Depletion of pre-beta-high density lipoprotein by human chymase impairs ATP-binding cassette transporter A1- but not scavenger receptor class B type I-mediated lipid efflux to high density lipoprotein

J Biol Chem. 2004 Mar 12;279(11):9930-6. doi: 10.1074/jbc.M312476200. Epub 2003 Dec 29.

Abstract

The ATP-binding cassette transporter A1 (ABCA1) mediates the efflux of cellular unesterified cholesterol and phospholipid to lipid-poor apolipoprotein A-I. Chymase, a protease secreted by mast cells, selectively cleaves pre-beta-migrating particles from high density lipoprotein (HDL)(3) and reduces the efflux of cholesterol from macrophages. To evaluate whether this effect is the result of reduction of ABCA1-dependent or -independent pathways of cholesterol efflux, in this study we examined the efflux of cholesterol to preparations of chymase-treated HDL(3) in two types of cell: 1) in J774 murine macrophages endogenously expressing low levels of scavenger receptor class B, type I (SR-BI), and high levels of ABCA1 upon treatment with cAMP; and 2) in Fu5AH rat hepatoma cells endogenously expressing high levels of the SR-BI and low levels of ABCA1. Treatment of HDL(3) with the human chymase resulted in rapid depletion of pre-beta-HDL and a concomitant decrease in the efflux of cholesterol and phospholipid (2-fold and 3-fold, respectively) from the ABCA1-expressing J774 cells. In contrast, efflux of free cholesterol from Fu5AH to chymase-treated and to untreated HDL(3) was similar. Incubation of HDL(3) with phospholipid transfer protein led to an increase in pre-beta-HDL contents as well as in ABCA1-mediated cholesterol efflux. A decreased cholesterol efflux to untreated HDL(3) but not to chymase-treated HDL(3) was observed in ABCA1-expressing J774 with probucol, an inhibitor of cholesterol efflux to lipid-poor apoA-I. Similar results were obtained using brefeldin and gliburide, two inhibitors of ABCA1-mediated efflux. These results indicate that chymase treatment of HDL(3) specifically impairs the ABCA1-dependent pathway without influencing either aqueous or SR-BI-facilitated diffusion and that this effect is caused by depletion of lipid-poor pre-beta-migrating particles in HDL(3). Our results are compatible with the view that HDL(3) promotes ABCA1-mediated lipid efflux entirely through its lipid-poor fraction with pre-beta mobility.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ATP Binding Cassette Transporter 1
  • ATP-Binding Cassette Transporters / metabolism*
  • Animals
  • Brefeldin A / pharmacology
  • Cell Line
  • Cells, Cultured
  • Cholesterol / metabolism
  • Chymases
  • Cyclic AMP / metabolism
  • Dose-Response Relationship, Drug
  • Electrophoresis, Gel, Two-Dimensional
  • Glyburide / pharmacology
  • Humans
  • Immunoblotting
  • Lipid Metabolism
  • Lipoproteins, HDL / metabolism*
  • Mice
  • Models, Biological
  • Phospholipids / metabolism
  • Protein Structure, Tertiary
  • Protein Transport
  • Rats
  • Recombinant Proteins / chemistry
  • Serine Endopeptidases / chemistry
  • Serine Endopeptidases / metabolism*
  • Time Factors

Substances

  • ABCA1 protein, human
  • ATP Binding Cassette Transporter 1
  • ATP-Binding Cassette Transporters
  • Lipoproteins, HDL
  • Phospholipids
  • Recombinant Proteins
  • Brefeldin A
  • Cholesterol
  • Cyclic AMP
  • Serine Endopeptidases
  • Chymases
  • Glyburide