In vivo CRISPR screens reveal a HIF-1α-mTOR-network regulates T follicular helper versus Th1 cells.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
10 02 2022
Historique:
received: 15 07 2021
accepted: 20 01 2022
entrez: 11 2 2022
pubmed: 12 2 2022
medline: 4 3 2022
Statut: epublish

Résumé

T follicular helper (Tfh) cells provide signals to initiate and maintain the germinal center (GC) reaction and are crucial for the generation of robust, long-lived antibody responses, but how the GC microenvironment affects Tfh cells is not well understood. Here we develop an in vivo T cell-intrinsic CRISPR-knockout screen to evaluate Tfh and Th1 cells in an acute viral infection model to identify regulators of Tfh cells in their physiological setting. Using a screen of druggable-targets, alongside genetic, transcriptomic and cellular analyses, we identify a function of HIF-1α in suppressing mTORC1-mediated and Myc-related pathways, and provide evidence that VHL-mediated degradation of HIF-1α is required for Tfh development; an expanded in vivo CRISPR screen reveals multiple components of these pathways that regulate Tfh versus Th1 cells, including signaling molecules, cell-cycle regulators, nutrient transporters, metabolic enzymes and autophagy mediators. Collectively, our data serve as a resource for studying Tfh versus Th1 decisions, and implicate the VHL-HIF-1α axis in fine-tuning Tfh generation.

Identifiants

pubmed: 35145086
doi: 10.1038/s41467-022-28378-6
pii: 10.1038/s41467-022-28378-6
pmc: PMC8831505
doi:

Substances chimiques

Hif1a protein, mouse 0
Hypoxia-Inducible Factor 1, alpha Subunit 0
mTOR protein, mouse EC 2.7.1.1
Mechanistic Target of Rapamycin Complex 1 EC 2.7.11.1
TOR Serine-Threonine Kinases EC 2.7.11.1

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

805

Informations de copyright

© 2022. This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply.

Références

Immunity. 2017 May 16;46(5):743-755
pubmed: 28514675
Immunity. 2019 May 21;50(5):1132-1148
pubmed: 31117010
J Immunol. 2010 Oct 1;185(7):4042-52
pubmed: 20826752
Immunity. 2019 Jan 15;50(1):91-105.e4
pubmed: 30638736
J Biol Chem. 2007 Dec 7;282(49):35803-13
pubmed: 17928295
Cell. 2013 May 9;153(4):785-96
pubmed: 23663778
J Cell Sci. 2015 Jun 1;128(11):2003-8
pubmed: 26034061
Cancer Res. 2000 Aug 1;60(15):4010-5
pubmed: 10945599
Cells. 2019 Nov 17;8(11):
pubmed: 31744227
J Virol. 2017 Jan 31;91(4):
pubmed: 27974559
Nat Cell Biol. 2013 Apr;15(4):406-16
pubmed: 23524951
Nat Cell Biol. 2015 Jan;17(1):20-30
pubmed: 25438055
Mol Immunol. 2015 Dec;68(2 Pt C):527-35
pubmed: 26298577
Cell. 2002 Nov 27;111(5):709-20
pubmed: 12464182
Proc Natl Acad Sci U S A. 2019 Apr 30;116(18):8975-8984
pubmed: 30988188
Immunity. 2015 Feb 17;42(2):239-251
pubmed: 25692700
Cell Rep. 2015 Sep 29;12(12):2099-110
pubmed: 26365183
Elife. 2020 Feb 05;9:
pubmed: 32022686
J Immunol. 2016 Nov 15;197(10):4014-4020
pubmed: 27798169
Immunity. 2017 Jun 20;46(6):1045-1058.e6
pubmed: 28636954
Nat Commun. 2019 Apr 10;10(1):1668
pubmed: 30971695
Nature. 2018 Aug;560(7718):387-391
pubmed: 29925955
Nature. 2016 Sep 8;537(7619):234-238
pubmed: 27501247
Nature. 2021 Apr;592(7856):789-793
pubmed: 33854235
Nat Biotechnol. 2016 Feb;34(2):184-191
pubmed: 26780180
Eur J Immunol. 2015 Nov;45(11):3010-21
pubmed: 26332258
Cell. 2021 Mar 4;184(5):1262-1280.e22
pubmed: 33636129
Immunity. 2015 Oct 20;43(4):690-702
pubmed: 26410627
Bioinformatics. 2014 Aug 1;30(15):2114-20
pubmed: 24695404
Genome Biol. 2014;15(12):550
pubmed: 25516281
J Clin Immunol. 2018 Jan;38(1):129-143
pubmed: 29226301
Cell. 2018 Dec 13;175(7):1958-1971.e15
pubmed: 30449619
Nucleic Acids Res. 2015 Dec 15;43(22):e157
pubmed: 26253739
Nat Immunol. 2018 Sep;19(9):986-1000
pubmed: 30127432
Nat Rev Cancer. 2008 Jan;8(1):51-6
pubmed: 18046334
Methods Mol Biol. 2015;1291:49-61
pubmed: 25836301
Cell. 2019 Aug 22;178(5):1189-1204.e23
pubmed: 31442407
Immunity. 2011 Nov 23;35(5):671-80
pubmed: 22118524
Eur J Immunol. 2020 Jul;50(7):1067-1077
pubmed: 32133634
Nat Immunol. 2020 Mar;21(3):331-342
pubmed: 32066950
Nature. 2021 Jul;595(7869):724-729
pubmed: 34234346
J Exp Med. 2011 Jul 4;208(7):1367-76
pubmed: 21708926
Immunity. 2011 Jun 24;34(6):932-46
pubmed: 21636296
Cell Rep. 2017 Feb 14;18(7):1699-1712
pubmed: 28199842
Mol Cell Biol. 2011 Jan;31(1):127-37
pubmed: 20956554
Nat Methods. 2013 Dec;10(12):1209-10
pubmed: 24122041
Eur J Immunol. 1998 Jan;28(1):390-400
pubmed: 9485218
Science. 2018 Sep 14;361(6407):
pubmed: 30213884
Cell Cycle. 2010 Jul 15;9(14):2749-63
pubmed: 20603601
Sci Transl Med. 2020 Apr 8;12(538):
pubmed: 32269165
Genome Biol. 2014;15(12):554
pubmed: 25476604
Proc Natl Acad Sci U S A. 2001 Feb 13;98(4):1583-8
pubmed: 11171994
Cell. 2017 Mar 9;168(6):960-976
pubmed: 28283069
Immunity. 2014 Nov 20;41(5):789-801
pubmed: 25464855
Cell Rep. 2020 Nov 17;33(7):108403
pubmed: 33207194
Nat Immunol. 2017 Mar;18(3):303-312
pubmed: 28114292
Nature. 2021 Mar;591(7850):458-463
pubmed: 33536617
J Immunol. 2018 Sep 1;201(5):1359-1372
pubmed: 30030323
J Exp Med. 2012 Dec 17;209(13):2441-53
pubmed: 23183047
Cell Host Microbe. 2016 Aug 10;20(2):202-14
pubmed: 27476413
Cell. 2017 May 4;169(4):570-586
pubmed: 28475890
Proc Natl Acad Sci U S A. 2005 Oct 25;102(43):15545-50
pubmed: 16199517
Immunity. 2010 Aug 27;33(2):241-53
pubmed: 20691615
Cell. 2021 Mar 4;184(5):1245-1261.e21
pubmed: 33636132
Cell. 2019 Feb 7;176(4):882-896.e18
pubmed: 30639098
Proc Natl Acad Sci U S A. 2009 Dec 1;106(48):20371-6
pubmed: 19915142
Immunity. 2014 May 15;40(5):692-705
pubmed: 24792914
J Exp Med. 2019 Jul 1;216(7):1664-1681
pubmed: 31123085
Nat Commun. 2018 Oct 22;9(1):4369
pubmed: 30348969
Bioinformatics. 2013 Jan 1;29(1):15-21
pubmed: 23104886
Sci Immunol. 2020 Mar 6;5(45):
pubmed: 32144185
Immunol Rev. 2020 May;295(1):15-38
pubmed: 32212344
Curr Protoc Immunol. 2019 Feb;124(1):e62
pubmed: 30312021
Nature. 2021 Apr;592(7856):794-798
pubmed: 33854239
Nat Commun. 2019 Sep 27;10(1):4415
pubmed: 31562329
Mol Cell. 2020 Nov 5;80(3):384-395
pubmed: 32997964
J Immunol. 2013 Oct 1;191(7):3705-11
pubmed: 23980208
Cell. 2014 Oct 9;159(2):440-55
pubmed: 25263330
Nature. 2021 Apr;592(7856):799-803
pubmed: 33854232
Nature. 2008 Oct 9;455(7214):764-9
pubmed: 18843362
Immunity. 2016 Sep 20;45(3):540-554
pubmed: 27637146
Nat Biotechnol. 2019 Nov;37(11):1302-1313
pubmed: 31548728
Immunity. 2022 Jan 11;55(1):65-81.e9
pubmed: 34767747
Nat Rev Cancer. 2008 Nov;8(11):851-64
pubmed: 18846101
Immunity. 2014 Aug 21;41(2):325-38
pubmed: 25148027
Cancer Cell. 2007 May;11(5):407-20
pubmed: 17482131
Mol Cell. 2016 Nov 17;64(4):835-849
pubmed: 27818143
Front Immunol. 2018 May 23;9:1127
pubmed: 29875775
J Biol Chem. 2017 Jan 27;292(4):1211-1217
pubmed: 27974461
Immunity. 2001 Nov;15(5):763-74
pubmed: 11728338
Methods Enzymol. 2014;546:193-213
pubmed: 25398342
Elife. 2015 Oct 23;4:
pubmed: 26496200
Nat Rev Immunol. 2016 Oct;16(10):612-25
pubmed: 27573485
Nat Immunol. 2012 Nov;13(11):1083-91
pubmed: 23001145
Immunity. 2011 Dec 23;35(6):871-82
pubmed: 22195744
J Exp Med. 2021 Apr 5;218(4):
pubmed: 33332554
Cell. 2016 Oct 6;167(2):457-470.e13
pubmed: 27667687
Cell Rep Med. 2021 May 07;2(5):100262
pubmed: 34095875
Elife. 2016 Sep 30;5:
pubmed: 27690224
Int J Cell Biol. 2011;2011:470597
pubmed: 22190938

Auteurs

Bonnie Huang (B)

National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, 20892, USA. bonniehuangnih@gmail.com.
National Human Genome Research Institute, National Institutes of Health, Bethesda, MD, 20892, USA. bonniehuangnih@gmail.com.

James D Phelan (JD)

National Cancer Institute, National Institutes of Health, Bethesda, MD, 20892, USA.

Silvia Preite (S)

National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, 20892, USA.
National Human Genome Research Institute, National Institutes of Health, Bethesda, MD, 20892, USA.

Julio Gomez-Rodriguez (J)

National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, 20892, USA.
National Human Genome Research Institute, National Institutes of Health, Bethesda, MD, 20892, USA.
TCR2 Therapeutics, Cambridge, MA, 02142, USA.

Kristoffer H Johansen (KH)

National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, 20892, USA.
National Human Genome Research Institute, National Institutes of Health, Bethesda, MD, 20892, USA.

Hirofumi Shibata (H)

National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, 20892, USA.

Arthur L Shaffer (AL)

National Cancer Institute, National Institutes of Health, Bethesda, MD, 20892, USA.

Qin Xu (Q)

National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, 20892, USA.

Brendan Jeffrey (B)

National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, 20892, USA.

Martha Kirby (M)

National Human Genome Research Institute, National Institutes of Health, Bethesda, MD, 20892, USA.

Stacie Anderson (S)

National Human Genome Research Institute, National Institutes of Health, Bethesda, MD, 20892, USA.

Yandan Yang (Y)

National Cancer Institute, National Institutes of Health, Bethesda, MD, 20892, USA.

Selamawit Gossa (S)

National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD, 20892, USA.

Dorian B McGavern (DB)

National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD, 20892, USA.

Louis M Staudt (LM)

National Cancer Institute, National Institutes of Health, Bethesda, MD, 20892, USA.

Pamela L Schwartzberg (PL)

National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, 20892, USA. pams@nih.gov.
National Human Genome Research Institute, National Institutes of Health, Bethesda, MD, 20892, USA. pams@nih.gov.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH