TNF-α exacerbates SARS-CoV-2 infection by stimulating CXCL1 production from macrophages

PLoS Pathog. 2024 Dec 9;20(12):e1012776. doi: 10.1371/journal.ppat.1012776. eCollection 2024 Dec.

Abstract

Since most genetically modified mice are C57BL/6 background, a mouse-adapted SARS-CoV-2 that causes lethal infection in young C57BL/6 mice is useful for studying innate immune protection against SARS-CoV-2 infection. Here, we established two mouse-adapted SARS-CoV-2, ancestral and Delta variants, by serial passaging 80 times in C57BL/6 mice. Although young C57BL/6 mice were resistant to infection with the mouse-adapted ancestral SARS-CoV-2, the mouse-adapted SARS-CoV-2 Delta variant caused lethal infection in young C57BL/6 mice. In contrast, MyD88 and IFNAR1 KO mice exhibited resistance to lethal infection with the mouse-adapted SARS-CoV-2 Delta variant. Treatment with recombinant IFN-α/β at the time of infection protected mice from lethal infection with the mouse-adapted SARS-CoV-2 Delta variant, but intranasal administration of recombinant IFN-α/β at 2 days post infection exacerbated the disease severity following the mouse-adapted ancestral SARS-CoV-2 infection. Moreover, we showed that TNF-α amplified by type I IFN signals exacerbated the SARS-CoV-2 infection by stimulating CXCL1 production from macrophages and neutrophil recruitment into the lung tissue. Finally, we showed that intravenous administration to mice or hamsters with TNF protease inhibitor 2 alleviated the severity of SARS-CoV-2 and influenza virus infection. Our results uncover an unexpected mechanism by which type I interferon-mediated TNF-α signaling exacerbates the disease severity and will aid in the development of novel therapeutic strategies to treat respiratory virus infection and associated diseases such as influenza and COVID-19.

MeSH terms

  • Animals
  • COVID-19* / immunology
  • COVID-19* / virology
  • Chemokine CXCL1* / metabolism
  • Female
  • Humans
  • Macrophages* / immunology
  • Macrophages* / metabolism
  • Macrophages* / virology
  • Mice
  • Mice, Inbred C57BL*
  • Mice, Knockout*
  • Myeloid Differentiation Factor 88 / genetics
  • Myeloid Differentiation Factor 88 / metabolism
  • Receptor, Interferon alpha-beta / genetics
  • Receptor, Interferon alpha-beta / metabolism
  • SARS-CoV-2* / immunology
  • Tumor Necrosis Factor-alpha* / immunology
  • Tumor Necrosis Factor-alpha* / metabolism

Substances

  • Tumor Necrosis Factor-alpha
  • Chemokine CXCL1
  • Cxcl1 protein, mouse
  • Receptor, Interferon alpha-beta
  • Myeloid Differentiation Factor 88

Supplementary concepts

  • SARS-CoV-2 variants

Grants and funding

This work was supported in part by research grants from the Japan Agency for Medical Research and Development (AMED) (JP233fa627001 to T.I. and K.M, JP22gm1010009 to S.F.), JSPS KAKENHI (22H03541 to S.F.), JST ERATO (JPMJER1902 to S.F.), the Food Science Institute Foundation (to S.F.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.