Absence of N-glycosylation at asparagine 43 in human lipoprotein lipase induces its accumulation in the rough endoplasmic reticulum and alters this cellular compartment

J Lipid Res. 1995 May;36(5):939-51.

Abstract

Lipoprotein lipase (LPL) is the enzyme responsible for the hydrolysis of plasma triglycerides from apolipoprotein C-II-containing lipoproteins at the capillary endothelium and it is synthesized in parenchymal cells of several tissues. Intracellular LPL processing is a major aspect of LPL regulation. The present study aims to determine the intracellular accumulation site of the LPL that is not glycosylated at Asn43. Human LPL (hLPL) cDNA was mutated by site-directed mutagenesis. An Ala residue was substituted for Asn at position 43 of the protein generating N43A hLPL. Wild type hLPL and the mutant hLPL were expressed in COS1 cells. Using immunofluorescence and immunoelectron microscopy we found that wild type hLPL in addition to being secreted into the medium was present in the rough endoplasmic reticulum (ER), Golgi compartments, and vesicles. Neither LPL activity nor protein was found in medium of cells expressing the mutant hLPL and all detectable protein was present exclusively in the ER identified witha specific antibody against the protein disulfide isomerase (PDI), an ER marker. In addition, the intracellular distribution of the ER of the cells that expressed the mutant protein was grossly altered. Treatment of COS1 cells with tunicamycin for 24 h had the same effect on wild type hLPL processing and edoplasmic reticulum distribution. Next, we investigated the influence of the accumulation of mutant hLPL on the intracellular transport of three other proteins that are N-glycosylated before reaching the plasma membrane: the related Bo,+ amino acid transporter (rBAT), the insulin-regulated glucose transporter (GLUT4), and the placental alkaline phosphatase (PLAP) protein. Coexpression of the mutant hLPL (but not wild type) caused the accumulation of rBAT and GLUT4 in the ER while PLAP reached the plasma membrane. Our findings demonstrate that glycosylation of Asn43 of human lipoprotein lipase in the endoplasmic reticulum is essential for its efflux from this compartment and that the retention of the non-glycosylated LPL induces morphological changes in the ER that could also affect its ability to modify the transport of other proteins.

Publication types

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

MeSH terms

  • Asparagine / chemistry*
  • Base Sequence
  • Cell Compartmentation / physiology*
  • Endoplasmic Reticulum / enzymology*
  • Enzyme Induction
  • Fluorescent Antibody Technique
  • Glycosylation
  • Humans
  • Lipoprotein Lipase / biosynthesis
  • Lipoprotein Lipase / chemistry*
  • Lipoprotein Lipase / drug effects
  • Lipoproteins, LDL / metabolism*
  • Microscopy, Immunoelectron
  • Molecular Sequence Data
  • Mutagenesis, Site-Directed*
  • Transfection
  • Tunicamycin / pharmacology

Substances

  • Lipoproteins, LDL
  • Tunicamycin
  • Asparagine
  • Lipoprotein Lipase