Humoral immune activation within tertiary lymphoid structures is correlated with poor outcomes in oral lichen planus and lichenoid lesions

Front Immunol. 2025 Oct 22:16:1667976. doi: 10.3389/fimmu.2025.1667976. eCollection 2025.

Abstract

Background: Oral lichen planus (OLP) and oral lichenoid lesions (OLL) are chronic immune-mediated mucosal disorders with heterogeneous clinical presentations. While T cell-mediated mechanisms have been extensively studied, the role of humoral immunity, particularly B cell activation and plasma cell differentiation, remains insufficiently understood.

Methods: RNA sequencing datasets from healthy oral mucosa and OLP lesions were integrated and analyzed to identify differentially expressed genes. Consensus clustering based on a validated tertiary lymphoid structure (TLS) signature genes (TSGs) was used to define immune subtypes. Associations with clinical severity and recurrence were validated in an independent RNA-seq cohort. Immunohistochemistry analysis of CD20+ B cells and CD38+ plasma cells was conducted in a separate clinical cohort of OLP/OLL patients.

Results: Based on TSGs, two immune subtypes were identified: Subtype A was enriched for CCL3, IL2RA, and IL1R2. Subtype B exhibited elevated expression of humoral activation markers IRF4 and TNFRSF17 and enrichment of B cell-related pathways. Transcriptomic features of Subtype B were significantly associated with erosive and recurrent OLP cases. Immunohistochemistry confirmed that CD20+ B cells were enriched in TLS-like structures (P < 0.001), whereas CD38+ plasma cells were closely linked to erosive phenotypes (P = 0.038).

Conclusions: TLS-associated B cell maturation and plasma cell infiltration define a humoral activation axis linked to unfavorable clinical outcomes in OLP/OLL. The presence of activated B cells and plasma cells correlates with erosive and recurrent disease phenotypes, highlighting their potential as prognostic biomarkers and therapeutic targets for improving disease management.

Keywords: B cells; humoral immunity; immune subtyping; oral lichen planus; plasma cells; tertiary lymphoid structure.

MeSH terms

  • Adult
  • Aged
  • B-Lymphocytes / immunology
  • Female
  • Gene Expression Profiling
  • Humans
  • Immunity, Humoral*
  • Lichen Planus, Oral* / genetics
  • Lichen Planus, Oral* / immunology
  • Lichen Planus, Oral* / pathology
  • Lymphocyte Activation / immunology
  • Male
  • Middle Aged
  • Mouth Mucosa / immunology
  • Mouth Mucosa / pathology
  • Plasma Cells / immunology
  • Prognosis
  • Tertiary Lymphoid Structures* / genetics
  • Tertiary Lymphoid Structures* / immunology
  • Tertiary Lymphoid Structures* / pathology
  • Transcriptome