JAG1 mediates apoptosis in herpes simplex keratitis by suppressing autophagy via ROS/JAG1/NOTCH1/pULK1 signaling pathway

Cell Biol Toxicol. 2024 Dec 20;41(1):1. doi: 10.1007/s10565-024-09968-0.

Abstract

Herpes simplex keratitis (HSK), an ocular disease resulted from herpes simplex virus type 1 (HSV-1) infection, leads to the majority of infectious corneal blindness worldwide. The apoptosis of corneal epithelial cells (CECs) resulted from HSV-1 disrupts the epithelial barrier and exacerbates the infection; however, there is no definitive cure for HSK. Jagged1 (JAG1), one of the primary functional ligands for NOTCH receptors, plays a crucial role in regulating apoptosis and autophagy; however, its role in HSK is unclear. Our transcriptome analysis showed JAG1 was significantly upregulated in HSV-1-infected human CECs. We aimed to explore JAG1's role in regulating apoptosis in HSV-1-infected human CECs and in HSK mice. HSV-1 infection induced apoptosis and reactive oxygen species (ROS) generation in CECs. HSV-1 also activated the JAG1/NOTCH1 signaling pathway. The ROS scavenger N-acetylcysteine significantly mitigated these effects. Additionally, inhibiting the JAG1/NOTCH1 pathway with short hairpin RNA against JAG1 or a NOTCH1 inhibitor (N-[N-{3,5-difuorophenacetyl}-1-alanyl]-S-phenylglycine t-butyl ester [DAPT]) alleviated HSV-1-induced CEC apoptosis. Transmission electron microscopy and western blotting revealed that HSV-1 infection suppressed ULK1-mediated autophagy in CECs, while DAPT treatment enhanced autophagy by suppressing ULK1 phosphorylation. The activation of autophagy by rapamycin treatment markedly reduced ROS levels and apoptosis in HSV-1-infected CECs, revealing a synergistic effect between the suppressed autophagy and increased ROS levels, ultimately leading to apoptosis. Thus, HSV-1 induces CEC apoptosis by suppressing autophagy through ROS/JAG1/NOTCH1/pULK1 signaling pathway in vitro and in vivo, providing potential therapeutic targets for HSK.

Keywords: Apoptosis; Autophagy; Corneal epithelial cell; Herpes simplex virus; JAG1; Reactive oxygen species.

MeSH terms

  • Animals
  • Apoptosis* / drug effects
  • Autophagy* / drug effects
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism
  • Epithelial Cells / pathology
  • Epithelial Cells / virology
  • Female
  • Herpesvirus 1, Human / physiology
  • Humans
  • Jagged-1 Protein* / genetics
  • Jagged-1 Protein* / metabolism
  • Keratitis, Herpetic* / metabolism
  • Keratitis, Herpetic* / pathology
  • Keratitis, Herpetic* / virology
  • Mice
  • Reactive Oxygen Species* / metabolism
  • Receptor, Notch1* / genetics
  • Receptor, Notch1* / metabolism
  • Signal Transduction* / drug effects

Substances

  • Receptor, Notch1
  • Jagged-1 Protein
  • Reactive Oxygen Species
  • NOTCH1 protein, human
  • JAG1 protein, human