Golgi enzymes do not cycle through the endoplasmic reticulum during protein secretion or mitosis

Mol Biol Cell. 2017 Jan 1;28(1):141-151. doi: 10.1091/mbc.E16-08-0560. Epub 2016 Nov 2.

Abstract

Golgi-specific sialyltransferase (ST) expressed as a chimera with the rapamycin-binding domain of mTOR, FRB, relocates to the endoplasmic reticulum (ER) in cells exposed to rapamycin that also express invariant chain (Ii)-FKBP in the ER. This result has been taken to indicate that Golgi-resident enzymes cycle to the ER constitutively. We show that ST-FRB is trapped in the ER even without Ii-FKBP upon rapamycin addition. This is because ER-Golgi-cycling FKBP proteins contain a C-terminal KDEL-like sequence, bind ST-FRB in the Golgi, and are transported together back to the ER by KDEL receptor-mediated retrograde transport. Moreover, depletion of KDEL receptor prevents trapping of ST-FRB in the ER by rapamycin. Thus ST-FRB cycles artificially by binding to FKBP domain-containing proteins. In addition, Golgi-specific O-linked glycosylation of a resident ER protein occurs only upon artificial fusion of Golgi membranes with ER. Together these findings support the consensus view that there is no appreciable mixing of Golgi-resident enzymes with ER under normal conditions.

MeSH terms

  • Animals
  • Biological Transport
  • COS Cells
  • Chlorocebus aethiops
  • Endoplasmic Reticulum / metabolism*
  • Golgi Apparatus / metabolism*
  • Golgi Apparatus / physiology
  • HeLa Cells
  • Humans
  • Intracellular Membranes / metabolism
  • Mitosis / physiology
  • Protein Domains
  • Protein Translocation Systems
  • Protein Transport / physiology*
  • Receptors, Peptide / metabolism
  • Sialyltransferases / metabolism
  • Sirolimus
  • TOR Serine-Threonine Kinases

Substances

  • KDEL receptor
  • Protein Translocation Systems
  • Receptors, Peptide
  • Sialyltransferases
  • TOR Serine-Threonine Kinases
  • Sirolimus