Amplified Type I Interferon Response in Sjögren's Disease via Ectopic Toll-Like Receptor 7 Expression in Salivary Gland Epithelial Cells Induced by Lysosome-Associated Membrane Protein 3

Arthritis Rheumatol. 2024 Jul;76(7):1109-1119. doi: 10.1002/art.42844. Epub 2024 Jun 4.

Abstract

Objective: Lysosome-associated membrane protein 3 (LAMP3) misexpression in salivary gland epithelial cells plays a causal role in the development of salivary gland dysfunction and autoimmunity associated with Sjögren's disease (SjD). This study aimed to clarify how epithelial LAMP3 misexpression is induced in SjD.

Methods: To explore upstream signaling pathways associated with LAMP3 expression, we conducted multiple RNA sequencing analyses of minor salivary glands from patients with SjD, submandibular glands from a mouse model of SjD, and salivary gland epithelial cell lines. A hypothesis generated by the RNA sequencing analyses was further tested by in vitro and in vivo assays with gene manipulation.

Results: Transcriptome analysis suggested LAMP3 expression was associated with enhanced type I interferon (IFN) and IFNγ signaling pathways in patients with SjD. In vitro studies showed that type I IFN but not IFNγ stimulation could induce LAMP3 expression in salivary gland epithelial cells. Moreover, we discovered that LAMP3 overexpression could induce ectopic Toll-like receptor 7 (TLR-7) expression and type I IFN production in salivary gland epithelial cells both in vitro and in vivo. TLR-7 knockout mice did not develop any SjD-related symptoms following LAMP3 induction.

Conclusion: Epithelial LAMP3 misexpression can be induced through enhanced type I IFN response in salivary glands. In addition, LAMP3 can promote type I IFN production via ectopic TLR-7 expression in salivary gland epithelial cells. This positive feedback loop can contribute to maintaining LAMP3 misexpression and amplifying type I IFN production in salivary glands, which plays an essential role in the pathophysiology of SjD.

MeSH terms

  • Animals
  • Cell Line
  • Epithelial Cells* / metabolism
  • Female
  • Humans
  • Interferon Type I* / metabolism
  • Interferon-gamma / metabolism
  • Lysosomal Membrane Proteins* / genetics
  • Lysosomal Membrane Proteins* / metabolism
  • Lysosomal-Associated Membrane Protein 3
  • Mice
  • Neoplasm Proteins
  • Salivary Glands* / immunology
  • Salivary Glands* / metabolism
  • Salivary Glands, Minor / immunology
  • Salivary Glands, Minor / metabolism
  • Signal Transduction
  • Sjogren's Syndrome* / genetics
  • Sjogren's Syndrome* / immunology
  • Sjogren's Syndrome* / metabolism
  • Toll-Like Receptor 7* / genetics
  • Toll-Like Receptor 7* / metabolism

Substances

  • Interferon Type I
  • Toll-Like Receptor 7
  • Lysosomal Membrane Proteins
  • LAMP3 protein, human
  • Interferon-gamma
  • Neoplasm Proteins
  • Lysosomal-Associated Membrane Protein 3