, Cambridge, MA 02139.
Department of Chemistry, Massachusetts Institute of Technology, Cambridge, MA 02139.

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