Arginine methylation next to the PY-NLS modulates Transportin binding and nuclear import of FUS

EMBO J. 2012 Nov 14;31(22):4258-75. doi: 10.1038/emboj.2012.261. Epub 2012 Sep 11.

Abstract

Fused in sarcoma (FUS) is a nuclear protein that carries a proline-tyrosine nuclear localization signal (PY-NLS) and is imported into the nucleus via Transportin (TRN). Defects in nuclear import of FUS have been implicated in neurodegeneration, since mutations in the PY-NLS of FUS cause amyotrophic lateral sclerosis (ALS). Moreover, FUS is deposited in the cytosol in a subset of frontotemporal lobar degeneration (FTLD) patients. Here, we show that arginine methylation modulates nuclear import of FUS via a novel TRN-binding epitope. Chemical or genetic inhibition of arginine methylation restores TRN-mediated nuclear import of ALS-associated FUS mutants. The unmethylated arginine-glycine-glycine domain preceding the PY-NLS interacts with TRN and arginine methylation in this domain reduces TRN binding. Inclusions in ALS-FUS patients contain methylated FUS, while inclusions in FTLD-FUS patients are not methylated. Together with recent findings that FUS co-aggregates with two related proteins of the FET family and TRN in FTLD-FUS but not in ALS-FUS, our study provides evidence that these two diseases may be initiated by distinct pathomechanisms and implicates alterations in arginine methylation in pathogenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Active Transport, Cell Nucleus
  • Amino Acid Sequence
  • Amyotrophic Lateral Sclerosis / genetics
  • Amyotrophic Lateral Sclerosis / metabolism*
  • Arginine / metabolism*
  • Cell Nucleus / metabolism*
  • Frontotemporal Lobar Degeneration / metabolism
  • Gene Silencing
  • HeLa Cells
  • Humans
  • Karyopherins / genetics
  • Karyopherins / metabolism*
  • Methylation
  • Molecular Sequence Data
  • Nuclear Localization Signals / metabolism*
  • Proline / metabolism
  • Protein Binding
  • Protein-Arginine N-Methyltransferases / genetics
  • Protein-Arginine N-Methyltransferases / metabolism
  • RNA-Binding Protein FUS / genetics
  • RNA-Binding Protein FUS / metabolism*
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism
  • Signal Transduction
  • Tyrosine / metabolism

Substances

  • Karyopherins
  • Nuclear Localization Signals
  • RNA-Binding Protein FUS
  • Repressor Proteins
  • Tyrosine
  • Arginine
  • Proline
  • PRMT1 protein, human
  • Protein-Arginine N-Methyltransferases