p38 MAPK-dependent eNOS upregulation is critical for 17beta-estradiol-mediated cardioprotection following trauma-hemorrhage

Am J Physiol Heart Circ Physiol. 2008 Jun;294(6):H2627-36. doi: 10.1152/ajpheart.91444.2007. Epub 2008 Apr 11.

Abstract

Studies have shown that p38 MAPK and nitric oxide (NO), generated by endothelial NO synthase (eNOS), play key roles under physiological and pathophysiological conditions. Although administration of 17beta-estradiol (E2) protects cardiovascular injury from trauma-hemorrhage, the mechanism by which E2 produces those effects remains unknown. Our objective was to determine whether the E2-mediated activation of myocardial p38 MAPK and subsequent eNOS expression/phosphorylation would protect the heart following trauma-hemorrhage. To study this, male Sprague-Dawley rats underwent soft-tissue trauma (midline laparatomy) and hemorrhagic shock (mean blood pressure 35-40 mmHg for 90 min), followed by fluid resuscitation. Animals were pretreated with specific p38 MAPK inhibitor SB-203580 (SB; 2 mg/kg), and nonselective NO synthase inhibitor NG-nitro-l-arginine methyl ester (l-NAME; 30 mg/kg) 30 min before vehicle (cyclodextrin) or E2 (100 microg/kg) treatment, followed by resuscitation, and were killed 2 h thereafter. Cardiovascular performance and other parameters were measured. E2 administration following trauma-hemorrhage increased cardiac p38 MAPK activity, eNOS expression and phosphorylation at Ser(1177), and nitrate/nitrite levels in plasma and heart tissues; these were associated with normalized cardiac performance, which was reversed by SB administration. In addition, E2 also prevented trauma-hemorrhage-induced increase in cytokines (IL-6 and TNF-alpha), chemokines (macrophage inflammatory protein-2 and cytokine-induced neutrophil chemoattractant-1), and ICAM-1, which was reversed by l-NAME administration. Administration of E2 following trauma-hemorrhage attenuated cardiac tissue injury markers, myeloperoxidase activity, and nitrotyrosine level, which were reversed by treatment with SB and l-NAME. The salutary effects of E2 on cardiac functions and tissue protection following trauma-hemorrhage are mediated, in part, through activation of p38 MAPK and subsequent eNOS expression and phosphorylation.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Abdomen / surgery
  • Animals
  • Calmodulin / metabolism
  • Cardiotonic Agents / pharmacology*
  • Caveolin 1 / metabolism
  • Chemokine CXCL1 / metabolism
  • Chemokine CXCL2 / metabolism
  • Disease Models, Animal
  • Enzyme Activation
  • Enzyme Inhibitors / pharmacology
  • Estradiol / pharmacology*
  • Heart Diseases / enzymology
  • Heart Diseases / etiology
  • Heart Diseases / pathology
  • Heart Diseases / physiopathology
  • Heart Diseases / prevention & control*
  • Imidazoles / pharmacology
  • Intercellular Adhesion Molecule-1 / metabolism
  • Interleukin-6 / metabolism
  • Male
  • Mitogen-Activated Protein Kinase 11 / antagonists & inhibitors
  • Mitogen-Activated Protein Kinase 11 / metabolism*
  • Myocardium / enzymology*
  • Myocardium / pathology
  • NG-Nitroarginine Methyl Ester / pharmacology
  • Nitrates / metabolism
  • Nitric Oxide Synthase Type II / antagonists & inhibitors
  • Nitric Oxide Synthase Type II / metabolism
  • Nitric Oxide Synthase Type III
  • Nitrites / metabolism
  • Peroxidase / metabolism
  • Phosphorylation
  • Pyridines / pharmacology
  • Rats
  • Rats, Sprague-Dawley
  • Shock, Hemorrhagic / complications
  • Shock, Hemorrhagic / drug therapy*
  • Shock, Hemorrhagic / enzymology
  • Shock, Hemorrhagic / pathology
  • Shock, Hemorrhagic / physiopathology
  • Tumor Necrosis Factor-alpha / metabolism
  • Tyrosine / analogs & derivatives
  • Tyrosine / metabolism
  • Up-Regulation
  • Ventricular Function / drug effects

Substances

  • Calmodulin
  • Cardiotonic Agents
  • Cav1 protein, rat
  • Caveolin 1
  • Chemokine CXCL1
  • Chemokine CXCL2
  • Cxcl1 protein, rat
  • Cxcl2 protein, rat
  • Enzyme Inhibitors
  • Imidazoles
  • Interleukin-6
  • Nitrates
  • Nitrites
  • Pyridines
  • Tumor Necrosis Factor-alpha
  • Intercellular Adhesion Molecule-1
  • 3-nitrotyrosine
  • Tyrosine
  • Estradiol
  • Peroxidase
  • Nitric Oxide Synthase Type II
  • Nitric Oxide Synthase Type III
  • Nos3 protein, rat
  • Mitogen-Activated Protein Kinase 11
  • SB 203580
  • NG-Nitroarginine Methyl Ester