The CoV-Y domain of SARS-CoV-2 Nsp3 interacts with BRAP to stimulate NF-κB signaling and induce host inflammatory responses

Int J Biol Macromol. 2024 Nov;280(Pt 4):136123. doi: 10.1016/j.ijbiomac.2024.136123. Epub 2024 Sep 28.

Abstract

Non-structural protein 3 (Nsp3) is the largest protein encoded by the coronavirus (CoV) genome. It consists of multiple domains that perform critical functions during the viral life cycle. CoV-Y is the most C-terminal domain of Nsp3, and it exhibits evolutionary conservation across diverse CoVs; however, the exact biological function of CoV-Y remains unclear. Here, we determined the crystal structure of CoV-Y of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) Nsp3 using the single-wavelength anomalous diffraction method. We revealed the interaction between CoV-Y and the host BRCA1-associated protein (BRAP) using immunoprecipitation-mass spectrometry experiments. This interaction was subsequently confirmed in cellular assays, and the precise binding-regions between these two proteins were clarified. We found that this interaction is conserved in SARS-CoV and Middle East respiratory syndrome coronavirus. Next, we demonstrated that CoV-Y enhances IκBα and IκBβ phosphorylation and promotes the nuclear translocation of the downstream NF-κB members p50 and p65 through binding to BRAP. The CoV-Y-BRAP interaction can upregulate the transcript levels of the host inflammatory cytokines. Overall, our findings illustrate the biological function of CoV-Y for the first time and provide novel insights into coronavirus regulation of host inflammatory responses, as well as a possible target for antiviral drug development.

Keywords: Coronavirus; Host protein; NF-κB pathway; Non-structural protein; Protein–protein interaction.

MeSH terms

  • COVID-19 / metabolism
  • COVID-19 / virology
  • Coronavirus Papain-Like Proteases / chemistry
  • Coronavirus Papain-Like Proteases / metabolism
  • Humans
  • Inflammation / metabolism
  • NF-kappa B* / metabolism
  • Phosphorylation
  • Protein Binding
  • Protein Domains
  • SARS-CoV-2* / metabolism
  • Signal Transduction*
  • Viral Nonstructural Proteins / chemistry
  • Viral Nonstructural Proteins / genetics
  • Viral Nonstructural Proteins / metabolism

Substances

  • NF-kappa B
  • Viral Nonstructural Proteins
  • Coronavirus Papain-Like Proteases