The hereditary spastic paraplegia-related enzyme DDHD2 is a principal brain triglyceride lipase

Proc Natl Acad Sci U S A. 2014 Oct 14;111(41):14924-9. doi: 10.1073/pnas.1413706111. Epub 2014 Sep 29.

Abstract

Complex hereditary spastic paraplegia (HSP) is a genetic disorder that causes lower limb spasticity and weakness and intellectual disability. Deleterious mutations in the poorly characterized serine hydrolase DDHD2 are a causative basis for recessive complex HSP. DDHD2 exhibits phospholipase activity in vitro, but its endogenous substrates and biochemical functions remain unknown. Here, we report the development of DDHD2(-/-) mice and a selective, in vivo-active DDHD2 inhibitor and their use in combination with mass spectrometry-based lipidomics to discover that DDHD2 regulates brain triglycerides (triacylglycerols, or TAGs). DDHD2(-/-) mice show age-dependent TAG elevations in the central nervous system, but not in several peripheral tissues. Large lipid droplets accumulated in DDHD2(-/-) brains and were localized primarily to the intracellular compartments of neurons. These metabolic changes were accompanied by impairments in motor and cognitive function. Recombinant DDHD2 displays TAG hydrolase activity, and TAGs accumulated in the brains of wild-type mice treated subchronically with a selective DDHD2 inhibitor. These findings, taken together, indicate that the central nervous system possesses a specialized pathway for metabolizing TAGs, disruption of which leads to massive lipid accumulation in neurons and complex HSP syndrome.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Brain / metabolism
  • Brain / ultrastructure
  • Cognition
  • Enzyme Activation / drug effects
  • Enzyme Inhibitors / chemistry
  • Enzyme Inhibitors / pharmacology
  • Gene Deletion
  • Gene Targeting
  • HEK293 Cells
  • Humans
  • Lipase / antagonists & inhibitors
  • Lipase / metabolism*
  • Lipid Droplets / metabolism
  • Lipid Droplets / ultrastructure
  • Locomotion
  • Mice, Inbred C57BL
  • Neurons / metabolism
  • Phospholipases
  • Phospholipases A1 / antagonists & inhibitors
  • Phospholipases A1 / deficiency
  • Phospholipases A1 / metabolism*
  • Reproducibility of Results
  • Spastic Paraplegia, Hereditary / enzymology*
  • Spastic Paraplegia, Hereditary / genetics
  • Triglycerides / metabolism

Substances

  • Enzyme Inhibitors
  • Triglycerides
  • DDHD2 protein, mouse
  • Phospholipases
  • Lipase
  • Phospholipases A1