B cell subpopulations and their role in the pathogenesis of primary Sjögren's syndrome: insights from single-cell RNA sequencing

B细胞亚群及其在原发性干燥综合征发病机制中的作用:来自单细胞RNA测序的启示

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Abstract

OBJECTIVE: This study aims to investigate the potential role of B cells in the pathogenesis of Primary Sjögren's Syndrome (pSS) by analyzing cell types, differentially expressed genes, and associated signaling pathways using single-cell RNA sequencing. METHODS: Peripheral blood mononuclear cells (PBMCs) from 3 pSS patients and 3 healthy controls (HCs) were collected. Single-cell transcriptomic analysis was performed, including Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment analysis, transcription factor analysis, pseudotime analysis, cell communication analysis, and B cell receptor (BCR) repertoire analysis. Genes and pathways potentially involved in the pathogenesis of pSS were identified, and key genes were validated by qRT-PCR. Statistical significance was assessed using T-tests and the Wilcoxon rank-sum test, with a p-value < 0.05 considered statistically significant. RESULTS: Single-cell RNA sequencing of peripheral blood B cells from three patients with primary Sjögren's syndrome (pSS) and three healthy controls (HCs) identified three subpopulations: memory B (Bmem), naïve B (NaiveB), and plasma cells (PlasmaCells). In pSS, differentially expressed genes were enriched in Type I interferon signaling, antigen processing/presentation, and MHC class II binding. Transcription factors related to interferon responses, including NR2F6, IRF5, STAT2, and IRF9, were upregulated. Cell-cell communication analysis highlighted frequent interactions via TNFSF10-TNFRSF10C and TGFB1-TGFBR3. Pseudotime analysis indicated accelerated NaiveB differentiation along the effector branch. B cell receptor repertoire analysis revealed increased IGHV4-34 usage and higher IGHJ4/IGHJ6 usage in PlasmaCells, with reduced IGHV1-3, IGHV1-69D, and IGHV2-7D usage. qRT-PCR validation in 22 pSS patients and 22 HCs confirmed significant ISG15 upregulation (p < 0.0001). CONCLUSION: B cells contribute to the pathogenesis of pSS through the Type I IFN signaling pathway mediated by genes such as ISG15, alterations in BCR clonality, IGHV-J gene rearrangements, and abnormal gene usage.

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