Human apolipoprotein A-I induces cyclooxygenase-2 expression and prostaglandin I-2 release in endothelial cells through ATP-binding cassette transporter A1

Am J Physiol Cell Physiol. 2011 Sep;301(3):C739-48. doi: 10.1152/ajpcell.00055.2011. Epub 2011 Jul 6.

Abstract

High-density lipoprotein (HDL) can induce cyclooxygenase-2 (COX-2) expression and prostacyclin I-2 (PGI-2) release in endothelial cells to exert multiple antiatherogenic functions. This effect has been attributed mainly to the role of sphingosine-1-phosphate (S1P) integrated in HDL. However, whether apolipoprotein A-I (apoA-I), the major apolipoprotein of HDL, could induce COX-2 expression and PGI-2 release still remains unclear. In the present study, we selectively delipidated HDL and confirmed that apoA-I could facilitate COX-2 expression and PGI-2 production in human umbilical vein endothelial cells (HUVECs). ApoA-I, but not trypsinized apoA-I, induced COX-2 expression in a time- and dose-dependent manner consistent with a key role for apoA-I in this process. Additionally, cotreatment of apoA-I with S1P further enhanced COX-2 expression and PGI-2 production in HUVECs. These effects triggered by apoA-I were not inhibited by pertussis toxin, consistent with SIP receptor independent pathway for apoA-I effect. Moreover, we demonstrated that the activation of p38 mitogen-activated protein kinase (MAPK), extracellular receptor kinase (ERK) 1/2, and JAK2 pathways by apoA-I was involved in the expression of COX-2 and the release of PGI-2 in HUVECs, and these effects were inhibited by their specific inhibitors, respectively. Small interfering RNA experiments showed that ATP binding-cassette transporter A1 (ABCA1) was required for COX-2 expression and PGI-2 release induced by apoA-I. Thus our results indicate that apoA-I induces COX-2 expression and PGI-2 release through ABCA1 and the activation of intracellular p38 MAPK, ERK1/2, as well as JAK2 pathways, and apoA-I can reinforce these effects with S1P in HUVECs. These novel effects of apoA-I could in part mediate antiatherogenic effects of HDL.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ATP Binding Cassette Transporter 1
  • ATP-Binding Cassette Transporters / genetics
  • ATP-Binding Cassette Transporters / metabolism*
  • Apolipoprotein A-I / analysis
  • Apolipoprotein A-I / isolation & purification
  • Apolipoprotein A-I / metabolism
  • Apolipoprotein A-I / pharmacology*
  • Apolipoproteins / analysis
  • Cells, Cultured
  • Cholesterol / analysis
  • Cyclooxygenase 2 / metabolism*
  • Down-Regulation / drug effects
  • Down-Regulation / genetics
  • Drug Synergism
  • Epoprostenol / metabolism*
  • Extracellular Signal-Regulated MAP Kinases / antagonists & inhibitors
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Fatty Acids, Nonesterified / analysis
  • Flavonoids / pharmacology
  • Gene Expression / drug effects*
  • Human Umbilical Vein Endothelial Cells / drug effects
  • Human Umbilical Vein Endothelial Cells / metabolism*
  • Humans
  • Imidazoles / pharmacology
  • Janus Kinase 2 / antagonists & inhibitors
  • Janus Kinase 2 / metabolism
  • Lipoproteins, HDL / chemistry
  • Lipoproteins, HDL / pharmacology
  • Lysophospholipids / antagonists & inhibitors
  • Lysophospholipids / pharmacology
  • Pertussis Toxin / pharmacology
  • Phospholipids / analysis
  • Phospholipids / isolation & purification
  • Phospholipids / pharmacology
  • Phosphorylation / drug effects
  • Protein Kinase Inhibitors / pharmacology
  • Pyridines / pharmacology
  • RNA, Small Interfering / genetics
  • Signal Transduction / drug effects
  • Signal Transduction / physiology
  • Sphingosine / analogs & derivatives
  • Sphingosine / antagonists & inhibitors
  • Sphingosine / pharmacology
  • Trypsin / metabolism
  • Tyrphostins / pharmacology
  • Up-Regulation / drug effects
  • Up-Regulation / genetics
  • p38 Mitogen-Activated Protein Kinases / antagonists & inhibitors
  • p38 Mitogen-Activated Protein Kinases / metabolism

Substances

  • ABCA1 protein, human
  • APOA1 protein, human
  • ATP Binding Cassette Transporter 1
  • ATP-Binding Cassette Transporters
  • Apolipoprotein A-I
  • Apolipoproteins
  • Fatty Acids, Nonesterified
  • Flavonoids
  • Imidazoles
  • Lipoproteins, HDL
  • Lysophospholipids
  • Phospholipids
  • Protein Kinase Inhibitors
  • Pyridines
  • RNA, Small Interfering
  • Tyrphostins
  • alpha-cyano-(3,4-dihydroxy)-N-benzylcinnamide
  • sphingosine 1-phosphate
  • Cholesterol
  • Epoprostenol
  • Cyclooxygenase 2
  • Pertussis Toxin
  • JAK2 protein, human
  • Janus Kinase 2
  • Extracellular Signal-Regulated MAP Kinases
  • p38 Mitogen-Activated Protein Kinases
  • Trypsin
  • Sphingosine
  • SB 203580
  • 2-(2-amino-3-methoxyphenyl)-4H-1-benzopyran-4-one