Efficient phagocytosis requires triacylglycerol hydrolysis by adipose triglyceride lipase

J Biol Chem. 2010 Jun 25;285(26):20192-201. doi: 10.1074/jbc.M110.107854. Epub 2010 Apr 27.

Abstract

Macrophage phagocytosis is an essential biological process in host defense and requires large amounts of energy. To date, glucose is believed to represent the prime substrate for ATP production in macrophages. To investigate the relative contribution of free fatty acids (FFAs) in this process, we determined the phagocytosis rates in normal mouse macrophages and macrophages of adipose triglyceride lipase (ATGL)-deficient mice. ATGL was shown to be the rate-limiting enzyme for the hydrolysis of lipid droplet-associated triacylglycerol (TG) in many tissues. Here, we demonstrate that Atgl(-/-) macrophages fail to efficiently hydrolyze cellular TG stores leading to decreased cellular FFA concentrations and concomitant accumulation of lipid droplets, even in the absence of exogenous lipid loading. The reduced availability of FFAs results in decreased cellular ATP concentrations and impaired phagocytosis suggesting that fatty acids must first go through a cycle of esterification and re-hydrolysis before they are available as energy substrate. Exogenously added glucose cannot fully compensate for the phagocytotic defect in Atgl(-/-) macrophages. Hence, phagocytosis was also decreased in vivo when Atgl(-/-) mice were challenged with bacterial particles. These findings imply that phagocytosis in macrophages depends on the availability of FFAs and that ATGL is required for their hydrolytic release from cellular TG stores. This novel mechanism links ATGL-mediated lipolysis to macrophage function in host defense and opens the way to explore possible roles of ATGL in immune response, inflammation, and atherosclerosis.

Publication types

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

MeSH terms

  • Adenosine Diphosphate / metabolism
  • Adenosine Triphosphate / metabolism
  • Animals
  • Blotting, Western
  • Carboxylic Ester Hydrolases / genetics
  • Carboxylic Ester Hydrolases / metabolism*
  • Cell Line
  • Cells, Cultured
  • Escherichia coli / physiology
  • Fatty Acids, Nonesterified / metabolism
  • Fatty Acids, Nonesterified / pharmacokinetics
  • Foam Cells / cytology
  • Foam Cells / metabolism
  • Gene Expression
  • Genes, Mitochondrial / genetics
  • Humans
  • Hydrolysis
  • Lipase
  • Lipid Metabolism
  • Macrophages / cytology
  • Macrophages / metabolism*
  • Macrophages / ultrastructure
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Microscopy, Electron
  • Phagocytosis / physiology*
  • Reverse Transcriptase Polymerase Chain Reaction
  • Triglycerides / metabolism*

Substances

  • Fatty Acids, Nonesterified
  • Triglycerides
  • Adenosine Diphosphate
  • Adenosine Triphosphate
  • Carboxylic Ester Hydrolases
  • Lipase
  • PNPLA2 protein, mouse