Selective haematological cancer eradication with preserved haematopoiesis.


Journal

Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462

Informations de publication

Date de publication:
22 May 2024
Historique:
received: 07 08 2023
accepted: 23 04 2024
medline: 23 5 2024
pubmed: 23 5 2024
entrez: 22 5 2024
Statut: aheadofprint

Résumé

Haematopoietic stem cell (HSC) transplantation (HSCT) is the only curative treatment for a broad range of haematological malignancies, but the standard of care relies on untargeted chemotherapies and limited possibilities to treat malignant cells after HSCT without affecting the transplanted healthy cells

Identifiants

pubmed: 38778101
doi: 10.1038/s41586-024-07456-3
pii: 10.1038/s41586-024-07456-3
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s).

Références

Copelan, E. A. Hematopoietic stem-cell transplantation. N. Engl. J. Med. 354, 1813–1826 (2006).
pubmed: 16641398 doi: 10.1056/NEJMra052638
June, C. H. & Sadelain, M. Chimeric antigen receptor therapy. N. Engl. J. Med. 379, 64–73 (2018).
pubmed: 29972754 pmcid: 7433347 doi: 10.1056/NEJMra1706169
Perna, F. et al. Integrating proteomics and transcriptomics for systematic combinatorial chimeric antigen receptor therapy of AML. Cancer Cell 32, 506–519 (2017).
pubmed: 29017060 pmcid: 7025434 doi: 10.1016/j.ccell.2017.09.004
Haubner, S. et al. Coexpression profile of leukemic stem cell markers for combinatorial targeted therapy in AML. Leukemia 33, 64–74 (2019).
pubmed: 29946192 doi: 10.1038/s41375-018-0180-3
Majzner, R. G. & Mackall, C. L. Clinical lessons learned from the first leg of the CAR T cell journey. Nat. Med. 25, 1341–1355 (2019).
pubmed: 31501612 doi: 10.1038/s41591-019-0564-6
Becker, A. J., McCulloch, E. A. & Till, J. E. Cytological demonstration of the clonal nature of spleen colonies derived from transplanted mouse marrow cells. Nature 197, 452–454 (1963).
pubmed: 13970094 doi: 10.1038/197452a0
Li, Z., Czechowicz, A., Scheck, A., Rossi, D. J. & Murphy, P. M. Hematopoietic chimerism and donor-specific skin allograft tolerance after non-genotoxic CD117 antibody-drug-conjugate conditioning in MHC-mismatched allotransplantation. Nat. Commun. 10, 616 (2019).
pubmed: 30728353 pmcid: 6365540 doi: 10.1038/s41467-018-08202-w
Czechowicz, A. et al. Selective hematopoietic stem cell ablation using CD117-antibody-drug-conjugates enables safe and effective transplantation with immunity preservation. Nat. Commun. 10, 617 (2019).
pubmed: 30728354 pmcid: 6365495 doi: 10.1038/s41467-018-08201-x
Russkamp, N. F., Myburgh, R., Kiefer, J. D., Neri, D. & Manz, M. G. Anti-CD117 immunotherapy to eliminate hematopoietic and leukemia stem cells. Exp. Hematol. 95, 31–45 (2021).
pubmed: 33484750 doi: 10.1016/j.exphem.2021.01.003
Carter, P. J. & Rajpal, A. Designing antibodies as therapeutics. Cell 185, 2789–2805 (2022).
pubmed: 35868279 doi: 10.1016/j.cell.2022.05.029
Gill, S. et al. Preclinical targeting of human acute myeloid leukemia and myeloablation using chimeric antigen receptor-modified T cells. Blood 123, 2343–2354 (2014).
pubmed: 24596416 pmcid: 3983612 doi: 10.1182/blood-2013-09-529537
Palchaudhuri, R. et al. Non-genotoxic conditioning for hematopoietic stem cell transplantation using a hematopoietic-cell-specific internalizing immunotoxin. Nat. Biotechnol. 34, 738–745 (2016).
pubmed: 27272386 pmcid: 5179034 doi: 10.1038/nbt.3584
Mujal, A. M. & Krummel, M. F. Immunity as a continuum of archetypes. Science 364, 28–29 (2019).
pubmed: 30948539 doi: 10.1126/science.aau8694
Borot, F. et al. Gene-edited stem cells enable CD33-directed immune therapy for myeloid malignancies. Proc. Natl Acad. Sci. USA 116, 11978–11987 (2019).
pubmed: 31138698 pmcid: 6575599 doi: 10.1073/pnas.1819992116
Humbert, O. et al. Engineering resistance to CD33-targeted immunotherapy in normal hematopoiesis by CRISPR/Cas9-deletion of CD33 exon 2. Leukemia 33, 762–808 (2019).
pubmed: 30291334 doi: 10.1038/s41375-018-0277-8
Kim, M. Y. et al. Genetic inactivation of CD33 in hematopoietic stem cells to enable CAR T cell immunotherapy for acute myeloid leukemia. Cell 173, 1439–1453 (2018).
pubmed: 29856956 pmcid: 6003425 doi: 10.1016/j.cell.2018.05.013
Kung, C. et al. Mutations in the tyrosine phosphatase CD45 gene in a child with severe combined immunodeficiency disease. Nat. Med. 6, 343–345 (2000).
pubmed: 10700239 doi: 10.1038/73208
Kornete, M., Marone, R. & Jeker, L. T. Highly efficient and versatile plasmid-based gene editing in primary T cells. J Immunol 200, 2489–2501 (2018).
pubmed: 29445007 pmcid: 5857648 doi: 10.4049/jimmunol.1701121
Marone, R. et al. Epitope-engineered human hematopoietic stem cells are shielded from CD123-targeted immunotherapy. J. Exp. Med. https://doi.org/10.1084/jem.20231235 (2023).
Casirati, G. et al. Epitope editing enables targeted immunotherapy of acute myeloid leukaemia. Nature 621, 404–414 (2023).
pubmed: 37648862 pmcid: 10499609 doi: 10.1038/s41586-023-06496-5
Wellhausen, N. et al. Epitope base editing CD45 in hematopoietic cells enables universal blood cancer immune therapy. Sci. Transl. Med. 15, eadi1145 (2023).
pubmed: 37651540 pmcid: 10682510 doi: 10.1126/scitranslmed.adi1145
Chang, V. T. et al. Initiation of T cell signaling by CD45 segregation at ‘close contacts’. Nat. Immunol. 17, 574–582 (2016).
pubmed: 26998761 pmcid: 4839504 doi: 10.1038/ni.3392
Anzalone, A. V., Koblan, L. W. & Liu, D. R. Genome editing with CRISPR–Cas nucleases, base editors, transposases and prime editors. Nat. Biotechnol. 38, 824–844 (2020).
pubmed: 32572269 doi: 10.1038/s41587-020-0561-9
Richter, M. F. et al. Phage-assisted evolution of an adenine base editor with improved Cas domain compatibility and activity. Nat. Biotechnol. 38, 883–891 (2020).
pubmed: 32433547 pmcid: 7357821 doi: 10.1038/s41587-020-0453-z
Walton, R. T., Christie, K. A., Whittaker, M. N. & Kleinstiver, B. P. Unconstrained genome targeting with near-PAMless engineered CRISPR-Cas9 variants. Science 368, 290–296 (2020).
pubmed: 32217751 pmcid: 7297043 doi: 10.1126/science.aba8853
Kinneer, K. et al. SLC46A3 as a potential predictive biomarker for antibody-drug conjugates bearing noncleavable linked maytansinoid and pyrrolobenzodiazepine warheads. Clin. Cancer Res. 24, 6570–6582 (2018).
pubmed: 30131388 doi: 10.1158/1078-0432.CCR-18-1300
Caimi, P. F. et al. Loncastuximab tesirine in relapsed or refractory diffuse large B-cell lymphoma (LOTIS-2): a multicentre, open-label, single-arm, phase 2 trial. Lancet Oncol. 22, 790–800 (2021).
pubmed: 33989558 doi: 10.1016/S1470-2045(21)00139-X
Lazzarotto, C. R. et al. CHANGE-seq-BE enables simultaneously sensitive and unbiased in vitro profiling of base editor genome-wide activity. Preprint at biorxiv https://doi.org/10.1101/2024.03.28.586621 (2024).
Yin, H. et al. Partial DNA-guided Cas9 enables genome editing with reduced off-target activity. Nat. Chem. Biol. 14, 311–316 (2018).
pubmed: 29377001 pmcid: 5902734 doi: 10.1038/nchembio.2559
Donohoue, P. D. et al. Conformational control of Cas9 by CRISPR hybrid RNA-DNA guides mitigates off-target activity in T cells. Mol. Cell 81, 3637–3649 (2021).
pubmed: 34478654 doi: 10.1016/j.molcel.2021.07.035
Naldini, M. M. et al. Longitudinal single-cell profiling of chemotherapy response in acute myeloid leukemia. Nat. Commun. 14, 1285 (2023).
pubmed: 36890137 pmcid: 9995364 doi: 10.1038/s41467-023-36969-0
Dahlke, M. H., Larsen, S. R., Rasko, J. E. J. & Schlitt, H. J. The biology of CD45 and its use as a therapeutic target. Leuk. Lymphoma 45, 229–236 (2004).
pubmed: 15101706 doi: 10.1080/1042819031000151932
Webber, B. R. et al. Highly efficient multiplex human T cell engineering without double-strand breaks using Cas9 base editors. Nat. Commun. 10, 5222 (2019).
pubmed: 31745080 pmcid: 6864045 doi: 10.1038/s41467-019-13007-6
Anzalone, A. V. et al. Search-and-replace genome editing without double-strand breaks or donor DNA. Nature 576, 149–157 (2019).
pubmed: 31634902 pmcid: 6907074 doi: 10.1038/s41586-019-1711-4
Vaxman, I. et al. Secondary malignancies following high dose therapy and autologous hematopoietic cell transplantation-systematic review and meta-analysis. Bone Marrow Transplant. 50, 706–714 (2015).
pubmed: 25665042 doi: 10.1038/bmt.2014.325
Li, Z. & Murphy, P. M. CD45: a niche marker for allotransplantation. Blood 139, 1614–1616 (2022).
pubmed: 35298604 pmcid: 8931515 doi: 10.1182/blood.2021015024
Alves, C. R. R. et al. Optimization of base editors for the functional correction of SMN2 as a treatment for spinal muscular atrophy. Nat. Biomed. Eng. https://doi.org/10.1038/s41551-023-01132-z (2024).
doi: 10.1038/s41551-023-01132-z pubmed: 38057426
Turchiano, G. et al. Quantitative evaluation of chromosomal rearrangements in gene-edited human stem cells by CAST-Seq. Cell Stem Cell 28, 1136–1147 (2021).
pubmed: 33626327 doi: 10.1016/j.stem.2021.02.002
Dumontet, C., Reichert, J. M., Senter, P. D., Lambert, J. M. & Beck, A. Antibody–drug conjugates come of age in oncology. Nat. Rev. Drug Discov. 22, 641–661 (2023).
pubmed: 37308581 doi: 10.1038/s41573-023-00709-2
Persaud, S. P. et al. Antibody–drug conjugates plus Janus kinase inhibitors enable MHC-mismatched allogeneic hematopoietic stem cell transplantation. J. Clin. Invest. 131, https://doi.org/10.1172/JCI145501 (2021).
Saha, A. et al. A CD45-targeted antibody-drug conjugate successfully conditions for allogeneic hematopoietic stem cell transplantation in mice. Blood 139, 1743–1759 (2022).
pubmed: 34986233 pmcid: 8931510 doi: 10.1182/blood.2021012366
Dickinson, M. J. et al. Glofitamab for relapsed or refractory diffuse large B-cell lymphoma. N. Engl. J. Med. 387, 2220–2231 (2022).
pubmed: 36507690 doi: 10.1056/NEJMoa2206913
Majzner, R. G. & Mackall, C. L. Tumor antigen escape from CAR T-cell therapy. Cancer Discov. 8, 1219–1226 (2018).
pubmed: 30135176 doi: 10.1158/2159-8290.CD-18-0442
Mackensen, A. et al. Anti-CD19 CAR T cell therapy for refractory systemic lupus erythematosus. Nat. Med. 28, 2124–2132 (2022).
pubmed: 36109639 doi: 10.1038/s41591-022-02017-5
Lee, B. & Richards, F. M. The interpretation of protein structures: estimation of static accessibility. J. Mol. Biol. 55, 379–400 (1971).
pubmed: 5551392 doi: 10.1016/0022-2836(71)90324-X
Mitternacht, S. FreeSASA: An open source C library for solvent accessible surface area calculations. F1000Res. 5, 189 (2016).
pubmed: 26973785 pmcid: 4776673 doi: 10.12688/f1000research.7931.1
Jespersen, M. C., Peters, B., Nielsen, M. & Marcatili, P. BepiPred-2.0: improving sequence-based B-cell epitope prediction using conformational epitopes. Nucleic Acids Res. 45, W24–w29 (2017).
pubmed: 28472356 pmcid: 5570230 doi: 10.1093/nar/gkx346
Hopf, T. A. et al. Mutation effects predicted from sequence co-variation. Nat. Biotechnol. 35, 128–135 (2017).
pubmed: 28092658 pmcid: 5383098 doi: 10.1038/nbt.3769
Suzek, B. E. et al. UniRef clusters: a comprehensive and scalable alternative for improving sequence similarity searches. Bioinformatics 31, 926–932 (2015).
pubmed: 25398609 doi: 10.1093/bioinformatics/btu739
Finn, R. D. et al. HMMER web server: 2015 update. Nucleic Acids Res. 43, W30–W38 (2015).
pubmed: 25943547 pmcid: 4489315 doi: 10.1093/nar/gkv397
Kluesner, M. G. et al. EditR: a method to quantify base editing from Sanger sequencing. CRISPR J. 1, 239–250 (2018).
pubmed: 31021262 pmcid: 6694769 doi: 10.1089/crispr.2018.0014
Andrews, S. FastQC: a quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/ (Babraham Bioinformatics, 2010).
Clement, K. et al. CRISPResso2 provides accurate and rapid genome editing sequence analysis. Nat. Biotechnol. 37, 224–226 (2019).
pubmed: 30809026 pmcid: 6533916 doi: 10.1038/s41587-019-0032-3
Lazzarotto, C. R. et al. CHANGE-seq reveals genetic and epigenetic effects on CRISPR–Cas9 genome-wide activity. Nat. Biotechnol. 38, 1317–1327 (2020).
pubmed: 32541958 pmcid: 7652380 doi: 10.1038/s41587-020-0555-7
Newby, G. A. et al. Base editing of haematopoietic stem cells rescues sickle cell disease in mice. Nature 595, 295–302 (2021).
pubmed: 34079130 pmcid: 8266759 doi: 10.1038/s41586-021-03609-w
Chattopadhyay, G. & Varadarajan, R. Facile measurement of protein stability and folding kinetics using a nano differential scanning fluorimeter. Protein Sci. 28, 1127–1134 (2019).
pubmed: 30993730 pmcid: 6511731 doi: 10.1002/pro.3622
Gao, K., Oerlemans, R. & Groves, M. R. Theory and applications of differential scanning fluorimetry in early-stage drug discovery. Biophys. Rev. 12, 85–104 (2020).
pubmed: 32006251 pmcid: 7040159 doi: 10.1007/s12551-020-00619-2
Hong, P., Koza, S. & Bouvier, E. S. P. Size-exclusion chromatography for the analysis of protein biotherapeutics and their aggregates. J. Liq. Chromatogr. Relat. Technol. 35, 2923–2950 (2012).
pubmed: 23378719 pmcid: 3556795 doi: 10.1080/10826076.2012.743724
Larrue, C. et al. Mitochondrial fusion is a therapeutic vulnerability of acute myeloid leukemia. Leukemia 37, 765–775 (2023).
pubmed: 36739349 pmcid: 10079528 doi: 10.1038/s41375-023-01835-x
Sabatier, M. et al. C/EBPα confers dependence to fatty acid anabolic pathways and vulnerability to lipid oxidative stress-induced ferroptosis in FLT3-mutant leukemia. Cancer Discov. 13, 1720–1747 (2023).
pubmed: 37012202 doi: 10.1158/2159-8290.CD-22-0411

Auteurs

Simon Garaudé (S)

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

Romina Marone (R)

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

Rosalba Lepore (R)

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

Anna Devaux (A)

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

Astrid Beerlage (A)

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

Denis Seyres (D)

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

Alessandro Dell' Aglio (A)

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

Darius Juskevicius (D)

Department of Laboratory Medicine, Diagnostic Hematology, Basel University Hospital, Basel, Switzerland.

Jessica Zuin (J)

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

Thomas Burgold (T)

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

Sisi Wang (S)

Division of Hematology, Department of Oncology, Geneva University Hospitals, Geneva, Switzerland.

Varun Katta (V)

Department of Hematology, St. Jude Children's Research Hospital, Memphis, TN, USA.

Garret Manquen (G)

Department of Hematology, St. Jude Children's Research Hospital, Memphis, TN, USA.

Yichao Li (Y)

Department of Hematology, St. Jude Children's Research Hospital, Memphis, TN, USA.

Clément Larrue (C)

Translational Research Center for Oncohematology, Department of Medicine, Faculty of Medicine, University of Geneva, Geneva, Switzerland.
Centre de Recherches en Cancérologie de Toulouse, Université de Toulouse, Inserm, CNRS, Toulouse, France.

Anna Camus (A)

Cimeio Therapeutics, Basel, Switzerland.

Izabela Durzynska (I)

Ridgeline Discovery, Basel, Switzerland.

Lisa C Wellinger (LC)

Ridgeline Discovery, Basel, Switzerland.

Ian Kirby (I)

ADC Therapeutics (UK), London, UK.

Patrick H Van Berkel (PH)

ADC Therapeutics (UK), London, UK.

Christian Kunz (C)

Ridgeline Discovery, Basel, Switzerland.

Jérôme Tamburini (J)

Translational Research Center for Oncohematology, Department of Medicine, Faculty of Medicine, University of Geneva, Geneva, Switzerland.

Francesco Bertoni (F)

Institute of Oncology Research, Faculty of Biomedical Sciences, USI, Bellinzona, Switzerland.
Oncology Institute of Southern Switzerland, Ente Ospedaliero Cantonale, Bellinzona, Switzerland.

Corinne C Widmer (CC)

Department of Hematology, Basel University Hospital, Basel, Switzerland.
Department of Laboratory Medicine, Diagnostic Hematology, Basel University Hospital, Basel, Switzerland.

Shengdar Q Tsai (SQ)

Department of Hematology, St. Jude Children's Research Hospital, Memphis, TN, USA.

Federico Simonetta (F)

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

Stefanie Urlinger (S)

Cimeio Therapeutics, Basel, Switzerland.

Lukas T Jeker (LT)

Department of Biomedicine, Basel University Hospital and University of Basel, Basel, Switzerland. lukas.jeker@unibas.ch.
Transplantation Immunology & Nephrology, Basel University Hospital, Basel, Switzerland. lukas.jeker@unibas.ch.
Innovation Focus Cell Therapy, Basel University Hospital, Basel, Switzerland. lukas.jeker@unibas.ch.

Classifications MeSH