Bro1 stimulates Vps4 to promote intralumenal vesicle formation during multivesicular body biogenesis

J Cell Biol. 2021 Aug 2;220(8):e202102070. doi: 10.1083/jcb.202102070. Epub 2021 Jun 23.

Abstract

Endosomal sorting complexes required for transport (ESCRT-0, -I, -II, -III) execute cargo sorting and intralumenal vesicle (ILV) formation during conversion of endosomes to multivesicular bodies (MVBs). The AAA-ATPase Vps4 regulates the ESCRT-III polymer to facilitate membrane remodeling and ILV scission during MVB biogenesis. Here, we show that the conserved V domain of ESCRT-associated protein Bro1 (the yeast homologue of mammalian proteins ALIX and HD-PTP) directly stimulates Vps4. This activity is required for MVB cargo sorting. Furthermore, the Bro1 V domain alone supports Vps4/ESCRT-driven ILV formation in vivo without efficient MVB cargo sorting. These results reveal a novel activity of the V domains of Bro1 homologues in licensing ESCRT-III-dependent ILV formation and suggest a role in coordinating cargo sorting with membrane remodeling during MVB sorting. Moreover, ubiquitin binding enhances V domain stimulation of Vps4 to promote ILV formation via the Bro1-Vps4-ESCRT-III axis, uncovering a novel role for ubiquitin during MVB biogenesis in addition to facilitating cargo recognition.

Publication types

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

MeSH terms

  • Adenosine Triphosphatases / genetics
  • Adenosine Triphosphatases / metabolism*
  • Binding Sites
  • Endosomal Sorting Complexes Required for Transport / genetics
  • Endosomal Sorting Complexes Required for Transport / metabolism*
  • Enzyme Activation
  • Microscopy, Fluorescence
  • Models, Molecular
  • Multivesicular Bodies / enzymology*
  • Multivesicular Bodies / genetics
  • Mutation
  • Organelle Biogenesis*
  • Protein Domains
  • Protein Transport
  • Saccharomyces cerevisiae / enzymology*
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae Proteins / genetics
  • Saccharomyces cerevisiae Proteins / metabolism*
  • Ubiquitin / metabolism
  • Ubiquitination

Substances

  • Bro1 protein, S cerevisiae
  • Endosomal Sorting Complexes Required for Transport
  • Saccharomyces cerevisiae Proteins
  • Ubiquitin
  • VPS4 protein, S cerevisiae
  • Adenosine Triphosphatases