Adoptive T cell therapy cures mice from active hemophagocytic lymphohistiocytosis (HLH).

adoptive T cell therapy hemophagocytic lymphohistiocytosis hyperinflammation virus-specific T cells

Journal

EMBO molecular medicine
ISSN: 1757-4684
Titre abrégé: EMBO Mol Med
Pays: England
ID NLM: 101487380

Informations de publication

Date de publication:
07 12 2022
Historique:
revised: 27 09 2022
received: 05 04 2022
accepted: 29 09 2022
pubmed: 25 10 2022
medline: 15 12 2022
entrez: 24 10 2022
Statut: ppublish

Résumé

Primary hemophagocytic lymphohistiocytosis (HLH) is a hyperinflammatory syndrome caused by impaired lymphocyte cytotoxicity. First-line therapeutic regimens directed against activated immune cells or secreted cytokines show limited efficacy since they do not target the underlying immunological problem: defective lymphocyte cytotoxicity causing prolonged immune stimulation. A potential rescue strategy would be the adoptive transfer of ex vivo gene-corrected autologous T cells. However, transfusion of cytotoxicity-competent T cells under conditions of hyperinflammation may cause more harm than benefit. As a proof-of-concept for adoptive T cell therapy (ATCT) under hyperinflammatory conditions, we transferred syngeneic, cytotoxicity-competent T cells into mice with virally triggered active primary HLH. ATCT with functional syngeneic trigger-specific T cells cured Jinx mice from active HLH without life-threatening side effects and protected Perforin-deficient mice from lethal HLH progression by reconstituting cytotoxicity. Cured mice were protected long-term from HLH relapses. A threshold frequency of transferred T cells with functional differentiation was identified as a predictive biomarker for long-term survival. This study is the first proof-of-concept for ATCT in active HLH.

Identifiants

pubmed: 36278424
doi: 10.15252/emmm.202216085
pmc: PMC9728053
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e16085

Informations de copyright

© 2022 The Authors. Published under the terms of the CC BY 4.0 license.

Références

Hum Gene Ther. 2016 Oct;27(10):847-859
pubmed: 27471778
Hum Gene Ther. 2020 Jun;31(11-12):626-638
pubmed: 32253931
Pediatr Blood Cancer. 2007 Feb;48(2):124-31
pubmed: 16937360
J Allergy Clin Immunol. 2016 Sep;138(3):920-924.e3
pubmed: 27246524
J Exp Med. 1998 Dec 21;188(12):2199-204
pubmed: 9858506
Proc Natl Acad Sci U S A. 2011 Dec 27;108(52):21182-7
pubmed: 22160724
Blood. 2004 Aug 1;104(3):735-43
pubmed: 15069016
Nat Med. 2018 Jun;24(6):739-748
pubmed: 29808007
Hum Gene Ther. 2019 Aug;30(8):975-984
pubmed: 31032638
Science. 1994 Jul 22;265(5171):528-30
pubmed: 7518614
EMBO Mol Med. 2022 Dec 7;14(12):e16085
pubmed: 36278424
N Engl J Med. 2020 May 7;382(19):1811-1822
pubmed: 32374962
Blood Adv. 2017 Nov 02;1(24):2193-2205
pubmed: 29296867
Blood. 2016 Jun 30;127(26):3331-40
pubmed: 27207801
Blood. 2010 Feb 4;115(5):925-35
pubmed: 19880495
Blood Adv. 2020 Aug 11;4(15):3754-3766
pubmed: 32780845
Br J Haematol. 2019 Oct;187(2):206-218
pubmed: 31219185
Blood. 2013 Oct 10;122(15):2618-21
pubmed: 23974195
Transplantation. 2001 Oct 27;72(8):1399-402
pubmed: 11685111
J Virol. 1994 Dec;68(12):8056-63
pubmed: 7966595
J Virol. 2005 Sep;79(18):12112-6
pubmed: 16140789
Blood. 2016 Mar 31;127(13):1666-75
pubmed: 26825707
Nat Med. 2018 Jun;24(6):731-738
pubmed: 29808005
Blood. 2019 Nov 21;134(21):1783-1786
pubmed: 31537529
Cell. 2002 Dec 13;111(6):837-51
pubmed: 12526810
Transpl Int. 2016 May;29(5):515-26
pubmed: 26284570
Transpl Immunol. 2022 Apr;71:101539
pubmed: 35051589
J Exp Med. 2007 Apr 16;204(4):853-63
pubmed: 17420270
Blood. 2018 Jul 5;132(1):89-100
pubmed: 29632024
J Clin Oncol. 2017 Nov 1;35(31):3547-3557
pubmed: 28783452
J Allergy Clin Immunol. 2018 Sep;142(3):904-913.e3
pubmed: 29355678
Immunity. 2007 Aug;27(2):281-95
pubmed: 17723218
Pediatrics. 2007 Sep;120(3):e622-8
pubmed: 17698967
Immune Netw. 2020 Feb 20;20(1):e2
pubmed: 32158590
J Allergy Clin Immunol. 2016 May;137(5):1498-1505.e1
pubmed: 26920464
Leukemia. 2017 Oct;31(10):2161-2171
pubmed: 28090089
Eur J Pediatr. 1983 Jun-Jul;140(3):221-30
pubmed: 6354720
Eur J Immunol. 2022 May;52(5):705-716
pubmed: 35355253
Blood. 2016 Dec 15;128(24):2859-2862
pubmed: 27799161
Acta Paediatr. 2021 Nov;110(11):2903-2911
pubmed: 34192386
Blood. 2011 Oct 27;118(17):4620-9
pubmed: 21878672
Front Immunol. 2020 May 08;11:808
pubmed: 32457750
Eur J Immunol. 2017 Feb;47(2):364-373
pubmed: 27925643
J Virol Methods. 1991 Jun;33(1-2):191-8
pubmed: 1939506
Cell. 2020 Apr 2;181(1):46-62
pubmed: 32243795
Blood. 2016 Jul 7;128(1):60-71
pubmed: 27222478
Mol Ther. 2015 Apr;23(4):737-45
pubmed: 25523759
J Immunol. 1998 Jun 15;160(12):6204-9
pubmed: 9637540
J Allergy Clin Immunol Pract. 2019 Mar;7(3):809-818
pubmed: 30581131
Haematologica. 2021 Jul 01;106(7):1892-1901
pubmed: 32732367
Front Immunol. 2013 Dec 16;4:448
pubmed: 24379813
Blood. 2009 Nov 5;114(19):4283-92
pubmed: 19700662
Sci Transl Med. 2014 Jun 25;6(242):242ra83
pubmed: 24964991
Blood Rev. 2014 Jul;28(4):135-42
pubmed: 24792320
F1000Res. 2015 Sep 30;4(F1000 Faculty Rev):930
pubmed: 26594351
Blood. 2016 May 26;127(21):2513-22
pubmed: 26903548
Eur J Immunol. 2020 Nov;50(11):1770-1782
pubmed: 32419134
J Allergy Clin Immunol Pract. 2018 Sep - Oct;6(5):1508-1517
pubmed: 30201097
J Allergy Clin Immunol. 2022 May;149(5):1592-1606.e16
pubmed: 35304157
J Immunol. 2001 Nov 1;167(9):4838-43
pubmed: 11673487
Blood. 2012 Mar 15;119(11):2644-56
pubmed: 22138512
J Exp Med. 2008 Mar 17;205(3):625-40
pubmed: 18316415
Blood. 2020 Apr 16;135(16):1332-1343
pubmed: 32107531
J Clin Immunol. 2021 Nov;41(8):1794-1803
pubmed: 34389889
Blood Adv. 2017 Dec 21;1(27):2781-2789
pubmed: 29296930
Br J Haematol. 2021 Feb;192(3):433-443
pubmed: 33280098
Blood. 2017 Dec 21;130(25):2692-2693
pubmed: 29269529
Pediatr Blood Cancer. 2015 Feb;62(2):346-352
pubmed: 25382070
Blood. 2013 Jun 27;121(26):5184-91
pubmed: 23660960
Front Immunol. 2021 Feb 16;12:614704
pubmed: 33664745
Blood. 2014 Jul 24;124(4):628-37
pubmed: 24855206
J Allergy Clin Immunol. 2018 Jul;142(1):235-245.e6
pubmed: 29705247
Blood. 2013 Jan 24;121(4):604-13
pubmed: 23190531
Nat Rev Immunol. 2019 Nov;19(11):665-674
pubmed: 31570879
Nature. 1994 May 5;369(6475):31-7
pubmed: 8164737
Pediatr Blood Cancer. 2018 Nov;65(11):e27344
pubmed: 30070073
Immunol Rev. 2010 May;235(1):10-23
pubmed: 20536552
Blood. 2020 Feb 27;135(9):620-628
pubmed: 31942610
Semin Immunol. 2009 Apr;21(2):62-8
pubmed: 19269852
Front Immunol. 2013 Jan 28;3:410
pubmed: 23372567
Immunity. 2014 Jul 17;41(1):116-26
pubmed: 25035956
Blood. 2017 Dec 21;130(25):2728-2738
pubmed: 28935695
Blood. 2016 Jun 23;127(25):3281-90
pubmed: 27099148
Nat Rev Immunol. 2002 Apr;2(4):251-62
pubmed: 12001996
J Hematol Oncol. 2019 Feb 6;12(1):13
pubmed: 30728058
Acta Paediatr Scand. 1991 Apr;80(4):428-35
pubmed: 2058392
Br J Clin Pharmacol. 2021 Jun;87(6):2414-2424
pubmed: 32463929

Auteurs

Kristoffer Weißert (K)

Institute for Immunodeficiency, Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
Center for Chronic Immunodeficiency (CCI), Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
Faculty of Biology, Albert-Ludwigs-University of Freiburg, Freiburg, Germany.

Sandra Ammann (S)

Institute for Immunodeficiency, Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
Center for Chronic Immunodeficiency (CCI), Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.

Tamara Kögl (T)

Center for Chronic Immunodeficiency (CCI), Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
Institute for Immunology, Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.

Viviane Dettmer-Monaco (V)

Center for Chronic Immunodeficiency (CCI), Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
Institute for Transfusion Medicine and Gene Therapy, Medical Center, University of Freiburg, Freiburg, Germany.

Christoph Schell (C)

Institute of Surgical Pathology, Medical Center, University of Freiburg, Freiburg, Germany.

Toni Cathomen (T)

Center for Chronic Immunodeficiency (CCI), Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
Institute for Transfusion Medicine and Gene Therapy, Medical Center, University of Freiburg, Freiburg, Germany.

Stephan Ehl (S)

Institute for Immunodeficiency, Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
Center for Chronic Immunodeficiency (CCI), Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
Center for Integrative Biological Signalling Studies, Albert-Ludwigs-University of Freiburg, Freiburg, Germany.

Peter Aichele (P)

Institute for Immunodeficiency, Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
Center for Chronic Immunodeficiency (CCI), Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.

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