eNOS deficiency acts through endothelin to aggravate sFlt-1-induced pre-eclampsia-like phenotype

J Am Soc Nephrol. 2012 Apr;23(4):652-60. doi: 10.1681/ASN.2011040369. Epub 2012 Jan 26.

Abstract

Excess soluble fms-like tyrosine kinase 1 (sFlt-1) of vascular endothelial growth factor receptor 1 secreted from the placenta causes pre-eclampsia-like features by antagonizing vascular endothelial growth factor signaling, which can lead to reduced endothelial nitric oxide synthase (eNOS) activity; the effect of this concomitant decrease in eNOS activity is unknown. We tested whether the decrease in nitric oxide occurring in female mice lacking eNOS aggravates the pre-eclampsia-like phenotype induced by increased sFlt-1. Untreated eNOS-deficient female mice had higher BP than wild-type mice. Adenovirus-mediated overexpression of sFlt-1 increased systolic BP by approximately 27 mmHg and led to severe loss of fenestration of glomerular capillary endothelial cells in both eNOS-deficient and wild-type mice. However, only the eNOS-deficient sFlt-1 mice exhibited severe foot process effacement. Compared with wild-type sFlt-1 mice, eNOS-deficient sFlt-1 mice also showed markedly higher urinary albumin excretion (467±74 versus 174±23 μg/d), lower creatinine clearance (126±29 versus 452±63 μl/min), and more severe endotheliosis. Expression of preproendothelin-1 (ET-1) and its ET(A) receptor in the kidney was higher in eNOS-deficient sFlt-1 mice than in wild-type sFlt-1 mice. Furthermore, the selective ET(A) receptor antagonist ambrisentan attenuated the increases in BP and urinary albumin excretion and ameliorated endotheliosis in both wild-type and eNOS-deficient sFlt-1 mice. Ambrisentan improved creatinine clearance and podocyte effacement in eNOS-deficient sFlt-1 mice. In conclusion, reduced maternal eNOS/nitric oxide exacerbates the sFlt1-related pre-eclampsia-like phenotype through activation of the endothelin system.

Publication types

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

MeSH terms

  • Albuminuria / physiopathology
  • Animals
  • Disease Models, Animal
  • Endothelin-1 / genetics
  • Endothelin-1 / metabolism*
  • Female
  • Glomerular Filtration Rate
  • Mice
  • Mice, Inbred C57BL
  • Nitric Oxide Synthase Type III / deficiency*
  • Phenotype
  • Phenylpropionates / pharmacology
  • Placenta / metabolism
  • Pre-Eclampsia / genetics
  • Pre-Eclampsia / metabolism*
  • Pregnancy
  • Pregnancy, Animal
  • Pyridazines / pharmacology
  • Random Allocation
  • Receptors, Endothelin / metabolism
  • Sensitivity and Specificity
  • Vascular Endothelial Growth Factor Receptor-1 / genetics
  • Vascular Endothelial Growth Factor Receptor-1 / metabolism*

Substances

  • Endothelin-1
  • Phenylpropionates
  • Pyridazines
  • Receptors, Endothelin
  • Nitric Oxide Synthase Type III
  • Flt1 protein, mouse
  • Vascular Endothelial Growth Factor Receptor-1
  • ambrisentan