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J Med Virol . The SARS-unique domain (SUD) of SARS-CoV-2 nsp3 protein inhibits the antiviral immune responses through the NF-κB pathway

tetano

Editor, Senior Moderator
J Med Virol


. 2024 Oct;96(10):e70007.
doi: 10.1002/jmv.70007. The SARS-unique domain (SUD) of SARS-CoV-2 nsp3 protein inhibits the antiviral immune responses through the NF-κB pathway

Siyi Xie[SUP] 1 [/SUP], Zheng Song[SUP] 2 [/SUP], Ran Chen[SUP] 2 [/SUP], Xu Zhang[SUP] 2 [/SUP], Shuangxin Wu[SUP] 3 [/SUP], Jingliang Chen[SUP] 4 [/SUP], Peiming Huang[SUP] 1 [/SUP], Hanxin Liu[SUP] 1 [/SUP], Kaixin Yu[SUP] 1 [/SUP], Yixin Zhang[SUP] 1 [/SUP], Siyu Tan[SUP] 1 [/SUP], Jun Liu[SUP] 2 [/SUP], Xiancai Ma[SUP] 5 [/SUP], Hui Zhang[SUP] 2 5 [/SUP], Xin He[SUP] 2 [/SUP], Ting Pan[SUP] 1 [/SUP]



Affiliations
Abstract

Nuclear factor κB (NF-κB) plays a crucial role in various cellular processes, including inflammatory and immune responses. Its activation is tightly regulated by the IKK (IκB kinase) complex. Upon severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection, the virus is initially recognized by the innate immune system and typically activates the NF-κB pathway, leading to a severe inflammatory response. However, the influence of viral proteins upon pro-inflammatory pathway is complicated. Here, we demonstrated that the viral protein nsp3 of SARS-CoV-2 exhibits an unusual function, which attenuated the NF-κB-mediated inflammatory response against SARS-CoV-2 infection in a unique manner. nsp3 interacted with the essential NF-κB modulator NEMO/IKKγ and promoted its polyubiquitylation via the E3 ubiquitin ligase CBL (Cbl Proto-Oncogene). Consequently, polyubiquitylated NEMO undergoes proteasome-dependent degradation, which disrupts NF-κB activation. Moreover, we found that the SARS unique domain (SUD) in nsp3 of SARS-CoV-2 is essential for inducing NEMO degradation, whereas this function is absent in SUD of SARS-CoV. The reduced activation of pro-inflammatory response at an early stage could mask the host immune response and faciliate excessive viral replication. Conversely, this finding may partially explain why SARS-CoV-2 causes a less inflammatory reaction than SARS-CoV, resulting in more mild or moderate COVID-19 cases and greater transmissibility. Given that NEMO is important for NF-κB activation, we propose that inhibiting polyubiquitylation and degradation of NEMO upon SARS-CoV-2 infection is a novel strategy to modulate the host inflammatory response.

Keywords: CBL; NEMO; NF‐κB; Nsp3; SARS‐CoV‐2.

 
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