Decoding the immune microenvironment of secondary chronic myelomonocytic leukemia due to diffuse large B-cell lymphoma with CD19 CAR-T failure by single-cell RNA-sequencing

Abstract. Background:. Several studies have demonstrated the occurrence of secondary tumors as a rare but significant complication of chimeric antigen receptor T (CAR-T) cell therapy, underscoring the need for a detailed investigation. Given the limited variety of secondary tumor types reported to...

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Main Authors: Xudong Li, Hong Huang, Fang Wang, Mengjia Li, Binglei Zhang, Jianxiang Shi, Yuke Liu, Mengya Gao, Mingxia Sun, Haixia Cao, Danfeng Zhang, Na Shen, Weijie Cao, Zhilei Bian, Haizhou Xing, Wei Li, Linping Xu, Shiyu Zuo, Yongping Song, Tingting Yang, Xiuyuan Hao
Format: Article
Language:English
Published: Wolters Kluwer 2025-08-01
Series:Chinese Medical Journal
Online Access:http://journals.lww.com/10.1097/CM9.0000000000003690
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author Xudong Li
Hong Huang
Fang Wang
Mengjia Li
Binglei Zhang
Jianxiang Shi
Yuke Liu
Mengya Gao
Mingxia Sun
Haixia Cao
Danfeng Zhang
Na Shen
Weijie Cao
Zhilei Bian
Haizhou Xing
Wei Li
Linping Xu
Shiyu Zuo
Yongping Song
Tingting Yang
Xiuyuan Hao
author_facet Xudong Li
Hong Huang
Fang Wang
Mengjia Li
Binglei Zhang
Jianxiang Shi
Yuke Liu
Mengya Gao
Mingxia Sun
Haixia Cao
Danfeng Zhang
Na Shen
Weijie Cao
Zhilei Bian
Haizhou Xing
Wei Li
Linping Xu
Shiyu Zuo
Yongping Song
Tingting Yang
Xiuyuan Hao
author_sort Xudong Li
collection DOAJ
description Abstract. Background:. Several studies have demonstrated the occurrence of secondary tumors as a rare but significant complication of chimeric antigen receptor T (CAR-T) cell therapy, underscoring the need for a detailed investigation. Given the limited variety of secondary tumor types reported to date, a comprehensive characterization of the various secondary tumors arising after CAR-T therapy is essential to understand the associated risks and to define the role of the immune microenvironment in malignant transformation. This study aims to characterize the immune microenvironment of a newly identified secondary tumor post-CAR-T therapy, to clarify its pathogenesis and potential therapeutic targets. Methods:. In this study, the bone marrow (BM) samples were collected by aspiration from the primary and secondary tumors before and after CD19 CAR-T treatment. The CD45+ BM cells were enriched with human CD45 microbeads. The CD45+ cells were then sent for 10× genomics single-cell RNA sequencing (scRNA-seq) to identify cell populations. The Cell Ranger pipeline and CellChat were used for detailed analysis. Results:. In this study, a rare type of secondary chronic myelomonocytic leukemia (CMML) were reported in a patient with diffuse large B-cell lymphoma (DLBCL) who had previously received CD19 CAR-T therapy. The scRNA-seq analysis revealed increased inflammatory cytokines, chemokines, and an immunosuppressive state of monocytes/macrophages, which may impair cytotoxic activity in both T and natural killer (NK) cells in secondary CMML before treatment. In contrast, their cytotoxicity was restored in secondary CMML after treatment. Conclusions:. This finding delineates a previously unrecognized type of secondary tumor, CMML, after CAR-T therapy and provide a framework for defining the immune microenvironment of secondary tumor occurrence after CAR-T therapy. In addition, the results provide a rationale for targeting macrophages to improve treatment strategies for CMML treatment.
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spelling doaj-art-a152dcf7ee0c4a4ca548a05031777efe2025-08-20T03:01:41ZengWolters KluwerChinese Medical Journal0366-69992542-56412025-08-01138151866188110.1097/CM9.0000000000003690202508050-00010Decoding the immune microenvironment of secondary chronic myelomonocytic leukemia due to diffuse large B-cell lymphoma with CD19 CAR-T failure by single-cell RNA-sequencingXudong Li0Hong Huang1Fang Wang2Mengjia Li3Binglei Zhang4Jianxiang Shi5Yuke Liu6Mengya Gao7Mingxia Sun8Haixia Cao9Danfeng Zhang10Na Shen11Weijie Cao12Zhilei Bian13Haizhou Xing14Wei Li15Linping Xu16Shiyu Zuo17Yongping Song18Tingting YangXiuyuan Hao1 Department of Hematology, First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan 450000, China1 Department of Hematology, First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan 450000, China1 Department of Hematology, First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan 450000, China1 Department of Hematology, First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan 450000, China1 Department of Hematology, First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan 450000, China3 BGI College & Henan Institute of Medical and Pharmaceutical Sciences in Academy of Medical Science, Zhengzhou University, Zhengzhou, Henan 450052, China1 Department of Hematology, First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan 450000, China4 Department of Research and Foreign Affairs, The Affiliated Cancer Hospital of Zhengzhou University & Henan Cancer Hospital, Zhengzhou, Henan 450008, China5 School of Public Health, Zhengzhou University, Zhengzhou, Henan 450000, China1 Department of Hematology, First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan 450000, China1 Department of Hematology, First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan 450000, China1 Department of Hematology, First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan 450000, China1 Department of Hematology, First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan 450000, China1 Department of Hematology, First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan 450000, China1 Department of Hematology, First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan 450000, China1 Department of Hematology, First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan 450000, China4 Department of Research and Foreign Affairs, The Affiliated Cancer Hospital of Zhengzhou University & Henan Cancer Hospital, Zhengzhou, Henan 450008, China1 Department of Hematology, First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan 450000, China1 Department of Hematology, First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan 450000, ChinaAbstract. Background:. Several studies have demonstrated the occurrence of secondary tumors as a rare but significant complication of chimeric antigen receptor T (CAR-T) cell therapy, underscoring the need for a detailed investigation. Given the limited variety of secondary tumor types reported to date, a comprehensive characterization of the various secondary tumors arising after CAR-T therapy is essential to understand the associated risks and to define the role of the immune microenvironment in malignant transformation. This study aims to characterize the immune microenvironment of a newly identified secondary tumor post-CAR-T therapy, to clarify its pathogenesis and potential therapeutic targets. Methods:. In this study, the bone marrow (BM) samples were collected by aspiration from the primary and secondary tumors before and after CD19 CAR-T treatment. The CD45+ BM cells were enriched with human CD45 microbeads. The CD45+ cells were then sent for 10× genomics single-cell RNA sequencing (scRNA-seq) to identify cell populations. The Cell Ranger pipeline and CellChat were used for detailed analysis. Results:. In this study, a rare type of secondary chronic myelomonocytic leukemia (CMML) were reported in a patient with diffuse large B-cell lymphoma (DLBCL) who had previously received CD19 CAR-T therapy. The scRNA-seq analysis revealed increased inflammatory cytokines, chemokines, and an immunosuppressive state of monocytes/macrophages, which may impair cytotoxic activity in both T and natural killer (NK) cells in secondary CMML before treatment. In contrast, their cytotoxicity was restored in secondary CMML after treatment. Conclusions:. This finding delineates a previously unrecognized type of secondary tumor, CMML, after CAR-T therapy and provide a framework for defining the immune microenvironment of secondary tumor occurrence after CAR-T therapy. In addition, the results provide a rationale for targeting macrophages to improve treatment strategies for CMML treatment.http://journals.lww.com/10.1097/CM9.0000000000003690
spellingShingle Xudong Li
Hong Huang
Fang Wang
Mengjia Li
Binglei Zhang
Jianxiang Shi
Yuke Liu
Mengya Gao
Mingxia Sun
Haixia Cao
Danfeng Zhang
Na Shen
Weijie Cao
Zhilei Bian
Haizhou Xing
Wei Li
Linping Xu
Shiyu Zuo
Yongping Song
Tingting Yang
Xiuyuan Hao
Decoding the immune microenvironment of secondary chronic myelomonocytic leukemia due to diffuse large B-cell lymphoma with CD19 CAR-T failure by single-cell RNA-sequencing
Chinese Medical Journal
title Decoding the immune microenvironment of secondary chronic myelomonocytic leukemia due to diffuse large B-cell lymphoma with CD19 CAR-T failure by single-cell RNA-sequencing
title_full Decoding the immune microenvironment of secondary chronic myelomonocytic leukemia due to diffuse large B-cell lymphoma with CD19 CAR-T failure by single-cell RNA-sequencing
title_fullStr Decoding the immune microenvironment of secondary chronic myelomonocytic leukemia due to diffuse large B-cell lymphoma with CD19 CAR-T failure by single-cell RNA-sequencing
title_full_unstemmed Decoding the immune microenvironment of secondary chronic myelomonocytic leukemia due to diffuse large B-cell lymphoma with CD19 CAR-T failure by single-cell RNA-sequencing
title_short Decoding the immune microenvironment of secondary chronic myelomonocytic leukemia due to diffuse large B-cell lymphoma with CD19 CAR-T failure by single-cell RNA-sequencing
title_sort decoding the immune microenvironment of secondary chronic myelomonocytic leukemia due to diffuse large b cell lymphoma with cd19 car t failure by single cell rna sequencing
url http://journals.lww.com/10.1097/CM9.0000000000003690
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