Gamma-Secretase Inhibitors Downregulate the Profibrotic NOTCH Signaling Pathway in Recessive Dystrophic Epidermolysis Bullosa

J Invest Dermatol. 2024 Jul;144(7):1522-1533.e10. doi: 10.1016/j.jid.2023.10.045. Epub 2024 Jan 17.

Abstract

Recessive dystrophic epidermolysis bullosa (RDEB) is a rare skin fragility disorder caused by mutations in COL7A1. RDEB is hallmarked by trauma-induced unremitting blistering, chronic wounds with inflammation, and progressive fibrosis, leading to severe disease complications. There is currently no cure for RDEB-associated fibrosis. Our previous studies and increasing evidence highlighted the profibrotic role of NOTCH pathway in different skin disorders, including RDEB. In this study, we further investigated the role of NOTCH signaling in RDEB pathogenesis and explored the effects of its inhibition by γ-secretase inhibitors DAPT and PF-03084014 (nirogacestat). Our analyses demonstrated that JAG1 and cleaved NOTCH1 are upregulated in primary RDEB fibroblasts (ie, RDEB-derived fibroblasts) compared with controls, and their protein levels are further increased by TGF-β1 stimulation. Functional assays unveiled the involvement of JAG1/NOTCH1 axis in RDEB fibrosis and demonstrated that its blockade counteracts a variety of fibrotic traits. In particular, RDEB-derived fibroblasts treated with PF-03084014 showed (i) a significant reduction of contractility, (ii) a diminished secretion of TGF-β1 and collagens, and (iii) the downregulation of several fibrotic proteins. Although less marked than PF-03084014-treated cells, RDEB-derived fibroblasts exhibited a reduction of fibrotic traits also upon DAPT treatment. This study provides potential therapeutic strategies to antagonize RDEB fibrosis onset and progression.

Keywords: DAPT; Fibroblasts; JAG1; Nirogacestat (PF-03084014); skin fibrosis.

MeSH terms

  • Amyloid Precursor Protein Secretases* / antagonists & inhibitors
  • Amyloid Precursor Protein Secretases* / metabolism
  • Cells, Cultured
  • Collagen Type VII / genetics
  • Collagen Type VII / metabolism
  • Diamines
  • Dipeptides / pharmacology
  • Down-Regulation / drug effects
  • Epidermolysis Bullosa Dystrophica* / drug therapy
  • Epidermolysis Bullosa Dystrophica* / genetics
  • Epidermolysis Bullosa Dystrophica* / pathology
  • Female
  • Fibroblasts* / drug effects
  • Fibroblasts* / metabolism
  • Fibrosis*
  • Humans
  • Jagged-1 Protein* / genetics
  • Jagged-1 Protein* / metabolism
  • Male
  • Receptor, Notch1 / antagonists & inhibitors
  • Receptor, Notch1 / genetics
  • Receptor, Notch1 / metabolism
  • Signal Transduction* / drug effects
  • Skin / drug effects
  • Skin / metabolism
  • Skin / pathology
  • Tetrahydronaphthalenes
  • Thiazoles
  • Transforming Growth Factor beta1 / metabolism
  • Valine / analogs & derivatives

Substances

  • Amyloid Precursor Protein Secretases
  • Jagged-1 Protein
  • JAG1 protein, human
  • Receptor, Notch1
  • Dipeptides
  • nirogacestat
  • NOTCH1 protein, human
  • Collagen Type VII
  • COL7A1 protein, human
  • Transforming Growth Factor beta1
  • 24-diamino-5-phenylthiazole
  • Diamines
  • Tetrahydronaphthalenes
  • Thiazoles
  • Valine