PDL1-expressing macrophages infiltrate diffuse large B-cell lymphoma and promote lymphoma growth in a MYC-driven experimental model

Abstract The infiltration of diffuse large- and other mature B-cell lymphomas with T- and myeloid cells is a key tumor microenvironmental feature but is not currently factored into treatment decisions. Here, we have used multiplex immunofluorescence microscopy to quantify the immune infiltrates of &...

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Main Authors: Ningxuan Cui, Peter Leary, Vanesa-Sindi Ivanova, Kristin Stirm, Lydia Kirsche, Nicola Aceto, Frank Stenner, Lothar C. Dieterich, Michael Detmar, Ekaterina Petrova, Sarah Mundt, Melanie Greter, Alexandar Tzankov, Anne Müller
Format: Article
Language:English
Published: Nature Publishing Group 2025-04-01
Series:Blood Cancer Journal
Online Access:https://doi.org/10.1038/s41408-025-01281-1
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author Ningxuan Cui
Peter Leary
Vanesa-Sindi Ivanova
Kristin Stirm
Lydia Kirsche
Nicola Aceto
Frank Stenner
Lothar C. Dieterich
Michael Detmar
Ekaterina Petrova
Sarah Mundt
Melanie Greter
Alexandar Tzankov
Anne Müller
author_facet Ningxuan Cui
Peter Leary
Vanesa-Sindi Ivanova
Kristin Stirm
Lydia Kirsche
Nicola Aceto
Frank Stenner
Lothar C. Dieterich
Michael Detmar
Ekaterina Petrova
Sarah Mundt
Melanie Greter
Alexandar Tzankov
Anne Müller
author_sort Ningxuan Cui
collection DOAJ
description Abstract The infiltration of diffuse large- and other mature B-cell lymphomas with T- and myeloid cells is a key tumor microenvironmental feature but is not currently factored into treatment decisions. Here, we have used multiplex immunofluorescence microscopy to quantify the immune infiltrates of >260 diffuse large B-cell- (DLBCL), follicular- (FL) and mantle cell lymphomas (MCL), and chronic lymphocytic leukemias (CLL) relative to clinical outcomes, mutational landscape and phenotype. MCL were found to be the “coldest” and DLBCL the “hottest” entities. The lymphoma microenvironment of DLBCL featured numerically dominant populations of CD8+ and T-follicular helper (Tfh) T-cells that were indicative of superior prognosis. Mutations in EZH2, PTEN and KMT2D were overrepresented in DLBCL with low CD8+ T-cell infiltration. A unique feature of DLBCL was its infiltration by large numbers of PDL1+ macrophages that constituted up to 70% of total cellularity. PDL1+ macrophage infiltration was mutually exclusive with regulatory T-cell infiltration. The inducible ablation of PDL1 on macrophages was sufficient to improve immune control of MYC-expressing lymphoma in a syngeneic immunocompetent model. These results implicate the macrophage/CD8+ T-cell axis as a key pathogenetic determinant and immunotherapeutic target in a subset of DLBCL patients with poor prognosis.
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spelling doaj-art-e41fe8356e144e5697f5f20c39e511162025-08-20T03:18:34ZengNature Publishing GroupBlood Cancer Journal2044-53852025-04-0115111510.1038/s41408-025-01281-1PDL1-expressing macrophages infiltrate diffuse large B-cell lymphoma and promote lymphoma growth in a MYC-driven experimental modelNingxuan Cui0Peter Leary1Vanesa-Sindi Ivanova2Kristin Stirm3Lydia Kirsche4Nicola Aceto5Frank Stenner6Lothar C. Dieterich7Michael Detmar8Ekaterina Petrova9Sarah Mundt10Melanie Greter11Alexandar Tzankov12Anne Müller13Institute of Molecular Cancer Research, University of ZürichInstitute of Molecular Cancer Research, University of ZürichInstitute of Medical Genetics and Pathology, University Hospital BaselInstitute of Molecular Cancer Research, University of ZürichInstitute of Molecular Cancer Research, University of ZürichInstitute of Molecular Health Sciences, Swiss Federal Institute of Technology ZürichClinic for Medical Oncology, University Hospital BaselEuropean Center for Angioscience and Mannheim Institute of Innate Immunoscience, Medical Faculty Mannheim, Heidelberg UniversityInstitute of Pharmaceutical Sciences, Swiss Federal Institute of Technology ZürichInstitute of Experimental Immunology, University of ZürichInstitute of Experimental Immunology, University of ZürichInstitute of Experimental Immunology, University of ZürichInstitute of Medical Genetics and Pathology, University Hospital BaselInstitute of Molecular Cancer Research, University of ZürichAbstract The infiltration of diffuse large- and other mature B-cell lymphomas with T- and myeloid cells is a key tumor microenvironmental feature but is not currently factored into treatment decisions. Here, we have used multiplex immunofluorescence microscopy to quantify the immune infiltrates of >260 diffuse large B-cell- (DLBCL), follicular- (FL) and mantle cell lymphomas (MCL), and chronic lymphocytic leukemias (CLL) relative to clinical outcomes, mutational landscape and phenotype. MCL were found to be the “coldest” and DLBCL the “hottest” entities. The lymphoma microenvironment of DLBCL featured numerically dominant populations of CD8+ and T-follicular helper (Tfh) T-cells that were indicative of superior prognosis. Mutations in EZH2, PTEN and KMT2D were overrepresented in DLBCL with low CD8+ T-cell infiltration. A unique feature of DLBCL was its infiltration by large numbers of PDL1+ macrophages that constituted up to 70% of total cellularity. PDL1+ macrophage infiltration was mutually exclusive with regulatory T-cell infiltration. The inducible ablation of PDL1 on macrophages was sufficient to improve immune control of MYC-expressing lymphoma in a syngeneic immunocompetent model. These results implicate the macrophage/CD8+ T-cell axis as a key pathogenetic determinant and immunotherapeutic target in a subset of DLBCL patients with poor prognosis.https://doi.org/10.1038/s41408-025-01281-1
spellingShingle Ningxuan Cui
Peter Leary
Vanesa-Sindi Ivanova
Kristin Stirm
Lydia Kirsche
Nicola Aceto
Frank Stenner
Lothar C. Dieterich
Michael Detmar
Ekaterina Petrova
Sarah Mundt
Melanie Greter
Alexandar Tzankov
Anne Müller
PDL1-expressing macrophages infiltrate diffuse large B-cell lymphoma and promote lymphoma growth in a MYC-driven experimental model
Blood Cancer Journal
title PDL1-expressing macrophages infiltrate diffuse large B-cell lymphoma and promote lymphoma growth in a MYC-driven experimental model
title_full PDL1-expressing macrophages infiltrate diffuse large B-cell lymphoma and promote lymphoma growth in a MYC-driven experimental model
title_fullStr PDL1-expressing macrophages infiltrate diffuse large B-cell lymphoma and promote lymphoma growth in a MYC-driven experimental model
title_full_unstemmed PDL1-expressing macrophages infiltrate diffuse large B-cell lymphoma and promote lymphoma growth in a MYC-driven experimental model
title_short PDL1-expressing macrophages infiltrate diffuse large B-cell lymphoma and promote lymphoma growth in a MYC-driven experimental model
title_sort pdl1 expressing macrophages infiltrate diffuse large b cell lymphoma and promote lymphoma growth in a myc driven experimental model
url https://doi.org/10.1038/s41408-025-01281-1
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