Rocaglates convert DEAD-box protein eIF4A into a sequence-selective translational repressor

Nature. 2016 Jun 23;534(7608):558-61. doi: 10.1038/nature17978. Epub 2016 Jun 15.

Abstract

Rocaglamide A (RocA) typifies a class of protein synthesis inhibitors that selectively kill aneuploid tumour cells and repress translation of specific messenger RNAs. RocA targets eukaryotic initiation factor 4A (eIF4A), an ATP-dependent DEAD-box RNA helicase; its messenger RNA selectivity is proposed to reflect highly structured 5' untranslated regions that depend strongly on eIF4A-mediated unwinding. However, rocaglate treatment may not phenocopy the loss of eIF4A activity, as these drugs actually increase the affinity between eIF4A and RNA. Here we show that secondary structure in 5' untranslated regions is only a minor determinant for RocA selectivity and that RocA does not repress translation by reducing eIF4A availability. Rather, in vitro and in cells, RocA specifically clamps eIF4A onto polypurine sequences in an ATP-independent manner. This artificially clamped eIF4A blocks 43S scanning, leading to premature, upstream translation initiation and reducing protein expression from transcripts bearing the RocA-eIF4A target sequence. In elucidating the mechanism of selective translation repression by this lead anti-cancer compound, we provide an example of a drug stabilizing sequence-selective RNA-protein interactions.

Publication types

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

MeSH terms

  • 5' Untranslated Regions / genetics
  • Adenosine Triphosphate / metabolism
  • Benzofurans / pharmacology*
  • DEAD-box RNA Helicases / chemistry
  • DEAD-box RNA Helicases / metabolism
  • Eukaryotic Initiation Factor-4A / chemistry
  • Eukaryotic Initiation Factor-4A / metabolism*
  • HEK293 Cells
  • Humans
  • Hydrolysis
  • Nucleic Acid Conformation
  • Nucleotide Motifs
  • Open Reading Frames / genetics
  • Peptide Chain Initiation, Translational / drug effects
  • Protein Binding / drug effects
  • Protein Biosynthesis / drug effects*
  • Protein Stability / drug effects
  • RNA, Messenger / chemistry
  • RNA, Messenger / genetics*
  • RNA, Messenger / metabolism*
  • RNA-Binding Proteins / chemistry
  • RNA-Binding Proteins / metabolism
  • Repressor Proteins / chemistry
  • Repressor Proteins / metabolism*
  • Substrate Specificity / drug effects
  • Thermodynamics

Substances

  • 5' Untranslated Regions
  • Benzofurans
  • RNA, Messenger
  • RNA-Binding Proteins
  • Repressor Proteins
  • rocaglamide
  • Adenosine Triphosphate
  • Eukaryotic Initiation Factor-4A
  • DEAD-box RNA Helicases