Possible involvement of Toll-like receptor 8-positive monocytes/macrophages in the pathogenesis of Sjögren's disease

Front Immunol. 2024 Oct 31:15:1480675. doi: 10.3389/fimmu.2024.1480675. eCollection 2024.

Abstract

Background: Sjögren's disease (SjD) is an autoimmune disease marked by lymphocytic infiltration of salivary and lacrimal glands, leading to glandular dysfunction, where CD4-positive helper T (Th) cells and their cytokines are crucial in the pathogenesis. Recent studies have demonstrated that Toll-like receptors (TLRs), particularly those recognizing immune complexes containing DNA and RNA, contribute to Th cell activation in various autoimmune diseases. This study explores the expression and function of these TLRs in SjD.

Methods: DNA microarray analysis of salivary gland tissue from six SjD patients and real-time PCR (n = 32) was used to identify overexpressed TLRs. Single-cell RNA sequencing (scRNA-seq) was performed using tissue lesions and integrated with published scRNA-seq data from tissues and peripheral blood mononuclear cells to examine gene expression in macrophages and monocytes. Finally, multi-color immunofluorescence staining was conducted to confirm TLR8 expression and function in SjD lesions (n = 19).

Results: DNA microarray analysis revealed the up-regulation of TLR8, along with other TLRs and innate immune response genes in SjD. Real-time PCR showed significant up-regulation of TLR7 and TLR8. TLR8 up-regulated in both analyses. In scRNA-seq analysis, the TLR8-expressing cluster comprised macrophages and monocytes, which also produced T cell activation genes like CD86. TLR8-positive macrophages infiltrated inflammatory sites and frequently expressed CD86 in quantitative imaging approaches.

Conclusions: These results suggest that infiltrating monocytes and macrophages may produce cytokines and chemokines through TLR8 stimulation, potentially enhancing B7 molecule expression, promoting the adaptive immune response, and contributing to SjD pathogenesis.

Keywords: CD86; Sjögren’s disease; Toll-like receptor 8; macrophage; monocyte.

MeSH terms

  • Adult
  • Aged
  • B7-2 Antigen / genetics
  • B7-2 Antigen / metabolism
  • Female
  • Humans
  • Macrophages* / immunology
  • Macrophages* / metabolism
  • Male
  • Middle Aged
  • Monocytes* / immunology
  • Monocytes* / metabolism
  • Salivary Glands / immunology
  • Salivary Glands / metabolism
  • Salivary Glands / pathology
  • Sjogren's Syndrome* / immunology
  • Sjogren's Syndrome* / metabolism
  • Toll-Like Receptor 8* / genetics
  • Toll-Like Receptor 8* / metabolism

Substances

  • Toll-Like Receptor 8
  • TLR8 protein, human
  • B7-2 Antigen

Grants and funding

The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. NK was supported by JSPS KAKENHI (Grant numbers: 21KK0163, 22H03290, and 23K18362), the JST FOREST PROGRAM (JPMJFR220M), the Takeda Foundation, the Nakajima Foundation, and the Uehara Memorial Foundation. MM was supported by JSPS KAKENHI (Grant numbers: 22K19631, 23KK0164, and 23K18362). MS was supported by JSPS KAKENHI (Grant number: 24K19996).