The SARS-CoV-2 ORF6 protein inhibits nuclear export of mRNA and spliceosomal U snRNA

PLoS One. 2024 Oct 31;19(10):e0312098. doi: 10.1371/journal.pone.0312098. eCollection 2024.

Abstract

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is the causative agent of coronavirus disease 19 (COVID-19). SARS-CoV-2 infection suppresses host innate immunity and impairs cell viability. Among the viral proteins, ORF6 exhibits potent interferon (IFN) antagonistic activity and cellular toxicity. It also interacts with the RNA export factor RAE1, which bridges the nuclear pore complex and nuclear export receptors, suggesting an effect on RNA export. Using the Xenopus oocyte microinjection system, I found that ORF6 blocked the export of not only mRNA but also spliceosomal U snRNA. I further demonstrated that ORF6 affects the interaction between RAE1 and nuclear export receptors and inhibits the RNA binding of RAE1. These effects of ORF6 may cumulatively block the export of several classes of RNA. I also found that ORF6 binds RNA and forms oligomers. These findings provide insights into the suppression of innate immune responses and the reduction in cell viability caused by SARS-CoV-2 infection, contributing to the development of antiviral drugs targeting ORF6.

MeSH terms

  • Active Transport, Cell Nucleus*
  • Animals
  • COVID-19 / metabolism
  • COVID-19 / virology
  • Humans
  • Nuclear Matrix-Associated Proteins / genetics
  • Nuclear Matrix-Associated Proteins / metabolism
  • Nucleocytoplasmic Transport Proteins* / genetics
  • Nucleocytoplasmic Transport Proteins* / metabolism
  • Oocytes / metabolism
  • Oocytes / virology
  • RNA, Messenger* / genetics
  • RNA, Messenger* / metabolism
  • RNA, Small Nuclear* / genetics
  • RNA, Small Nuclear* / metabolism
  • SARS-CoV-2* / genetics
  • SARS-CoV-2* / metabolism
  • Spliceosomes* / metabolism
  • Viral Proteins / genetics
  • Viral Proteins / metabolism
  • Xenopus laevis

Substances

  • RNA, Messenger
  • RNA, Small Nuclear
  • ORF6 protein, SARS-CoV-2
  • Nucleocytoplasmic Transport Proteins
  • Viral Proteins
  • RAE1 protein, human
  • Nuclear Matrix-Associated Proteins

Grants and funding

This project has received funding from: The Japan Society for the Promotion of Science (JSPS) KAKENHI (21K06016 to I.T) The Shimizu Foundation for Immunology and Neuroscience Grant for 2020 (to I.T.) The Kao Research Council for the Study of Healthcare Science (C-213005 to I.T) The Fujiwara Memorial Foundation (to I.T.) The LiMe Office of Director's Research Grants Program (to I.T.) The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.