Inhibition of Syk promotes chemical reprogramming of fibroblasts via metabolic rewiring and H2 S production

EMBO J. 2021 Jun 1;40(11):e106771. doi: 10.15252/embj.2020106771. Epub 2021 Apr 28.

Abstract

Chemical compounds have recently been introduced as alternative and non-integrating inducers of pluripotent stem cell fate. However, chemical reprogramming is hampered by low efficiency and the molecular mechanisms remain poorly characterized. Here, we show that inhibition of spleen tyrosine kinase (Syk) by R406 significantly promotes mouse chemical reprogramming. Mechanistically, R406 alleviates Syk / calcineurin (Cn) / nuclear factor of activated T cells (NFAT) signaling-mediated suppression of glycine, serine, and threonine metabolic genes and dependent metabolites. Syk inhibition upregulates glycine level and downstream transsulfuration cysteine biosynthesis, promoting cysteine metabolism and cellular hydrogen sulfide (H2 S) production. This metabolic rewiring decreased oxidative phosphorylation and ROS levels, enhancing chemical reprogramming. In sum, our study identifies Syk-Cn-NFAT signaling axis as a new barrier of chemical reprogramming and suggests metabolic rewiring and redox homeostasis as important opportunities for controlling cell fates.

Keywords: R406; Syk; chemical reprogramming; hydrogen sulfide; metabolism.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Calcineurin / metabolism
  • Cells, Cultured
  • Cysteine / metabolism
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism*
  • Glycine / metabolism
  • Hydrogen Sulfide / metabolism*
  • Mice
  • NFATC Transcription Factors / metabolism
  • Oxazines / pharmacology
  • Protein Kinase Inhibitors / pharmacology
  • Pyridines / pharmacology
  • Reactive Oxygen Species / metabolism
  • Signal Transduction
  • Syk Kinase / antagonists & inhibitors*

Substances

  • N4-(2,2-dimethyl-3-oxo-4H-pyrid(1,4)oxazin-6-yl)-5-fluoro-N2-(3,4,5-trimethoxyphenyl)-2,4-pyrimidinediamine
  • NFATC Transcription Factors
  • Oxazines
  • Protein Kinase Inhibitors
  • Pyridines
  • Reactive Oxygen Species
  • Syk Kinase
  • Syk protein, mouse
  • Calcineurin
  • Cysteine
  • Glycine
  • Hydrogen Sulfide