Single-cell transcriptomics analysis of bullous pemphigoid unveils immune-stromal crosstalk in type 2 inflammatory disease

Nat Commun. 2024 Jul 15;15(1):5949. doi: 10.1038/s41467-024-50283-3.

Abstract

Bullous pemphigoid (BP) is a type 2 inflammation- and immunity-driven skin disease, yet a comprehensive understanding of the immune landscape, particularly immune-stromal crosstalk in BP, remains elusive. Herein, using single-cell RNA sequencing (scRNA-seq) and in vitro functional analyzes, we pinpoint Th2 cells, dendritic cells (DCs), and fibroblasts as crucial cell populations. The IL13-IL13RA1 ligand-receptor pair is identified as the most significant mediator of immune-stromal crosstalk in BP. Notably, fibroblasts and DCs expressing IL13RA1 respond to IL13-secreting Th2 cells, thereby amplifying Th2 cell-mediated cascade responses, which occurs through the specific upregulation of PLA2G2A in fibroblasts and CCL17 in myeloid cells, creating a positive feedback loop integral to immune-stromal crosstalk. Furthermore, PLA2G2A and CCL17 contribute to an increased titer of pathogenic anti-BP180-NC16A autoantibodies in BP patients. Our work provides a comprehensive insight into BP pathogenesis and shows a mechanism governing immune-stromal interactions, providing potential avenues for future therapeutic research.

MeSH terms

  • Autoantibodies / immunology
  • Autoantigens / genetics
  • Autoantigens / immunology
  • Autoantigens / metabolism
  • Chemokine CCL17* / genetics
  • Chemokine CCL17* / metabolism
  • Collagen Type XVII
  • Dendritic Cells* / immunology
  • Dendritic Cells* / metabolism
  • Female
  • Fibroblasts* / immunology
  • Fibroblasts* / metabolism
  • Gene Expression Profiling / methods
  • Humans
  • Inflammation / genetics
  • Inflammation / immunology
  • Inflammation / metabolism
  • Interleukin-13 / genetics
  • Interleukin-13 / immunology
  • Interleukin-13 / metabolism
  • Male
  • Myeloid Cells / immunology
  • Myeloid Cells / metabolism
  • Non-Fibrillar Collagens / genetics
  • Non-Fibrillar Collagens / immunology
  • Non-Fibrillar Collagens / metabolism
  • Pemphigoid, Bullous* / genetics
  • Pemphigoid, Bullous* / immunology
  • Single-Cell Analysis* / methods
  • Stromal Cells / immunology
  • Stromal Cells / metabolism
  • Th2 Cells* / immunology
  • Transcriptome

Substances

  • Chemokine CCL17
  • Autoantibodies
  • CCL17 protein, human
  • Interleukin-13
  • Non-Fibrillar Collagens
  • Autoantigens
  • Collagen Type XVII