Ectopic adenine nucleotide translocase activity controls extracellular ADP levels and regulates the F1-ATPase-mediated HDL endocytosis pathway on hepatocytes

Biochim Biophys Acta Mol Cell Biol Lipids. 2017 Sep;1862(9):832-841. doi: 10.1016/j.bbalip.2017.05.005. Epub 2017 May 11.

Abstract

Ecto-F1-ATPase is a complex related to mitochondrial ATP synthase which has been identified as a plasma membrane receptor for apolipoprotein A-I (apoA-I), the major protein of high-density lipoprotein (HDL), and has been shown to contribute to HDL endocytosis in several cell types. On hepatocytes, apoA-I binding to ecto-F1-ATPase stimulates extracellular ATP hydrolysis into ADP, which subsequently activates a P2Y13-mediated HDL endocytosis pathway. Interestingly, other mitochondrial proteins have been found to be expressed at the plasma membrane of several cell types. Among these, adenine nucleotide translocase (ANT) is an ADP/ATP carrier but its role in controlling extracellular ADP levels and F1-ATPase-mediated HDL endocytosis has never been investigated. Here we confirmed the presence of ANT at the plasma membrane of human hepatocytes. We then showed that ecto-ANT activity increases or reduces extracellular ADP level, depending on the extracellular ADP/ATP ratio. Interestingly, ecto-ANT co-localized with ecto-F1-ATPase at the hepatocyte plasma membrane and pharmacological inhibition of ecto-ANT activity increased extracellular ADP level when ecto-F1-ATPase was activated by apoA-I. This increase in the bioavailability of extracellular ADP accordingly translated into an increase of HDL endocytosis on human hepatocytes. This study thus uncovered a new location and function of ANT for which activity at the cell surface of hepatocytes modulates the concentration of extracellular ADP and regulates HDL endocytosis.

Keywords: ATP synthase; Adenine nucleotide translocase; Apolipoprotein A-I; High density lipoprotein; Inhibitory Factor 1; Nucleotide.

MeSH terms

  • Adenosine Diphosphate / metabolism*
  • Adenosine Triphosphate / metabolism*
  • Apolipoprotein A-I / metabolism
  • Cell Line
  • Cell Line, Tumor
  • Cell Membrane / metabolism
  • Endocytosis / physiology*
  • Hep G2 Cells
  • Hepatocytes / metabolism*
  • Humans
  • Lipoproteins, HDL / metabolism*
  • Mitochondrial ADP, ATP Translocases / metabolism*
  • Mitochondrial Proteins / metabolism
  • Proton-Translocating ATPases / metabolism*
  • Signal Transduction / physiology

Substances

  • Apolipoprotein A-I
  • Lipoproteins, HDL
  • Mitochondrial Proteins
  • Adenosine Diphosphate
  • Adenosine Triphosphate
  • Mitochondrial ADP, ATP Translocases
  • Proton-Translocating ATPases