The benzoylphenylurea derivative BPU17 acts as an inhibitor of prohibitin and exhibits antifibrotic activity

Exp Cell Res. 2024 Sep 1;442(1):114221. doi: 10.1016/j.yexcr.2024.114221. Epub 2024 Aug 23.

Abstract

Inflammation-induced choroidal neovascularization followed by the epithelial-mesenchymal transition (EMT) of retinal pigment epithelial cells (RPEs) is a cause of neovascular age-related macular degeneration (nAMD). RPE-derived myofibroblasts overproduce extracellular matrix, leading to subretinal fibrosis. We already have demonstrated that benzylphenylurea (BPU) derivatives inhibit the function of cancer-associated fibroblasts. Here, we investigated the anti-myofibroblast effects of BPU derivatives and examined such BPU activity on subretinal fibrosis. A BPU derivative, BPU17, exhibits the most potent anti-myofibroblast activity among dozens of BPU derivatives and inhibits subretinal fibrosis in a mouse model of retinal degeneration. Investigations with primary cultured RPEs reveal that BPU17 suppresses cell motility and collagen synthesis in RPE-derived myofibroblasts. These effects depend on repressing the serum response factor (SRF)/CArG-box-dependent transcription. BPU17 inhibits the expression of SRF cofactor, cysteine and glycine-rich protein 2 (CRP2), which activates the SRF function. Proteomics analysis reveals that BPU17 binds to prohibitin 1 (PHB1) and inhibits the PHB1-PHB2 interaction, resulting in mild defects in mitochondrial function. This impairment causes a decrease in the expression of CRP2 and suppresses collagen synthesis. Our findings suggest that BPU17 is a promising agent against nAMD and the close relationship between PHB function and EMT.

Keywords: Benzylphenylure; Epithelial-mesenchymal transition; Prohibitin; Retinal fibrosis; Retinal pigment epithelial cell.

MeSH terms

  • Animals
  • Antifibrotic Agents / pharmacology
  • Cell Movement / drug effects
  • Cells, Cultured
  • Epithelial-Mesenchymal Transition / drug effects
  • Fibrosis* / drug therapy
  • Humans
  • Macular Degeneration / drug therapy
  • Macular Degeneration / metabolism
  • Macular Degeneration / pathology
  • Mice
  • Mice, Inbred C57BL
  • Myofibroblasts* / drug effects
  • Myofibroblasts* / metabolism
  • Myofibroblasts* / pathology
  • Prohibitins*
  • Repressor Proteins* / metabolism
  • Retinal Pigment Epithelium / drug effects
  • Retinal Pigment Epithelium / metabolism
  • Retinal Pigment Epithelium / pathology
  • Serum Response Factor / antagonists & inhibitors
  • Serum Response Factor / metabolism

Substances

  • Prohibitins
  • Repressor Proteins
  • Antifibrotic Agents
  • PHB protein, human
  • Serum Response Factor