<i>Xenopus</i> U3 snoRNA docks on pre-rRNA through a novel base-pairing interaction

Borovjagin, Anton V.; Gerbi, Susan A.

doi:10.1261/rna.5256704

Cited by 30 publications

(40 citation statements)

References 48 publications

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“…In response to c-Myc or a heightened cellular proliferation rate, nucleolin levels can increase B4-fold (Sirri et al, 1997;Greasley et al, 2000). Nucleolin functions at an early step in precursor ribosomal RNA (rRNA) processing (Ginisty et al, 1998;Borovjagin and Gerbi, 2004), and disruption of nucleolin homologs in yeast cause unbalanced production of the large and small ribosome subunits (Kondo and Inouye, 1992;Lee et al, 1992;Gulli et al, 1995). Although the yeast strains lacking expression of the homologs are viable, they show severe defects in growth, strongly suggesting that knockouts (ko) of the mammalian protein will be lethal.…”

Section: Introductionmentioning

confidence: 99%

Nucleolin inhibits Hdm2 by multiple pathways leading to p53 stabilization

et al. 2006

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Section: Introductionmentioning

confidence: 99%

Nucleolin inhibits Hdm2 by multiple pathways leading to p53 stabilization

et al. 2006

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mentioning

confidence: 99%

“…Its 5Ј domain forms several base pair interactions with the 5Ј external transcribed spacer and the 18S part of the pre-rRNA. These intermolecular interactions define the positions of early cleavages (sites AЈ, A0, 1, and 2 in X. laevis and sites A0, A1, and A2 in yeast) (5,10,9,27,40,58,59,64). The 3Ј domain of U3 snoRNA contains the two anchoring sites for the core proteins, namely, the phylogenetically conserved CЈ/D and B/C box pairs (26,40,51,54).…”

mentioning

confidence: 99%

Analysis of Sequence and Structural Features That Identify the B/C Motif of U3 Small Nucleolar RNA as the Recognition Site for the Snu13p-Rrp9p Protein Pair

Cléry¹,

Senty-Ségault²,

Leclerc³

et al. 2007

Molecular and Cellular Biology

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The eukaryal Snu13p/15.5K protein binds K-turn motifs in U4 snRNA and snoRNAs. Two Snu13p/15.5K molecules bind the nucleolar U3 snoRNA required for the early steps of preribosomal processing. Binding of one molecule on the C/D motif allows association of proteins Nop1p, Nop56p, and Nop58p, whereas binding of the second molecule on the B/C motif allows Rrp9p recruitment. To understand how the Snu13p-Rrp9p pair recognizes the B/C motif, we first improved the identification of RNA determinants required for Snu13p binding by experiments using the systematic evolution of ligands by exponential enrichment. This demonstrated the importance of a U⅐U pair stacked on the sheared pairs and revealed a direct link between Snu13p affinity and the stability of helices I and II. Sequence and structure requirements for efficient association of Rrp9p on the B/C motif were studied in yeast cells by expression of variant U3 snoRNAs and immunoselection assays. A G-C pair in stem II, a G residue at position 1 in the bulge, and a short stem I were found to be required. The data identify the in vivo function of most of the conserved residues of the U3 snoRNA B/C motif. They bring important information to understand how different K-turn motifs can recruit different sets of proteins after Snu13p association.In eukaryotes, the 5.8S, 18S, and 25S (yeast)/28S (vertebrates) ribosomal RNAs (rRNAs) are transcribed by RNA polymerase I as a long precursor RNA (pre-rRNA) (for review, see reference 65). Mature rRNAs are then produced by an ordered series of cleavages, with simultaneous modifications of some of the bases and riboses (for reviews, see references 20 and 65). Several small nucleolar ribonucleoprotein particles (snoRNPs) containing a single small nucleolar RNA (snoRNA) and several proteins are involved in these maturation processes (for reviews, see references 2, 28, 31, 39, and 62). One of these RNPs (the U3 snoRNP) contains a highly conserved RNA and is essential for the early pre-rRNA cleavage steps (sites AЈ, A0, 1, 2, and 3 in Xenopus laevis [7,8,27] and sites A0, A1, and A2 in yeast [4,23,40,42]). These early steps are needed for 18S rRNA production (23,40,59). Most of the other snoRNPs direct and catalyze nucleotide modifications. The C/D box snoRNPs are responsible for 2Ј O methylations, whereas H/ACA snoRNPs catalyze pseudouridylations (for reviews, see references 2, 16, 28, 39, and 62). In spite of the presence of two C/D-like motifs (RUGAUGA/CUGA) in U3 snoRNA, no 2Ј O-methylation guiding activity was attributed to this RNA. Its 5Ј domain forms several base pair interactions with the 5Ј external transcribed spacer and the 18S part of the pre-rRNA. These intermolecular interactions define the positions of early cleavages (sites AЈ, A0, 1, and 2 in X. laevis and sites A0, A1, and A2 in yeast) (5,10,9,27,40,58,59,64). The

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“…The resulting 20S U3 snoRNA-protein particle is recruited to the pre-rRNA by protein-protein interactions (Perez-Fernandez et al 2011). After recruitment, formation of three U3-pre-rRNA duplexes is a prerequisite for the U3-dependent pre-rRNA cleavages at A 0 , A 1 , and A 2 that are essential for cellular growth: the U3-ETS duplex (Beltrame and Tollervey 1995), the U3-ETS2 duplex (Borovjagin and Gerbi 2004;Dutca et al 2011;Marmier-Gourrier et al 2011), and the U3-18S duplex ( Fig. 1A,B; Hughes et al 1987;Mereau et al 1997;Sharma and Tollervey 1999).…”

Section: Introductionmentioning

confidence: 99%

Imp3 unfolds stem structures in pre-rRNA and U3 snoRNA to form a duplex essential for small subunit processing

Shah¹,

Liu²,

Correll³

2013

RNA

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Eukaryotic ribosome biogenesis requires rapid hybridization between the U3 snoRNA and the pre-rRNA to direct cleavages at the A 0 , A 1 , and A 2 sites in pre-rRNA that liberate the small subunit precursor. The bases involved in hybridization of one of the three duplexes that U3 makes with pre-rRNA, designated the U3-18S duplex, are buried in conserved structures: box A/A ′ stem-loop in U3 snoRNA and helix 1 (H1) in the 18S region of the pre-rRNA. These conserved structures must be unfolded to permit the necessary hybridization. Previously, we reported that Imp3 and Imp4 promote U3-18S hybridization in vitro, but the mechanism by which these proteins facilitate U3-18S duplex formation remained unclear. Here, we directly addressed this question by probing base accessibility with chemical modification and backbone accessibility with ribonuclease activity of U3 and pre-rRNA fragments that mimic the secondary structure observed in vivo. Our results demonstrate that U3-18S hybridization requires only Imp3. Binding to each RNA by Imp3 provides sufficient energy to unfold both the 18S H1 and the U3 box A/A ′ stem structures. The Imp3 unfolding activity also increases accessibility at the U3-dependent A 0 and A 1 sites, perhaps signaling cleavage at these sites to generate the 5 ′ mature end of 18S. Imp4 destabilizes the U3-18S duplex to aid U3 release, thus differentiating the roles of these proteins. Protein-dependent unfolding of these structures may serve as a switch to block U3-pre-rRNA interactions until recruitment of Imp3, thereby preventing premature and inaccurate U3-dependent prerRNA cleavage and folding events in eukaryotic ribosome biogenesis.

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Xenopus U3 snoRNA docks on pre-rRNA through a novel base-pairing interaction

Cited by 30 publications

References 48 publications

Nucleolin inhibits Hdm2 by multiple pathways leading to p53 stabilization

Nucleolin inhibits Hdm2 by multiple pathways leading to p53 stabilization

Analysis of Sequence and Structural Features That Identify the B/C Motif of U3 Small Nucleolar RNA as the Recognition Site for the Snu13p-Rrp9p Protein Pair

Imp3 unfolds stem structures in pre-rRNA and U3 snoRNA to form a duplex essential for small subunit processing

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