Distinct Genetically Determined Origins of Myd88/BCL2-Driven Aggressive Lymphoma Rationalize Targeted Therapeutic Intervention Strategies.


Journal

Blood cancer discovery
ISSN: 2643-3249
Titre abrégé: Blood Cancer Discov
Pays: United States
ID NLM: 101764786

Informations de publication

Date de publication:
06 01 2023
Historique:
received: 20 01 2022
revised: 06 10 2022
accepted: 04 11 2022
pubmed: 9 11 2022
medline: 10 1 2023
entrez: 8 11 2022
Statut: ppublish

Résumé

Genomic profiling revealed the identity of at least 5 subtypes of diffuse large B-cell lymphoma (DLBCL), including the MCD/C5 cluster characterized by aberrations in MYD88, BCL2, PRDM1, and/or SPIB. We generated mouse models harboring B cell-specific Prdm1 or Spib aberrations on the background of oncogenic Myd88 and Bcl2 lesions. We deployed whole-exome sequencing, transcriptome, flow-cytometry, and mass cytometry analyses to demonstrate that Prdm1- or Spib-altered lymphomas display molecular features consistent with prememory B cells and light-zone B cells, whereas lymphomas lacking these alterations were enriched for late light-zone and plasmablast-associated gene sets. Consistent with the phenotypic evidence for increased B cell receptor signaling activity in Prdm1-altered lymphomas, we demonstrate that combined BTK/BCL2 inhibition displays therapeutic activity in mice and in five of six relapsed/refractory DLBCL patients. Moreover, Prdm1-altered lymphomas were immunogenic upon transplantation into immuno-competent hosts, displayed an actionable PD-L1 surface expression, and were sensitive to antimurine-CD19-CAR-T cell therapy, in vivo. Relapsed/refractory DLBCL remains a major medical challenge, and most of these patients succumb to their disease. Here, we generated mouse models, faithfully recapitulating the biology of MYD88-driven human DLBCL. These models revealed robust preclinical activity of combined BTK/BCL2 inhibition. We confirmed activity of this regimen in pretreated non-GCB-DLBCL patients. See related commentary by Leveille et al., p. 8. This article is highlighted in the In This Issue feature, p. 1.

Identifiants

pubmed: 36346827
pii: 712650
doi: 10.1158/2643-3230.BCD-22-0007
pmc: PMC9816818
doi:

Substances chimiques

Myeloid Differentiation Factor 88 0
Proto-Oncogene Proteins c-bcl-2 0
BCL2 protein, human 0
Myd88 protein, mouse 0

Types de publication

Editorial Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

78-97

Subventions

Organisme : German-Israeli Foundation for Scientific Research and Development (GIF)
ID : I-65-412.20-2016
Organisme : Deutsche Krebshilfe (German Cancer Aid)
ID : 1117240 and 70113041
Organisme : Deutsche Jose Carreras Leukämie-Stiftung
ID : R12/08
Organisme : Bundesministerium für Bildung und Forschung (BMBF)
ID : e:Med 01ZX1303A
Organisme : Deutsche Forschungsgemeinschaft (DFG)
ID : RE 2246/13-1
Organisme : Else Kröner-Fresenius-Stiftung (EKFS)
ID : EKFS-2014-A06
Organisme : Medical Research Council
ID : MR/J008060/1
Pays : United Kingdom
Organisme : Else Kröner-Fresenius-Stiftung (EKFS)
ID : 2016_Kolleg.19
Organisme : Dr. Mildred Scheel Stiftung für Krebsforschung
ID : 70113307

Commentaires et corrections

Type : CommentIn

Informations de copyright

©2022 The Authors; Published by the American Association for Cancer Research.

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Auteurs

Ruth Flümann (R)

Department I of Internal Medicine, Center for Integrated Oncology, Aachen Bonn Cologne Duesseldorf, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.
Center for Molecular Medicine, University of Cologne, Cologne, Germany.
Cologne Excellence Cluster on Cellular Stress Response in Aging-Associated Diseases (CECAD), University of Cologne, Cologne, Germany.
Mildred Scheel School of Oncology, Aachen Bonn Cologne Düsseldorf, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.
Max Planck Institute for Biology of Ageing, Cologne, Germany.

Julia Hansen (J)

Max Planck Institute for Biology of Ageing, Cologne, Germany.

Benedikt W Pelzer (BW)

Department I of Internal Medicine, Center for Integrated Oncology, Aachen Bonn Cologne Duesseldorf, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.
Mildred Scheel School of Oncology, Aachen Bonn Cologne Düsseldorf, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.
Division of Hematology/Oncology, Department of Medicine, Weill Cornell Medicine, Cornell University, New York, New York.

Pascal Nieper (P)

Department I of Internal Medicine, Center for Integrated Oncology, Aachen Bonn Cologne Duesseldorf, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.
Center for Molecular Medicine, University of Cologne, Cologne, Germany.
Cologne Excellence Cluster on Cellular Stress Response in Aging-Associated Diseases (CECAD), University of Cologne, Cologne, Germany.
Mildred Scheel School of Oncology, Aachen Bonn Cologne Düsseldorf, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.

Tim Lohmann (T)

Department I of Internal Medicine, Center for Integrated Oncology, Aachen Bonn Cologne Duesseldorf, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.
Center for Molecular Medicine, University of Cologne, Cologne, Germany.
Cologne Excellence Cluster on Cellular Stress Response in Aging-Associated Diseases (CECAD), University of Cologne, Cologne, Germany.
Mildred Scheel School of Oncology, Aachen Bonn Cologne Düsseldorf, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.

Ilmars Kisis (I)

Department I of Internal Medicine, Center for Integrated Oncology, Aachen Bonn Cologne Duesseldorf, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.
Center for Molecular Medicine, University of Cologne, Cologne, Germany.
Cologne Excellence Cluster on Cellular Stress Response in Aging-Associated Diseases (CECAD), University of Cologne, Cologne, Germany.
Mildred Scheel School of Oncology, Aachen Bonn Cologne Düsseldorf, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.
Department of Translational Genomics, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.

Tobias Riet (T)

Department I of Internal Medicine, Center for Integrated Oncology, Aachen Bonn Cologne Duesseldorf, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.
Center for Molecular Medicine, University of Cologne, Cologne, Germany.

Viktoria Kohlhas (V)

Department I of Internal Medicine, Center for Integrated Oncology, Aachen Bonn Cologne Duesseldorf, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.
Center for Molecular Medicine, University of Cologne, Cologne, Germany.
Cologne Excellence Cluster on Cellular Stress Response in Aging-Associated Diseases (CECAD), University of Cologne, Cologne, Germany.

Phuong-Hien Nguyen (PH)

Department I of Internal Medicine, Center for Integrated Oncology, Aachen Bonn Cologne Duesseldorf, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.
Center for Molecular Medicine, University of Cologne, Cologne, Germany.
Cologne Excellence Cluster on Cellular Stress Response in Aging-Associated Diseases (CECAD), University of Cologne, Cologne, Germany.

Martin Peifer (M)

Center for Molecular Medicine, University of Cologne, Cologne, Germany.
Department of Translational Genomics, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.

Nima Abedpour (N)

Center for Molecular Medicine, University of Cologne, Cologne, Germany.
Department of Translational Genomics, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.

Graziella Bosco (G)

Department of Translational Genomics, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.

Roman K Thomas (RK)

Department of Translational Genomics, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.

Moritz Kochanek (M)

Department I of Internal Medicine, Center for Integrated Oncology, Aachen Bonn Cologne Duesseldorf, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.

Jacqueline Knüfer (J)

Department I of Internal Medicine, Center for Integrated Oncology, Aachen Bonn Cologne Duesseldorf, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.

Lorenz Jonigkeit (L)

Department I of Internal Medicine, Center for Integrated Oncology, Aachen Bonn Cologne Duesseldorf, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.

Filippo Beleggia (F)

Department I of Internal Medicine, Center for Integrated Oncology, Aachen Bonn Cologne Duesseldorf, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.
Center for Molecular Medicine, University of Cologne, Cologne, Germany.
Cologne Excellence Cluster on Cellular Stress Response in Aging-Associated Diseases (CECAD), University of Cologne, Cologne, Germany.
Mildred Scheel School of Oncology, Aachen Bonn Cologne Düsseldorf, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.
Department of Translational Genomics, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.

Alessandra Holzem (A)

Department I of Internal Medicine, Center for Integrated Oncology, Aachen Bonn Cologne Duesseldorf, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.
Center for Molecular Medicine, University of Cologne, Cologne, Germany.
Cologne Excellence Cluster on Cellular Stress Response in Aging-Associated Diseases (CECAD), University of Cologne, Cologne, Germany.
Mildred Scheel School of Oncology, Aachen Bonn Cologne Düsseldorf, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.

Reinhard Büttner (R)

Institute of Pathology, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.

Philipp Lohneis (P)

Institute of Pathology, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.

Jörn Meinel (J)

Institute of Pathology, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.

Monika Ortmann (M)

Institute of Pathology, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.

Thorsten Persigehl (T)

Department of Radiology and Interventional Radiology, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.

Michael Hallek (M)

Department I of Internal Medicine, Center for Integrated Oncology, Aachen Bonn Cologne Duesseldorf, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.
Center for Molecular Medicine, University of Cologne, Cologne, Germany.
Cologne Excellence Cluster on Cellular Stress Response in Aging-Associated Diseases (CECAD), University of Cologne, Cologne, Germany.
Mildred Scheel School of Oncology, Aachen Bonn Cologne Düsseldorf, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.

Dinis Pedro Calado (DP)

The Francis Crick Institute, London, United Kingdom.

Markus Chmielewski (M)

Department I of Internal Medicine, Center for Integrated Oncology, Aachen Bonn Cologne Duesseldorf, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.
Center for Molecular Medicine, University of Cologne, Cologne, Germany.

Sebastian Klein (S)

Department of Hematology and Stem Cell Transplantation, University Hospital Essen, University Duisburg-Essen, West German Cancer Center, German Cancer Consortium (DKTK partner site Essen), Center for Molecular Biotechnology, Essen, Germany.

Joachim R Göthert (JR)

Department of Hematology and Stem Cell Transplantation, University Hospital Essen, University Duisburg-Essen, West German Cancer Center, German Cancer Consortium (DKTK partner site Essen), Center for Molecular Biotechnology, Essen, Germany.

Bjoern Chapuy (B)

Department of Hematology, Oncology and Tumorimmunology, Charité, University Medical Center Berlin, Campus Benjamin Franklin, Berlin, Germany.

Branko Zevnik (B)

Center for Molecular Medicine, University of Cologne, Cologne, Germany.

F Thomas Wunderlich (FT)

Department of Neuronal Control of Metabolism, Max Planck Institute for Metabolism Research, Cologne, Germany.

Bastian von Tresckow (B)

Department of Hematology and Stem Cell Transplantation, University Hospital Essen, University Duisburg-Essen, West German Cancer Center, German Cancer Consortium (DKTK partner site Essen), Center for Molecular Biotechnology, Essen, Germany.

Ron D Jachimowicz (RD)

Department I of Internal Medicine, Center for Integrated Oncology, Aachen Bonn Cologne Duesseldorf, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.
Center for Molecular Medicine, University of Cologne, Cologne, Germany.
Cologne Excellence Cluster on Cellular Stress Response in Aging-Associated Diseases (CECAD), University of Cologne, Cologne, Germany.
Mildred Scheel School of Oncology, Aachen Bonn Cologne Düsseldorf, University of Cologne, Faculty of Medicine and University Hospital Cologne, Cologne, Germany.
Max Planck Institute for Biology of Ageing, Cologne, Germany.

Ari M Melnick (AM)

Division of Hematology/Oncology, Department of Medicine, Weill Cornell Medicine, Cornell University, New York, New York.

Hans Christian Reinhardt (HC)

Department of Hematology and Stem Cell Transplantation, University Hospital Essen, University Duisburg-Essen, West German Cancer Center, German Cancer Consortium (DKTK partner site Essen), Center for Molecular Biotechnology, Essen, Germany.

Gero Knittel (G)

Department of Hematology and Stem Cell Transplantation, University Hospital Essen, University Duisburg-Essen, West German Cancer Center, German Cancer Consortium (DKTK partner site Essen), Center for Molecular Biotechnology, Essen, Germany.

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