The assembly of neutrophil inflammasomes during COVID-19 is mediated by type I interferons

PLoS Pathog. 2024 Aug 22;20(8):e1012368. doi: 10.1371/journal.ppat.1012368. eCollection 2024 Aug.

Abstract

The severity of COVID-19 is linked to excessive inflammation. Neutrophils represent a critical arm of the innate immune response and are major mediators of inflammation, but their role in COVID-19 pathophysiology remains poorly understood. We conducted transcriptomic profiling of neutrophils obtained from patients with mild and severe COVID-19, as well as from SARS-CoV-2 infected mice, in comparison to non-infected healthy controls. In addition, we investigated the inflammasome formation potential in neutrophils from patients and mice upon SARS-CoV-2 infection. Transcriptomic analysis of polymorphonuclear cells (PMNs), consisting mainly of mature neutrophils, revealed a striking type I interferon (IFN-I) gene signature in severe COVID-19 patients, contrasting with mild COVID-19 and healthy controls. Notably, low-density granulocytes (LDGs) from severe COVID-19 patients exhibited an immature neutrophil phenotype and lacked this IFN-I signature. Moreover, PMNs from severe COVID-19 patients showed heightened nigericin-induced caspase1 activation, but reduced responsiveness to exogenous inflammasome priming. Furthermore, IFN-I emerged as a priming stimulus for neutrophil inflammasomes. These findings suggest a potential role for neutrophil inflammasomes in driving inflammation during severe COVID-19. Altogether, these findings open promising avenues for targeted therapeutic interventions to mitigate the pathological processes associated with the disease.

MeSH terms

  • Adult
  • Animals
  • COVID-19* / immunology
  • Female
  • Humans
  • Immunity, Innate
  • Inflammasomes* / immunology
  • Inflammasomes* / metabolism
  • Interferon Type I* / immunology
  • Interferon Type I* / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Middle Aged
  • Neutrophils* / immunology
  • Neutrophils* / metabolism
  • SARS-CoV-2* / immunology

Substances

  • Interferon Type I
  • Inflammasomes

Grants and funding

This work was financed by grants by the Academy of Finland to T.S. (321809), A.K. (336439 and 335527); grants by the Helsinki University Hospital funds to O.V. (TYH 2021343); EU Horizon 2020 programme VEO (874735) to O.V.; Finnish governmental subsidy for Health Science Research (TYH 2021315) to A.K.; Paulon Säätiö to L.E.C.; Suomen Lääketieteen Säätiö to L.E.C.; Jane and Aatos Erkko foundation to O.V. The funders had no role in study design, data collection and analysis, nor decision to publish, or preparation of the manuscript.