The stem-loop binding protein stimulates histone translation at an early step in the initiation pathway

B. Gorgoni, Stuart C Andrews, A. Schaller, D. Schümperli, K. Gray, Berndt Marino Muller

Research output: Contribution to journalArticle

51 Citations (Scopus)

Abstract

Metazoan replication-dependent histone mRNAs do not have a poly(A) tail but end instead in a conserved stem-loop structure. Efficient translation of these mRNAs is dependent on the stem-loop binding protein (SLOP). Here we explore the mechanism by which SLBP stimulates translation in vertebrate cells, using the tethered function assay and analyzing protein-protein interactions. We show for the first time that translational stimulation by SLBP increases during oocyte maturation and that SLBP stimulates translation at the level of initiation. we demonstrate that SLBP can interact directly with subunit h of eIF3 and with Paip1; however, neither of these interactions is sufficient to mediate its effects on translation. We find that Xenopus SLBP1 functions primarily at an early stage in the cap-dependent initiation pathway, targeting small ribosomal subunit recruitment. Analysis of IRES-driven translation in Xenopus oocytes suggests that SLBP activity requires eIF4E. We propose a model in which a novel factor contacts eIF4E bound to the 5' cap and SLBP bound to the 3' end simultaneously, mediating formation of an alternative end-to-end complex.

Original languageEnglish
Pages (from-to)1030-1042
Number of pages12
JournalRNA
Volume11
Issue number7
DOIs
Publication statusPublished - Jul 2005

Keywords

  • histone mRNA
  • histone hairpin-binding protein (HBP)
  • translation initiation
  • oocyte maturation
  • translational control
  • poly(A) tail
  • MESSENGER-RNA EXPRESSION
  • CELL-CYCLE PROGRESSION
  • CAENORHABDITIS-ELEGANS
  • GENE-EXPRESSION
  • IN-VIVO
  • ENHANCES TRANSLATION
  • MEIOTIC MATURATION
  • OOCYTE MATURATION
  • 3-HYBRID SYSTEM
  • POLY(A) TAIL

Cite this

The stem-loop binding protein stimulates histone translation at an early step in the initiation pathway. / Gorgoni, B.; Andrews, Stuart C; Schaller, A.; Schümperli, D.; Gray, K.; Muller, Berndt Marino.

In: RNA , Vol. 11, No. 7, 07.2005, p. 1030-1042.

Research output: Contribution to journalArticle

Gorgoni, B, Andrews, SC, Schaller, A, Schümperli, D, Gray, K & Muller, BM 2005, 'The stem-loop binding protein stimulates histone translation at an early step in the initiation pathway', RNA , vol. 11, no. 7, pp. 1030-1042. https://doi.org/10.1261/rna.7281305
Gorgoni, B. ; Andrews, Stuart C ; Schaller, A. ; Schümperli, D. ; Gray, K. ; Muller, Berndt Marino. / The stem-loop binding protein stimulates histone translation at an early step in the initiation pathway. In: RNA . 2005 ; Vol. 11, No. 7. pp. 1030-1042.
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AB - Metazoan replication-dependent histone mRNAs do not have a poly(A) tail but end instead in a conserved stem-loop structure. Efficient translation of these mRNAs is dependent on the stem-loop binding protein (SLOP). Here we explore the mechanism by which SLBP stimulates translation in vertebrate cells, using the tethered function assay and analyzing protein-protein interactions. We show for the first time that translational stimulation by SLBP increases during oocyte maturation and that SLBP stimulates translation at the level of initiation. we demonstrate that SLBP can interact directly with subunit h of eIF3 and with Paip1; however, neither of these interactions is sufficient to mediate its effects on translation. We find that Xenopus SLBP1 functions primarily at an early stage in the cap-dependent initiation pathway, targeting small ribosomal subunit recruitment. Analysis of IRES-driven translation in Xenopus oocytes suggests that SLBP activity requires eIF4E. We propose a model in which a novel factor contacts eIF4E bound to the 5' cap and SLBP bound to the 3' end simultaneously, mediating formation of an alternative end-to-end complex.

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