Epitope-engineered human hematopoietic stem cells are shielded from CD123-targeted immunotherapy.


Journal

The Journal of experimental medicine
ISSN: 1540-9538
Titre abrégé: J Exp Med
Pays: United States
ID NLM: 2985109R

Informations de publication

Date de publication:
04 12 2023
Historique:
received: 17 07 2023
revised: 01 09 2023
accepted: 08 09 2023
medline: 5 10 2023
pubmed: 29 9 2023
entrez: 29 9 2023
Statut: ppublish

Résumé

Targeted eradication of transformed or otherwise dysregulated cells using monoclonal antibodies (mAb), antibody-drug conjugates (ADC), T cell engagers (TCE), or chimeric antigen receptor (CAR) cells is very effective for hematologic diseases. Unlike the breakthrough progress achieved for B cell malignancies, there is a pressing need to find suitable antigens for myeloid malignancies. CD123, the interleukin-3 (IL-3) receptor alpha-chain, is highly expressed in various hematological malignancies, including acute myeloid leukemia (AML). However, shared CD123 expression on healthy hematopoietic stem and progenitor cells (HSPCs) bears the risk for myelotoxicity. We demonstrate that epitope-engineered HSPCs were shielded from CD123-targeted immunotherapy but remained functional, while CD123-deficient HSPCs displayed a competitive disadvantage. Transplantation of genome-edited HSPCs could enable tumor-selective targeted immunotherapy while rebuilding a fully functional hematopoietic system. We envision that this approach is broadly applicable to other targets and cells, could render hitherto undruggable targets accessible to immunotherapy, and will allow continued posttransplant therapy, for instance, to treat minimal residual disease (MRD).

Identifiants

pubmed: 37773046
pii: 276306
doi: 10.1084/jem.20231235
pmc: PMC10541312
pii:
doi:

Substances chimiques

Interleukin-3 Receptor alpha Subunit 0
Epitopes 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2023 Marone et al.

Références

Cancer Discov. 2018 Oct;8(10):1219-1226
pubmed: 30135176
Sci Transl Med. 2011 Aug 10;3(95):95ra73
pubmed: 21832238
J Immunol Methods. 2008 Jan 1;329(1-2):112-24
pubmed: 17996249
Sci Transl Med. 2015 May 27;7(289):289ra82
pubmed: 26019218
Nat Commun. 2019 Feb 6;10(1):617
pubmed: 30728354
Cardiooncology. 2021 Oct 22;7(1):36
pubmed: 34686212
Blood. 2014 Jun 26;123(26):4064-76
pubmed: 24786772
Leukemia. 2000 Oct;14(10):1777-84
pubmed: 11021753
J Mol Biol. 1971 Feb 14;55(3):379-400
pubmed: 5551392
Bioinformatics. 2015 Mar 15;31(6):926-32
pubmed: 25398609
Cell Rep. 2014 Jul 24;8(2):410-9
pubmed: 25043189
Science. 2019 Apr 19;364(6437):286-289
pubmed: 31000663
CRISPR J. 2020 Dec;3(6):440-453
pubmed: 33346710
Cell. 2018 May 31;173(6):1439-1453.e19
pubmed: 29856956
Leukemia. 2019 Jan;33(1):64-74
pubmed: 29946192
N Engl J Med. 2011 Aug 25;365(8):725-33
pubmed: 21830940
Nature. 2022 Feb;602(7897):503-509
pubmed: 35110735
Nat Commun. 2019 Feb 6;10(1):616
pubmed: 30728353
Trends Biotechnol. 2022 Jul;40(7):875-890
pubmed: 35078657
J Immunother Cancer. 2020 Jun;8(1):
pubmed: 32527933
N Engl J Med. 2014 Oct 16;371(16):1507-17
pubmed: 25317870
Lancet. 2015 Feb 7;385(9967):517-528
pubmed: 25319501
Nat Biotechnol. 2017 Feb;35(2):128-135
pubmed: 28092658
Nat Biomed Eng. 2023 May;7(5):616-628
pubmed: 37069266
J Clin Invest. 1988 Oct;82(4):1282-7
pubmed: 3049674
Nat Med. 2022 Jun;28(6):1212-1223
pubmed: 35618837
Nat Biotechnol. 2020 Jan;38(1):44-49
pubmed: 31819258
Blood. 2011 Nov 3;118(18):4817-28
pubmed: 21849486
Cancer Cell. 2022 Jan 10;40(1):20-22
pubmed: 35016027
Bioinformatics. 2019 May 1;35(9):1582-1584
pubmed: 30304492
Bioinformatics. 2014 May 15;30(10):1473-5
pubmed: 24463181
Nat Med. 2022 Apr;28(4):678-689
pubmed: 35440724
Bioinformatics. 2008 Feb 1;24(3):333-40
pubmed: 18057019
Blood. 2014 Apr 10;123(15):2343-54
pubmed: 24596416
Cancer Discov. 2023 Jul 7;13(7):1720-1747
pubmed: 37012202
Nature. 2016 Nov 17;539(7629):384-389
pubmed: 27820943
Leukemia. 2019 Mar;33(3):762-808
pubmed: 30291334
Cell Stem Cell. 2021 Jun 3;28(6):1136-1147.e5
pubmed: 33626327
Nat Biotechnol. 2020 Jul;38(7):824-844
pubmed: 32572269
Nature. 2017 Mar 2;543(7643):113-117
pubmed: 28225754
Eur J Immunol. 2021 Sep;51(9):2151-2163
pubmed: 34196410
Sci Immunol. 2021 Aug 19;6(62):
pubmed: 34413140
Exp Hematol. 2004 Mar;32(3):277-81
pubmed: 15003313
Proc Natl Acad Sci U S A. 2019 Jun 11;116(24):11978-11987
pubmed: 31138698
Cell. 2022 Jul 21;185(15):2789-2805
pubmed: 35868279
F1000Res. 2016 Feb 18;5:189
pubmed: 26973785
Sci Transl Med. 2016 Oct 12;8(360):360ra134
pubmed: 27733558
N Engl J Med. 2021 Aug 5;385(6):567-569
pubmed: 34347960
Science. 2018 Mar 23;359(6382):1361-1365
pubmed: 29567707
Phys Rev E Stat Nonlin Soft Matter Phys. 2013 Jan;87(1):012707
pubmed: 23410359
Nat Med. 2019 Sep;25(9):1341-1355
pubmed: 31501612
Nat Commun. 2018 Jan 26;9(1):386
pubmed: 29374162
Nat Biotechnol. 2019 Mar;37(3):224-226
pubmed: 30809026
Nat Biotechnol. 2016 Jul;34(7):738-45
pubmed: 27272386
Cell. 2020 Apr 30;181(3):728-744.e21
pubmed: 32302591
Nature. 2019 Dec;576(7786):293-300
pubmed: 31802004
Leukemia. 2023 Apr;37(4):765-775
pubmed: 36739349
J Am Coll Cardiol. 2014 Mar 18;63(10):1011-9
pubmed: 24184252
N Engl J Med. 2023 Sep 7;389(10):899-910
pubmed: 37314354
Haematologica. 2023 Feb 01;108(2):457-471
pubmed: 35950535
Nature. 2018 Jul;559(7714):405-409
pubmed: 29995861
J Immunol. 2018 Apr 1;200(7):2489-2501
pubmed: 29445007
Blood Adv. 2018 Apr 24;2(8):848-858
pubmed: 29661755
J Cell Physiol. 1989 Aug;140(2):323-34
pubmed: 2663885
Cancer Cell. 2017 Oct 9;32(4):506-519.e5
pubmed: 29017060
Science. 2007 Nov 23;318(5854):1296-9
pubmed: 18033883
Front Genome Ed. 2023 Feb 20;5:1130736
pubmed: 36890979
Leukemia. 2014 Nov;28(11):2213-21
pubmed: 24705479
Leuk Res. 2019 Sep;84:106178
pubmed: 31326578
J Clin Invest. 2016 Nov 1;126(11):4262-4272
pubmed: 27760047
Nat Commun. 2022 Aug 11;13(1):4724
pubmed: 35953477
Blood. 2010 Nov 18;116(20):4099-102
pubmed: 20668228
Mol Ther. 2018 May 2;26(5):1181-1197
pubmed: 29622475
Antibodies (Basel). 2019 Jul 03;8(3):
pubmed: 31544847
Leukemia. 2020 Oct;34(10):2688-2703
pubmed: 32358567

Auteurs

Romina Marone (R)

Department of Biomedicine, Basel University Hospital and University of Basel, Basel, Switzerland.
Transplantation Immunology and Nephrology, Basel University Hospital, Basel, Switzerland.

Emmanuelle Landmann (E)

Department of Biomedicine, Basel University Hospital and University of Basel, Basel, Switzerland.
Transplantation Immunology and Nephrology, Basel University Hospital, Basel, Switzerland.

Anna Devaux (A)

Department of Biomedicine, Basel University Hospital and University of Basel, Basel, Switzerland.
Transplantation Immunology and Nephrology, Basel University Hospital, Basel, Switzerland.

Rosalba Lepore (R)

Department of Biomedicine, Basel University Hospital and University of Basel, Basel, Switzerland.
Transplantation Immunology and Nephrology, Basel University Hospital, Basel, Switzerland.
Cimeio Therapeutics AG , Basel, Switzerland.
Ridgeline Discovery GmbH , Basel, Switzerland.

Denis Seyres (D)

Department of Biomedicine, Basel University Hospital and University of Basel, Basel, Switzerland.
Transplantation Immunology and Nephrology, Basel University Hospital, Basel, Switzerland.

Jessica Zuin (J)

Department of Biomedicine, Basel University Hospital and University of Basel, Basel, Switzerland.
Transplantation Immunology and Nephrology, Basel University Hospital, Basel, Switzerland.

Thomas Burgold (T)

Department of Biomedicine, Basel University Hospital and University of Basel, Basel, Switzerland.
Transplantation Immunology and Nephrology, Basel University Hospital, Basel, Switzerland.

Corinne Engdahl (C)

Department of Biomedicine, Basel University Hospital and University of Basel, Basel, Switzerland.
Transplantation Immunology and Nephrology, Basel University Hospital, Basel, Switzerland.

Giuseppina Capoferri (G)

Department of Biomedicine, Basel University Hospital and University of Basel, Basel, Switzerland.
Transplantation Immunology and Nephrology, Basel University Hospital, Basel, Switzerland.

Alessandro Dell'Aglio (A)

Department of Biomedicine, Basel University Hospital and University of Basel, Basel, Switzerland.
Transplantation Immunology and Nephrology, Basel University Hospital, Basel, Switzerland.

Clément Larrue (C)

Translational Research Centre in Onco-Hematology, Faculty of Medicine, University of Geneva, and Swiss Cancer Center Leman, Geneva, Switzerland.

Federico Simonetta (F)

Division of Hematology, Department of Oncology, Geneva University Hospitals, Geneva, Switzerland.
Department of Medicine, Translational Research Center for Onco-Hematology, Faculty of Medicine, University of Geneva, Geneva, Switzerland.

Julia Rositzka (J)

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

Manuel Rhiel (M)

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

Geoffroy Andrieux (G)

Institute of Medical Bioinformatics and Systems Medicine, Medical Center-University of Freiburg , Freiburg, Germany.

Danielle N Gallagher (DN)

Department of Biology, Institute of Molecular Health Sciences, ETH Zürich, Zürich, Switzerland.

Markus S Schröder (MS)

Department of Biology, Institute of Molecular Health Sciences, ETH Zürich, Zürich, Switzerland.

Amélie Wiederkehr (A)

Ridgeline Discovery GmbH , Basel, Switzerland.

Alessandro Sinopoli (A)

Ridgeline Discovery GmbH , Basel, Switzerland.

Valentin Do Sacramento (V)

Cimeio Therapeutics AG , Basel, Switzerland.

Anna Haydn (A)

Ridgeline Discovery GmbH , Basel, Switzerland.

Laura Garcia-Prat (L)

Cimeio Therapeutics AG , Basel, Switzerland.

Christopher Divsalar (C)

Ridgeline Discovery GmbH , Basel, Switzerland.

Anna Camus (A)

Cimeio Therapeutics AG , Basel, Switzerland.

Liwen Xu (L)

Department of Pediatrics, School of Medicine, Stanford University, Stanford, CA, USA.

Lorenza Bordoli (L)

Biozentrum, University of Basel , Basel, Switzerland.
SIB Swiss Institute of Bioinformatics , Basel, Switzerland.

Torsten Schwede (T)

Biozentrum, University of Basel , Basel, Switzerland.
SIB Swiss Institute of Bioinformatics , Basel, Switzerland.

Matthew Porteus (M)

Department of Pediatrics, School of Medicine, Stanford University, Stanford, CA, USA.

Jérôme Tamburini (J)

Department of Medicine, Translational Research Center for Onco-Hematology, Faculty of Medicine, University of Geneva, Geneva, Switzerland.

Jacob E Corn (JE)

Department of Biology, Institute of Molecular Health Sciences, ETH Zürich, Zürich, Switzerland.

Toni Cathomen (T)

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

Tatjana I Cornu (TI)

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

Stefanie Urlinger (S)

Cimeio Therapeutics AG , Basel, Switzerland.
Ridgeline Discovery GmbH , Basel, Switzerland.

Lukas T Jeker (LT)

Department of Biomedicine, Basel University Hospital and University of Basel, Basel, Switzerland.
Transplantation Immunology and Nephrology, Basel University Hospital, Basel, Switzerland.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH