Reep1 null mice reveal a converging role for hereditary spastic paraplegia proteins in lipid droplet regulation

Hum Mol Genet. 2016 Dec 1;25(23):5111-5125. doi: 10.1093/hmg/ddw315.

Abstract

Hereditary spastic paraplegias (HSPs; SPG1-76 plus others) are length-dependent disorders affecting long corticospinal axons, and the most common autosomal dominant forms are caused by mutations in genes that encode the spastin (SPG4), atlastin-1 (SPG3A) and REEP1 (SPG31) proteins. These proteins bind one another and shape the tubular endoplasmic reticulum (ER) network throughout cells. They also are involved in lipid droplet formation, enlargement, or both in cells, though mechanisms remain unclear. Here we have identified evidence of partial lipoatrophy in Reep1 null mice in addition to prominent spastic paraparesis. Furthermore, Reep1-/- embryonic fibroblasts and neurons in the cerebral cortex both show lipid droplet abnormalities. The apparent partial lipodystrophy in Reep1 null mice, although less severe, is reminiscent of the lipoatrophy phenotype observed in the most common form of autosomal recessive lipodystrophy, Berardinelli-Seip congenital lipodystrophy. Berardinelli-Seip lipodystrophy is caused by autosomal recessive mutations in the BSCL2 gene that encodes an ER protein, seipin, that is also mutated in the autosomal dominant HSP SPG17 (Silver syndrome). Furthermore, REEP1 co-immunoprecipitates with seipin in cells. This strengthens the link between alterations in ER morphogenesis and lipid abnormalities, with important pathogenic implications for the most common forms of HSP.

MeSH terms

  • Animals
  • Axons / metabolism
  • Axons / pathology
  • Cerebral Cortex / metabolism
  • Cerebral Cortex / pathology
  • Endoplasmic Reticulum / genetics*
  • GTP-Binding Protein gamma Subunits
  • Heterotrimeric GTP-Binding Proteins / genetics
  • Humans
  • Lipid Droplets / metabolism
  • Lipid Droplets / pathology
  • Lipodystrophy, Congenital Generalized / genetics*
  • Lipodystrophy, Congenital Generalized / metabolism
  • Lipodystrophy, Congenital Generalized / physiopathology
  • Membrane Transport Proteins / genetics*
  • Membrane Transport Proteins / metabolism
  • Mice
  • Mice, Knockout
  • Morphogenesis / genetics
  • Mutation
  • Pyramidal Tracts / metabolism
  • Pyramidal Tracts / pathology
  • Spastic Paraplegia, Hereditary / genetics*
  • Spastic Paraplegia, Hereditary / metabolism
  • Spastic Paraplegia, Hereditary / physiopathology

Substances

  • Bscl2 protein, mouse
  • GTP-Binding Protein gamma Subunits
  • Membrane Transport Proteins
  • REEP1 protein, human
  • Heterotrimeric GTP-Binding Proteins