Antigen presentation safeguards the integrity of the hematopoietic stem cell pool.

CD4(+) T cells acute myeloid leukemia antigen presentation hematopoietic stem cells immune regulation immunosurveillance leukemia

Journal

Cell stem cell
ISSN: 1875-9777
Titre abrégé: Cell Stem Cell
Pays: United States
ID NLM: 101311472

Informations de publication

Date de publication:
05 05 2022
Historique:
received: 29 06 2020
revised: 08 12 2021
accepted: 08 04 2022
pubmed: 7 5 2022
medline: 11 5 2022
entrez: 6 5 2022
Statut: ppublish

Résumé

Hematopoietic stem and progenitor cells (HSPCs) are responsible for the production of blood and immune cells. Throughout life, HSPCs acquire oncogenic aberrations that can cause hematological cancers. Although molecular programs maintaining stem cell integrity have been identified, safety mechanisms eliminating malignant HSPCs from the stem cell pool remain poorly characterized. Here, we show that HSPCs constitutively present antigens via major histocompatibility complex class II. The presentation of immunogenic antigens, as occurring during malignant transformation, triggers bidirectional interactions between HSPCs and antigen-specific CD4

Identifiants

pubmed: 35523139
pii: S1934-5909(22)00160-6
doi: 10.1016/j.stem.2022.04.007
pmc: PMC9202612
mid: NIHMS1803993
pii:
doi:

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

760-775.e10

Subventions

Organisme : NIAID NIH HHS
ID : P01 AI056299
Pays : United States
Organisme : NIAID NIH HHS
ID : P01 AI073748
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI144166
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS030843
Pays : United States

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2022 Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests V.K.K. is a cofounder, has ownership interest, and is on the SAB of Celsius Therapeutics and Tizona Therapeutics.

Références

Nat Methods. 2013 Nov;10(11):1096-8
pubmed: 24056875
J Exp Med. 2003 May 5;197(9):1073-81
pubmed: 12732654
Cell Stem Cell. 2012 Feb 3;10(2):120-36
pubmed: 22305562
Nat Rev Immunol. 2017 Jun;17(6):349-362
pubmed: 28436425
Nature. 2017 Mar 9;543(7644):205-210
pubmed: 28241143
Front Pharmacol. 2019 Jun 06;10:609
pubmed: 31244654
Cell Stem Cell. 2015 Oct 1;17(4):422-34
pubmed: 26299573
Blood. 1998 Sep 1;92(5):1677-84
pubmed: 9716596
Nature. 2018 Jun;558(7710):454-459
pubmed: 29899446
Blood. 2002 Sep 1;100(5):1570-4
pubmed: 12176872
Nat Protoc. 2014 Jan;9(1):171-81
pubmed: 24385147
N Engl J Med. 2014 Dec 25;371(26):2477-87
pubmed: 25426838
Sci Immunol. 2020 Feb 21;5(44):
pubmed: 32086381
Nat Commun. 2019 Jun 3;10(1):2395
pubmed: 31160568
Nature. 1991 Oct 17;353(6345):660-2
pubmed: 1656278
Blood. 1982 Sep;60(3):703-13
pubmed: 6286014
Immunol Rev. 2010 Nov;238(1):247-62
pubmed: 20969597
Cell. 2018 Nov 1;175(4):908-920
pubmed: 30388451
Immunol Cell Biol. 1998 Feb;76(1):34-40
pubmed: 9553774
Annu Rev Immunol. 2013;31:563-604
pubmed: 23516985
Cell. 1996 Feb 9;84(3):443-50
pubmed: 8608598
Cell. 1993 Oct 8;75(1):135-46
pubmed: 8402893
Nat Med. 2009 Jun;15(6):696-700
pubmed: 19483695
Front Immunol. 2021 Mar 10;12:633436
pubmed: 33777019
Cell Stem Cell. 2021 Nov 4;28(11):1922-1935.e5
pubmed: 34529935
Science. 1994 Jul 1;265(5168):106-9
pubmed: 8016643
Nat Rev Immunol. 2011 Nov 11;11(12):823-36
pubmed: 22076556
Nat Med. 2019 Apr;25(4):603-611
pubmed: 30911134
Cell. 2018 Nov 15;175(5):1307-1320.e22
pubmed: 30392957
OMICS. 2012 May;16(5):284-7
pubmed: 22455463
Nature. 2009 Apr 16;458(7240):904-8
pubmed: 19212321
Genome Biol. 2014;15(12):550
pubmed: 25516281
Nature. 1989 Apr 27;338(6218):765-8
pubmed: 2469959
Leukemia. 1999 Oct;13(10):1513-8
pubmed: 10516751
Nat Rev Immunol. 2014 Nov;14(11):719-30
pubmed: 25324123
Nat Immunol. 2010 Dec;11(12):1093-101
pubmed: 20953201
J Exp Med. 1998 Feb 16;187(4):571-8
pubmed: 9463407
N Engl J Med. 1981 Jul 2;305(1):17-25
pubmed: 6785649
Nature. 2014 Jun 12;510(7504):268-72
pubmed: 24776803
Stem Cell Reports. 2016 Jun 14;6(6):940-956
pubmed: 27264973
Blood. 2015 Apr 23;125(17):2605-13
pubmed: 25762175
Leukemia. 2015 Mar;29(3):647-59
pubmed: 25092142
Eur J Immunol. 1983 Feb;13(2):172-6
pubmed: 6187581
Cell Stem Cell. 2017 Aug 3;21(2):225-240.e5
pubmed: 28736216
Cell Rep. 2020 Nov 24;33(8):108433
pubmed: 33238123
Nat Methods. 2007 Nov;4(11):923-5
pubmed: 17952086
Leukemia. 2012 Sep;26(9):1908-75
pubmed: 22552007
Cell Stem Cell. 2014 Oct 2;15(4):507-522
pubmed: 25158935
Nature. 2014 Aug 21;512(7514):324-7
pubmed: 25043048
Cancer Res. 2019 May 15;79(10):2466-2479
pubmed: 30940663
Blood. 1985 Apr;65(4):819-22
pubmed: 3884061
Cell. 2011 Jan 21;144(2):296-309
pubmed: 21241896
Nature. 2005 Jun 2;435(7042):590-7
pubmed: 15931211
Exp Hematol. 2018 Dec;68:51-61
pubmed: 30243574
N Engl J Med. 2013 May 30;368(22):2059-74
pubmed: 23634996
Stem Cell Reports. 2014 Nov 11;3(5):858-75
pubmed: 25418729
Eur J Immunol. 2007 Nov;37 Suppl 1:S53-60
pubmed: 17972346
Bioinformatics. 2016 Sep 15;32(18):2847-9
pubmed: 27207943
Acta Haematol. 1982;68(1):3-13
pubmed: 6214917
Cell. 2015 Aug 27;162(5):1078-89
pubmed: 26317471
Leukemia. 2013 Apr;27(4):852-60
pubmed: 23235717
J Clin Invest. 2020 Apr 1;130(4):1552-1564
pubmed: 32235097
Immunogenetics. 2019 Mar;71(3):171-187
pubmed: 30421030
PLoS One. 2016 Sep 09;11(9):e0162382
pubmed: 27611583
N Engl J Med. 2018 Oct 25;379(17):1643-1656
pubmed: 30354958
Blood. 1994 Dec 15;84(12):4257-61
pubmed: 7994040
Leukemia. 2010 Jun;24(6):1216-20
pubmed: 20428199
Blood. 1994 Aug 1;84(3):923-7
pubmed: 8043874
Blood. 2010 Jun 10;115(23):4934-43
pubmed: 20200356
Blood. 1997 Aug 1;90(3):1083-90
pubmed: 9242539
Nature. 2006 Aug 17;442(7104):818-22
pubmed: 16862118
Nat Commun. 2017 May 09;8:15068
pubmed: 28485401
Cell Stem Cell. 2018 Mar 1;22(3):445-453.e5
pubmed: 29456159
Nature. 2010 Jun 10;465(7299):793-7
pubmed: 20535209
Methods Mol Biol. 2013;960:145-157
pubmed: 23329485
Nature. 1991 May 23;351(6324):290-6
pubmed: 1709722
Immunity. 2003 May;18(5):605-17
pubmed: 12753738
Nat Rev Immunol. 2015 Apr;15(4):203-16
pubmed: 25720354
Cell Rep. 2017 Jun 13;19(11):2345-2356
pubmed: 28614719
Cell. 2017 Jun 1;169(6):1119-1129.e11
pubmed: 28552347
Nature. 2015 Apr 23;520(7548):549-52
pubmed: 25707806
Nature. 2011 Jun 08;474(7350):216-9
pubmed: 21654805
Cell. 2013 Dec 5;155(6):1282-95
pubmed: 24315098
Br J Haematol. 2020 Jan;188(1):147-158
pubmed: 31782805
Nature. 2016 Dec 15;540(7633):433-437
pubmed: 27926740
Leukemia. 2019 Apr;33(4):1043-1047
pubmed: 30622284
Immunol Invest. 2009;38(8):812-9
pubmed: 19860590
N Engl J Med. 2014 Dec 25;371(26):2488-98
pubmed: 25426837
Nature. 2007 Nov 22;450(7169):566-9
pubmed: 18033300
Hum Immunol. 2011 Oct;72(10):889-92
pubmed: 21762745
N Engl J Med. 2018 Dec 13;379(24):2330-2341
pubmed: 30380364
J Exp Med. 2010 Jan 18;207(1):189-206
pubmed: 20038600
Cancer Res. 2004 Nov 15;64(22):8451-5
pubmed: 15548717
Tissue Antigens. 1979 Jan;13(1):45-22
pubmed: 84415

Auteurs

Pablo Hernández-Malmierca (P)

Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM gGmbH), Heidelberg, Germany; Division of Stem Cells and Cancer, Deutsches Krebsforschungszentrum (DKFZ), and DKFZ-ZMBH Alliance, Heidelberg, Germany; Faculty of Biosciences, Heidelberg University, Heidelberg, Germany.

Dominik Vonficht (D)

Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM gGmbH), Heidelberg, Germany; Division of Stem Cells and Cancer, Deutsches Krebsforschungszentrum (DKFZ), and DKFZ-ZMBH Alliance, Heidelberg, Germany; Faculty of Biosciences, Heidelberg University, Heidelberg, Germany.

Alexandra Schnell (A)

Evergrande Center for Immunologic Diseases, Harvard Medical School, and Brigham and Women's Hospital, Boston, MA, USA; Klarman Cell Observatory, Broad Institute of MIT and Harvard, Cambridge, MA, USA.

Hannah J Uckelmann (HJ)

Department of Pediatric Oncology, Dana-Farber Cancer Institute, and Division of Hematology/Oncology, Boston, MA, USA; Boston Children's Hospital and Harvard Medical School, Boston, MA, USA.

Alina Bollhagen (A)

Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM gGmbH), Heidelberg, Germany; Division of Stem Cells and Cancer, Deutsches Krebsforschungszentrum (DKFZ), and DKFZ-ZMBH Alliance, Heidelberg, Germany.

Mohamed A A Mahmoud (MAA)

Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM gGmbH), Heidelberg, Germany; Division of Stem Cells and Cancer, Deutsches Krebsforschungszentrum (DKFZ), and DKFZ-ZMBH Alliance, Heidelberg, Germany.

Sophie-Luise Landua (SL)

Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM gGmbH), Heidelberg, Germany; Division of Stem Cells and Cancer, Deutsches Krebsforschungszentrum (DKFZ), and DKFZ-ZMBH Alliance, Heidelberg, Germany.

Elise van der Salm (E)

Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM gGmbH), Heidelberg, Germany; Division of Stem Cells and Cancer, Deutsches Krebsforschungszentrum (DKFZ), and DKFZ-ZMBH Alliance, Heidelberg, Germany.

Christine L Trautmann (CL)

Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM gGmbH), Heidelberg, Germany; Division of Stem Cells and Cancer, Deutsches Krebsforschungszentrum (DKFZ), and DKFZ-ZMBH Alliance, Heidelberg, Germany.

Simon Raffel (S)

Department of Hematology, Oncology and Rheumatology, University of Heidelberg, Heidelberg, Germany.

Florian Grünschläger (F)

Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM gGmbH), Heidelberg, Germany; Division of Stem Cells and Cancer, Deutsches Krebsforschungszentrum (DKFZ), and DKFZ-ZMBH Alliance, Heidelberg, Germany; Faculty of Biosciences, Heidelberg University, Heidelberg, Germany.

Raphael Lutz (R)

Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM gGmbH), Heidelberg, Germany; Division of Stem Cells and Cancer, Deutsches Krebsforschungszentrum (DKFZ), and DKFZ-ZMBH Alliance, Heidelberg, Germany; Department of Hematology, Oncology and Rheumatology, University of Heidelberg, Heidelberg, Germany.

Michael Ghosh (M)

Department of Immunology, Institute for Cell Biology, University of Tübingen, Tübingen, Germany.

Simon Renders (S)

Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM gGmbH), Heidelberg, Germany; Division of Stem Cells and Cancer, Deutsches Krebsforschungszentrum (DKFZ), and DKFZ-ZMBH Alliance, Heidelberg, Germany; Department of Hematology, Oncology and Rheumatology, University of Heidelberg, Heidelberg, Germany.

Nádia Correia (N)

Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM gGmbH), Heidelberg, Germany; Division of Stem Cells and Cancer, Deutsches Krebsforschungszentrum (DKFZ), and DKFZ-ZMBH Alliance, Heidelberg, Germany.

Elisa Donato (E)

Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM gGmbH), Heidelberg, Germany; Division of Stem Cells and Cancer, Deutsches Krebsforschungszentrum (DKFZ), and DKFZ-ZMBH Alliance, Heidelberg, Germany.

Karin O Dixon (KO)

Evergrande Center for Immunologic Diseases, Harvard Medical School, and Brigham and Women's Hospital, Boston, MA, USA; Klarman Cell Observatory, Broad Institute of MIT and Harvard, Cambridge, MA, USA.

Christoph Hirche (C)

Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM gGmbH), Heidelberg, Germany; Division of Inflammatory Stress in Stem Cells, Deutsches Krebsforschungszentrum (DKFZ) and DKFZ-ZMBH Alliance, Heidelberg, Germany.

Carolin Andresen (C)

Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM gGmbH), Heidelberg, Germany; Division of Stem Cells and Cancer, Deutsches Krebsforschungszentrum (DKFZ), and DKFZ-ZMBH Alliance, Heidelberg, Germany; Faculty of Biosciences, Heidelberg University, Heidelberg, Germany.

Claudia Robens (C)

Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM gGmbH), Heidelberg, Germany; Division of Stem Cells and Cancer, Deutsches Krebsforschungszentrum (DKFZ), and DKFZ-ZMBH Alliance, Heidelberg, Germany.

Paula S Werner (PS)

Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM gGmbH), Heidelberg, Germany; Division of Inflammatory Stress in Stem Cells, Deutsches Krebsforschungszentrum (DKFZ) and DKFZ-ZMBH Alliance, Heidelberg, Germany.

Tobias Boch (T)

Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM gGmbH), Heidelberg, Germany; Division of Stem Cells and Cancer, Deutsches Krebsforschungszentrum (DKFZ), and DKFZ-ZMBH Alliance, Heidelberg, Germany; Department of Hematology and Oncology, University Hospital Mannheim, Mannheim, Germany; Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.

David Eisel (D)

Research Group GMP & T Cell Therapy, Deutsches Krebsforschungszentrum (DKFZ), Heidelberg, Germany.

Wolfram Osen (W)

Research Group GMP & T Cell Therapy, Deutsches Krebsforschungszentrum (DKFZ), Heidelberg, Germany.

Franziska Pilz (F)

Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM gGmbH), Heidelberg, Germany; Division of Inflammatory Stress in Stem Cells, Deutsches Krebsforschungszentrum (DKFZ) and DKFZ-ZMBH Alliance, Heidelberg, Germany.

Adriana Przybylla (A)

Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM gGmbH), Heidelberg, Germany; Division of Stem Cells and Cancer, Deutsches Krebsforschungszentrum (DKFZ), and DKFZ-ZMBH Alliance, Heidelberg, Germany.

Corinna Klein (C)

Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM gGmbH), Heidelberg, Germany; Division of Stem Cells and Cancer, Deutsches Krebsforschungszentrum (DKFZ), and DKFZ-ZMBH Alliance, Heidelberg, Germany.

Frank Buchholz (F)

Medical Faculty, University Hospital Carl Gustav Carus, NCT/UCC Section Medical Systems Biology, TU Dresden, Dresden, Germany.

Michael D Milsom (MD)

Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM gGmbH), Heidelberg, Germany; Division of Experimental Hematology, Deutsches Krebsforschungszentrum (DKFZ) and DKFZ-ZMBH Alliance, Heidelberg, Germany.

Marieke A G Essers (MAG)

Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM gGmbH), Heidelberg, Germany; Division of Inflammatory Stress in Stem Cells, Deutsches Krebsforschungszentrum (DKFZ) and DKFZ-ZMBH Alliance, Heidelberg, Germany.

Stefan B Eichmüller (SB)

Research Group GMP & T Cell Therapy, Deutsches Krebsforschungszentrum (DKFZ), Heidelberg, Germany.

Wolf-Karsten Hofmann (WK)

Department of Hematology and Oncology, University Hospital Mannheim, Mannheim, Germany; Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.

Daniel Nowak (D)

Department of Hematology and Oncology, University Hospital Mannheim, Mannheim, Germany; Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.

Daniel Hübschmann (D)

Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM gGmbH), Heidelberg, Germany; Computational Oncology, Molecular Precision Oncology Program, National Center for Tumor Diseases (NCT) Heidelberg and Deutsches Krebsforschungszentrum (DKFZ), Heidelberg, Germany; German Cancer Consortium (DKTK), Heidelberg, Germany.

Michael Hundemer (M)

Department of Hematology, Oncology and Rheumatology, University of Heidelberg, Heidelberg, Germany.

Christian Thiede (C)

German Cancer Consortium (DKTK), Heidelberg, Germany; Medical Department 1, University Hospital Carl Gustav Carus, TU Dresden, Dresden, Germany.

Lars Bullinger (L)

German Cancer Consortium (DKTK), Heidelberg, Germany; Charité-Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Department of Hematology, Oncology and Cancer Immunology, Berlin, Germany.

Carsten Müller-Tidow (C)

Department of Hematology, Oncology and Rheumatology, University of Heidelberg, Heidelberg, Germany; Molecular Medicine Partnership Unit, European Molecular Biology Laboratory, University of Heidelberg, Heidelberg, Germany.

Scott A Armstrong (SA)

Department of Pediatric Oncology, Dana-Farber Cancer Institute, and Division of Hematology/Oncology, Boston, MA, USA; Boston Children's Hospital and Harvard Medical School, Boston, MA, USA.

Andreas Trumpp (A)

Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM gGmbH), Heidelberg, Germany; Division of Stem Cells and Cancer, Deutsches Krebsforschungszentrum (DKFZ), and DKFZ-ZMBH Alliance, Heidelberg, Germany; German Cancer Consortium (DKTK), Heidelberg, Germany. Electronic address: a.trumpp@dkfz.de.

Vijay K Kuchroo (VK)

Evergrande Center for Immunologic Diseases, Harvard Medical School, and Brigham and Women's Hospital, Boston, MA, USA; Klarman Cell Observatory, Broad Institute of MIT and Harvard, Cambridge, MA, USA. Electronic address: vkuchroo@evergrande.hms.harvard.edu.

Simon Haas (S)

Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM gGmbH), Heidelberg, Germany; Division of Stem Cells and Cancer, Deutsches Krebsforschungszentrum (DKFZ), and DKFZ-ZMBH Alliance, Heidelberg, Germany; German Cancer Consortium (DKTK), Heidelberg, Germany; Charité-Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Department of Hematology, Oncology and Cancer Immunology, Berlin, Germany; Berlin Institute of Health (BIH) at Charité - Universitätsmedizin Berlin, Berlin, Germany; Berlin Institute for Medical Systems Biology, Max Delbrück Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany. Electronic address: simon.haas@bih-charite.de.

Articles similaires

Humans Receptors, Antigen, T-Cell Proto-Oncogene Proteins p21(ras) Pancreatic Neoplasms T-Lymphocytes

A key role for P2RX5 in brown adipocyte differentiation and energy homeostasis.

Maria Razzoli, Seth McGonigle, Bhavani Shankar Sahu et al.
1.00
Animals Adipocytes, Brown Mice Cell Differentiation Male
Dendritic Cells Animals Cross-Priming Mice Mice, Inbred C57BL
Humans Formins Phosphorylation Exosomes Jurkat Cells

Classifications MeSH