Hspa13 Deficiency Impaired Marginal Zone B Cells Regulatory Function and Contributed to Lupus Pathogenesis

Abstract Dysregulated IL‐10 producing regulatory B cells (Bregs) are associated with the progression of systemic lupus erythematosus. An immunomodulatory role of heat shock proteins (HSPs) is implicated in autoimmune diseases. However, the molecular basis underlying the role of Hspa13 in regulating...

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Main Authors: Chen Xing, Haoran Cui, Ge Li, Xiaoling Liu, Kun Liu, Qing Wen, Xin Huang, Renxi Wang, Lun Song
Format: Article
Language:English
Published: Wiley 2025-02-01
Series:Advanced Science
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Online Access:https://doi.org/10.1002/advs.202413144
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author Chen Xing
Haoran Cui
Ge Li
Xiaoling Liu
Kun Liu
Qing Wen
Xin Huang
Renxi Wang
Lun Song
author_facet Chen Xing
Haoran Cui
Ge Li
Xiaoling Liu
Kun Liu
Qing Wen
Xin Huang
Renxi Wang
Lun Song
author_sort Chen Xing
collection DOAJ
description Abstract Dysregulated IL‐10 producing regulatory B cells (Bregs) are associated with the progression of systemic lupus erythematosus. An immunomodulatory role of heat shock proteins (HSPs) is implicated in autoimmune diseases. However, the molecular basis underlying the role of Hspa13 in regulating Bregs function and lupus pathogenesis remains unclear. In this study, Bregs display higher Hspa13 expression than IL‐10− B cells. Induction of IL‐10 production is weakened in B cells with Hspa13 knockdown or knockout. Hspa13 binds to the IL‐10 promoter via the TATA or CAAT box and activates IL‐10 transcription in the nucleus. Furthermore, Hspa13 positive cells are enriched in marginal zone (MZ) B cells to regulate IL‐10 production. Stimulated B220+ B or MZ B cells from CD19creHspa13fl/fl mice for Breg induction show an impaired capacity to promote CD4+Foxp3+ regulatory T cells (Treg) differentiation. In lupus MRL/lpr mice, a decline in Treg differentiation is accompanied by decreased Hspa13 expression in both Bregs and MZ B cells. Moreover, adoptive transfusion of Bregs and MZ B cells from CD19creHspa13fl/fl mice fails to increase the frequency of Tregs, attenuate renal pathology, or decrease anti‐dsDNA antibody levels. These results explain the unique role of Hspa13 in determining MZ regulatory function and affecting lupus pathogenesis.
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spelling doaj-art-31ea677333004db2b6ed62a68d25dac42025-08-20T03:09:54ZengWileyAdvanced Science2198-38442025-02-01128n/an/a10.1002/advs.202413144Hspa13 Deficiency Impaired Marginal Zone B Cells Regulatory Function and Contributed to Lupus PathogenesisChen Xing0Haoran Cui1Ge Li2Xiaoling Liu3Kun Liu4Qing Wen5Xin Huang6Renxi Wang7Lun Song8Beijing Institute of Basic Medical Sciences Beijing 100850 ChinaBeijing Institute of Basic Medical Sciences Beijing 100850 ChinaBeijing Institute of Basic Medical Sciences Beijing 100850 ChinaDepartment of Dermatology First Medical Centre of Chinese PLA General Hospital Beijing 100853 ChinaBeijing Institute of Basic Medical Sciences Beijing 100850 ChinaBeijing Institute of Basic Medical Sciences Beijing 100850 ChinaBeijing Institute of Basic Medical Sciences Beijing 100850 ChinaBeijing Institute of Brain Disorders, Laboratory of Brain Disorders, Ministry of Science and Technology Collaborative Innovation Center for Brain Disorders Capital Medical University Beijing 100069 ChinaBeijing Institute of Basic Medical Sciences Beijing 100850 ChinaAbstract Dysregulated IL‐10 producing regulatory B cells (Bregs) are associated with the progression of systemic lupus erythematosus. An immunomodulatory role of heat shock proteins (HSPs) is implicated in autoimmune diseases. However, the molecular basis underlying the role of Hspa13 in regulating Bregs function and lupus pathogenesis remains unclear. In this study, Bregs display higher Hspa13 expression than IL‐10− B cells. Induction of IL‐10 production is weakened in B cells with Hspa13 knockdown or knockout. Hspa13 binds to the IL‐10 promoter via the TATA or CAAT box and activates IL‐10 transcription in the nucleus. Furthermore, Hspa13 positive cells are enriched in marginal zone (MZ) B cells to regulate IL‐10 production. Stimulated B220+ B or MZ B cells from CD19creHspa13fl/fl mice for Breg induction show an impaired capacity to promote CD4+Foxp3+ regulatory T cells (Treg) differentiation. In lupus MRL/lpr mice, a decline in Treg differentiation is accompanied by decreased Hspa13 expression in both Bregs and MZ B cells. Moreover, adoptive transfusion of Bregs and MZ B cells from CD19creHspa13fl/fl mice fails to increase the frequency of Tregs, attenuate renal pathology, or decrease anti‐dsDNA antibody levels. These results explain the unique role of Hspa13 in determining MZ regulatory function and affecting lupus pathogenesis.https://doi.org/10.1002/advs.202413144Hspa13IL‐10MZ B cellsregulatory B cellsregulatory T cellsSLE
spellingShingle Chen Xing
Haoran Cui
Ge Li
Xiaoling Liu
Kun Liu
Qing Wen
Xin Huang
Renxi Wang
Lun Song
Hspa13 Deficiency Impaired Marginal Zone B Cells Regulatory Function and Contributed to Lupus Pathogenesis
Advanced Science
Hspa13
IL‐10
MZ B cells
regulatory B cells
regulatory T cells
SLE
title Hspa13 Deficiency Impaired Marginal Zone B Cells Regulatory Function and Contributed to Lupus Pathogenesis
title_full Hspa13 Deficiency Impaired Marginal Zone B Cells Regulatory Function and Contributed to Lupus Pathogenesis
title_fullStr Hspa13 Deficiency Impaired Marginal Zone B Cells Regulatory Function and Contributed to Lupus Pathogenesis
title_full_unstemmed Hspa13 Deficiency Impaired Marginal Zone B Cells Regulatory Function and Contributed to Lupus Pathogenesis
title_short Hspa13 Deficiency Impaired Marginal Zone B Cells Regulatory Function and Contributed to Lupus Pathogenesis
title_sort hspa13 deficiency impaired marginal zone b cells regulatory function and contributed to lupus pathogenesis
topic Hspa13
IL‐10
MZ B cells
regulatory B cells
regulatory T cells
SLE
url https://doi.org/10.1002/advs.202413144
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