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18S rRNA processing requires base pairings of snR30 H/ACA snoRNA to eukaryote-specific 18S sequences.

Fayet-Lebaron E, Atzorn V, Henry Y, Kiss T - EMBO J. (2009)

Bottom Line: Here, we provide biochemical and genetic evidence demonstrating that during pre-rRNA processing, two evolutionarily conserved sequence elements in the 3'-hairpin of snR30 base-pair with short pre-rRNA sequences located in the eukaryote-specific internal region of 18S rRNA.The newly discovered snR30-18S base-pairing interactions are essential for 18S rRNA production and they constitute a complex snoRNA target RNA transient structure that is novel to H/ACA RNAs.We also demonstrate that besides the 18S recognition motifs, the distal part of the 3'-hairpin of snR30 contains an additional snoRNA element that is essential for 18S rRNA processing and that functions most likely as a snoRNP protein-binding site.

View Article: PubMed Central - PubMed

Affiliation: Laboratoire de Biologie Moléculaire Eucaryote du CNRS, UMR5099, IFR109 CNRS, Université Paul Sabatier, Toulouse, France.

ABSTRACT
The H/ACA RNAs represent an abundant, evolutionarily conserved and functionally diverse class of non-coding RNAs. Many H/ACA RNAs direct pseudouridylation of rRNAs and snRNAs, while members of the rapidly growing group of 'orphan' H/ACA RNAs participate in pre-rRNA processing, telomere synthesis and probably, in other nuclear processes. The yeast snR30 'orphan' H/ACA snoRNA has long been known to function in the nucleolytic processing of 18S rRNA, but its molecular role remained unknown. Here, we provide biochemical and genetic evidence demonstrating that during pre-rRNA processing, two evolutionarily conserved sequence elements in the 3'-hairpin of snR30 base-pair with short pre-rRNA sequences located in the eukaryote-specific internal region of 18S rRNA. The newly discovered snR30-18S base-pairing interactions are essential for 18S rRNA production and they constitute a complex snoRNA target RNA transient structure that is novel to H/ACA RNAs. We also demonstrate that besides the 18S recognition motifs, the distal part of the 3'-hairpin of snR30 contains an additional snoRNA element that is essential for 18S rRNA processing and that functions most likely as a snoRNP protein-binding site.

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Functionally essential elements of yeast snR30. The 5′-terminal and internal hairpins (shown schematically) lack functionally important elements (Atzorn et al, 2004). Sequences binding either box H/ACA or snR30-specific proteins are in shaded boxes. The m1 and m2 18S recognition sequences are in open boxes.
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f7: Functionally essential elements of yeast snR30. The 5′-terminal and internal hairpins (shown schematically) lack functionally important elements (Atzorn et al, 2004). Sequences binding either box H/ACA or snR30-specific proteins are in shaded boxes. The m1 and m2 18S recognition sequences are in open boxes.

Mentions: Similarly to the antisense elements of H/ACA pseudouridylation guide RNAs, the m1 and m2 18S recognition motifs of snR30 are located on the opposite strands of an internal pseudouridylation loop-like structure of the 3′-terminal hairpin of the snoRNA. However, contrary to this obvious resemblance, there are fundamental structural differences between the interaction of pseudouridylation guide RNAs formed with their target sequences and the proposed association of snR30 with 18S rRNA. The antisense elements of H/ACA guide RNAs are located in the upper (distal) part of the pseudouridylation loop (Figure 1A), whereas the m1 and m2 elements of snR30/U17 snoRNAs occupy the lower (proximal) part of an internal loop of the 3′-hairpin (Figure 7). The pseudouridylation guide elements bind to contiguous rRNA sequences, whereas the m1 and m2 elements interact with two distantly located sequence motifs that are folded together by an evolutionarily conserved stem-loop structure of 18S/17S rRNAs (Alkemar and Nygard, 2006). Consequently, snR30/U17 forms a complex three-dimensional local structure with 18S/17S sequences that is novel to box H/ACA RNAs and according to our knowledge no similar interaction has been reported for other cellular RNAs either (Figure 3C).


18S rRNA processing requires base pairings of snR30 H/ACA snoRNA to eukaryote-specific 18S sequences.

Fayet-Lebaron E, Atzorn V, Henry Y, Kiss T - EMBO J. (2009)

Functionally essential elements of yeast snR30. The 5′-terminal and internal hairpins (shown schematically) lack functionally important elements (Atzorn et al, 2004). Sequences binding either box H/ACA or snR30-specific proteins are in shaded boxes. The m1 and m2 18S recognition sequences are in open boxes.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2664660&req=5

f7: Functionally essential elements of yeast snR30. The 5′-terminal and internal hairpins (shown schematically) lack functionally important elements (Atzorn et al, 2004). Sequences binding either box H/ACA or snR30-specific proteins are in shaded boxes. The m1 and m2 18S recognition sequences are in open boxes.
Mentions: Similarly to the antisense elements of H/ACA pseudouridylation guide RNAs, the m1 and m2 18S recognition motifs of snR30 are located on the opposite strands of an internal pseudouridylation loop-like structure of the 3′-terminal hairpin of the snoRNA. However, contrary to this obvious resemblance, there are fundamental structural differences between the interaction of pseudouridylation guide RNAs formed with their target sequences and the proposed association of snR30 with 18S rRNA. The antisense elements of H/ACA guide RNAs are located in the upper (distal) part of the pseudouridylation loop (Figure 1A), whereas the m1 and m2 elements of snR30/U17 snoRNAs occupy the lower (proximal) part of an internal loop of the 3′-hairpin (Figure 7). The pseudouridylation guide elements bind to contiguous rRNA sequences, whereas the m1 and m2 elements interact with two distantly located sequence motifs that are folded together by an evolutionarily conserved stem-loop structure of 18S/17S rRNAs (Alkemar and Nygard, 2006). Consequently, snR30/U17 forms a complex three-dimensional local structure with 18S/17S sequences that is novel to box H/ACA RNAs and according to our knowledge no similar interaction has been reported for other cellular RNAs either (Figure 3C).

Bottom Line: Here, we provide biochemical and genetic evidence demonstrating that during pre-rRNA processing, two evolutionarily conserved sequence elements in the 3'-hairpin of snR30 base-pair with short pre-rRNA sequences located in the eukaryote-specific internal region of 18S rRNA.The newly discovered snR30-18S base-pairing interactions are essential for 18S rRNA production and they constitute a complex snoRNA target RNA transient structure that is novel to H/ACA RNAs.We also demonstrate that besides the 18S recognition motifs, the distal part of the 3'-hairpin of snR30 contains an additional snoRNA element that is essential for 18S rRNA processing and that functions most likely as a snoRNP protein-binding site.

View Article: PubMed Central - PubMed

Affiliation: Laboratoire de Biologie Moléculaire Eucaryote du CNRS, UMR5099, IFR109 CNRS, Université Paul Sabatier, Toulouse, France.

ABSTRACT
The H/ACA RNAs represent an abundant, evolutionarily conserved and functionally diverse class of non-coding RNAs. Many H/ACA RNAs direct pseudouridylation of rRNAs and snRNAs, while members of the rapidly growing group of 'orphan' H/ACA RNAs participate in pre-rRNA processing, telomere synthesis and probably, in other nuclear processes. The yeast snR30 'orphan' H/ACA snoRNA has long been known to function in the nucleolytic processing of 18S rRNA, but its molecular role remained unknown. Here, we provide biochemical and genetic evidence demonstrating that during pre-rRNA processing, two evolutionarily conserved sequence elements in the 3'-hairpin of snR30 base-pair with short pre-rRNA sequences located in the eukaryote-specific internal region of 18S rRNA. The newly discovered snR30-18S base-pairing interactions are essential for 18S rRNA production and they constitute a complex snoRNA target RNA transient structure that is novel to H/ACA RNAs. We also demonstrate that besides the 18S recognition motifs, the distal part of the 3'-hairpin of snR30 contains an additional snoRNA element that is essential for 18S rRNA processing and that functions most likely as a snoRNP protein-binding site.

Show MeSH