Regulation of myofibroblast differentiation by cardiac glycosides

Am J Physiol Lung Cell Mol Physiol. 2016 May 1;310(9):L815-23. doi: 10.1152/ajplung.00322.2015. Epub 2016 Feb 5.

Abstract

Myofibroblast differentiation is a key process in pathogenesis of fibrotic diseases. Cardiac glycosides (ouabain, digoxin) inhibit Na(+)-K(+)-ATPase, resulting in increased intracellular [Na(+)]-to-[K(+)] ratio in cells. Microarray analysis suggested that increased intracellular [Na(+)]/[K(+)] ratio may promote the expression of cyclooxygenase-2 (COX-2), a critical enzyme in the synthesis of prostaglandins. Given antifibrotic effects of prostaglandins through activation of protein kinase A (PKA), we examined if cardiac glycosides stimulate COX-2 expression in human lung fibroblasts and how they affect myofibroblast differentiation. Ouabain stimulated a profound COX-2 expression and a sustained PKA activation, which was blocked by COX-2 inhibitor or by COX-2 knockdown. Ouabain-induced COX-2 expression and PKA activation were abolished by the inhibitor of the Na(+)/Ca(2+) exchanger, KB-R4943. Ouabain inhibited transforming growth factor-β (TGF-β)-induced Rho activation, stress fiber formation, serum response factor activation, and the expression of smooth muscle α-actin, collagen-1, and fibronectin. These effects were recapitulated by an increase in intracellular [Na(+)]/[K(+)] ratio through the treatment of cells with K(+)-free medium or with digoxin. Although inhibition of COX-2 or of the Na(+)/Ca(2+) exchanger blocked ouabain-induced PKA activation, this failed to reverse the inhibition of TGF-β-induced Rho activation or myofibroblast differentiation by ouabain. Together, these data demonstrate that ouabain, through the increase in intracellular [Na(+)]/[K(+)] ratio, drives the induction of COX-2 expression and PKA activation, which is accompanied by a decreased Rho activation and myofibroblast differentiation in response to TGF-β. However, COX-2 expression and PKA activation are not sufficient for inhibition of the fibrotic effects of TGF-β by ouabain, suggesting that additional mechanisms must exist.

Keywords: cyclooxygenase-2; digoxin; intracellular sodium-to-potassium ion ratio; ouabain.

Publication types

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

MeSH terms

  • Cardiac Glycosides / pharmacology*
  • Cell Differentiation*
  • Cells, Cultured
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • Cyclooxygenase 2 / genetics
  • Cyclooxygenase 2 / metabolism
  • Digoxin / pharmacology*
  • Enzyme Activation
  • Gene Expression
  • Humans
  • Idiopathic Pulmonary Fibrosis / pathology
  • Lung / pathology
  • Myofibroblasts / drug effects
  • Myofibroblasts / physiology*
  • Ouabain / pharmacology*

Substances

  • Cardiac Glycosides
  • Ouabain
  • Digoxin
  • Cyclooxygenase 2
  • PTGS2 protein, human
  • Cyclic AMP-Dependent Protein Kinases