Tofacitinib therapy intercepts macrophage metabolic reprogramming instigated by SARS-CoV-2 Spike protein

Eur J Immunol. 2021 Sep;51(9):2330-2340. doi: 10.1002/eji.202049159. Epub 2021 Jun 24.

Abstract

The molecular mechanism of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) Spike protein was characterized to identify novel therapies. The impact of tofacitinib, IL-6R Ab, or TNFi therapy was determined on Spike protein or LPS/IFN-γ-induced signaling, inflammation, and metabolic reprogramming in MΦs and/or rheumatoid arthritis (RA) fibroblast-like synoviocyte (FLS). ACE2 frequency was markedly expanded in MΦs compared to T cells and RA FLS. Tofacitinib suppresses Spike protein potentiated STAT1 signaling, whereas this function was unchanged by TNFi. Tofacitinib impairs IL-6/IFN/LPS-induced STAT1 and STAT3 phosphorylation in RA MΦs and FLS. Interestingly, tofacitinib had a broader inhibitory effect on the monokines, glycolytic regulators, or oxidative metabolites compared to IL-6R Ab and TNFi in Spike-protein-activated MΦs. In contrast, all three therapies disrupted IFN-α and IFN-β secretion in response to Spike protein; nonetheless, the IFN-γ was only curtailed by tofacitinib or IL-6R Ab. While tofacitinib counteracted MΦ metabolic rewiring instigated by Spike protein, it was inconsequential on the glycolysis expansion mediated via HK2 and/or LDHA in the activated RA MΦ and FLS. Nevertheless, the potentiated inflammatory response and the diminished oxidative phosphorylation modulated by Spike protein and/or LPS/IFN-γ stimulation in MΦs or RA FLS were reversed by tofacitinib. In conclusion, tofacitinib suppresses MΦ inflammation and immunometabolism triggered by Spike protein and may provide a promising strategy for COVID-19 patients.

Keywords: Macrophages; Osteoclasts; RA FLS; Spike protein; Tofacitinib.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Arthritis, Rheumatoid / metabolism
  • COVID-19 / metabolism
  • COVID-19 Drug Treatment*
  • Cells, Cultured
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism
  • Humans
  • Interleukin-6 / metabolism
  • Macrophages / drug effects*
  • Macrophages / metabolism
  • Piperidines / pharmacology*
  • Pyrimidines / pharmacology*
  • Receptors, Interleukin-6 / metabolism
  • SARS-CoV-2 / drug effects*
  • STAT1 Transcription Factor / metabolism
  • STAT3 Transcription Factor / metabolism
  • Signal Transduction / drug effects
  • Spike Glycoprotein, Coronavirus / metabolism*
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Interleukin-6
  • Piperidines
  • Pyrimidines
  • Receptors, Interleukin-6
  • STAT1 Transcription Factor
  • STAT3 Transcription Factor
  • Spike Glycoprotein, Coronavirus
  • Tumor Necrosis Factor-alpha
  • spike protein, SARS-CoV-2
  • tofacitinib