Activation of p38 mitogen-activated protein kinase contributes to the early cardiodepressant action of tumor necrosis factor

J Am Coll Cardiol. 2006 Aug 1;48(3):545-55. doi: 10.1016/j.jacc.2006.02.072. Epub 2006 Jul 12.

Abstract

Objectives: The purpose of this study was to determine whether p38 mitogen-activated protein kinase (p38-MAPK) contributes to tumor necrosis factor-alpha (TNFalpha)-induced contractile depression.

Background: Tumor necrosis factor has both beneficial and detrimental consequences that may result from the activation of different downstream pathways. Tumor necrosis factor activates p38-MAPK, a stress-responsive kinase implicated in contractile depression and cardiac injury.

Methods: In isolated hearts from mice lacking the p38-MAPK activator, MAPK kinase 3 (MKK3), perfused at constant coronary pressure or flow, we measured the left ventricular developed pressure (LVDP) and the relationship between end-diastolic volume and LVDP in the presence and absence of 10 ng/ml TNFalpha.

Results: Within 15 min at constant pressure, TNFalpha significantly reduced LVDP and coronary flow in outbred and mkk3(+/+) mice. This early negative inotropic effect was associated with a marked phosphorylation of both p38-MAPK and its indirect substrate, HSP27. In hearts lacking MKK3, TNFalpha failed to activate p38-MAPK or to cause significant contractile dysfunction. The actions of TNFalpha were similarly attenuated in MAPK-activated protein kinase 2 (MK2)-deficient hearts, which have a marked reduction in myocardial p38-MAPK protein content, and by the p38-MAPK catalytic site inhibitor SB203580 (1 micromol/l). Under conditions of constant coronary flow, the p38-MAPK activation and contractile depression induced by TNFalpha, though attenuated, remained sensitive to the absence of MKK3 or the presence of SB203580. The role of p38-MAPK in TNFalpha-induced contractile depression was confirmed in isolated murine cardiac myocytes exposed to SB203580 or lacking MKK3.

Conclusions: Tumor necrosis factor activates p38-MAPK in the intact heart and in isolated cardiac myocytes through MKK3. This activation likely contributes to the early cardiodepressant action of TNFalpha.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Enzyme Activation / physiology
  • Enzyme Inhibitors / pharmacology
  • Imidazoles / pharmacology
  • In Vitro Techniques
  • Intracellular Signaling Peptides and Proteins
  • MAP Kinase Kinase 3 / deficiency
  • Male
  • Mice
  • Mice, Knockout
  • Myocardial Contraction / drug effects*
  • Myocardial Contraction / physiology*
  • Myocardium / enzymology
  • Myocytes, Cardiac / drug effects
  • Myocytes, Cardiac / enzymology
  • Protein Kinases / deficiency
  • Protein Serine-Threonine Kinases
  • Pyridines / pharmacology
  • Stroke Volume / drug effects
  • Tumor Necrosis Factor-alpha / pharmacology*
  • p38 Mitogen-Activated Protein Kinases / metabolism*

Substances

  • Enzyme Inhibitors
  • Imidazoles
  • Intracellular Signaling Peptides and Proteins
  • Pyridines
  • Tumor Necrosis Factor-alpha
  • Protein Kinases
  • MAP-kinase-activated kinase 2
  • Protein Serine-Threonine Kinases
  • p38 Mitogen-Activated Protein Kinases
  • MAP Kinase Kinase 3
  • SB 203580