Gene transfer of inducible nitric oxide synthase affords cardioprotection by upregulating heme oxygenase-1 via a nuclear factor-{kappa}B-dependent pathway

Circulation. 2009 Sep 29;120(13):1222-30. doi: 10.1161/CIRCULATIONAHA.108.778688. Epub 2009 Sep 14.

Abstract

Background: Although inducible nitric oxide synthase (iNOS) is known to impart powerful protection against myocardial infarction, the mechanism for this salubrious action remains unclear.

Methods and results: Adenovirus-mediated iNOS gene transfer in mice resulted 48 to 72 hours later in increased expression not only of iNOS protein but also of heme oxygenase (HO)-1 mRNA and protein; HO-2 protein expression did not change. iNOS gene transfer markedly reduced infarct size in wild-type mice, but this effect was completely abrogated in HO-1(-/-) mice. At 48 hours after iNOS gene transfer, nuclear factor-kappaB was markedly activated. In transgenic mice with cardiomyocyte-restricted expression of a dominant negative mutant of IkappaBalpha (IkappaBalpha(S32A,S36A)), both basal HO-1 levels and upregulation of HO-1 by iNOS gene transfer were suppressed. Chromatin immunoprecipitation analysis of mouse hearts provided direct evidence that nuclear factor-kappaB subunits p50 and p65 were recruited to the HO-1 gene promoter (-468 to -459 bp) 48 hours after iNOS gene transfer.

Conclusions: This study demonstrates for the first time the existence of a close functional coupling between cardiac iNOS and cardiac HO-1: iNOS upregulates HO-1 by augmenting nuclear factor-kappaB binding to the region of the HO-1 gene promoter from -468 to -459 bp, and HO-1 then mediates the cardioprotective effects of iNOS. These results also reveal an important role of nuclear factor-kappaB in both basal and iNOS-induced expression of cardiac HO-1. Collectively, the present findings significantly expand our understanding of the regulation of cardiac HO-1 and of the mechanism whereby iNOS exerts its cardioprotective actions.

Publication types

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

MeSH terms

  • Adenoviridae / genetics
  • Animals
  • Bilirubin / metabolism
  • Body Temperature
  • Female
  • Gene Transfer Techniques
  • Genetic Therapy / methods*
  • Heart / physiology*
  • Heart Rate
  • Heme Oxygenase-1 / genetics
  • Heme Oxygenase-1 / metabolism*
  • I-kappa B Proteins / genetics
  • Male
  • Mice
  • Mice, Transgenic
  • Myocardial Infarction / metabolism
  • Myocardial Infarction / pathology
  • Myocardial Infarction / therapy*
  • NF-KappaB Inhibitor alpha
  • NF-kappa B / metabolism*
  • Nitric Oxide Synthase Type II / genetics*
  • Nitric Oxide Synthase Type II / metabolism
  • Promoter Regions, Genetic / physiology
  • RNA, Messenger / metabolism
  • Up-Regulation / physiology

Substances

  • I-kappa B Proteins
  • NF-kappa B
  • Nfkbia protein, mouse
  • RNA, Messenger
  • NF-KappaB Inhibitor alpha
  • Nitric Oxide Synthase Type II
  • Nos2 protein, mouse
  • Heme Oxygenase-1
  • Bilirubin

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