Downregulation of FcRn promotes ferroptosis in herpes simplex virus-1-induced lung injury

Cell Mol Life Sci. 2025 Jan 6;82(1):36. doi: 10.1007/s00018-024-05555-y.

Abstract

Herpes simplex virus type I (HSV-1) infection is associated with lung injury; however, no specific treatment is currently available. In this study, we found a significant negative correlation between FcRn levels and the severity of HSV-1-induced lung injury. HSV-1 infection increases the methylation of the FcRn promoter, which suppresses FcRn expression by upregulating DNMT3b expression. Analysis of the FcRn promoter revealed that the -1296- to -919-bp region is the key regulatory region, with the CG site at -967/-966 bp being the critical methylation site. The transcription factor JUN binds to this CG site to increase FcRn transcription; however, its activity was significantly inhibited by DNMT3b overexpression. Moreover, 5-Aza-2 effectively reduced HSV-1-induced lung injury and inhibited ferroptosis. Transcriptomic sequencing revealed that the ferroptosis pathway was highly activated in the lung tissues of FcRn-knockout mice via the p53/SLC7A11 pathway. Furthermore, in vivo and in vivo experiments showed that FcRn knockout aggravated lung epithelial cell inflammation by promoting ferroptosis; however, this effect was reversed by a ferroptosis inhibitor. Thus, HSV-1 infection suppressed FcRn expression through promoter methylation and promoted ferroptosis and lung injury. These findings reveal a novel molecular mechanism underlying viral lung injury and suggest potential therapeutic strategies for targeting FcRn.

Keywords: DNMT3b; FcRn; Ferroptosis; HSV-1; Lung injury.

MeSH terms

  • Amino Acid Transport System y+ / genetics
  • Amino Acid Transport System y+ / metabolism
  • Animals
  • DNA Methylation
  • Down-Regulation / genetics
  • Ferroptosis* / genetics
  • Herpes Simplex / genetics
  • Herpes Simplex / metabolism
  • Herpes Simplex / pathology
  • Herpes Simplex / virology
  • Herpesvirus 1, Human* / genetics
  • Herpesvirus 1, Human* / pathogenicity
  • Herpesvirus 1, Human* / physiology
  • Histocompatibility Antigens Class I* / genetics
  • Histocompatibility Antigens Class I* / metabolism
  • Humans
  • Lung Injury / genetics
  • Lung Injury / metabolism
  • Lung Injury / pathology
  • Lung Injury / virology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout*
  • Promoter Regions, Genetic* / genetics
  • Receptors, Fc* / genetics
  • Receptors, Fc* / metabolism
  • Tumor Suppressor Protein p53 / genetics
  • Tumor Suppressor Protein p53 / metabolism

Substances

  • Histocompatibility Antigens Class I
  • Receptors, Fc
  • Fc receptor, neonatal
  • Slc7a11 protein, mouse
  • Amino Acid Transport System y+
  • Tumor Suppressor Protein p53