Deletion of the basement membrane heparan sulfate proteoglycan type XVIII collagen causes hypertriglyceridemia in mice and humans

PLoS One. 2010 Nov 10;5(11):e13919. doi: 10.1371/journal.pone.0013919.

Abstract

Background: Lipoprotein lipase (Lpl) acts on triglyceride-rich lipoproteins in the peripheral circulation, liberating free fatty acids for energy metabolism or storage. This essential enzyme is synthesized in parenchymal cells of adipose tissue, heart, and skeletal muscle and migrates to the luminal side of the vascular endothelium where it acts upon circulating lipoproteins. Prior studies suggested that Lpl is immobilized by way of heparan sulfate proteoglycans on the endothelium, but genetically altering endothelial cell heparan sulfate had no effect on Lpl localization or lipolysis. The objective of this study was to determine if extracellular matrix proteoglycans affect Lpl distribution and triglyceride metabolism.

Methods and findings: We examined mutant mice defective in collagen XVIII (Col18), a heparan sulfate proteoglycan present in vascular basement membranes. Loss of Col18 reduces plasma levels of Lpl enzyme and activity, which results in mild fasting hypertriglyceridemia and diet-induced hyperchylomicronemia. Humans with Knobloch Syndrome caused by a null mutation in the vascular form of Col18 also present lower than normal plasma Lpl mass and activity and exhibit fasting hypertriglyceridemia.

Conclusions: This is the first report demonstrating that Lpl presentation on the lumenal side of the endothelium depends on a basement membrane proteoglycan and demonstrates a previously unrecognized phenotype in patients lacking Col18.

Publication types

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

MeSH terms

  • Animals
  • Basement Membrane / metabolism*
  • Collagen Type XVIII / blood
  • Collagen Type XVIII / genetics
  • Collagen Type XVIII / metabolism*
  • Encephalocele / blood
  • Encephalocele / genetics
  • Encephalocele / metabolism
  • Enzyme-Linked Immunosorbent Assay
  • Female
  • Gene Expression Regulation, Enzymologic
  • Heparan Sulfate Proteoglycans / genetics
  • Heparan Sulfate Proteoglycans / metabolism
  • Humans
  • Hypertriglyceridemia / genetics
  • Hypertriglyceridemia / metabolism*
  • Hypertriglyceridemia / pathology
  • Immunohistochemistry
  • Lipoprotein Lipase / blood
  • Lipoprotein Lipase / genetics
  • Lipoprotein Lipase / metabolism*
  • Lipoproteins / blood
  • Lipoproteins / metabolism
  • Lipoproteins / ultrastructure
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Microscopy, Electron, Transmission
  • Mutation
  • Retinal Degeneration
  • Retinal Detachment / blood
  • Retinal Detachment / congenital
  • Retinal Detachment / genetics
  • Retinal Detachment / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Triglycerides / blood
  • Triglycerides / metabolism

Substances

  • Collagen Type XVIII
  • Heparan Sulfate Proteoglycans
  • Lipoproteins
  • Triglycerides
  • Lipoprotein Lipase

Supplementary concepts

  • Knobloch syndrome