Spastin tethers lipid droplets to peroxisomes and directs fatty acid trafficking through ESCRT-III

J Cell Biol. 2019 Aug 5;218(8):2583-2599. doi: 10.1083/jcb.201902061. Epub 2019 Jun 21.

Abstract

Lipid droplets (LDs) are neutral lipid storage organelles that transfer lipids to various organelles including peroxisomes. Here, we show that the hereditary spastic paraplegia protein M1 Spastin, a membrane-bound AAA ATPase found on LDs, coordinates fatty acid (FA) trafficking from LDs to peroxisomes through two interrelated mechanisms. First, M1 Spastin forms a tethering complex with peroxisomal ABCD1 to promote LD-peroxisome contact formation. Second, M1 Spastin recruits the membrane-shaping ESCRT-III proteins IST1 and CHMP1B to LDs via its MIT domain to facilitate LD-to-peroxisome FA trafficking, possibly through IST1- and CHMP1B-dependent modifications in LD membrane morphology. Furthermore, LD-to-peroxisome FA trafficking mediated by M1 Spastin is required to relieve LDs of lipid peroxidation. M1 Spastin's dual roles in tethering LDs to peroxisomes and in recruiting ESCRT-III components to LD-peroxisome contact sites for FA trafficking may underlie the pathogenesis of diseases associated with defective FA metabolism in LDs and peroxisomes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ATP Binding Cassette Transporter, Subfamily D, Member 1 / metabolism
  • Adenosine Triphosphatases / metabolism
  • Amino Acid Motifs
  • Biological Transport
  • Endosomal Sorting Complexes Required for Transport / metabolism*
  • Fatty Acids / metabolism*
  • HeLa Cells
  • Humans
  • Hydrolysis
  • Lauric Acids / metabolism
  • Lipid Droplets / metabolism*
  • Models, Biological
  • Mutant Proteins / metabolism
  • Oncogene Proteins / metabolism
  • Peroxisomes / metabolism*
  • Spastin / chemistry
  • Spastin / metabolism*

Substances

  • ABCD1 protein, human
  • ATP Binding Cassette Transporter, Subfamily D, Member 1
  • CHMP1B protein, human
  • Endosomal Sorting Complexes Required for Transport
  • Fatty Acids
  • IST1 protein, human
  • Lauric Acids
  • Mutant Proteins
  • Oncogene Proteins
  • lauric acid
  • Adenosine Triphosphatases
  • Spastin

Associated data

  • RefSeq/NM_014946
  • RefSeq/NM_178819
  • RefSeq/NM_001270975
  • RefSeq/NM_020412