The ESCRT Regulator Did2 Maintains the Balance Between Long-Distance Endosomal Transport and Endocytic Trafficking

PLoS Genet. 2017 Apr 19;13(4):e1006734. doi: 10.1371/journal.pgen.1006734. eCollection 2017 Apr.

Abstract

In highly polarised cells, like fungal hyphae, early endosomes function in both endocytosis as well as long-distance transport of various cargo including mRNA and protein complexes. However, knowledge on the crosstalk between these seemingly different trafficking processes is scarce. Here, we demonstrate that the ESCRT regulator Did2 coordinates endosomal transport in fungal hyphae of Ustilago maydis. Loss of Did2 results in defective vacuolar targeting, less processive long-distance transport and abnormal shuttling of early endosomes. Importantly, the late endosomal protein Rab7 and vacuolar protease Prc1 exhibit increased shuttling on these aberrant endosomes suggesting defects in endosomal maturation and identity. Consistently, molecular motors fail to attach efficiently explaining the disturbed processive movement. Furthermore, the endosomal mRNP linker protein Upa1 is hardly present on endosomes resulting in defects in long-distance mRNA transport. In conclusion, the ESCRT regulator Did2 coordinates precise maturation of endosomes and thus provides the correct membrane identity for efficient endosomal long-distance transport.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cathepsin A / genetics
  • Cell Polarity / genetics
  • Endocytosis / genetics
  • Endosomal Sorting Complexes Required for Transport / genetics*
  • Endosomal Sorting Complexes Required for Transport / metabolism
  • Endosomes / genetics*
  • Endosomes / metabolism
  • Hyphae / genetics
  • Hyphae / growth & development
  • Hyphae / metabolism
  • Protein Transport / genetics*
  • RNA Transport / genetics*
  • RNA, Messenger / metabolism
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae / growth & development
  • Saccharomyces cerevisiae Proteins / genetics*
  • Saccharomyces cerevisiae Proteins / metabolism
  • Transport Vesicles / genetics
  • Transport Vesicles / metabolism
  • Ustilago / genetics*
  • Ustilago / growth & development
  • rab GTP-Binding Proteins / genetics

Substances

  • DID2 protein, S cerevisiae
  • Endosomal Sorting Complexes Required for Transport
  • RNA, Messenger
  • Saccharomyces cerevisiae Proteins
  • rab7 protein
  • Cathepsin A
  • PRC1 protein, S cerevisiae
  • rab GTP-Binding Proteins

Grant support

The work was funded by grants from the Deutsche Forschungsgemeinschaft to MF (FE 448/7-1, CRC1208 and CEPLAS EXC1028) as well as by the graduate school iGRAD MOI. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.