Severe COVID-19 is often characterized by hyper-inflammation due to excessive immune cell infiltration to the site of infection and pro-inflammatory cytokine production. However, the immunological mechanisms underlying the excessive inflammation in the lung remain elusive. We recently discovered that oxidised cholesterols, so called oxysterols, are produced in the lung upon SARS-CoV-2 infection in mice. These oxysterols chemotactically attract infiltrating macrophages to the site of infection via the oxysterol-sensing receptor GPR183. We therefore hypothesised that GPR183 is a novel host target for therapeutic intervention to reduce macrophage-mediated hyperinflammation and disease severity in viral respiratory infections.
Here we demonstrate that either genetic deletion or pharmacological antagonism of GPR183 in mice reduced macrophage infiltration into the lungs after SARS-CoV-2 infection without impairing type I IFN responses. Further, we found that animals treated with the GPR183 antagonist had reduced expression of pro-inflammatory cytokines in the lung. Most strikingly, animals treated with the GPR183 antagonist had lower viral loads, lost significantly less weight, and were clinically less ill compared to vehicle-treated mice. Single-cell RNA Seq analysis of bronchoalveolar lavage samples from healthy controls and COVID-19 patients with moderate and severe disease revealed that macrophages are the primary producers of the oxysterol producing enzymes and that expression of these enzymes positively correlates with COVID-19 severity.
Together, we identified a novel chemo-attractant role for oxysterols in the lung and provide the first preclinical evidence for the benefits of inhibiting GPR183 activity to reduce severity of viral respiratory infections.