Activation of extracellular signal-regulated kinase 5 reduces cardiac apoptosis and dysfunction via inhibition of a phosphodiesterase 3A/inducible cAMP early repressor feedback loop

Circ Res. 2007 Mar 2;100(4):510-9. doi: 10.1161/01.RES.0000259045.49371.9c. Epub 2007 Feb 1.

Abstract

Substantial evidence suggests that the progressive loss of cardiomyocytes caused by apoptosis significantly contributes to the development of heart failure. beta-Adrenergic receptor activation and subsequent persistent phosphodiesterase 3A (PDE3A) downregulation and concomitant inducible cAMP early repressor (ICER) upregulation (PDE3A/ICER feedback loop) has been proposed to play a key role in the pathogenesis of cardiomyocyte apoptosis. In contrast, insulin-like growth factor-1 can activate cell survival pathways, providing protection against cell death and restoring muscle function. In this study, we found that insulin-like growth factor-1 activates extracellular signal-regulated kinase 5 (ERK5) and inhibits PDE3A/ICER feedback loop. Insulin-like growth factor-1 normalized isoproterenol-mediated PDE3A downregulation and ICER upregulation via ERK5/MEF2 activation, and also inhibited isoproterenol-induced myocyte apoptosis. To determine the physiological relevance of ERK5 activation in regulating PDE3A/ICER feedback loop, we investigated the PDE3A/ICER expression and cardiomyocyte apoptosis in transgenic mice with cardiac specific expression of a constitutively active form of mitogen-activated protein (MAP)/extracellular signal-regulated protein kinase (ERK) kinase 5alpha (MEK5alpha) (CA-MEK5alpha-Tg). In wild-type mice, pressure overload- or doxorubicin-induced significant reduction of PDE3A expression and subsequent ICER induction. Cardiac specific expression of CA-MEK5alpha rescued pressure overload- or doxorubicin-mediated PDE3A downregulation and ICER upregulation and inhibited myocyte apoptosis as well as subsequent cardiac dysfunction in vivo. These data suggest that preventing the feedback loop of PDE3A/ICER by ERK5 activation could inhibit progression of myocyte apoptosis as well as cardiac dysfunction. These data suggest a new therapeutic paradigm for end stage of heart failure by inhibiting the PDE3A/ICER feedback loop via activating ERK5.

Publication types

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

MeSH terms

  • 3',5'-Cyclic-AMP Phosphodiesterases / antagonists & inhibitors*
  • 3',5'-Cyclic-AMP Phosphodiesterases / genetics
  • 3',5'-Cyclic-AMP Phosphodiesterases / metabolism
  • Animals
  • Apoptosis / genetics
  • Apoptosis / physiology*
  • Blood Pressure / genetics
  • Cyclic AMP Response Element Modulator / antagonists & inhibitors*
  • Cyclic AMP Response Element Modulator / genetics
  • Cyclic AMP Response Element Modulator / metabolism
  • Cyclic Nucleotide Phosphodiesterases, Type 3
  • Doxorubicin / administration & dosage
  • Doxorubicin / antagonists & inhibitors
  • Enzyme Activation / genetics
  • Feedback, Physiological / physiology*
  • Heart Failure / enzymology
  • Heart Failure / genetics
  • Heart Failure / pathology
  • Mice
  • Mice, Transgenic
  • Mitogen-Activated Protein Kinase 7 / antagonists & inhibitors*
  • Mitogen-Activated Protein Kinase 7 / metabolism
  • Mitogen-Activated Protein Kinase 7 / physiology
  • Myocytes, Cardiac / enzymology*
  • Myocytes, Cardiac / pathology
  • Rats

Substances

  • Cyclic AMP Response Element Modulator
  • Doxorubicin
  • Mitogen-Activated Protein Kinase 7
  • 3',5'-Cyclic-AMP Phosphodiesterases
  • Cyclic Nucleotide Phosphodiesterases, Type 3
  • Pde3a protein, mouse
  • Pde3a protein, rat