B‐cell depletion limits HTLV‐1‐infected T‐cell expansion and ameliorate HTLV‐1‐associated myelopathy

Abstract Objective Human T‐cell leukemia virus type 1‐associated myelopathy (HAM) is a chronic, progressive, inflammatory disease with unclear pathogenesis and no effective treatments. We aimed to investigate a novel mechanistic theory and treat HAM patients with rituximab, which can deplete CD20+ B...

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Main Authors: Aowei Lv, Yaofeng Fang, Xiaohong Lin, Jiaying Chen, Huanhuan Song, Ning Wang, Wan‐Jin Chen, Ying Fu, Rui Li, Yi Lin
Format: Article
Language:English
Published: Wiley 2024-10-01
Series:Annals of Clinical and Translational Neurology
Online Access:https://doi.org/10.1002/acn3.52190
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author Aowei Lv
Yaofeng Fang
Xiaohong Lin
Jiaying Chen
Huanhuan Song
Ning Wang
Wan‐Jin Chen
Ying Fu
Rui Li
Yi Lin
author_facet Aowei Lv
Yaofeng Fang
Xiaohong Lin
Jiaying Chen
Huanhuan Song
Ning Wang
Wan‐Jin Chen
Ying Fu
Rui Li
Yi Lin
author_sort Aowei Lv
collection DOAJ
description Abstract Objective Human T‐cell leukemia virus type 1‐associated myelopathy (HAM) is a chronic, progressive, inflammatory disease with unclear pathogenesis and no effective treatments. We aimed to investigate a novel mechanistic theory and treat HAM patients with rituximab, which can deplete CD20+ B lymphocytes in circulation. Methods Single‐cell RNA sequencing (scRNA‐seq) data was analyzed to identify HTLV‐1‐associated B cells and their effect on T cells. An observational analysis of our HAM cohort was conducted to elucidate changes in the immunological microenvironment of these patients. Peripheral blood mononuclear cells (PBMC) from HAM patients were isolated to explore the efficacy of B cell depletion in vitro. To assess the effect of B‐cell depletion on HAM patients, eligible participants in our cohort received rituximab therapy (NCT04004819). Results ScRNA‐seq results suggest a significant effect of HTLV‐1‐associated B cells on T cells. Additionally, HTLV‐1 was found to infect B cells and depletion of B cells inhibited the proliferation of T cells. Number of B cells in HAM patients had positive correlation with the proviral load and infected cell counts. Depletion of B cells led to a reduction in HTLV‐1 proviral load in vitro. Furthermore, in clinical trial, 14 HAM patients were enrolled. Three patients (21.4%) who received rituximab failed to achieve remission, compared to 24 (85.7%) patients received any other therapy that failed to achieve remission. With a low level of circulating B cells, the proportion of Ki67‐positive cells in CD4+ T cells fell. Interpretation This study provided evidence that depleting B‐lymphocytes is an innovative strategy for treating patients with HAM and broadens the understanding of the role of B cells in infectious immunity.
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spelling doaj-art-6cb39f91c5bb4323a7933f975e206e102025-08-20T02:12:02ZengWileyAnnals of Clinical and Translational Neurology2328-95032024-10-0111102756276810.1002/acn3.52190B‐cell depletion limits HTLV‐1‐infected T‐cell expansion and ameliorate HTLV‐1‐associated myelopathyAowei Lv0Yaofeng Fang1Xiaohong Lin2Jiaying Chen3Huanhuan Song4Ning Wang5Wan‐Jin Chen6Ying Fu7Rui Li8Yi Lin9Department of Neurology and Institute of Neurology of First Affiliated Hospital, Institute of Neuroscience, and Fujian Key Laboratory of Molecular Neurology Fujian Medical University Fuzhou 350005 ChinaDepartment of Neurology and Institute of Neurology of First Affiliated Hospital, Institute of Neuroscience, and Fujian Key Laboratory of Molecular Neurology Fujian Medical University Fuzhou 350005 ChinaDepartment of Rehabilitation The First Affiliated Hospital of Fujian Medical University Fuzhou 350005 ChinaDepartment of Neurology and Institute of Neurology of First Affiliated Hospital, Institute of Neuroscience, and Fujian Key Laboratory of Molecular Neurology Fujian Medical University Fuzhou 350005 ChinaDepartment of Neurology and Institute of Neurology of First Affiliated Hospital, Institute of Neuroscience, and Fujian Key Laboratory of Molecular Neurology Fujian Medical University Fuzhou 350005 ChinaDepartment of Neurology and Institute of Neurology of First Affiliated Hospital, Institute of Neuroscience, and Fujian Key Laboratory of Molecular Neurology Fujian Medical University Fuzhou 350005 ChinaDepartment of Neurology and Institute of Neurology of First Affiliated Hospital, Institute of Neuroscience, and Fujian Key Laboratory of Molecular Neurology Fujian Medical University Fuzhou 350005 ChinaDepartment of Neurology and Institute of Neurology of First Affiliated Hospital, Institute of Neuroscience, and Fujian Key Laboratory of Molecular Neurology Fujian Medical University Fuzhou 350005 ChinaDepartment of Neurology and Institute of Neurology of First Affiliated Hospital, Institute of Neuroscience, and Fujian Key Laboratory of Molecular Neurology Fujian Medical University Fuzhou 350005 ChinaDepartment of Neurology and Institute of Neurology of First Affiliated Hospital, Institute of Neuroscience, and Fujian Key Laboratory of Molecular Neurology Fujian Medical University Fuzhou 350005 ChinaAbstract Objective Human T‐cell leukemia virus type 1‐associated myelopathy (HAM) is a chronic, progressive, inflammatory disease with unclear pathogenesis and no effective treatments. We aimed to investigate a novel mechanistic theory and treat HAM patients with rituximab, which can deplete CD20+ B lymphocytes in circulation. Methods Single‐cell RNA sequencing (scRNA‐seq) data was analyzed to identify HTLV‐1‐associated B cells and their effect on T cells. An observational analysis of our HAM cohort was conducted to elucidate changes in the immunological microenvironment of these patients. Peripheral blood mononuclear cells (PBMC) from HAM patients were isolated to explore the efficacy of B cell depletion in vitro. To assess the effect of B‐cell depletion on HAM patients, eligible participants in our cohort received rituximab therapy (NCT04004819). Results ScRNA‐seq results suggest a significant effect of HTLV‐1‐associated B cells on T cells. Additionally, HTLV‐1 was found to infect B cells and depletion of B cells inhibited the proliferation of T cells. Number of B cells in HAM patients had positive correlation with the proviral load and infected cell counts. Depletion of B cells led to a reduction in HTLV‐1 proviral load in vitro. Furthermore, in clinical trial, 14 HAM patients were enrolled. Three patients (21.4%) who received rituximab failed to achieve remission, compared to 24 (85.7%) patients received any other therapy that failed to achieve remission. With a low level of circulating B cells, the proportion of Ki67‐positive cells in CD4+ T cells fell. Interpretation This study provided evidence that depleting B‐lymphocytes is an innovative strategy for treating patients with HAM and broadens the understanding of the role of B cells in infectious immunity.https://doi.org/10.1002/acn3.52190
spellingShingle Aowei Lv
Yaofeng Fang
Xiaohong Lin
Jiaying Chen
Huanhuan Song
Ning Wang
Wan‐Jin Chen
Ying Fu
Rui Li
Yi Lin
B‐cell depletion limits HTLV‐1‐infected T‐cell expansion and ameliorate HTLV‐1‐associated myelopathy
Annals of Clinical and Translational Neurology
title B‐cell depletion limits HTLV‐1‐infected T‐cell expansion and ameliorate HTLV‐1‐associated myelopathy
title_full B‐cell depletion limits HTLV‐1‐infected T‐cell expansion and ameliorate HTLV‐1‐associated myelopathy
title_fullStr B‐cell depletion limits HTLV‐1‐infected T‐cell expansion and ameliorate HTLV‐1‐associated myelopathy
title_full_unstemmed B‐cell depletion limits HTLV‐1‐infected T‐cell expansion and ameliorate HTLV‐1‐associated myelopathy
title_short B‐cell depletion limits HTLV‐1‐infected T‐cell expansion and ameliorate HTLV‐1‐associated myelopathy
title_sort b cell depletion limits htlv 1 infected t cell expansion and ameliorate htlv 1 associated myelopathy
url https://doi.org/10.1002/acn3.52190
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