Nuclear export competence of pre-40S subunits in fission yeast requires the ribosomal protein Rps2

Ribosome biogenesis is an evolutionarily conserved pathway that requires ribosomal and nonribosomal proteins. Here, we investigated the role of the ribosomal protein S2 (Rps2) in fission yeast ribosome synthesis. As for many budding yeast ribosomal proteins, Rps2 was essential for cell viability in fission yeast and the genetic depletion of Rps2 caused a complete inhibition of 40S ribosomal subunit production. The pattern of pre-rRNA processing upon depletion of Rps2 revealed a reduction of 27SA2 pre-rRNAs and the concomitant production of 21S rRNA precursors, consistent with a role for Rps2 in efficient cleavage at site A2 within the 32S pre-rRNA. Importantly, kinetics of pre-rRNA accumulation as determined by rRNA pulse-chases assays indicated that a small fraction of 35S precursors matured into 20S-containing particles, suggesting that most 40S precursors were rapidly degraded in the absence of Rps2. Analysis of steady-state RNA levels revealed that some pre-40S particles were produced in Rps2-depleted cells, but that these precursors were retained in the nucleolus. Our findings suggest a role for Rps2 in a mechanism that monitors pre-40S export competence.

• Publication year

  2008

• Venue

  Nucleic Acids Research

• Publication date

  2008-09-27

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1093/nar/gkn625PMID 18820293PMCID 2577348
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

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  2000cited by this paper
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  2000cited by this paper
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  1999cited by this paper
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  1998cited by this paper
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  1996cited by this paper
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  1994cited by this paper
• Thiamine-repressible expression vectors pREP and pRIP for fission yeast.

  1993cited by this paper
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  1990cited by this paper
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  1990cited by this paper
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  1990cited by this paper
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  1988cited by this paper
• Genomic sequencing.

  1984cited by this paper
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  1974cited by this paper
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