Single-cell RNA sequencing reveals the heterogeneity and regulatory modules of cell-specific RNA-binding proteins in patients with systemic lupus erythematosus

单细胞RNA测序揭示了系统性红斑狼疮患者细胞特异性RNA结合蛋白的异质性和调控模块

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Abstract

BACKGROUND: Systemic lupus erythematosus (SLE) is an autoimmune disorder characterized by immune dysregulation, heterogeneous clinical phenotypes, and a complex interplay of pathogenic mechanisms. RNA-binding proteins (RBPs), which orchestrate post-transcriptional gene regulation through dynamic interactions with target transcripts, are increasingly implicated in autoimmune pathogenesis. However, the cell-type-specific heterogeneity of RBPs expression and their regulatory networks in SLE remain poorly characterized. METHODS: To delineate RBPs dynamics in SLE skin microenvironment, we conducted a comprehensive single-cell transcriptomic analysis of publicly accessible single cell RNA sequencing (scRNA-seq) datasets from lesional skin biopsies of SLE patients and healthy controls (HC). Cell-type-specific RBPs expression patterns were systematically profiled across epidermal keratinocytes, dermal endothelial cells, and T cells. Complementary bulk RNA-Seq analyses employing Splicing Site Usage Variation Analysis (SUVA) were performed to identify immune gene-associated regulatory alternative splicing (RAS) events. Integrative co-expression networks linking RBPs, RAS events, and immune pathways were subsequently constructed. RESULTS: Single-cell resolution revealed marked heterogeneity in RBPs expression across keratinocyte, endothelial cell, and T cell in SLE compared to HC. Notably, disease-specific RBPs were enriched in pathways governing interferon response, cytokine signaling, and leukocyte activation. Cross-analysis with bulk transcriptomic data highlighted JUN and HLA-A as hub regulators exhibiting elevated expression in SLE T cells. Network modeling further uncovered coordinated interactions between JUN, HLA-A, and RAS events in immune genes, implicating their synergistic roles in modulating T cell effector functions. CONCLUSION: Our multi-omics integration identifies JUN and HLA-A as central coordinators of alternative splicing programs in SLE T cells. These molecular hubs, embedded within immune regulatory networks, may drive pathogenic rewiring of T cell responses in SLE.

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