Accumulation of H/ACA snoRNPs depends on the integrity of the conserved central domain of the RNA-binding protein Nhp2p

Nucleic Acids Res. 2001 Jul 1;29(13):2733-46. doi: 10.1093/nar/29.13.2733.

Abstract

Box H/ACA small nucleolar ribonucleoprotein particles (H/ACA snoRNPs) play key roles in the synthesis of eukaryotic ribosomes. How box H/ACA snoRNPs are assembled remains unknown. Here we show that yeast Nhp2p, a core component of these particles, directly binds RNA. In vitro, Nhp2p interacts with high affinity with RNAs containing irregular stem-loop structures but shows weak affinity for poly(A), poly(C) or for double-stranded RNAs. The central region of Nhp2p is believed to function as an RNA-binding domain, since it is related to motifs found in various RNA-binding proteins. Removal of two amino acids that shortens a putative beta-strand element within Nhp2p central domain impairs the ability of the protein to interact with H/ACA snoRNAs in cell extracts. In vivo, this deletion prevents cell viability and leads to a strong defect in the accumulation of H/ACA snoRNAs and Gar1p. These data suggest that proper direct binding of Nhp2p to H/ACA snoRNAs is required for the assembly of H/ACA snoRNPs and hence for the stability of some of their components. In addition, we show that converting a highly conserved glycine residue (G(59)) within Nhp2p central domain to glutamate significantly reduces cell growth at 30 and 37 degrees C. Remarkably, this modification affects the steady-state levels of H/ACA snoRNAs and the strength of Nhp2p association with these RNAs to varying degrees, depending on the nature of the H/ACA snoRNA. Finally, we show that the modified Nhp2p protein whose interaction with H/ACA snoRNAs is impaired cannot accumulate in the nucleolus, suggesting that only the assembled H/ACA snoRNP particles can be efficiently retained in the nucleolus.

MeSH terms

  • Amino Acid Substitution / genetics
  • Base Sequence
  • Binding, Competitive
  • Cell Nucleolus / metabolism
  • Conserved Sequence*
  • Fungal Proteins / chemistry*
  • Fungal Proteins / genetics
  • Fungal Proteins / metabolism*
  • Microscopy, Immunoelectron
  • Nuclear Proteins / chemistry*
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • Nucleic Acid Conformation
  • Protein Binding
  • Protein Structure, Tertiary
  • RNA / chemistry
  • RNA / genetics
  • RNA / metabolism
  • RNA, Fungal / chemistry
  • RNA, Fungal / genetics
  • RNA, Fungal / metabolism
  • RNA-Binding Proteins / chemistry*
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism*
  • Ribonucleoproteins, Small Nuclear*
  • Ribonucleoproteins, Small Nucleolar / chemistry
  • Ribonucleoproteins, Small Nucleolar / metabolism*
  • Saccharomyces cerevisiae Proteins*
  • Saccharomyces cerevisiae* / cytology
  • Saccharomyces cerevisiae* / genetics
  • Saccharomyces cerevisiae* / growth & development
  • Sequence Deletion / genetics
  • Substrate Specificity

Substances

  • Fungal Proteins
  • Nuclear Proteins
  • RNA, Fungal
  • RNA-Binding Proteins
  • Ribonucleoproteins, Small Nuclear
  • Ribonucleoproteins, Small Nucleolar
  • Saccharomyces cerevisiae Proteins
  • NHP2 protein, S cerevisiae
  • GAR1 protein, S cerevisiae
  • RNA