C/D box sRNA-guided 2′-O-methylation patterns of archaeal rRNA molecules

Dennis, Patrick P.; Tripp, Vanessa; Lui, Lauren M.; Lowe, Todd M.; Randau, Lennart

doi:10.1186/s12864-015-1839-z

Cited by 36 publications

(62 citation statements)

References 41 publications

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“…The acceptance of variations in the boxC′ and boxD′ motifs that are involved in k‐loop formation fits to the observed higher degree of conservation of boxC and boxD elements among the 61 S. acidocaldarius C/D box sRNAs. However, the nucleotides of the boxC′ and boxD′ motifs that form the two GA base pairs in the k‐loop are also highly conserved (Dennis et al ., ). Northern Blot signals were not observed for C/D box sRNA Sac‐sR121* k‐turn mutants and GA base pair mutants of the k‐loop, which might indicate that k‐turn and k‐loop formation is crucial for C/D box sRNA stability.…”

Section: Resultsmentioning

confidence: 97%

“…In addition, rRNA folding may be influenced as several C/D box sRNAs exist that target nucleotides that are apart in the rRNA sequence but close in the rRNA secondary structure. Thus, C/D box s(no)RNAs have been suggested to act as RNA chaperones (Herschlag et al, 1993;Steitz and Tycowski, 1995;Gaspin et al, 2000;Helm, 2006;Watkins and Bohnsack, 2012;Dennis et al, 2015;Polikanov et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

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Plasticity of archaeal C/D box sRNA biogenesis

Tripp

Martin

Orell

et al. 2016

Molecular Microbiology

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SummaryArchaeal and eukaryotic organisms contain sets of C/D box s(no)RNAs with guide sequences that determine ribose 2 0 -O-methylation sites of target RNAs. The composition of these C/D box sRNA sets is highly variable between organisms and results in varying RNA modification patterns which are important for ribosomal RNA folding and stability. Little is known about the genomic organization of C/D box sRNA genes in archaea. Here, we aimed to obtain first insights into the biogenesis of these archaeal C/D box sRNAs and analyzed the genetic context of more than 300 archaeal sRNA genes. We found that the majority of these genes do not possess independent promoters but are rather located at positions that allow for co-transcription with neighboring genes and their start or stop codons were frequently incorporated into the conserved boxC and D motifs. The biogenesis of plasmidencoded C/D box sRNA variants was analyzed in vivo in Sulfolobus acidocaldarius. It was found that C/D box sRNA maturation occurs independent of their genetic context and relies solely on the presence of intact RNA kink-turn structures. The observed plasticity of C/D box sRNA biogenesis is suggested to enable their accelerated evolution and, consequently, allow for adjustments of the RNA modification landscape.

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Section: Resultsmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 99%

Plasticity of archaeal C/D box sRNA biogenesis

Tripp

Martin

Orell

et al. 2016

Molecular Microbiology

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“…2ʹ‐ O ‐methylation impairs phosphodiester bond cleavage resulting from the nucleophilic attack of a deprotonated 2ʹ OH group. Archaeal 2ʹ‐ O ‐methylations are usually introduced via C/D box sRNAs, or to a lesser degree, H/ACA box sRNAs, and elevated levels of these guide RNAs have been observed for hyperthermophiles . Individual C/D box sRNAs are characterized by two pairs of conserved C box (C and Cʹ: 5ʹ‐RUGAUGA‐3ʹ) and D box (D and Dʹ: 5ʹ‐CUGA‐3ʹ) sequences that flank unstructured guide sequences.…”

Section: Rna Modificationsmentioning

confidence: 99%

“…The sRNAs guide a ribonucleoprotein (RNP) complex consisting of L7Ae, Nop56/58 (also called Nop5), and fibrillarin subunits to their RNA targets, and the methyltransferase fibrillarin introduces the 2ʹ‐ O ‐methylation modification 5 nt upstream of the first complementary base of the D or Dʹ box sequence . RNA‐seq analyses of the small RNomes of hyperthermophilic archaea (e.g., Methanopyrus kandleri, Nanoarchaeum equitans , and Thermococcus kodakarensis ) have identified large numbers of C/D box sRNAs with different guides, which were used to map potential methylation sites in the most prominent rRNA targets . Methylation hotspots were identified in core regions of the ribosome, at the interface between the small and large ribosomal subunits and at sites of RNA–RNA interaction.…”

Section: Rna Modificationsmentioning

confidence: 99%

RNA stabilization in hyperthermophilic archaea

Gomes-Filho

Randau

2019

Annals of the New York Academy of Sciences

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Analyses of the RNA metabolism of hyperthermophilic archaea highlight the efficiency of regulatory RNAs and RNA‐guided processes at extreme temperatures. These organisms must overcome the intrinsic thermolability of RNAs. Elevated levels of RNA modifications and structured GC‐rich regions are observed for many universal noncoding RNA families. Guide RNAs are often protected from degradation by their presence within ribonucleoprotein complexes. Modification and ligation of RNA termini can be employed to impair exonucleolytic degradation. Finally, antisense strand transcription promotes the formation of RNA duplexes and can be used to stabilize RNA regions. In our review, we provide examples of these RNA stabilization mechanisms that have been observed in hyperthermophilic archaeal model organisms.

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“…Recently, 489 C/D RNAs were compiled from the RNA-Seq data from seven archaea, and 719 guide-rRNA interactions were predicted (39). Analysis of this large dataset showed that 57.8% of the spacers are 12 nt long (Fig.…”

Section: Discussionmentioning

confidence: 99%

Box C/D guide RNAs recognize a maximum of 10 nt of substrates

Yang

Lin

2016

Proc. Natl. Acad. Sci. U.S.A.

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Box C/D RNAs guide site-specific 2′-O-methylation of RNAs in archaea and eukaryotes. The spacer regions between boxes C to D′ and boxes C′ to D contain the guide sequence that can form a stretch of base pairs with substrate RNAs. The lengths of spacer regions and guide-substrate duplexes are variable among C/D RNAs. In a previously determined structure of C/D ribonucleoprotein (RNP), a 12-nt-long spacer forms 10 bp with the substrate. How spacers and guide-substrate duplexes of other lengths are accommodated remains unknown. Here we analyze how the lengths of spacers and guide-substrate duplexes affect the modification activity and determine three structures of C/D RNPs assembled with different spacers and substrates. We show that the guide can only form a duplex of a maximum of 10 bp with the substrate during modification. Slightly shorter duplexes are tolerated, but longer duplexes must be unwound to fit into a capped protein channel for modification. Spacers with <12 nucleotides are defective, mainly because they cannot load the substrate in the active conformation. For spacers with >12 nucleotides, the excessive unpaired sequences near the box C/C′ side are looped out. Our results provide insight into the substrate recognition mechanism of C/D RNA and refute the RNAswapped model for dimeric C/D RNP.B ox C/D RNAs are a large family of noncoding RNAs conserved in archaea and eukaryotes (1-3). The majority of these RNAs function as guides in site-specific 2′-O-methylation of ribosomal RNAs (rRNAs) and small nuclear RNAs (4-7). A few special members, including U3 and U14, small nucleolar RNAs are required for pre-rRNA processing and ribosome assembly. One of the most abundant modifications in rRNAs, 2′-O-methylated nucleotides cluster in functionally important regions and are believed to fine-tune ribosome structure and function (8)(9)(10)(11).Box C/D RNAs have a bipartite structure and contain the C (RUGAUGA; R is a purine) and D (CUGA) box motifs at two ends and the related C′ and D′ box motifs in the internal regions. Each pair of boxes C and D combine into a characteristic kink turn (K-turn) or K-loop structure (12-15). The spacer regions located between boxes D and C′ (D spacer) and between boxes D′ and C (D′ spacer) harbor the guide sequence. The guide sequence can potentially form 10-21 bp with complementary sequences in substrate RNAs and select the fifth nucleotide apart from box D′/D for modification (5).To form a functional ribonucleoprotein (RNP) enzyme, each C/D RNA associates with four core proteins [Snu13, fibrillarin (Nop1 in yeast), Nop56, and Nop58] in eukaryotes (16-23) and with three proteins (L7Ae, fibrillarin, and Nop5) in archaea (24). The homologous eukaryotic Nop56 and Nop58 proteins are replaced by a single protein, Nop5, in archaea. Fibrillarin is the catalyst that transfers a methyl group from S-adenosylmethionine to the target ribose (21, 25). The RNA-guided methylation activity has been reconstituted for archaeal C/D RNPs (24), but not yet for eukaryotic complexes (26).Structural st...

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C/D box sRNA-guided 2′-O-methylation patterns of archaeal rRNA molecules

Cited by 36 publications

References 41 publications

Plasticity of archaeal C/D box sRNA biogenesis

Plasticity of archaeal C/D box sRNA biogenesis

RNA stabilization in hyperthermophilic archaea

Box C/D guide RNAs recognize a maximum of 10 nt of substrates

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