Human endothelial dihydrofolate reductase low activity limits vascular tetrahydrobiopterin recycling

Free Radic Biol Med. 2013 Oct:63:143-50. doi: 10.1016/j.freeradbiomed.2013.04.035. Epub 2013 May 23.

Abstract

Tetrahydrobiopterin (BH₄) is required for NO synthesis and inhibition of superoxide release from endothelial NO synthase. Clinical trials using BH₄ to treat endothelial dysfunction have produced mixed results. Poor outcomes may be explained by the rapid systemic and cellular oxidation of BH₄. One of the oxidation products of BH₄, 7,8-dihydrobiopterin (7,8-BH₂), is recycled back to BH₄ by dihydrofolate reductase (DHFR). This enzyme is ubiquitously distributed and shows a wide range of activity depending on species-specific factors and cell type. Information about the kinetics and efficiency of BH4 recycling in human endothelial cells receiving BH₄ treatment is lacking. To characterize this reaction, we applied a novel multielectrode coulometric HPLC method that enabled the direct quantification of 7,8-BH₂ and BH₄, which is not possible with fluorescence-based methodologies. We found that basal untreated BH₄ and 7,8-BH₂ concentrations in human endothelial cells (ECs) are lower than in bovine and murine endothelioma cells. Treatment of human ECs with BH₄ transiently increased intracellular BH₄ while accumulating the more stable 7,8-BH₂. This was different from bovine or murine ECs, which resulted in preferential BH₄ increase. Using BH₄ diastereomers, 6S-BH₄ and 6R-BH₄, the narrow contribution of enzymatic DHFR recycling to total intracellular BH₄ was demonstrated. Reduction of 7,8-BH₂ to BH₄ occurs at very slow rates in cells and needs supraphysiological levels of 7,8-BH₂, indicating this reaction is kinetically limited. Activity assays verified that human DHFR has very low affinity for 7,8-BH₂ (DHF<Km>7,8-BH₂) and folic acid inhibits 7,8-BH₂ recycling. We conclude that low activity of endothelial DHFR is an important factor limiting the benefits of BH4 therapies, which may be further aggravated by folate supplements.

Keywords: Dihydrobiopterin; Dihydrofolate; Endothelial drug metabolism; Free radicals; Methotrexate; Nitric oxide synthase.

Publication types

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

MeSH terms

  • Animals
  • Biopterins / analogs & derivatives*
  • Biopterins / metabolism
  • Cattle
  • Cells, Cultured
  • Endothelial Cells / enzymology
  • Endothelial Cells / metabolism*
  • Endothelium, Vascular / enzymology
  • Endothelium, Vascular / metabolism*
  • Humans
  • Mice
  • Nitric Oxide / metabolism
  • Nitric Oxide Synthase / metabolism
  • Oxidation-Reduction
  • Superoxides / metabolism
  • Tetrahydrofolate Dehydrogenase / genetics
  • Tetrahydrofolate Dehydrogenase / metabolism*
  • Vascular Diseases / enzymology
  • Vascular Diseases / metabolism
  • Vascular Diseases / pathology

Substances

  • Superoxides
  • Biopterins
  • Nitric Oxide
  • 7,8-dihydrobiopterin
  • Nitric Oxide Synthase
  • Tetrahydrofolate Dehydrogenase
  • sapropterin