Transgenic expression of dominant-active IDOL in liver causes diet-induced hypercholesterolemia and atherosclerosis in mice

Circ Res. 2014 Aug 1;115(4):442-9. doi: 10.1161/CIRCRESAHA.115.304440. Epub 2014 Jun 16.

Abstract

Rationale: The E3 ubiquitin ligase inducible degrader of the low-density lipoprotein receptor (IDOL) triggers lysosomal degradation of the low-density lipoprotein receptor. The tissue-specific effects of the IDOL pathway on plasma cholesterol and atherosclerosis have not been examined.

Objective: Given that the liver is the primary determinant of plasma cholesterol levels, we sought to examine the consequence of effect of chronic liver-specific expression of a dominant-active form of IDOL in mice.

Methods and results: We expressed a degradation-resistant, dominant-active form of IDOL (super IDOL [sIDOL]) in C57Bl/6J mice from the liver-specific albumin promoter (L-sIDOL transgenics). L-sIDOL mice were fed a Western diet for 20 or 30 weeks and then analyzed for plasma lipid levels and atherosclerotic lesion formation. L-sIDOL mice showed dramatic reductions in hepatic low-density lipoprotein receptor protein and increased plasma low-density lipoprotein cholesterol levels on both chow and Western diets. Moreover, L-sIDOL mice developed marked atherosclerotic lesions when fed a Western diet. Lesion formation in L-sIDOL mice was more robust than in apolipoprotein E*3 Leiden mice and did not require the addition of cholate to the diet. Western diet-fed L-sIDOL mice had elevated expression of liver X receptor target genes and proinflammatory genes in their aortas.

Conclusions: Liver-specific expression of dominant-active IDOL is associated with hypercholesterolemia and a marked elevation in atherosclerotic lesions. Our results show that increased activity of the IDOL pathway in the liver can override other low-density lipoprotein receptor regulatory pathways leading to cardiovascular disease. L-sIDOL mice are a robust, dominantly inherited, diet-inducible model for the study of atherosclerosis.

Keywords: atherosclerosis; cholesterol, LDL; ubiquitin-protein ligases.

Publication types

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

MeSH terms

  • Albumins / genetics
  • Animals
  • Aorta / metabolism
  • Aorta / pathology
  • Aortic Diseases / enzymology*
  • Aortic Diseases / genetics
  • Aortic Diseases / pathology*
  • Apolipoprotein E3 / genetics
  • Apolipoprotein E3 / metabolism
  • Atherosclerosis / enzymology*
  • Atherosclerosis / genetics
  • Atherosclerosis / pathology
  • Cholesterol, LDL / blood
  • Diet, High-Fat*
  • Diet, Western*
  • Disease Models, Animal
  • Humans
  • Hypercholesterolemia / enzymology*
  • Hypercholesterolemia / genetics
  • Hypercholesterolemia / pathology
  • Inflammation Mediators / metabolism
  • Liver / enzymology*
  • Liver X Receptors
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Mutation
  • Orphan Nuclear Receptors / metabolism
  • Plaque, Atherosclerotic
  • Promoter Regions, Genetic
  • Receptors, LDL / metabolism
  • Time Factors
  • Ubiquitin-Protein Ligases / genetics
  • Ubiquitin-Protein Ligases / metabolism*

Substances

  • Albumins
  • Apolipoprotein E3
  • Cholesterol, LDL
  • Inflammation Mediators
  • Liver X Receptors
  • Orphan Nuclear Receptors
  • Receptors, LDL
  • MYLIP protein, human
  • Ubiquitin-Protein Ligases