Catch bond models may explain how force amplifies TCR signaling and antigen discrimination.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
05 05 2023
05 05 2023
Historique:
received:
20
05
2022
accepted:
24
04
2023
medline:
8
5
2023
pubmed:
6
5
2023
entrez:
5
5
2023
Statut:
epublish
Résumé
The TCR integrates forces in its triggering process upon interaction with pMHC. Force elicits TCR catch-slip bonds with strong pMHCs but slip-only bonds with weak pMHCs. We develop two models and apply them to analyze 55 datasets, demonstrating the models' ability to quantitatively integrate and classify a broad range of bond behaviors and biological activities. Comparing to a generic two-state model, our models can distinguish class I from class II MHCs and correlate their structural parameters with the TCR/pMHC's potency to trigger T cell activation. The models are tested by mutagenesis using an MHC and a TCR mutated to alter conformation changes. The extensive comparisons between theory and experiment provide model validation and testable hypothesis regarding specific conformational changes that control bond profiles, thereby suggesting structural mechanisms for the inner workings of the TCR mechanosensing machinery and plausible explanations of why and how force may amplify TCR signaling and antigen discrimination.
Identifiants
pubmed: 37147290
doi: 10.1038/s41467-023-38267-1
pii: 10.1038/s41467-023-38267-1
pmc: PMC10163261
doi:
Substances chimiques
Receptors, Antigen, T-Cell
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
2616Subventions
Organisme : NCI NIH HHS
ID : U01 CA214354
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM085586
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM124489
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA243486
Pays : United States
Organisme : NCI NIH HHS
ID : U01 CA250040
Pays : United States
Informations de copyright
© 2023. The Author(s).
Références
Proc Natl Acad Sci U S A. 2006 Jun 27;103(26):9844-9
pubmed: 16785439
J Biol Chem. 2010 Nov 12;285(46):35967-78
pubmed: 20819952
PLoS Comput Biol. 2018 Aug 17;14(8):e1006399
pubmed: 30118477
Science. 1978 May 12;200(4342):618-27
pubmed: 347575
J Immunol. 2007 Sep 15;179(6):3588-95
pubmed: 17785793
Phys Rev Lett. 2006 Mar 17;96(10):108101
pubmed: 16605793
J Immunol. 2015 Oct 15;195(8):3557-64
pubmed: 26336148
Science. 2021 Jun 4;372(6546):
pubmed: 34083463
J Cell Biol. 2009 Jun 29;185(7):1275-84
pubmed: 19564406
J Chem Theory Comput. 2008 Mar;4(3):435-47
pubmed: 26620784
Cell. 2014 Apr 10;157(2):357-368
pubmed: 24725404
Trends Biochem Sci. 2018 Feb;43(2):108-123
pubmed: 29269020
Annu Rev Immunol. 2015;33:169-200
pubmed: 25493333
Proc Natl Acad Sci U S A. 2014 Jan 7;111(1):379-84
pubmed: 24344262
Proc Natl Acad Sci U S A. 2019 Aug 20;116(34):16949-16954
pubmed: 31391300
Biophys J. 1998 Sep;75(3):1553-72
pubmed: 9726957
Science. 2017 Aug 18;357(6352):703-706
pubmed: 28818948
J Biol Chem. 2013 Nov 8;288(45):32289-32301
pubmed: 24062306
J Clin Invest. 2008 Sep;118(9):3195-207
pubmed: 18725999
Proc Natl Acad Sci U S A. 2013 Mar 26;110(13):5022-7
pubmed: 23460697
Nat Mater. 2019 Jul;18(7):760-769
pubmed: 30911119
Science. 1999 Mar 12;283(5408):1727-30
pubmed: 10073936
Eur J Immunol. 1995 Jun;25(6):1609-16
pubmed: 7614989
Nature. 2003 May 8;423(6936):190-3
pubmed: 12736689
Science. 2014 Oct 31;346(6209):1254211
pubmed: 25359979
Proc Natl Acad Sci U S A. 2022 Mar 8;119(10):e2109329119
pubmed: 35245171
Nat Commun. 2023 May 5;14(1):2616
pubmed: 37147290
J Biol Chem. 2004 Jan 16;279(3):2291-8
pubmed: 14573602
J Biol Chem. 2016 Dec 2;291(49):25292-25305
pubmed: 27707880
Matrix Biol. 2017 Jul;60-61:70-85
pubmed: 27423389
Proc Natl Acad Sci U S A. 2015 Jul 7;112(27):8373-8
pubmed: 26056289
Biophys J. 2010 Aug 9;99(4):1166-74
pubmed: 20713000
Biophys J. 2015 Apr 7;108(7):1709-1717
pubmed: 25863062
Cell Mol Bioeng. 2008 Dec 1;1(4):276-288
pubmed: 19890486
Annu Rev Biomed Eng. 2008;10:39-57
pubmed: 18647111
Proc Natl Acad Sci U S A. 2019 Aug 20;116(34):16943-16948
pubmed: 31315981
Nature. 2019 Sep;573(7775):546-552
pubmed: 31461748
Biophys J. 2017 Dec 19;113(12):2842-2845
pubmed: 29262376
Biophys J. 2007 Mar 1;92(5):1471-85
pubmed: 17142266
Front Immunol. 2018 Oct 15;9:2348
pubmed: 30374353
Proc Natl Acad Sci U S A. 2017 Sep 26;114(39):E8204-E8213
pubmed: 28811364
Nature. 2010 Nov 25;468(7323):576-9
pubmed: 21107429
Annu Rev Phys Chem. 2015 Apr;66:427-51
pubmed: 25580628
Nat Immunol. 2019 Oct;20(10):1269-1278
pubmed: 31534240
Biophys J. 1995 Jun;68(6):2580-7
pubmed: 7647261
J Clin Invest. 2017 Oct 2;127(10):3810-3826
pubmed: 28891817
Proc Natl Acad Sci U S A. 1995 May 23;92(11):5042-6
pubmed: 7761445
Nat Commun. 2022 Nov 17;13(1):7055
pubmed: 36396644
Nat Commun. 2021 May 4;12(1):2502
pubmed: 33947864
Nat Commun. 2014 Jun 02;5:3941
pubmed: 24887573
Science. 2022 Apr 8;376(6589):eabl5282
pubmed: 35389803
Nature. 2005 Mar 10;434(7030):238-43
pubmed: 15724150
Proc Natl Acad Sci U S A. 2020 Sep 1;117(35):21336-21345
pubmed: 32796106
Cell. 2022 Aug 18;185(17):3201-3213.e19
pubmed: 35985289
Biophys J. 2015 Dec 1;109(11):2338-51
pubmed: 26636945
Rev Sci Instrum. 2004 Sep;75(9):2787-809
pubmed: 16878180
Trends Immunol. 2018 Aug;39(8):596-609
pubmed: 30060805
Proc Natl Acad Sci U S A. 2016 May 17;113(20):5610-5
pubmed: 27140637
Science. 2017 Mar 24;355(6331):1320-1324
pubmed: 28254785
J Biol Chem. 2008 Apr 25;283(17):11596-605
pubmed: 18292092
Immunity. 2011 Nov 23;35(5):681-93
pubmed: 22101157
Nature. 2010 Apr 8;464(7290):932-6
pubmed: 20357766
Proc Natl Acad Sci U S A. 2004 Aug 3;101(31):11281-6
pubmed: 15277675
Proc R Soc Lond B Biol Sci. 1988 Jun 22;234(1274):55-83
pubmed: 2901109
Biophys J. 1999 Jan;76(1 Pt 1):409-13
pubmed: 9876152
Cell. 2018 Jul 26;174(3):672-687.e27
pubmed: 30053426
Biophys J. 2008 Jan 15;94(2):694-701
pubmed: 17890399
Biophys J. 2005 Sep;89(3):1446-54
pubmed: 15951391
Proc Natl Acad Sci U S A. 2019 Oct 8;116(41):20446-20452
pubmed: 31548393
Proc Natl Acad Sci U S A. 2010 Feb 2;107(5):2013-8
pubmed: 20133846
Eur J Immunol. 1989 Dec;19(12):2269-74
pubmed: 2558022
J Exp Med. 1996 Oct 1;184(4):1259-68
pubmed: 8879197
Cell Rep. 2015 Mar 17;10(10):1655-1664
pubmed: 25772353
Science. 1992 Nov 13;258(5085):1122-6
pubmed: 1439819
J Phys Chem Lett. 2021 Aug 12;12(31):7566-7573
pubmed: 34347491
Sci Rep. 2016 Oct 12;6:35058
pubmed: 27731359
Proc Natl Acad Sci U S A. 2015 Feb 3;112(5):1517-22
pubmed: 25605925
Cell Rep. 2016 Mar 29;14(12):2833-45
pubmed: 26997265
Proc Natl Acad Sci U S A. 2005 Feb 8;102(6):1835-9
pubmed: 15701706
EMBO J. 2023 Apr 3;42(7):e111841
pubmed: 36484367
Nat Immunol. 2018 Dec;19(12):1379-1390
pubmed: 30420628
J Biol Chem. 2020 Jan 24;295(4):914-925
pubmed: 31848223
Mol Cell. 2019 Mar 7;73(5):1015-1027.e7
pubmed: 30711376
Proteins. 2010 Jun;78(8):1950-8
pubmed: 20408171
Eur J Immunol. 2015 Jul;45(7):2099-110
pubmed: 25944482
Nano Lett. 2016 Jul 13;16(7):4552-9
pubmed: 27192323
Nat Commun. 2022 Jun 9;13(1):3222
pubmed: 35680882