The single-cell immune landscape of HIV-associated aggressive B-cell lymphoma

Background: Human immunodeficiency virus (HIV)-associated lymphomas (HAL), mainly aggressive B-cell lymphomas, pose a significant challenge in cancer research due to their multifaceted pathogenesis and aggressive clinical course. Despite the clinical importance, the genomic and immune characteristic...

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Main Authors: Xiaomei Zhang, Zailin Yang, Xiaoqing Xie, Jun Li, Qing Xiao, Guofa Xu, Ben Ma, Xudong Xie, Yi Liu, Liuyue Zhai, Yifeng Tang, Huihui Fu, Sanxiu He, Tingting Liu, Dehong Huang, Censi Zeng, Yixing Zhou, Renzhi Hu, Binling Guo, Chaoyu Wang, Shunsi Liang, Qin Luo, Jing Lv, Yingyu Nan, Jieping Li, Qiying Li, Shengqiang Wang, Yongzhong Wu, Yao Liu
Format: Article
Language:English
Published: Elsevier 2025-04-01
Series:Journal of the National Cancer Center
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Online Access:http://www.sciencedirect.com/science/article/pii/S2667005425000213
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author Xiaomei Zhang
Zailin Yang
Xiaoqing Xie
Jun Li
Qing Xiao
Guofa Xu
Ben Ma
Xudong Xie
Yi Liu
Liuyue Zhai
Yifeng Tang
Huihui Fu
Sanxiu He
Tingting Liu
Dehong Huang
Censi Zeng
Yixing Zhou
Renzhi Hu
Binling Guo
Chaoyu Wang
Shunsi Liang
Qin Luo
Jing Lv
Yingyu Nan
Jieping Li
Qiying Li
Shengqiang Wang
Yongzhong Wu
Yao Liu
author_facet Xiaomei Zhang
Zailin Yang
Xiaoqing Xie
Jun Li
Qing Xiao
Guofa Xu
Ben Ma
Xudong Xie
Yi Liu
Liuyue Zhai
Yifeng Tang
Huihui Fu
Sanxiu He
Tingting Liu
Dehong Huang
Censi Zeng
Yixing Zhou
Renzhi Hu
Binling Guo
Chaoyu Wang
Shunsi Liang
Qin Luo
Jing Lv
Yingyu Nan
Jieping Li
Qiying Li
Shengqiang Wang
Yongzhong Wu
Yao Liu
author_sort Xiaomei Zhang
collection DOAJ
description Background: Human immunodeficiency virus (HIV)-associated lymphomas (HAL), mainly aggressive B-cell lymphomas, pose a significant challenge in cancer research due to their multifaceted pathogenesis and aggressive clinical course. Despite the clinical importance, the genomic and immune characteristics of these lymphomas remain poorly elucidated. Methods: We employed single-cell RNA sequencing (scRNA-seq) on lymph node samples from aggressive B-cell lymphomas, mainly including 6 cases of diffuse large B-cell lymphoma (DLBCL) and 5 cases of Burkitt lymphoma (BL) from people living with HIV (PLWH), along with 3 DLBCL cases from individuals without HIV for comparison. Results: Malignant B cells in HAL consistently exhibited high proliferative and oxidative phosphorylation (OXPHOS)-type metabolic signatures. Moreover, these cells demonstrated loss expression of major histocompatibility complex class I (MHC-I), strategically reducing tumor immunogenicity. HAL harbors special populations of naive and atypical memory B cells that exhibited high metabolic and immune-activated transcriptional profiles. Additionally, HAL exhibited senescence-like dysfunction in T cells, characterized by the reductions in regulatory activity of Treg and cytotoxic activity of CD8+ T cells, as well as decreases expression of IL7R genes and increases expression of FOS and FOSB genes. Our immunofluorescence results showed that the cytotoxic CD8+ T cells in HAL may have a dysfunction of lytic granule polarization. Furthermore, macrophages from HAL exhibited stronger immunosuppressive transcriptional characteristics, and a robust immunosuppressive SPP1-CD44 interaction was predicted between C1QA+ macrophages and T cells. Conclusions: Our findings clearly indicate that HAL differs significantly from non-HAL, ranging from malignant B cells to the immune microenvironment. This study provides a comprehensive single-cell atlas of HIV-associated aggressive B-cell lymphomas, offering new insights into aggressiveness and immune evasion observed in HAL.
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spelling doaj-art-7ae40f3dd03a4c339646c81fe13eecc42025-08-20T02:16:02ZengElsevierJournal of the National Cancer Center2667-00542025-04-015222123510.1016/j.jncc.2025.02.001The single-cell immune landscape of HIV-associated aggressive B-cell lymphomaXiaomei Zhang0Zailin Yang1Xiaoqing Xie2Jun Li3Qing Xiao4Guofa Xu5Ben Ma6Xudong Xie7Yi Liu8Liuyue Zhai9Yifeng Tang10Huihui Fu11Sanxiu He12Tingting Liu13Dehong Huang14Censi Zeng15Yixing Zhou16Renzhi Hu17Binling Guo18Chaoyu Wang19Shunsi Liang20Qin Luo21Jing Lv22Yingyu Nan23Jieping Li24Qiying Li25Shengqiang Wang26Yongzhong Wu27Yao Liu28Department of Hematology and Oncology, Chongqing University Cancer Hospital, Chongqing, ChinaDepartment of Hematology and Oncology, Chongqing University Cancer Hospital, Chongqing, ChinaDepartment of Hematology and Oncology, Chongqing University Cancer Hospital, Chongqing, ChinaDepartment of Hematology and Oncology, Chongqing University Cancer Hospital, Chongqing, ChinaDepartment of Hematology and Oncology, Chongqing University Cancer Hospital, Chongqing, ChinaDepartment of Hematology and Oncology, Chongqing University Cancer Hospital, Chongqing, China; Department of Hematology and Medical Oncology, Chongqing University Fuling Hospital, Chongqing, ChinaDepartment of Integrated, Chongqing University Cancer Hospital, Chongqing, ChinaDepartment of Integrated, Chongqing University Cancer Hospital, Chongqing, ChinaDepartment of Hematology and Oncology, Chongqing University Cancer Hospital, Chongqing, ChinaDepartment of Hematology and Oncology, Chongqing University Cancer Hospital, Chongqing, ChinaDepartment of Hematology and Oncology, Chongqing University Cancer Hospital, Chongqing, ChinaDepartment of Hematology and Oncology, Chongqing University Cancer Hospital, Chongqing, ChinaDepartment of Hematology and Oncology, Chongqing University Cancer Hospital, Chongqing, ChinaDepartment of Hematology and Oncology, Chongqing University Cancer Hospital, Chongqing, ChinaDepartment of Hematology and Oncology, Chongqing University Cancer Hospital, Chongqing, ChinaDepartment of Hematology and Oncology, Chongqing University Cancer Hospital, Chongqing, ChinaDepartment of Hematology and Oncology, Chongqing University Cancer Hospital, Chongqing, ChinaDepartment of Hematology and Oncology, Chongqing University Cancer Hospital, Chongqing, ChinaDepartment of Hematology and Oncology, Chongqing University Cancer Hospital, Chongqing, ChinaDepartment of Hematology and Oncology, Chongqing University Cancer Hospital, Chongqing, ChinaDepartment of Hematology and Oncology, Chongqing University Cancer Hospital, Chongqing, ChinaDepartment of Hematology and Oncology, Chongqing University Cancer Hospital, Chongqing, ChinaDepartment of Hematology and Oncology, Chongqing University Cancer Hospital, Chongqing, ChinaDepartment of Hematology and Oncology, Chongqing University Cancer Hospital, Chongqing, ChinaDepartment of Hematology and Oncology, Chongqing University Cancer Hospital, Chongqing, ChinaDepartment of Hematology and Oncology, Chongqing University Cancer Hospital, Chongqing, ChinaDepartment of Integrated, Chongqing University Cancer Hospital, Chongqing, China; Corresponding authors.Department of Radiation Oncology, Chongqing University Cancer Hospital, Chongqing, China; Corresponding authors.Department of Hematology and Oncology, Chongqing University Cancer Hospital, Chongqing, China; Corresponding authors.Background: Human immunodeficiency virus (HIV)-associated lymphomas (HAL), mainly aggressive B-cell lymphomas, pose a significant challenge in cancer research due to their multifaceted pathogenesis and aggressive clinical course. Despite the clinical importance, the genomic and immune characteristics of these lymphomas remain poorly elucidated. Methods: We employed single-cell RNA sequencing (scRNA-seq) on lymph node samples from aggressive B-cell lymphomas, mainly including 6 cases of diffuse large B-cell lymphoma (DLBCL) and 5 cases of Burkitt lymphoma (BL) from people living with HIV (PLWH), along with 3 DLBCL cases from individuals without HIV for comparison. Results: Malignant B cells in HAL consistently exhibited high proliferative and oxidative phosphorylation (OXPHOS)-type metabolic signatures. Moreover, these cells demonstrated loss expression of major histocompatibility complex class I (MHC-I), strategically reducing tumor immunogenicity. HAL harbors special populations of naive and atypical memory B cells that exhibited high metabolic and immune-activated transcriptional profiles. Additionally, HAL exhibited senescence-like dysfunction in T cells, characterized by the reductions in regulatory activity of Treg and cytotoxic activity of CD8+ T cells, as well as decreases expression of IL7R genes and increases expression of FOS and FOSB genes. Our immunofluorescence results showed that the cytotoxic CD8+ T cells in HAL may have a dysfunction of lytic granule polarization. Furthermore, macrophages from HAL exhibited stronger immunosuppressive transcriptional characteristics, and a robust immunosuppressive SPP1-CD44 interaction was predicted between C1QA+ macrophages and T cells. Conclusions: Our findings clearly indicate that HAL differs significantly from non-HAL, ranging from malignant B cells to the immune microenvironment. This study provides a comprehensive single-cell atlas of HIV-associated aggressive B-cell lymphomas, offering new insights into aggressiveness and immune evasion observed in HAL.http://www.sciencedirect.com/science/article/pii/S2667005425000213HIV-associated lymphomasSingle-cell RNA sequencingDLBCL
spellingShingle Xiaomei Zhang
Zailin Yang
Xiaoqing Xie
Jun Li
Qing Xiao
Guofa Xu
Ben Ma
Xudong Xie
Yi Liu
Liuyue Zhai
Yifeng Tang
Huihui Fu
Sanxiu He
Tingting Liu
Dehong Huang
Censi Zeng
Yixing Zhou
Renzhi Hu
Binling Guo
Chaoyu Wang
Shunsi Liang
Qin Luo
Jing Lv
Yingyu Nan
Jieping Li
Qiying Li
Shengqiang Wang
Yongzhong Wu
Yao Liu
The single-cell immune landscape of HIV-associated aggressive B-cell lymphoma
Journal of the National Cancer Center
HIV-associated lymphomas
Single-cell RNA sequencing
DLBCL
title The single-cell immune landscape of HIV-associated aggressive B-cell lymphoma
title_full The single-cell immune landscape of HIV-associated aggressive B-cell lymphoma
title_fullStr The single-cell immune landscape of HIV-associated aggressive B-cell lymphoma
title_full_unstemmed The single-cell immune landscape of HIV-associated aggressive B-cell lymphoma
title_short The single-cell immune landscape of HIV-associated aggressive B-cell lymphoma
title_sort single cell immune landscape of hiv associated aggressive b cell lymphoma
topic HIV-associated lymphomas
Single-cell RNA sequencing
DLBCL
url http://www.sciencedirect.com/science/article/pii/S2667005425000213
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