Single-Cell RNA Sequencing Reveals Dysregulated POSTN+WNT5A+ Fibroblast Subclusters in Prurigo Nodularis

J Invest Dermatol. 2024 Jul;144(7):1568-1578.e5. doi: 10.1016/j.jid.2023.12.021. Epub 2024 Jan 20.

Abstract

Prurigo nodularis (PN) is an intensely pruritic, inflammatory skin disease with a poorly understood pathogenesis. We performed single-cell transcriptomic profiling of 28,695 lesional and nonlesional PN cells. Lesional PN has increased dysregulated fibroblasts (FBs) and myofibroblasts. FBs in lesional PN were shifted toward a cancer-associated FB-like phenotype, with POSTN+WNT5A+ cancer-associated FBs increased in PN and similarly so in squamous cell carcinoma. A multicenter cohort study revealed an increased risk of squamous cell carcinoma and cancer-associated FB-associated malignancies (breast and colorectal) in patients with PN. Systemic fibroproliferative diseases (renal sclerosis and idiopathic pulmonary fibrosis) were upregulated in patients with PN. Ligand-receptor analyses demonstrated an FB neuronal axis with FB-derived WNT5A and periostin interactions with neuronal receptors melanoma cell adhesion molecule and ITGAV. These findings identify a pathogenic and targetable POSTN+WNT5A+ FB subpopulation that may predispose cancer-associated FB-associated malignancies in patients with PN.

Keywords: Fibroblasts; Periostin; Prurigo nodularis; WNT5A; scRNAseq.

Publication types

  • Multicenter Study

MeSH terms

  • Adult
  • Carcinoma, Squamous Cell / genetics
  • Carcinoma, Squamous Cell / metabolism
  • Carcinoma, Squamous Cell / pathology
  • Cell Adhesion Molecules* / genetics
  • Cell Adhesion Molecules* / metabolism
  • Female
  • Fibroblasts* / metabolism
  • Fibroblasts* / pathology
  • Gene Expression Profiling
  • Humans
  • Male
  • Middle Aged
  • Prurigo* / genetics
  • Prurigo* / metabolism
  • Prurigo* / pathology
  • Sequence Analysis, RNA
  • Single-Cell Analysis*
  • Skin Neoplasms / genetics
  • Skin Neoplasms / metabolism
  • Skin Neoplasms / pathology
  • Wnt-5a Protein* / genetics
  • Wnt-5a Protein* / metabolism

Substances

  • Wnt-5a Protein
  • WNT5A protein, human
  • POSTN protein, human
  • Cell Adhesion Molecules