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Integration of tail-anchored proteins into the mitochondrial outer membrane does not require any known import components

J Cell Sci. 2008 Jun 15;121(Pt 12):1990-8. doi: 10.1242/jcs.024034. Epub 2008 May 21.

Abstract

Tail-anchored proteins form a distinct class of membrane proteins that are found in all intracellular membranes exposed to the cytosol. These proteins have a single membrane insertion sequence at their C-terminus and display a large N-terminal portion to the cytosol. Despite their importance for various cellular processes, the mechanisms by which these proteins are recognized at and inserted into their corresponding target membrane remained largely unclear. Here we address this issue and investigate the biogenesis of tail-anchored proteins residing in the mitochondrial outer membrane. To that goal we developed a highly specific assay to monitor the membrane insertion of the model tail-anchored protein Fis1. Using this assay, we show that in contrast to all other import pathways in yeast mitochondria, none of the import components at the outer membrane is involved in the insertion process of Fis1. Both the steady-state levels of Fis1 and its in vitro insertion into isolated mitochondria were unaffected when mitochondria mutated in known import factors were analyzed. Fis1 was inserted into lipid vesicles, and importantly, elevated ergosterol contents in these vesicles inhibited this insertion. Collectively, these results suggest that Fis1 is inserted into mitochondria in a novel pathway where the unique lipid composition of the mitochondrial outer membrane contributes to the selectivity of the process. Thus, this work demonstrates a novel role for lipids in the biogenesis of mitochondrial protein.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Biological Assay
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • Cell-Free System
  • Ergosterol / pharmacology
  • Membrane Lipids / chemistry
  • Membrane Lipids / metabolism
  • Mitochondrial Membranes / drug effects
  • Mitochondrial Membranes / metabolism*
  • Mitochondrial Precursor Protein Import Complex Proteins
  • Mitochondrial Proteins / genetics
  • Mitochondrial Proteins / metabolism*
  • Molecular Sequence Data
  • Protein Binding
  • Protein Transport / drug effects
  • Rabbits
  • Recombinant Fusion Proteins / analysis
  • Recombinant Fusion Proteins / genetics
  • Recombinant Fusion Proteins / metabolism
  • Saccharomyces cerevisiae
  • Saccharomyces cerevisiae Proteins / genetics
  • Saccharomyces cerevisiae Proteins / metabolism*

Substances

  • Carrier Proteins
  • FIS1 protein, S cerevisiae
  • Membrane Lipids
  • Mitochondrial Precursor Protein Import Complex Proteins
  • Mitochondrial Proteins
  • Recombinant Fusion Proteins
  • Saccharomyces cerevisiae Proteins
  • Ergosterol