Antagonism of Beclin 1-dependent autophagy by BCL-2 at the endoplasmic reticulum requires NAF-1

EMBO J. 2010 Feb 3;29(3):606-18. doi: 10.1038/emboj.2009.369. Epub 2009 Dec 10.

Abstract

In addition to mitochondria, BCL-2 is located at the endoplasmic reticulum (ER) where it is a constituent of several distinct complexes. Here, we identify the BCL-2-interacting protein at the ER, nutrient-deprivation autophagy factor-1 (NAF-1)-a bitopic integral membrane protein whose defective expression underlies the aetiology of the neurodegenerative disorder Wolfram syndrome 2 (WFS2). NAF-1 contains a two iron-two sulphur coordinating domain within its cytosolic region, which is necessary, but not sufficient for interaction with BCL-2. NAF-1 is displaced from BCL-2 by the ER-restricted BH3-only protein BIK and contributes to regulation of BIK-initiated autophagy, but not BIK-dependent activation of caspases. Similar to BCL-2, NAF-1 is found in association with the inositol 1,4,5-triphosphate receptor and is required for BCL-2-mediated depression of ER Ca(2+) stores. During nutrient deprivation as a physiological stimulus of autophagy, BCL-2 is known to function through inhibition of the autophagy effector and tumour suppressor Beclin 1. NAF-1 is required in this pathway for BCL-2 at the ER to functionally antagonize Beclin 1-dependent autophagy. Thus, NAF-1 is a BCL-2-associated co-factor that targets BCL-2 for antagonism of the autophagy pathway at the ER.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Apoptosis Regulatory Proteins / antagonists & inhibitors*
  • Apoptosis Regulatory Proteins / metabolism
  • Apoptosis Regulatory Proteins / physiology
  • Autophagy* / drug effects
  • Autophagy* / genetics
  • Autophagy* / physiology
  • Beclin-1
  • Caspases / metabolism
  • Cells, Cultured
  • DNA-Binding Proteins / antagonists & inhibitors
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • DNA-Binding Proteins / physiology*
  • Endoplasmic Reticulum / drug effects
  • Endoplasmic Reticulum / metabolism*
  • Endoplasmic Reticulum / physiology
  • Enzyme Activation / drug effects
  • Humans
  • Membrane Proteins / antagonists & inhibitors*
  • Membrane Proteins / metabolism
  • Membrane Proteins / physiology
  • Mitochondrial Proteins
  • Models, Biological
  • Molecular Sequence Data
  • Protein Binding / drug effects
  • Proto-Oncogene Proteins c-bcl-2 / metabolism
  • Proto-Oncogene Proteins c-bcl-2 / physiology*
  • RNA, Small Interfering / pharmacology
  • Signal Transduction / drug effects
  • Signal Transduction / genetics

Substances

  • Apoptosis Regulatory Proteins
  • BECN1 protein, human
  • BIK protein, human
  • Beclin-1
  • DNA-Binding Proteins
  • Membrane Proteins
  • Mitochondrial Proteins
  • Proto-Oncogene Proteins c-bcl-2
  • RNA, Small Interfering
  • TNIP1 protein, human
  • Caspases