The WWOX gene modulates high-density lipoprotein and lipid metabolism

Circ Cardiovasc Genet. 2014 Aug;7(4):491-504. doi: 10.1161/CIRCGENETICS.113.000248. Epub 2014 May 28.

Abstract

Background: Low levels of high-density lipoprotein (HDL) cholesterol constitutes a major risk factor for atherosclerosis. Recent studies from our group reported a genetic association between the WW domain-containing oxidoreductase (WWOX) gene and HDL cholesterol levels. Here, through next-generation resequencing, in vivo functional studies and gene microarray analyses, we investigated the role of WWOX in HDL and lipid metabolism.

Methods and results: Using next-generation resequencing of the WWOX region, we first identified 8 variants significantly associated and perfectly segregating with the low-HDL trait in 2 multigenerational French Canadian dyslipidemic families. To understand in vivo functions of WWOX, we used liver-specific Wwox(hep-/-) and total Wwox(-/-) mice models, where we found decreased ApoA-I and Abca1 levels in hepatic tissues. Analyses of lipoprotein profiles in Wwox(-/-), but not Wwox(hep-/-) littermates, also showed marked reductions in serum HDL cholesterol concentrations, concordant with the low-HDL findings observed in families. We next obtained evidence of a sex-specific effect in female Wwox(hep-/-) mice, where microarray analyses revealed an increase in plasma triglycerides and altered lipid metabolic pathways. We further identified a significant reduction in ApoA-I and Lpl and an upregulation in Fas, Angptl4, and Lipg, suggesting that the effects of Wwox involve multiple pathways, including cholesterol homeostasis, ApoA-I/ABCA1 pathway, and fatty acid biosynthesis/triglyceride metabolism.

Conclusions: Our data indicate that WWOX disruption alters HDL and lipoprotein metabolism through several mechanisms and may account for the low-HDL phenotype observed in families expressing the WWOX variants. These findings thus describe a novel gene involved in cellular lipid homeostasis, which effects may impact atherosclerotic disease development.

Keywords: ABCA1; Apolopoprotein A-I; HDL cholesterol; WWOX protein; cardiovascular diseases; genetics; lipids.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • ATP Binding Cassette Transporter 1 / metabolism
  • Adolescent
  • Adult
  • Aged
  • Alleles
  • Angiopoietin-Like Protein 4
  • Angiopoietins / metabolism
  • Animals
  • Apolipoprotein A-I / metabolism
  • Cholesterol, HDL / blood
  • Chromosomes, Human, Pair 16
  • Female
  • Haplotypes
  • High-Throughput Nucleotide Sequencing
  • Humans
  • Lipase / metabolism
  • Lipid Metabolism / physiology*
  • Lipoproteins, HDL / blood*
  • Liver / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Middle Aged
  • Oxidoreductases / deficiency
  • Oxidoreductases / genetics*
  • Oxidoreductases / metabolism
  • Polymorphism, Single Nucleotide
  • Sequence Analysis, DNA
  • Triglycerides / blood
  • Tumor Suppressor Proteins / genetics*
  • Tumor Suppressor Proteins / metabolism
  • Up-Regulation
  • WW Domain-Containing Oxidoreductase
  • fas Receptor / metabolism

Substances

  • ATP Binding Cassette Transporter 1
  • Angiopoietin-Like Protein 4
  • Angiopoietins
  • Angptl4 protein, mouse
  • Apolipoprotein A-I
  • Cholesterol, HDL
  • Fas protein, mouse
  • Lipoproteins, HDL
  • Triglycerides
  • Tumor Suppressor Proteins
  • fas Receptor
  • Oxidoreductases
  • WW Domain-Containing Oxidoreductase
  • WWOX protein, human
  • Wwox protein, mouse
  • Lipase
  • Lipg protein, mouse