The complexity of human ribosome biogenesis revealed by systematic nucleolar screening of Pre-rRNA processing factors

Mol Cell. 2013 Aug 22;51(4):539-51. doi: 10.1016/j.molcel.2013.08.011.

Abstract

Mature ribosomal RNAs (rRNAs) are produced from polycistronic precursors following complex processing. Precursor (pre)-rRNA processing has been extensively characterized in yeast and was assumed to be conserved in humans. We functionally characterized 625 nucleolar proteins in HeLa cells and identified 286 required for processing, including 74 without a yeast homolog. For selected candidates, we demonstrated that pre-rRNA processing defects are conserved in different cell types (including primary cells), defects are not due to activation of a p53-dependent nucleolar tumor surveillance pathway, and they precede cell-cycle arrest and apoptosis. We also investigated the exosome's role in processing internal transcribed spacers (ITSs) and report that 3' end maturation of 18S rRNA involves EXOSC10/Rrp6, a yeast ITS2 processing factor. We conclude that human cells adopt unique strategies and recruit distinct trans-acting factors to carry out essential processing steps, posing fundamental implications for understanding ribosomopathies at the molecular level and developing effective therapeutic agents.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Apoptosis
  • Blotting, Northern
  • Cell Cycle Checkpoints
  • Cell Nucleolus / genetics*
  • Cell Nucleolus / metabolism
  • Cells, Cultured
  • Exosome Multienzyme Ribonuclease Complex / genetics
  • Exosome Multienzyme Ribonuclease Complex / metabolism
  • HCT116 Cells
  • HeLa Cells
  • Human Umbilical Vein Endothelial Cells / metabolism
  • Humans
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • RNA Precursors / genetics*
  • RNA Precursors / metabolism
  • RNA Processing, Post-Transcriptional*
  • RNA, Ribosomal / genetics*
  • RNA, Ribosomal / metabolism
  • Ribosomes / metabolism*
  • Trans-Activators / genetics
  • Trans-Activators / metabolism*

Substances

  • Nuclear Proteins
  • RNA Precursors
  • RNA, Ribosomal
  • Trans-Activators
  • Exosome Multienzyme Ribonuclease Complex