TFG clusters COPII-coated transport carriers and promotes early secretory pathway organization

EMBO J. 2015 Mar 12;34(6):811-27. doi: 10.15252/embj.201489032. Epub 2015 Jan 13.

Abstract

In mammalian cells, cargo-laden secretory vesicles leave the endoplasmic reticulum (ER) en route to ER-Golgi intermediate compartments (ERGIC) in a manner dependent on the COPII coat complex. We report here that COPII-coated transport carriers traverse a submicron, TFG (Trk-fused gene)-enriched zone at the ER/ERGIC interface. The architecture of TFG complexes as determined by three-dimensional electron microscopy reveals the formation of flexible, octameric cup-like structures, which are able to self-associate to generate larger polymers in vitro. In cells, loss of TFG function dramatically slows protein export from the ER and results in the accumulation of COPII-coated carriers throughout the cytoplasm. Additionally, the tight association between ER and ERGIC membranes is lost in the absence of TFG. We propose that TFG functions at the ER/ERGIC interface to locally concentrate COPII-coated transport carriers and link exit sites on the ER to ERGIC membranes. Our findings provide a new mechanism by which COPII-coated carriers are retained near their site of formation to facilitate rapid fusion with neighboring ERGIC membranes upon uncoating, thereby promoting interorganellar cargo transport.

Keywords: COPII vesicle transport; intrinsic disorder; secretion; single particle electron microscopy.

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.

MeSH terms

  • Animals
  • Biological Transport / physiology
  • COP-Coated Vesicles / metabolism*
  • Cell Line
  • Chlorocebus aethiops
  • Circular Dichroism
  • Electroporation
  • Endoplasmic Reticulum / metabolism*
  • Fluorescence Recovery After Photobleaching
  • Fluorescent Antibody Technique
  • Humans
  • Immunohistochemistry
  • Microscopy, Electron
  • Multiprotein Complexes / metabolism*
  • Proteins / metabolism*
  • RNA, Small Interfering / genetics
  • Secretory Pathway / physiology*
  • trans-Golgi Network / metabolism*

Substances

  • Multiprotein Complexes
  • Proteins
  • RNA, Small Interfering
  • TFG protein, human