The TOX-RAGE axis mediates inflammatory activation and lung injury in severe pulmonary infectious diseases

Proc Natl Acad Sci U S A. 2024 Jun 25;121(26):e2319322121. doi: 10.1073/pnas.2319322121. Epub 2024 Jun 20.

Abstract

Thymocyte selection-associated high-mobility group box (TOX) is a transcription factor that is crucial for T cell exhaustion during chronic antigenic stimulation, but its role in inflammation is poorly understood. Here, we report that TOX extracellularly mediates drastic inflammation upon severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection by binding to the cell surface receptor for advanced glycation end-products (RAGE). In various diseases, including COVID-19, TOX release was highly detectable in association with disease severity, contributing to lung fibroproliferative acute respiratory distress syndrome (ARDS). Recombinant TOX-induced blood vessel rupture, similar to a clinical signature in patients experiencing a cytokine storm, further exacerbating respiratory function impairment. In contrast, disruption of TOX function by a neutralizing antibody and genetic removal of RAGE diminished TOX-mediated deleterious effects. Altogether, our results suggest an insight into TOX function as an inflammatory mediator and propose the TOX-RAGE axis as a potential target for treating severe patients with pulmonary infection and mitigating lung fibroproliferative ARDS.

Keywords: RAGE; TOX; fibroproliferative ARDS; septic shock; severe COVID-19.

MeSH terms

  • Animals
  • COVID-19* / complications
  • COVID-19* / immunology
  • COVID-19* / metabolism
  • COVID-19* / pathology
  • COVID-19* / virology
  • Female
  • High Mobility Group Proteins / genetics
  • High Mobility Group Proteins / metabolism
  • Humans
  • Inflammation / metabolism
  • Inflammation / pathology
  • Lung / immunology
  • Lung / metabolism
  • Lung / pathology
  • Lung Injury / immunology
  • Lung Injury / metabolism
  • Lung Injury / pathology
  • Male
  • Mice
  • Receptor for Advanced Glycation End Products* / metabolism
  • Respiratory Distress Syndrome / immunology
  • Respiratory Distress Syndrome / metabolism
  • Respiratory Distress Syndrome / pathology
  • Respiratory Distress Syndrome / virology
  • SARS-CoV-2*

Substances

  • Receptor for Advanced Glycation End Products
  • TOX protein, human
  • High Mobility Group Proteins