Dynamic modulation of interendothelial gap junctional communication by 11,12-epoxyeicosatrienoic acid

Circ Res. 2002 Apr 19;90(7):800-6. doi: 10.1161/01.res.0000015328.20581.d6.

Abstract

Functional gap junctional communication between vascular cells has been implicated in ascending dilatation and the cytochrome P-450 (CYP) inhibitor-sensitive and NO- and prostacyclin-independent dilatation of many vascular beds. Here, we assessed the mechanisms by which the epoxyeicosatrienoic acids (EETs) generated by a CYP 2C enzyme control interendothelial gap junctional communication. In CYP 2C-expressing porcine coronary endothelial cells, bradykinin, which enhances EET formation, elicited a biphasic effect on the electrical coupling and transfer of Lucifer yellow between endothelial cells, consisting of a transient increase in coupling followed by a sustained uncoupling. The initial phase was sensitive to the CYP 2C9 inhibitor sulfaphenazole and the protein kinase A (PKA) inhibitors Rp-cAMPS and KT5720 and could be mimicked by forskolin and caged cAMP as well as by the PKA activators 5,6-dichloro-1-beta-D-ribofuranosylbenzimidazole 3',5'-cyclic monophosphorothioate sodium salt and Sp-cAMPS. Gap junction uncoupling in bradykinin-stimulated porcine coronary endothelial cells was prevented by inhibiting the activation of extracellular signal-regulated kinase (ERK)1/2. In human endothelial cells, which express little CYP 2C, bradykinin elicited only an ERK1/2-mediated inhibition of intercellular communication. The CYP 2C9 product, 11,12-EET, also exerted a dual effect on the electrical and dye coupling of human endothelial cells, which was sensitive to PKA inhibition. These results demonstrate that an agonist-activated CYP-dependent pathway as well as 11,12-EET can positively regulate interendothelial gap junctional communication, most probably via the activation of PKA, an effect that is curtailed by the subsequent activation of ERK1/2.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 8,11,14-Eicosatrienoic Acid / analogs & derivatives*
  • 8,11,14-Eicosatrienoic Acid / pharmacology*
  • Animals
  • Aryl Hydrocarbon Hydroxylases*
  • Biological Transport / drug effects
  • Bradykinin / pharmacology
  • Cell Communication / drug effects*
  • Cell Communication / physiology
  • Cells, Cultured
  • Colforsin / pharmacology
  • Connexin 43 / metabolism
  • Cyclic AMP / analogs & derivatives*
  • Cyclic AMP / pharmacology
  • Cyclic AMP-Dependent Protein Kinases / drug effects
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • Cytochrome P-450 Enzyme Inhibitors
  • Cytochrome P-450 Enzyme System / genetics
  • Cytochrome P-450 Enzyme System / metabolism
  • Endothelium, Vascular / cytology
  • Endothelium, Vascular / drug effects*
  • Endothelium, Vascular / metabolism
  • Enzyme Activators / pharmacology
  • Enzyme Inhibitors / pharmacology
  • Fluorescent Dyes / pharmacokinetics
  • Gap Junctions / drug effects*
  • Gap Junctions / metabolism
  • Humans
  • Isoquinolines / pharmacokinetics
  • Mitogen-Activated Protein Kinase 1 / antagonists & inhibitors
  • Mitogen-Activated Protein Kinase 3
  • Mitogen-Activated Protein Kinases / antagonists & inhibitors
  • Patch-Clamp Techniques
  • RNA, Messenger / metabolism
  • Signal Transduction / drug effects
  • Signal Transduction / physiology
  • Steroid 16-alpha-Hydroxylase*
  • Steroid Hydroxylases / antagonists & inhibitors
  • Steroid Hydroxylases / genetics
  • Steroid Hydroxylases / metabolism
  • Swine
  • Vasodilator Agents / pharmacology

Substances

  • (2-nitrophenyl)ethyl-cyclic adenosine monophosphate
  • Connexin 43
  • Cytochrome P-450 Enzyme Inhibitors
  • Enzyme Activators
  • Enzyme Inhibitors
  • Fluorescent Dyes
  • Isoquinolines
  • RNA, Messenger
  • Vasodilator Agents
  • Colforsin
  • 11,12-epoxy-5,8,14-eicosatrienoic acid
  • Cytochrome P-450 Enzyme System
  • lucifer yellow
  • Cyclic AMP
  • Steroid Hydroxylases
  • Aryl Hydrocarbon Hydroxylases
  • Steroid 16-alpha-Hydroxylase
  • Cyclic AMP-Dependent Protein Kinases
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • Mitogen-Activated Protein Kinases
  • 8,11,14-Eicosatrienoic Acid
  • Bradykinin