Nitric oxide induces hypoxia-inducible factor 1 activation that is dependent on MAPK and phosphatidylinositol 3-kinase signaling

J Biol Chem. 2004 Jan 23;279(4):2550-8. doi: 10.1074/jbc.M308197200. Epub 2003 Nov 4.

Abstract

Hypoxia-inducible factor-1 (HIF-1) is a master regulator of cellular adaptive responses to hypoxia. Levels of the HIF-1alpha subunit increase under hypoxic conditions. Exposure of cells to certain nitric oxide (NO) donors also induces HIF-1alpha expression under nonhypoxic conditions. We demonstrate that exposure of cells to the NO donor NOC18 or S-nitrosoglutathione induces HIF-1alpha expression and transcriptional activity. In contrast to hypoxia, NOC18 did not inhibit HIF-1alpha hydroxylation, ubiquitination, and degradation, indicating an effect on HIF-1alpha protein synthesis that was confirmed by pulse labeling studies. NOC18 stimulation of HIF-1alpha protein and HIF-1-dependent gene expression was blocked by treating cells with an inhibitor of the phosphatidylinositol 3-kinase or MAPK-signaling pathway. These inhibitors also blocked NOC18-induced phosphorylation of the translational regulatory proteins 4E-BP1, p70 S6 kinase, and eIF-4E, thus providing a mechanism for the modulation of HIF-1alpha protein synthesis. In addition, expression of a dominant-negative form of Ras significantly suppressed HIF-1 activation by NOC18. We conclude that the NO donor NOC18 induces HIF-1alpha synthesis under conditions of NO formation during normoxia and that hydroxylation of HIF-1alpha is not regulated by NOC18.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Line
  • DNA-Binding Proteins / biosynthesis*
  • Humans
  • Hypoxia-Inducible Factor 1
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • MAP Kinase Signaling System / drug effects
  • Nitric Oxide / metabolism*
  • Nitric Oxide Donors / pharmacology
  • Nitroso Compounds / pharmacology
  • Nuclear Proteins / biosynthesis*
  • Phosphatidylinositol 3-Kinases / metabolism*
  • S-Nitrosoglutathione / pharmacology
  • Transcription Factors*

Substances

  • DNA-Binding Proteins
  • HIF1A protein, human
  • Hypoxia-Inducible Factor 1
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • NOC 18
  • Nitric Oxide Donors
  • Nitroso Compounds
  • Nuclear Proteins
  • Transcription Factors
  • Nitric Oxide
  • S-Nitrosoglutathione
  • Phosphatidylinositol 3-Kinases