A new hypertrophic mechanism of serotonin in cardiac myocytes: receptor-independent ROS generation

FASEB J. 2005 Apr;19(6):641-3. doi: 10.1096/fj.04-2518fje. Epub 2005 Feb 9.

Abstract

Reactive oxygen species (ROS) play a critical role in cardiac hypertrophy. We have recently shown that the serotonin-degrading enzyme monoamine oxidase A (MAO A) is an important source of hydrogen peroxide in rat heart. In the present study, we investigated the potential role of hydrogen peroxide generated by MAO A in cardiomyocyte hypertrophy by serotonin. Serotonin (5 microM, 48 h) induced hypertrophy in cultured adult rat ventricular myocytes, as reflected by increased 3H-leucine incorporation (+43%, P<0.001) and total protein content (+22%, P<0.001). Serotonin also increased intracellular hydrogen peroxide and oxidative stress production, measured respectively by DCF fluorescence intensity and GSH/GSSG ratio, and promoted ERK1/2 phosphorylation (P<0.001). Serotonin effects were only partially inhibited by the 5-HT2B receptor antagonist SB 206553. In contrast, they were extensively (>80%) prevented by the amine uptake inhibitor imipramine, the MAO inhibitor pargyline and the MEK inhibitor PD 98059. Cardiomyocyte hypertrophy and ERK activation were also inhibited by decreasing intracellular ROS by adenoviral overexpression of catalase or cardiomyocytes treatment with the iron chelator deferoxamine. These data suggest that part of cardiac hypertrophic effect of serotonin requires hydrogen peroxide production by MAO A and ERK1/2 activation. This newly recognized, receptor-independent mechanism of serotonin may contribute to myocardial remodeling and failure.

Publication types

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

MeSH terms

  • Adrenergic Uptake Inhibitors / pharmacology
  • Animals
  • Catalase / genetics
  • Cells, Cultured
  • Enzyme Activation
  • Flavonoids / pharmacology
  • Gene Expression
  • Glutathione / analysis
  • Glutathione / metabolism
  • Hydrogen Peroxide / metabolism
  • Hypertrophy
  • Imipramine / pharmacology
  • Male
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinase 3 / metabolism
  • Mitogen-Activated Protein Kinase Kinases / antagonists & inhibitors
  • Monoamine Oxidase / metabolism
  • Monoamine Oxidase Inhibitors / pharmacology
  • Myocytes, Cardiac / drug effects*
  • Myocytes, Cardiac / pathology*
  • Oxidation-Reduction
  • Oxidative Stress / drug effects
  • Pargyline / pharmacology
  • Phosphorylation
  • Rats
  • Rats, Sprague-Dawley
  • Reactive Oxygen Species / metabolism*
  • Serotonin / pharmacology*
  • Transfection

Substances

  • Adrenergic Uptake Inhibitors
  • Flavonoids
  • Monoamine Oxidase Inhibitors
  • Reactive Oxygen Species
  • Serotonin
  • Pargyline
  • Hydrogen Peroxide
  • Catalase
  • Monoamine Oxidase
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • Mitogen-Activated Protein Kinase Kinases
  • Glutathione
  • Imipramine
  • 2-(2-amino-3-methoxyphenyl)-4H-1-benzopyran-4-one