The Liver Clock Controls Cholesterol Homeostasis through Trib1 Protein-mediated Regulation of PCSK9/Low Density Lipoprotein Receptor (LDLR) Axis

J Biol Chem. 2015 Dec 25;290(52):31003-12. doi: 10.1074/jbc.M115.685982. Epub 2015 Nov 7.

Abstract

Disruption of the body clock has been recognized as a risk factor for cardiovascular disease. How the circadian pacemaker interacts with the genetic factors associated with plasma lipid traits remains poorly understood. Recent genome-wide association studies have identified an expanding list of genetic variants that influence plasma cholesterol and triglyceride levels. Here we analyzed circadian regulation of lipid-associated candidate genes in the liver and identified two distinct groups exhibiting rhythmic and non-rhythmic patterns of expression during light-dark cycles. Liver-specific inactivation of Bmal1 led to elevated plasma LDL/VLDL cholesterol levels as a consequence of the disruption of the PCSK9/LDL receptor regulatory axis. Ablation of the liver clock perturbed diurnal regulation of lipid-associated genes in the liver and markedly reduced the expression of the non-rhythmically expressed gene Trib1. Adenovirus-mediated rescue of Trib1 expression lowered plasma PCSK9 levels, increased LDL receptor protein expression, and restored plasma cholesterol homeostasis in mice lacking a functional liver clock. These results illustrate an unexpected mechanism through which the biological clock regulates cholesterol homeostasis through its regulation of non-rhythmic genes in the liver.

Keywords: cholesterol metabolism; circadian clock; gwas; liver; metabolism; proprotein convertase subtilisin/kexin type 9 (PCSK9).

Publication types

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

MeSH terms

  • Animals
  • Cholesterol / genetics
  • Cholesterol / metabolism*
  • Circadian Clocks / physiology*
  • Gene Expression Regulation / physiology
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / metabolism*
  • Lipoproteins, LDL / genetics
  • Lipoproteins, LDL / metabolism
  • Lipoproteins, VLDL / genetics
  • Lipoproteins, VLDL / metabolism
  • Liver / metabolism*
  • Mice
  • Mice, Transgenic
  • Proprotein Convertase 9
  • Proprotein Convertases / biosynthesis*
  • Proprotein Convertases / genetics
  • Protein Serine-Threonine Kinases / antagonists & inhibitors*
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism
  • Receptors, LDL / biosynthesis*
  • Receptors, LDL / genetics
  • Serine Endopeptidases / biosynthesis*
  • Serine Endopeptidases / genetics

Substances

  • Intracellular Signaling Peptides and Proteins
  • Lipoproteins, LDL
  • Lipoproteins, VLDL
  • Receptors, LDL
  • Trib1 protein, mouse
  • Cholesterol
  • Protein Serine-Threonine Kinases
  • Pcsk9 protein, mouse
  • Proprotein Convertase 9
  • Proprotein Convertases
  • Serine Endopeptidases