Divergent roles of ALS-linked proteins FUS/TLS and TDP-43 intersect in processing long pre-mRNAs

Nat Neurosci. 2012 Nov;15(11):1488-97. doi: 10.1038/nn.3230. Epub 2012 Sep 30.

Abstract

FUS/TLS (fused in sarcoma/translocated in liposarcoma) and TDP-43 are integrally involved in amyotrophic lateral sclerosis (ALS) and frontotemporal dementia. We found that FUS/TLS binds to RNAs from >5,500 genes in mouse and human brain, primarily through a GUGGU-binding motif. We identified a sawtooth-like binding pattern, consistent with co-transcriptional deposition of FUS/TLS. Depletion of FUS/TLS from the adult nervous system altered the levels or splicing of >950 mRNAs, most of which are distinct from RNAs dependent on TDP-43. Abundance of only 45 RNAs was reduced after depletion of either TDP-43 or FUS/TLS from mouse brain, but among these were mRNAs that were transcribed from genes with exceptionally long introns and that encode proteins that are essential for neuronal integrity. Expression levels of a subset of these were lowered after TDP-43 or FUS/TLS depletion in stem cell-derived human neurons and in TDP-43 aggregate-containing motor neurons in sporadic ALS, supporting a common loss-of-function pathway as one component underlying motor neuron death from misregulation of TDP-43 or FUS/TLS.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Adaptor Proteins, Signal Transducing
  • Amyotrophic Lateral Sclerosis / genetics
  • Amyotrophic Lateral Sclerosis / metabolism*
  • Amyotrophic Lateral Sclerosis / pathology
  • Animals
  • Autophagy-Related Proteins
  • Brain / metabolism
  • Brain / pathology
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism
  • Cell Line, Transformed
  • DNA-Binding Proteins / deficiency
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • Excitatory Amino Acid Transporter 2 / genetics
  • Excitatory Amino Acid Transporter 2 / metabolism
  • Female
  • Frontotemporal Dementia / genetics
  • Frontotemporal Dementia / metabolism*
  • Frontotemporal Dementia / pathology
  • Gene Expression Profiling
  • Gene Expression Regulation / genetics
  • Histone-Lysine N-Methyltransferase / metabolism
  • Humans
  • Immunoprecipitation
  • Kv Channel-Interacting Proteins / metabolism
  • Membrane Proteins / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Motor Neurons / metabolism
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism
  • Neural Cell Adhesion Molecules / metabolism
  • Neural Stem Cells / metabolism
  • Neurofilament Proteins / metabolism
  • Oligonucleotide Array Sequence Analysis
  • Protein Binding / genetics
  • Protein Structure, Tertiary / genetics
  • RNA Precursors / genetics
  • RNA Precursors / metabolism*
  • RNA Splicing / genetics
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism*
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism
  • RNA-Binding Protein FUS / deficiency
  • RNA-Binding Protein FUS / genetics
  • RNA-Binding Protein FUS / metabolism*
  • Shal Potassium Channels / metabolism
  • Spinal Cord / metabolism
  • Ubiquitin-Protein Ligases / metabolism
  • tau Proteins / genetics
  • tau Proteins / metabolism

Substances

  • Adaptor Proteins, Signal Transducing
  • Autophagy-Related Proteins
  • Carrier Proteins
  • Cell Cycle Proteins
  • DNA-Binding Proteins
  • Excitatory Amino Acid Transporter 2
  • KCNIP4 protein, human
  • Kv Channel-Interacting Proteins
  • Membrane Proteins
  • Nerve Tissue Proteins
  • Neural Cell Adhesion Molecules
  • Neurofilament Proteins
  • RNA Precursors
  • RNA, Messenger
  • RNA, Small Interfering
  • RNA-Binding Protein FUS
  • Shal Potassium Channels
  • UBQLN1 protein, human
  • tau Proteins
  • Histone-Lysine N-Methyltransferase
  • SMYD2 protein, human
  • Ubiquitin-Protein Ligases
  • parkin protein

Associated data

  • GEO/GSE40653