Human cytomegalovirus RNA2.7 inhibits ferroptosis by upregulating ferritin and GSH via promoting ZNF395 degradation

PLoS Pathog. 2024 Dec 26;20(12):e1012815. doi: 10.1371/journal.ppat.1012815. eCollection 2024 Dec.

Abstract

Human cytomegalovirus (HCMV) is a herpes virus with a long replication cycle. HCMV encoded long non-coding RNA termed RNA2.7 is the dominant transcript with a length of about 2.5kb, accounting for 25% of total viral transcripts. Studies have shown that HCMV RNA2.7 inhibits apoptosis caused by infection. The effect of RNA2.7 on other forms of cell death is still unclear. In this work, we found that RNA2.7 deletion significantly decreased the viability of HCMV-infected cells, while treatment with ferroptosis inhibitor Fer-1 rescued the infection-induced cell death, demonstrating an anti-ferroptosis role of RNA2.7. The results further showed that RNA2.7 inhibited ferroptosis via enhancing Ferritin Heavy Chain 1 (FTH1) and Solute Carrier Family 7 Member 11 (SLC7A11) expression in Erastin treated cells without involving other viral components. Pooled Genome-wide CRISPR screening revealed zinc finger protein 395 (ZNF395) as a new regulator repressing the expression of FTH1 and SLC7A11. HCMV RNA2.7 promoted proteasome-mediated degradation of ZNF395 that resulted in upregulation of FTH1 and SLC7A11 to inhibit ferroptosis, therefore maintain survival in host cells and complete replication of virus.

MeSH terms

  • Amino Acid Transport System y+ / genetics
  • Amino Acid Transport System y+ / metabolism
  • Cytomegalovirus Infections* / genetics
  • Cytomegalovirus Infections* / metabolism
  • Cytomegalovirus Infections* / virology
  • Cytomegalovirus* / genetics
  • Cytomegalovirus* / physiology
  • Ferritins / genetics
  • Ferritins / metabolism
  • Ferroptosis*
  • Glutathione / metabolism
  • Humans
  • Oxidoreductases
  • RNA, Long Noncoding / genetics
  • RNA, Long Noncoding / metabolism
  • RNA, Viral / genetics
  • RNA, Viral / metabolism
  • Up-Regulation

Substances

  • Glutathione
  • Amino Acid Transport System y+
  • Ferritins
  • FTH1 protein, human
  • RNA, Long Noncoding
  • RNA, Viral
  • SLC7A11 protein, human
  • Oxidoreductases

Grants and funding

This work was supported by the National Natural Science Foundation of China (grant no. 82071664 to Q.R.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.