SPE-39 family proteins interact with the HOPS complex and function in lysosomal delivery

Mol Biol Cell. 2009 Feb;20(4):1223-40. doi: 10.1091/mbc.e08-07-0728. Epub 2008 Dec 24.

Abstract

Yeast and animal homotypic fusion and vacuole protein sorting (HOPS) complexes contain conserved subunits, but HOPS-mediated traffic in animals might require additional proteins. Here, we demonstrate that SPE-39 homologues, which are found only in animals, are present in RAB5-, RAB7-, and RAB11-positive endosomes where they play a conserved role in lysosomal delivery and probably function via their interaction with the core HOPS complex. Although Caenorhabditis elegans spe-39 mutants were initially identified as having abnormal vesicular biogenesis during spermatogenesis, we show that these mutants also have disrupted processing of endocytosed proteins in oocytes and coelomocytes. C. elegans SPE-39 interacts in vitro with both VPS33A and VPS33B, whereas RNA interference of VPS33B causes spe-39-like spermatogenesis defects. The human SPE-39 orthologue C14orf133 also interacts with VPS33 homologues and both coimmunoprecipitates and cosediments with other HOPS subunits. SPE-39 knockdown in cultured human cells altered the morphology of syntaxin 7-, syntaxin 8-, and syntaxin 13-positive endosomes. These effects occurred concomitantly with delayed mannose 6-phosphate receptor-mediated cathepsin D delivery and degradation of internalized epidermal growth factor receptors. Our findings establish that SPE-39 proteins are a previously unrecognized regulator of lysosomal delivery and that C. elegans spermatogenesis is an experimental system useful for identifying conserved regulators of metazoan lysosomal biogenesis.

Publication types

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

MeSH terms

  • Animals
  • Caenorhabditis elegans / metabolism*
  • Caenorhabditis elegans / ultrastructure
  • Caenorhabditis elegans Proteins / metabolism*
  • Carrier Proteins / metabolism*
  • Endocytosis
  • Endosomes / metabolism
  • HeLa Cells
  • Humans
  • Lysosomes / metabolism*
  • Male
  • Mice
  • Multiprotein Complexes / metabolism*
  • Protein Binding
  • Protein Processing, Post-Translational
  • Protein Transport
  • RNA, Small Interfering / metabolism
  • Receptor, IGF Type 2 / metabolism
  • Spermatocytes / ultrastructure
  • Spermatogenesis
  • Vesicular Transport Proteins / metabolism

Substances

  • Caenorhabditis elegans Proteins
  • Carrier Proteins
  • Multiprotein Complexes
  • RNA, Small Interfering
  • Receptor, IGF Type 2
  • Spe-39 protein, C elegans
  • VIPAS39 protein, human
  • VPS33A protein, human
  • VPS33B protein, human
  • Vesicular Transport Proteins