Mst1-mediated phosphorylation of FoxO1 and C/EBP-β stimulates cell-protective mechanisms in cardiomyocytes

Nat Commun. 2024 Jul 25;15(1):6279. doi: 10.1038/s41467-024-50393-y.

Abstract

The molecular mechanisms by which FoxO transcription factors mediate diametrically opposite cellular responses, namely death and survival, remain unknown. Here we show that Mst1 phosphorylates FoxO1 Ser209/Ser215/Ser218/Thr228/Ser232/Ser243, thereby inhibiting FoxO1-mediated transcription of proapoptotic genes. On the other hand, Mst1 increases FoxO1-C/EBP-β interaction and activates C/EBP-β by phosphorylating it at Thr299, thereby promoting transcription of prosurvival genes. Myocardial ischemia/reperfusion injury is larger in cardiac-specific FoxO1 knockout mice than in control mice. However, the concurrent presence of a C/EBP-β T299E phospho-mimetic mutation reduces infarct size in cardiac-specific FoxO1 knockout mice. The C/EBP-β phospho-mimetic mutant exhibits greater binding to the promoter of prosurvival genes than wild type C/EBP-β. In conclusion, phosphorylation of FoxO1 by Mst1 inhibits binding of FoxO1 to pro-apoptotic gene promoters but enhances its binding to C/EBP-β, phosphorylation of C/EBP-β, and transcription of prosurvival genes, which stimulate protective mechanisms in the heart.

MeSH terms

  • Animals
  • Apoptosis
  • CCAAT-Enhancer-Binding Protein-beta* / genetics
  • CCAAT-Enhancer-Binding Protein-beta* / metabolism
  • Forkhead Box Protein O1* / genetics
  • Forkhead Box Protein O1* / metabolism
  • Hepatocyte Growth Factor / metabolism
  • Humans
  • Male
  • Mice
  • Mice, Knockout
  • Myocardial Reperfusion Injury* / genetics
  • Myocardial Reperfusion Injury* / metabolism
  • Myocardial Reperfusion Injury* / pathology
  • Myocardial Reperfusion Injury* / prevention & control
  • Myocytes, Cardiac* / metabolism
  • Phosphorylation
  • Promoter Regions, Genetic
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism
  • Proto-Oncogene Proteins
  • Rats

Substances

  • CCAAT-Enhancer-Binding Protein-beta
  • Forkhead Box Protein O1
  • Foxo1 protein, mouse
  • Hepatocyte Growth Factor
  • macrophage stimulating protein
  • Protein Serine-Threonine Kinases
  • Proto-Oncogene Proteins
  • Stk4 protein, mouse