ISGylation controls exosome secretion by promoting lysosomal degradation of MVB proteins

Nat Commun. 2016 Nov 24:7:13588. doi: 10.1038/ncomms13588.

Abstract

Exosomes are vesicles secreted to the extracellular environment through fusion with the plasma membrane of specific endosomes called multivesicular bodies (MVB) and mediate cell-to-cell communication in many biological processes. Posttranslational modifications are involved in the sorting of specific proteins into exosomes. Here we identify ISGylation as a ubiquitin-like modification that controls exosome release. ISGylation induction decreases MVB numbers and impairs exosome secretion. Using ISG15-knockout mice and mice expressing the enzymatically inactive form of the de-ISGylase USP18, we demonstrate in vitro and in vivo that ISG15 conjugation regulates exosome secretion. ISG15 conjugation triggers MVB co-localization with lysosomes and promotes the aggregation and degradation of MVB proteins. Accordingly, inhibition of lysosomal function or autophagy restores exosome secretion. Specifically, ISGylation of the MVB protein TSG101 induces its aggregation and degradation, being sufficient to impair exosome secretion. These results identify ISGylation as a novel ubiquitin-like modifier in the control of exosome production.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Autophagy
  • Cytokines / genetics*
  • DNA-Binding Proteins / metabolism*
  • Endosomal Sorting Complexes Required for Transport / metabolism*
  • Exosomes / metabolism*
  • HEK293 Cells
  • Humans
  • Jurkat Cells
  • Lysosomes / metabolism*
  • Macrophages
  • Mice
  • Mice, Knockout
  • Multivesicular Bodies / metabolism*
  • T-Lymphocytes
  • Transcription Factors / metabolism*
  • Ubiquitin Thiolesterase / metabolism
  • Ubiquitins / genetics

Substances

  • Cytokines
  • DNA-Binding Proteins
  • Endosomal Sorting Complexes Required for Transport
  • G1p2 protein, mouse
  • Transcription Factors
  • Tsg101 protein
  • Ubiquitins
  • ISG15 protein, human
  • Usp18 protein, mouse
  • Ubiquitin Thiolesterase