The LXR-IDOL axis defines a clathrin-, caveolae-, and dynamin-independent endocytic route for LDLR internalization and lysosomal degradation

J Lipid Res. 2013 Aug;54(8):2174-2184. doi: 10.1194/jlr.M037713. Epub 2013 Jun 3.

Abstract

Low density lipoprotein (LDL) cholesterol is taken up into cells via clathrin-mediated endocytosis of the LDL receptor (LDLR). Following dissociation of the LDLR-LDL complex, LDL is directed to lysosomes whereas the LDLR recycles to the plasma membrane. Activation of the sterol-sensing nuclear receptors liver X receptors (LXRs) enhances degradation of the LDLR. This depends on the LXR target gene inducible degrader of the LDLR (IDOL), an E3-ubiquitin ligase that promotes ubiquitylation and lysosomal degradation of the LDLR. How ubiquitylation of the LDLR by IDOL controls its endocytic trafficking is currently unknown. Using genetic- and pharmacological-based approaches coupled to functional assessment of LDL uptake, we show that the LXR-IDOL axis targets a LDLR pool present in lipid rafts. IDOL-dependent internalization of the LDLR is independent of clathrin, caveolin, macroautophagy, and dynamin. Rather, it depends on the endocytic protein epsin. Consistent with LDLR ubiquitylation acting as a sorting signal, degradation of the receptor can be blocked by perturbing the endosomal sorting complex required for transport (ESCRT) or by USP8, a deubiquitylase implicated in sorting ubiquitylated cargo to multivesicular bodies. In summary, we provide evidence for the existence of an LXR-IDOL-mediated internalization pathway for the LDLR that is distinct from that used for lipoprotein uptake.

Keywords: E3-ubiquitin ligase; endocytosis; epsins; inducible degrader of low density lipoprotein receptor; lipoprotein receptors; liver X receptor; low density lipoprotein receptor.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Caveolae / metabolism
  • Cells, Cultured
  • Clathrin / metabolism
  • Dynamins / metabolism
  • Endocytosis*
  • HEK293 Cells
  • HeLa Cells
  • Hep G2 Cells
  • Humans
  • Liver X Receptors
  • Lysosomes / metabolism*
  • Orphan Nuclear Receptors / metabolism*
  • Receptors, LDL / metabolism*
  • Ubiquitin-Protein Ligases / metabolism*

Substances

  • Clathrin
  • Liver X Receptors
  • Orphan Nuclear Receptors
  • Receptors, LDL
  • MYLIP protein, human
  • Ubiquitin-Protein Ligases
  • Dynamins