Sterile activation of invariant natural killer T cells by ER-stressed antigen-presenting cells.
Animals
Antigen Presentation
Antigen-Presenting Cells
/ immunology
Antigens, CD1d
/ biosynthesis
Autoantigens
/ immunology
Carcinoma, Lewis Lung
/ pathology
Cell Line, Tumor
Coculture Techniques
Cytoskeleton
/ ultrastructure
Dendritic Cells
/ immunology
Endoplasmic Reticulum Stress
/ immunology
Endosomes
/ immunology
Glycosphingolipids
/ immunology
Humans
Interleukin-2 Receptor alpha Subunit
/ biosynthesis
Lipids
/ immunology
Lymphocyte Activation
Lysosomes
/ immunology
Mice
Mice, Inbred C57BL
Natural Killer T-Cells
/ immunology
THP-1 Cells
Thapsigargin
/ pharmacology
Unfolded Protein Response
/ immunology
eIF-2 Kinase
/ deficiency
CD1d
ER stress
NKT
cancer
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:
19 11 2019
19 11 2019
Historique:
pubmed:
7
11
2019
medline:
21
4
2020
entrez:
7
11
2019
Statut:
ppublish
Résumé
Invariant NKT (iNKT) cells have the unique ability to shape immunity during antitumor immune responses and other forms of sterile and nonsterile inflammation. Recent studies have highlighted a variety of classes of endogenous and pathogen-derived lipid antigens that can trigger iNKT cell activation under sterile and nonsterile conditions. However, the context and mechanisms that drive the presentation of self-lipid antigens in sterile inflammation remain unclear. Here we report that endoplasmic reticulum (ER)-stressed myeloid cells, via signaling events modulated by the protein kinase RNA-like ER kinase (PERK) pathway, increase CD1d-mediated presentation of immunogenic endogenous lipid species, which results in enhanced iNKT cell activation both in vitro and in vivo. In addition, we demonstrate that actin cytoskeletal reorganization during ER stress results in an altered distribution of CD1d on the cell surface, which contributes to enhanced iNKT cell activation. These results define a previously unidentified mechanism that controls iNKT cell activation during sterile inflammation.
Identifiants
pubmed: 31690657
pii: 1910097116
doi: 10.1073/pnas.1910097116
pmc: PMC6876220
doi:
Substances chimiques
Antigens, CD1d
0
Autoantigens
0
CD1D protein, human
0
CD1d antigen, mouse
0
Glycosphingolipids
0
IL2RA protein, human
0
Interleukin-2 Receptor alpha Subunit
0
Lipids
0
Thapsigargin
67526-95-8
EIF2AK3 protein, human
EC 2.7.11.1
eIF-2 Kinase
EC 2.7.11.1
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
23671-23681Subventions
Organisme : Medical Research Council
ID : MC_PC_15002
Pays : United Kingdom
Organisme : NIDDK NIH HHS
ID : R01 DK088199
Pays : United States
Organisme : Cancer Research UK
ID : C399/A2291
Pays : United Kingdom
Organisme : Medical Research Council
ID : G1000800
Pays : United Kingdom
Organisme : Medical Research Council
ID : G1001750
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 104924/14/Z/14
Pays : United Kingdom
Organisme : Medical Research Council
ID : G0700851
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_UU_12010/9
Pays : United Kingdom
Organisme : Medical Research Council
ID : G0800158
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_U137884181
Pays : United Kingdom
Organisme : Medical Research Council
ID : G0400421
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_UU_12010/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_UU_00008/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/K01577X/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : G0501975
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_UU_00008/9
Pays : United Kingdom
Organisme : Cancer Research UK
ID : 11331
Pays : United Kingdom
Organisme : NICHD NIH HHS
ID : K12 HD000850
Pays : United States
Organisme : NIDDK NIH HHS
ID : P30 DK034854
Pays : United States
Organisme : Wellcome Trust
ID : 202834/Z/16/Z
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/K021222/1
Pays : United Kingdom
Informations de copyright
Copyright © 2019 the Author(s). Published by PNAS.
Déclaration de conflit d'intérêts
The authors declare no competing interest.
Références
Proc Natl Acad Sci U S A. 2003 Feb 18;100(4):1849-54
pubmed: 12576547
Mol Cell. 2011 Jun 24;42(6):731-43
pubmed: 21700220
J Immunol. 2018 Oct 15;201(8):2452-2461
pubmed: 30171164
Science. 2008 Jun 13;320(5882):1492-6
pubmed: 18556558
J Exp Med. 2003 Jul 7;198(1):173-81
pubmed: 12847141
Science. 2001 Jan 26;291(5504):664-7
pubmed: 11158680
J Immunol. 2003 Nov 15;171(10):5140-7
pubmed: 14607913
Clin Dev Immunol. 2012;2012:720803
pubmed: 23118781
PLoS Biol. 2009 Oct;7(10):e1000228
pubmed: 19859526
Proc Natl Acad Sci U S A. 2007 Dec 18;104(51):20490-5
pubmed: 18077358
Nat Rev Immunol. 2013 Feb;13(2):101-17
pubmed: 23334244
Blood. 2008 Jun 15;111(12):5637-45
pubmed: 18417738
Immunogenetics. 2016 Aug;68(8):597-610
pubmed: 27377623
Sci Rep. 2015 Jun 29;5:11454
pubmed: 26118385
J Exp Med. 2007 Mar 19;204(3):533-45
pubmed: 17312007
Proc Natl Acad Sci U S A. 2011 Apr 19;108(16):6561-6
pubmed: 21464300
Proc Natl Acad Sci U S A. 2008 Jun 17;105(24):8339-44
pubmed: 18550809
J Clin Invest. 2004 Dec;114(12):1800-11
pubmed: 15599405
Cell Metab. 2008 Jun;7(6):520-32
pubmed: 18522833
PLoS One. 2012;7(12):e51845
pubmed: 23272178
Anal Chem. 2017 Jul 5;89(13):7046-7052
pubmed: 28570056
Cell Mol Life Sci. 2014 Aug;71(16):3069-79
pubmed: 24658584
Anal Chem. 2017 Dec 5;89(23):12857-12865
pubmed: 29111682
Nat Cell Biol. 2018 Aug;20(8):942-953
pubmed: 30013108
J Exp Med. 2003 Jul 21;198(2):267-79
pubmed: 12874260
EMBO Rep. 2016 Oct;17(10):1374-1395
pubmed: 27629041
Mol Cell. 2003 Mar;11(3):619-33
pubmed: 12667446
J Immunol. 2007 May 15;178(10):6181-90
pubmed: 17475845
Proc Natl Acad Sci U S A. 2013 Dec 3;110(49):E4753-61
pubmed: 24248359
J Exp Med. 2003 Apr 21;197(8):1051-7
pubmed: 12695492
Annu Rev Immunol. 2014;32:323-66
pubmed: 24499274
J Exp Med. 2007 Apr 16;204(4):921-8
pubmed: 17403933
Cell Metab. 2012 Oct 3;16(4):473-86
pubmed: 23040069
Cell Death Dis. 2015 Jul 30;6:e1822
pubmed: 26225772
Nature. 2018 Oct;562(7727):423-428
pubmed: 30305738
Am J Cancer Res. 2013 Apr 03;3(2):196-210
pubmed: 23593541
Sci Signal. 2017 Jun 06;10(482):null
pubmed: 28588081
Immunology. 2017 Sep;152(1):36-51
pubmed: 28419443
Nat Protoc. 2015 May;10(5):660-80
pubmed: 25837418
Biochem J. 1992 Apr 15;283 ( Pt 2):525-9
pubmed: 1533513
ACS Nano. 2018 Aug 28;12(8):8540-8546
pubmed: 30028588
Blood. 2006 Jun 15;107(12):4907-16
pubmed: 16507771
Eur J Gastroenterol Hepatol. 2009 Jun;21(6):673-80
pubmed: 19318971
Cell. 2015 Jun 18;161(7):1527-38
pubmed: 26073941
Hepatology. 2013 Apr;57(4):1366-77
pubmed: 23152128
Nature. 2006 Oct 5;443(7111):548-52
pubmed: 17024087
Cell. 2008 Sep 5;134(5):743-56
pubmed: 18775308
Proc Natl Acad Sci U S A. 2016 Feb 9;113(6):E772-81
pubmed: 26798067
J Cell Physiol. 2018 May;233(5):3867-3874
pubmed: 28777470
Blood. 2002 Feb 15;99(4):1259-66
pubmed: 11830474
J Biol Chem. 2015 Dec 11;290(50):30142-51
pubmed: 26504083
Annu Rev Immunol. 2015;33:107-38
pubmed: 25493331
Mol Cell Oncol. 2017 Jul 13;4(5):e1340105
pubmed: 29057305
Genome Biol. 2011;12(1):R8
pubmed: 21247462
Immunity. 2007 Oct;27(4):597-609
pubmed: 17950005
Proc Natl Acad Sci U S A. 2008 Oct 21;105(42):16314-9
pubmed: 18852460
Mol Cell. 2017 Mar 2;65(5):885-899.e6
pubmed: 28238652
Front Immunol. 2015 Aug 04;6:400
pubmed: 26300885
Immunity. 2014 Oct 16;41(4):543-54
pubmed: 25367571
J Exp Med. 2011 Jun 6;208(6):1163-77
pubmed: 21555485
World J Gastroenterol. 2011 Apr 7;17(13):1725-31
pubmed: 21483633
J Mass Spectrom. 2012 Jan;47(1):96-104
pubmed: 22282095
Immunity. 2010 Aug 27;33(2):216-28
pubmed: 20727792
Mol Biol Cell. 2017 Jun 1;28(11):1507-1518
pubmed: 28404749
Sci Adv. 2016 Apr 22;2(4):e1501337
pubmed: 27152338
Front Immunol. 2017 Dec 18;8:1829
pubmed: 29326711
Biophys J. 2004 Aug;87(2):1260-7
pubmed: 15298928
Oncotarget. 2017 Oct 11;8(53):90766-90780
pubmed: 29207602
Cell. 2008 Dec 12;135(6):1085-97
pubmed: 19070578
J Immunol. 1999 Dec 1;163(11):5871-6
pubmed: 10570271
J Exp Med. 2004 Jun 21;199(12):1607-18
pubmed: 15197224
Eur J Immunol. 2016 May;46(5):1224-34
pubmed: 26873393
Nat Immunol. 2018 Aug;19(8):821-827
pubmed: 30013143
Proc Natl Acad Sci U S A. 2005 Mar 1;102(9):3383-8
pubmed: 15722411
J Exp Med. 1999 Jul 5;190(1):31-41
pubmed: 10429668
J Exp Med. 2002 Jul 1;196(1):119-27
pubmed: 12093876
Proc Natl Acad Sci U S A. 2008 Jun 17;105(24):8345-50
pubmed: 18550831