Hypomorphic ASGR1 modulates lipid homeostasis via INSIG1-mediated SREBP signaling suppression

JCI Insight. 2021 Oct 8;6(19):e147038. doi: 10.1172/jci.insight.147038.

Abstract

A population genetic study identified that the asialoglycoprotein receptor 1 (ASGR1) mutation carriers had substantially lower non-HDL-cholesterol (non-HDL-c) levels and reduced risks of cardiovascular diseases. However, the mechanism behind this phenomenon remained unclear. Here, we established Asgr1-knockout mice that represented a plasma lipid profile with significantly lower non-HDL-c and triglyceride (TG) caused by decreased secretion and increased uptake of VLDL/LDL. These 2 phenotypes were linked with the decreased expression of microsomal triglyceride transfer protein and proprotein convertase subtilisin/kexin type 9, 2 key targeted genes of sterol regulatory element-binding proteins (SREBPs). Furthermore, there were fewer nuclear SREBPs (nSREBPs) on account of more SREBPs being trapped in endoplasmic reticulum, which was caused by an increased expression of insulin-induced gene 1 (INSIG1), an anchor of SREBPs. Overexpression and gene knockdown interventions, in different models, were conducted to rescue the ASGR1-deficient phenotypes, and we found that INSIG1 knockdown independently reversed the ASGR1-mutated phenotypes with increased serum total cholesterol, LDL-c, TG, and liver cholesterol content accompanied by restored SREBP signaling. ASGR1 rescue experiments reduced INSIG1 and restored the SREBP network defect as manifested by improved apolipoprotein B secretion and reduced LDL uptake. Our observation demonstrated that increased INSIG1 is a critical factor responsible for ASGR1 deficiency-associated lipid profile changes and nSREBP suppression. This finding of an ASGR1/INSIG1/SREBP axis regulating lipid hemostasis may provide multiple potential targets for lipid-lowering drug development.

Keywords: Atherosclerosis; Cholesterol; Lipoproteins; Metabolism.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Asialoglycoprotein Receptor / genetics*
  • Carrier Proteins / metabolism
  • Cell Nucleus / metabolism
  • Cholesterol, HDL / metabolism
  • Cholesterol, LDL / metabolism
  • Cholesterol, VLDL / metabolism
  • Endoplasmic Reticulum / metabolism
  • Homeostasis
  • Lipid Metabolism / genetics*
  • Membrane Proteins / metabolism*
  • Mice
  • Mice, Knockout
  • Proprotein Convertase 9 / metabolism
  • Signal Transduction
  • Sterol Regulatory Element Binding Proteins / metabolism*
  • Triglycerides / metabolism

Substances

  • Asialoglycoprotein Receptor
  • Carrier Proteins
  • Cholesterol, HDL
  • Cholesterol, LDL
  • Cholesterol, VLDL
  • Insig1 protein, mouse
  • Membrane Proteins
  • Sterol Regulatory Element Binding Proteins
  • Triglycerides
  • microsomal triglyceride transfer protein
  • Pcsk9 protein, mouse
  • Proprotein Convertase 9