Distinct mechanisms controlling rough and smooth endoplasmic reticulum contacts with mitochondria

J Cell Sci. 2015 Aug 1;128(15):2759-65. doi: 10.1242/jcs.171132. Epub 2015 Jun 11.

Abstract

Gp78 (also known as AMFR), an endoplasmic-reticulum (ER)-associated protein degradation (ERAD) E3 ubiquitin ligase, localizes to mitochondria-associated ER and targets the mitofusin (Mfn1 and Mfn2) mitochondrial fusion proteins for degradation. Gp78 is also the cell surface receptor for autocrine motility factor (AMF), which prevents Gp78-dependent mitofusin degradation. Gp78 ubiquitin ligase activity promotes ER-mitochondria association and ER-mitochondria Ca(2+) coupling, processes that are reversed by AMF. Electron microscopy of HT-1080 fibrosarcoma cancer cells identified both smooth ER (SER; ∼8 nm) and wider (∼50-60 nm) rough ER (RER)-mitochondria contacts. Both short hairpin RNA (shRNA)-mediated knockdown of Gp78 (shGp78) and AMF treatment selectively reduced the extent of RER-mitochondria contacts without impacting on SER--mitochondria contacts. Concomitant small interfering RNA (siRNA)-mediated knockdown of Mfn1 increased SER-mitochondria contacts in both control and shGp78 cells, whereas knockdown of Mfn2 increased RER-mitochondria contacts selectively in shGp78 HT-1080 cells. The mitofusins therefore inhibit ER-mitochondria interaction. Regulation of close SER-mitochondria contacts by Mfn1 and of RER-mitochondria contacts by AMF-sensitive Gp78-mediated degradation of Mfn2 define new mechanisms that regulate ER-mitochondria interactions.

Keywords: AMF; Ca2+ coupling; ER-mitochondria contacts; Gp78 E3 ubiquitin ligase; Mitofusin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • COS Cells
  • Cell Line
  • Chlorocebus aethiops
  • Endoplasmic Reticulum, Rough / genetics*
  • Endoplasmic Reticulum, Rough / metabolism
  • Endoplasmic Reticulum, Smooth / genetics*
  • Endoplasmic Reticulum, Smooth / metabolism
  • Endoplasmic Reticulum-Associated Degradation / physiology
  • GTP Phosphohydrolases / genetics*
  • Humans
  • Mitochondria
  • Mitochondrial Membrane Transport Proteins / genetics*
  • Mitochondrial Proteins / genetics*
  • RNA Interference
  • RNA, Small Interfering
  • Receptors, Autocrine Motility Factor / genetics*

Substances

  • Mitochondrial Membrane Transport Proteins
  • Mitochondrial Proteins
  • RNA, Small Interfering
  • AMFR protein, human
  • Receptors, Autocrine Motility Factor
  • GTP Phosphohydrolases
  • MFN2 protein, human
  • Mfn1 protein, human