The interaction of nitric oxide with distinct hemoglobins differentially amplifies endothelial heme uptake and heme oxygenase-1 expression

J Pharmacol Exp Ther. 2006 Jun;317(3):1125-33. doi: 10.1124/jpet.105.097907. Epub 2006 Feb 22.

Abstract

Heme is a strong inducer and substrate of the stress protein heme oxygenase-1 (HO-1), which produces carbon monoxide, iron, and bilirubin. We have reported recently that nitric oxide (NO) augments the incorporation of free hemin in endothelial cells, resulting in amplified HO-1 expression and production of bilirubin. Here, we extend our studies by showing that both NO+ and NO- donors interacted with reduced (HbA0) or oxidized (metHb) hemoglobin, as well as hemoglobin from sickle cell disease (HbS), to strongly magnify HO-1, with a pattern of induction dependent on the oxidation state of the hemoglobin used. A corresponding enhancement of endothelial heme uptake was observed following exposure of HbA0 or HbS to the NO donors, which also increased the uptake of free hemin. We postulated that this effect may be caused by formation of heme-nitrosyl (H-NO) complexes, and indeed endothelial cells exposed to preformed H-NO showed greater heme incorporation than free hemin. Furthermore, NO donors directly affected the permeability of membranes to free hemin. In conclusion, our data indicate a novel role for NO in the modulation of heme transport and HO-1 induction in endothelial cells, which may be relevant for hematological disorders characterized by disruption of the heme-NO equilibrium.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bilirubin / metabolism
  • Cattle
  • Cell Culture Techniques
  • Cell Line
  • Culture Media
  • Endothelial Cells / drug effects*
  • Endothelial Cells / metabolism
  • Heme / metabolism*
  • Heme Oxygenase-1 / biosynthesis*
  • Hemin / metabolism
  • Hemoglobin A / metabolism
  • Hemoglobin, Sickle / metabolism
  • Hemoglobins / metabolism*
  • Humans
  • Methemoglobin / metabolism
  • Mice
  • Nitric Oxide / metabolism*
  • Nitric Oxide Donors / pharmacology
  • Swine
  • Up-Regulation

Substances

  • Culture Media
  • Hemoglobin, Sickle
  • Hemoglobins
  • Nitric Oxide Donors
  • Nitric Oxide
  • Heme
  • hemoglobin A(0)
  • Hemin
  • Methemoglobin
  • Hemoglobin A
  • Heme Oxygenase-1
  • Bilirubin