The tip of the iceberg: RNA-binding proteins with prion-like domains in neurodegenerative disease

Brain Res. 2012 Jun 26:1462:61-80. doi: 10.1016/j.brainres.2012.01.016. Epub 2012 Jan 21.

Abstract

Prions are self-templating protein conformers that are naturally transmitted between individuals and promote phenotypic change. In yeast, prion-encoded phenotypes can be beneficial, neutral or deleterious depending upon genetic background and environmental conditions. A distinctive and portable 'prion domain' enriched in asparagine, glutamine, tyrosine and glycine residues unifies the majority of yeast prion proteins. Deletion of this domain precludes prionogenesis and appending this domain to reporter proteins can confer prionogenicity. An algorithm designed to detect prion domains has successfully identified 19 domains that can confer prion behavior. Scouring the human genome with this algorithm enriches a select group of RNA-binding proteins harboring a canonical RNA recognition motif (RRM) and a putative prion domain. Indeed, of 210 human RRM-bearing proteins, 29 have a putative prion domain, and 12 of these are in the top 60 prion candidates in the entire genome. Startlingly, these RNA-binding prion candidates are inexorably emerging, one by one, in the pathology and genetics of devastating neurodegenerative disorders, including: amyotrophic lateral sclerosis (ALS), frontotemporal lobar degeneration with ubiquitin-positive inclusions (FTLD-U), Alzheimer's disease and Huntington's disease. For example, FUS and TDP-43, which rank 1st and 10th among RRM-bearing prion candidates, form cytoplasmic inclusions in the degenerating motor neurons of ALS patients and mutations in TDP-43 and FUS cause familial ALS. Recently, perturbed RNA-binding proteostasis of TAF15, which is the 2nd ranked RRM-bearing prion candidate, has been connected with ALS and FTLD-U. We strongly suspect that we have now merely reached the tip of the iceberg. We predict that additional RNA-binding prion candidates identified by our algorithm will soon surface as genetic modifiers or causes of diverse neurodegenerative conditions. Indeed, simple prion-like transfer mechanisms involving the prion domains of RNA-binding proteins could underlie the classical non-cell-autonomous emanation of neurodegenerative pathology from originating epicenters to neighboring portions of the nervous system. This article is part of a Special Issue entitled RNA-Binding Proteins.

Publication types

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

MeSH terms

  • Algorithms
  • Amyotrophic Lateral Sclerosis / genetics
  • Animals
  • Calmodulin-Binding Proteins / genetics
  • Calmodulin-Binding Proteins / physiology
  • DNA-Binding Proteins / metabolism
  • Frontotemporal Lobar Degeneration / genetics
  • Frontotemporal Lobar Degeneration / pathology
  • Humans
  • Neurodegenerative Diseases / genetics*
  • Neurodegenerative Diseases / metabolism
  • Prions / genetics*
  • Prions / metabolism
  • Prions / physiology
  • RNA-Binding Protein EWS
  • RNA-Binding Protein FUS / genetics
  • RNA-Binding Protein FUS / physiology
  • RNA-Binding Proteins / genetics*
  • RNA-Binding Proteins / metabolism
  • RNA-Binding Proteins / physiology
  • TATA-Binding Protein Associated Factors / genetics
  • TATA-Binding Protein Associated Factors / physiology

Substances

  • Calmodulin-Binding Proteins
  • DNA-Binding Proteins
  • EWSR1 protein, human
  • Prions
  • RNA-Binding Protein EWS
  • RNA-Binding Protein FUS
  • RNA-Binding Proteins
  • TAF15 protein, human
  • TATA-Binding Protein Associated Factors