The Long-Lasting Protective Effect of HGF in Cardiomyoblasts Exposed to Doxorubicin Requires a Positive Feed-Forward Loop Mediated by Erk1,2-Timp1-Stat3

Int J Mol Sci. 2020 Jul 24;21(15):5258. doi: 10.3390/ijms21155258.

Abstract

Previous studies showed that the hepatocyte growth factor (HGF)-Met receptor axis plays long-lasting cardioprotection against doxorubicin anti-cancer therapy. Here, we explored the mechanism(s) underlying the HGF protective effect. DNA damage was monitored by histone H2AX phosphorylation and apoptosis by proteolytic cleavage of caspase 3. In doxorubicin-treated H9c2 cardiomyoblasts, the long-lasting cardioprotection is mediated by activation of the Ras/Raf/Mek/Erk (extracellular signal-regulated kinase 1,2) signaling pathway and requires Stat3 (signal transducer and activator of transcription 3) activation. The HGF protection was abrogated by the Erk1,2 inhibitor, PD98059. This translated into reduced Y705 phosphorylation and impaired nuclear translocation of Stat3, showing crosstalk between Erk1,2 and Stat3 signaling. An array of 29 cytokines, known to activate Stat3, was interrogated to identify the molecule(s) linking the two pathways. The analysis showed a selective increase in expression of the tissue inhibitor of metalloproteinases-1 (Timp1). Consistently, inhibition in cardiomyoblasts of Timp1 translation by siRNAs blunted both Stat3 activation and the cardioprotective effect of HGF. Thus, Timp1 is responsible for the generation of a feed-forward loop of Stat3 activation and helps cardiomyocytes to survive during the genotoxic stress induced by anthracyclines.

Keywords: DNA damage; Erk1,2; HGF; Met receptor; Stat3; Timp1; anthracycline; apoptosis; cardiac injury.

MeSH terms

  • Animals
  • Cell Line
  • Doxorubicin / adverse effects*
  • Doxorubicin / pharmacology
  • Flavonoids / pharmacology
  • Hepatocyte Growth Factor / pharmacology*
  • MAP Kinase Signaling System / drug effects*
  • Mitogen-Activated Protein Kinase 3 / antagonists & inhibitors
  • Mitogen-Activated Protein Kinase 3 / metabolism*
  • Myoblasts, Cardiac / metabolism*
  • Myoblasts, Cardiac / pathology
  • Rats
  • STAT3 Transcription Factor / metabolism*
  • Time Factors
  • Tissue Inhibitor of Metalloproteinase-1 / metabolism*

Substances

  • Flavonoids
  • Hgf protein, rat
  • STAT3 Transcription Factor
  • Stat3 protein, rat
  • TIMP1 protein, rat
  • Tissue Inhibitor of Metalloproteinase-1
  • Hepatocyte Growth Factor
  • Doxorubicin
  • Mitogen-Activated Protein Kinase 3
  • 2-(2-amino-3-methoxyphenyl)-4H-1-benzopyran-4-one