Novel Interconnections in Lipid Metabolism Revealed by Overexpression of Sphingomyelin Synthase-1

J Biol Chem. 2017 Mar 24;292(12):5110-5122. doi: 10.1074/jbc.M116.751602. Epub 2017 Jan 13.

Abstract

This study investigates the consequences of elevating sphingomyelin synthase 1 (SMS1) activity, which generates the main mammalian sphingolipid, sphingomyelin. HepG2 cells stably transfected with SMS1 (HepG2-SMS1) exhibit elevated enzyme activity in vitro and increased sphingomyelin content (mainly C22:0- and C24:0-sphingomyelin) but lower hexosylceramide (Hex-Cer) levels. HepG2-SMS1 cells have fewer triacylglycerols than controls but similar diacylglycerol acyltransferase activity, triacylglycerol secretion, and mitochondrial function. Treatment with 1 mm palmitate increases de novo ceramide synthesis in both cell lines to a similar degree, causing accumulation of C16:0-ceramide (and some C18:0-, C20:0-, and C22:0-ceramides) as well as C16:0- and C18:0-Hex-Cers. In these experiments, the palmitic acid is delivered as a complex with delipidated BSA (2:1, mol/mol) and does not induce significant lipotoxicity. Based on precursor labeling, the flux through SM synthase also increases, which is exacerbated in HepG2-SMS1 cells. In contrast, palmitate-induced lipid droplet formation is significantly reduced in HepG2-SMS1 cells. [14C]Choline and [3H]palmitate tracking shows that SMS1 overexpression apparently affects the partitioning of palmitate-enriched diacylglycerol between the phosphatidylcholine and triacylglycerol pathways, to the benefit of the former. Furthermore, triacylglycerols from HepG2-SMS1 cells are enriched in polyunsaturated fatty acids, which is indicative of active remodeling. Together, these results delineate novel metabolic interactions between glycerolipids and sphingolipids.

Keywords: ceramide; diacylglycerol; hepatocytes; lipid droplets; lipid metabolism; palmitic acid; phosphatidylcholine; phospholipid; sphingomyelin synthase; triacylglycerol.

Publication types

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

MeSH terms

  • Ceramides / metabolism
  • Diglycerides / metabolism
  • Fatty Acids / metabolism
  • Hep G2 Cells
  • Hepatocytes / metabolism
  • Humans
  • Lipid Metabolism*
  • Membrane Proteins / analysis
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Nerve Tissue Proteins / analysis
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism*
  • Transferases (Other Substituted Phosphate Groups) / analysis
  • Transferases (Other Substituted Phosphate Groups) / genetics
  • Transferases (Other Substituted Phosphate Groups) / metabolism*
  • Triglycerides / metabolism
  • Up-Regulation

Substances

  • 1,2-diacylglycerol
  • Ceramides
  • Diglycerides
  • Fatty Acids
  • Membrane Proteins
  • Nerve Tissue Proteins
  • Triglycerides
  • SGMS1 protein, human
  • Transferases (Other Substituted Phosphate Groups)