Direct inhibition of type 5 adenylyl cyclase prevents myocardial apoptosis without functional deterioration

J Biol Chem. 2004 Sep 24;279(39):40938-45. doi: 10.1074/jbc.M314238200. Epub 2004 Jul 15.

Abstract

Adenylyl cyclase, a major target enzyme of beta-adrenergic receptor signals, is potently and directly inhibited by P-site inhibitors, classic inhibitors of this enzyme, when the enzyme catalytic activity is high. Unlike beta-adrenergic receptor antagonists, this is a non- or uncompetitive inhibition with respect to ATP. We have examined whether we can utilize this enzymatic property to regulate the effects of beta-adrenergic receptor stimulation differentially. After screening multiple new and classic compounds, we found that some compounds, including 1R,4R-3-(6-aminopurin-9-yl)-cyclopentanecarboxylic acid hydroxyamide, potently inhibited type 5 adenylyl cyclase, the major cardiac isoform, but not other isoforms. In normal mouse cardiac myocytes, contraction induced by low beta-adrenergic receptor stimulation was poorly inhibited with this compound, but the induction of cardiac myocyte apoptosis by high beta-adrenergic receptor stimulation was effectively prevented by type 5 adenylyl cyclase inhibitors. In contrast, when cardiac myocytes from type 5 adenylyl cyclase knock-out mice were examined, beta-adrenergic stimulation poorly induced apoptosis. Our data suggest that the inhibition of beta-adrenergic signaling at the level of the type 5 adenylyl cyclase isoform by P-site inhibitors may serve as an effective method to prevent cardiac myocyte apoptosis induced by excessive beta-adrenergic stimulation without deleterious effect on cardiac myocyte contraction.

MeSH terms

  • Adenosine Triphosphate / chemistry
  • Adenylyl Cyclase Inhibitors*
  • Adenylyl Cyclases / metabolism
  • Animals
  • Apoptosis*
  • Binding Sites
  • Blotting, Western
  • Calcium-Binding Proteins / metabolism
  • Caspase 3
  • Caspases / metabolism
  • Cell Line
  • Cells, Cultured
  • Cyclic AMP / metabolism
  • Dose-Response Relationship, Drug
  • Enzyme Inhibitors / pharmacology
  • Enzyme-Linked Immunosorbent Assay
  • In Situ Nick-End Labeling
  • Insecta
  • Isoenzymes / antagonists & inhibitors*
  • Kinetics
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Models, Chemical
  • Myocardium / pathology*
  • Myocytes, Cardiac / metabolism
  • Protein Isoforms
  • Protein Structure, Tertiary

Substances

  • Adenylyl Cyclase Inhibitors
  • Calcium-Binding Proteins
  • Enzyme Inhibitors
  • Isoenzymes
  • Protein Isoforms
  • phospholamban
  • Adenosine Triphosphate
  • Cyclic AMP
  • Casp3 protein, mouse
  • Caspase 3
  • Caspases
  • Adenylyl Cyclases
  • adenylyl cyclase type V