SARS-CoV-2 NSP3/4 control formation of replication organelle and recruitment of RNA polymerase NSP12

J Cell Biol. 2025 Mar 3;224(3):e202306101. doi: 10.1083/jcb.202306101. Epub 2024 Dec 31.

Abstract

β-coronavirus rearranges the host cellular membranes to form double-membrane vesicles (DMVs) via NSP3/4, which anchor replication-transcription complexes (RTCs), thereby constituting the replication organelles (ROs). However, the impact of specific domains within NSP3/4 on DMV formation and RO assembly remains largely unknown. By using cryogenic-correlated light and electron microscopy (cryo-CLEM), we discovered that the N-terminal and C-terminal domains (NTD and CTD) of SARS-CoV-2 NSP3 are essential for DMV formation. Nevertheless, the CTD of NSP4 is not essential for DMV formation but regulates the DMV numbers. Additionally, the NTD of NSP3 is required for recruiting the RTC component to the cytosolic face of DMVs through direct interaction with NSP12 to assemble ROs. Furthermore, we observed that the size of NSP3/4-induced DMVs is smaller than virus-induced DMVs and established that RTC-mediated synthesis of double-stranded RNA (dsRNA) cargo plays a crucial role in determining DMV size. Collectively, our findings reveal that β-coronaviruses exploit the NSP3/4/12 axis to establish the viral ROs.

MeSH terms

  • Animals
  • COVID-19 / genetics
  • COVID-19 / metabolism
  • COVID-19 / pathology
  • COVID-19 / virology
  • Coronavirus Papain-Like Proteases / genetics
  • Coronavirus Papain-Like Proteases / metabolism
  • Coronavirus RNA-Dependent RNA Polymerase / genetics
  • Coronavirus RNA-Dependent RNA Polymerase / metabolism
  • Cryoelectron Microscopy
  • HEK293 Cells
  • Humans
  • Organelles / metabolism
  • Organelles / ultrastructure
  • Organelles / virology
  • Protein Domains
  • RNA, Viral / genetics
  • RNA, Viral / metabolism
  • SARS-CoV-2* / genetics
  • SARS-CoV-2* / metabolism
  • Viral Nonstructural Proteins* / genetics
  • Viral Nonstructural Proteins* / metabolism
  • Viral Replication Compartments / metabolism
  • Virus Replication*

Substances

  • Viral Nonstructural Proteins
  • NSP12 protein, SARS-CoV-2
  • Coronavirus Papain-Like Proteases
  • Coronavirus RNA-Dependent RNA Polymerase
  • RNA, Viral