Loss- and gain-of-function PCSK9 variants: cleavage specificity, dominant negative effects, and low density lipoprotein receptor (LDLR) degradation

J Biol Chem. 2012 Sep 28;287(40):33745-55. doi: 10.1074/jbc.M112.399725. Epub 2012 Aug 8.

Abstract

The proprotein convertase PCSK9 is a major target in the treatment of hypercholesterolemia because of its ability bind the LDL receptor (LDLR) and enhance its degradation in endosomes/lysosomes. In the endoplasmic reticulum, the zymogen pro-PCSK9 is first autocatalytically cleaved at its internal Gln(152)↓, resulting in a secreted enzymatically inactive complex of PCSK9 with its inhibitory prosegment (prosegment·PCSK9), which is the active form of PCSK9 on the LDLR. We mutagenized the P1 cleavage site Gln(152) into all other residues except Cys and analyzed the expression and secretion of the resulting mutants. The data demonstrated the following. 1) The only P1 residues recognized by PCSK9 are Gln > Met > Ala > Ser > Thr ≈ Asn, revealing an unsuspected specificity. 2) All other mutations led to the formation of an unprocessed zymogen that acted as a dominant negative retaining the native protein in the endoplasmic reticulum. Analysis of a large panoply of known natural and artificial point mutants revealed that this general dominant negative observation applies to all PCSK9 mutations that result in the inability of the protein to exit the endoplasmic reticulum. Such a tight quality control property of the endoplasmic reticulum may lead to the development of specific PCSK9 small molecule inhibitors that block its autocatalytic processing. Finally, inspired by the most active gain-of-function mutant, D374Y, we evaluated the LDLR degradation activity of 18 Asp(374) variants of PCSK9. All Asp(374) mutations resulted in similar gain-of-function activity on the LDLR except that D374E was as active as native PCSK9, D374G was relatively less active, and D374N and D374P were completely inactive.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alternative Splicing
  • Catalysis
  • Cholesterol / metabolism
  • Cholesterol, LDL / metabolism
  • Enzyme Precursors / chemistry
  • Flow Cytometry
  • Genes, Dominant
  • HEK293 Cells
  • Humans
  • Hypercholesterolemia / genetics
  • Models, Biological
  • Mutation*
  • Proprotein Convertase 9
  • Proprotein Convertases / genetics*
  • Proprotein Convertases / physiology*
  • Receptors, LDL / chemistry
  • Receptors, LDL / metabolism*
  • Serine Endopeptidases / genetics*
  • Serine Endopeptidases / physiology*
  • Transfection

Substances

  • Cholesterol, LDL
  • Enzyme Precursors
  • LDLR protein, human
  • Receptors, LDL
  • Cholesterol
  • PCSK9 protein, human
  • Proprotein Convertase 9
  • Proprotein Convertases
  • Serine Endopeptidases