Complementary sets of noncanonical base pairs mediate RNA helix packing in the group I intron active site

Strobel, Scott A.; Ortoleva-Donnelly, Lori; Ryder, Seán; Cate, J.H.D.; Moncoeur, Eileen

doi:10.1038/nsb0198-60

Cited by 110 publications

(102 citation statements)

References 38 publications

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“…1,2,6,14,65,66 Many interactions determine the structures and thermodynamic stabilities of internal loops with tandem GA pairs. The data here provide benchmarks to test computational approaches for understanding the relative importance of the various interactions and thus provide the power to predict structure, stability, and dynamics for other internal loops.…”

Section: Discussionmentioning

confidence: 99%

Stacking Effects on Local Structure in RNA: Changes in the Structure of Tandem GA Pairs when Flanking GC Pairs Are Replaced by isoG−isoC Pairs

et al. 2007

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The Watson-Crick like iGiC pair, with the amino and carbonyl groups transposed relative to the Watson-Crick GC pair, provides an expanded alphabet for understanding interactions that shape nucleic acid structure. Here, thermodynamic stabilities of tandem GA pairs flanked by iGiC pairs are reported along with the NMR structures of the the RNA self-complementary duplexes (GCiGGAiCGCA) 2 and (GGiCGAiGCCA) 2 . A sheared GA pairing forms in (GCiGGAiCGCA) 2 and an imino GA pairing forms in (GGiCGAiGCCA) 2 . The structures contrast with the formation of tandem imino and sheared GA pairs flanked by GC pairs in the RNA self-complementary duplexes (GCGGACGC) 2 and (GGCGAGCC) 2 , respectively. In both iGiC duplexes, WatsonCrick like hydrogen bonds are formed between iG and iC, and iGiC substitutions result in less favorable loop stability. The results provide benchmarks for testing computations of molecular interactions that shape RNA three-dimensional structure.

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Section: Discussionmentioning

confidence: 99%

Stacking Effects on Local Structure in RNA: Changes in the Structure of Tandem GA Pairs when Flanking GC Pairs Are Replaced by isoG−isoC Pairs

et al. 2007

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“…This large catalytic RNA leaves products with termini opposite to the HDV ribozyme and it has been shown that both the geometry and minor groove of the G d U wobble pair at the active site are important for positioning functional groups for RNA substrate recognition (Barfod and Cech 1989;Doudna et al 1989;Downs and Cech 1994;Knitt et al 1994;Cate and Doudna 1996;Strobel et al 1998;Adams et al 2004;Golden et al 2005). In addition, crystal (Cate and Doudna 1996) and NMR (Allain and Varani 1995;Kieft and Tinoco 1997) structures revealed that the active site G d U wobble pair, as well as tandem G d U wobble pairs in other parts of the ribozyme, FIGURE 1.…”

Section: Introductionmentioning

confidence: 99%

Mechanistic characterization of the HDV genomic ribozyme: The cleavage site base pair plays a structural role in facilitating catalysis

Cerrone-Szakal¹,

Chadalavada²,

Golden³

et al. 2008

RNA

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The hepatitis delta virus (HDV) ribozyme occurs in the genomic and antigenomic strands of the HDV RNA and within mammalian transcriptomes. Previous kinetic studies suggested that a wobble pair (is preferred at the cleavage site; however, the reasons for this are unclear. We conducted sequence comparisons, which indicated that while G d U is the most prevalent combination at the cleavage site, G-C occurs to a significant extent in genomic HDV isolates, and G d U, G-C, and A-U pairs are present in mammalian ribozymes. We analyzed the folding of genomic HDV ribozymes by free energy minimization and found that variants with purine-pyrimidine combinations at the cleavage site are predicted to form native structures while pyrimidine-purine combinations misfold, consistent with earlier kinetic data and sequence comparisons. To test whether the cleavage site base pair contributes to catalysis, we characterized the pH and Mg 2+ -dependence of reaction kinetics of fastfolding genomic HDV ribozymes with cleavage site base pair purine-pyrimidine combinations: G d U, A-U, G-C, and A C ribozyme as being more active with a wobble pair at the cleavage site than with no base pair at all. Overall, the data support a model in which the cleavage site base pair provides a structural role in catalysis and does not need to be a wobble pair.

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“…Four potential long-range RNA-RNA interactions (see inset in Fig. 2) appear to be exclusively found in the +P5ext introns, including interactions between (1) GAAA tetraloops in L5b and L9, and 11-nt receptors in P6 and J5/5a, respectively (Costa and Michel 1995;Ikawa et al 2000b), (2) the A-rich bulge and the P4 paired element (Cate et al 1996;Ikawa et al 2002), and (3) the highly conserved A in J4/5 that is involved in defining the universally conserved G·u wobble pair in P1 (Michel and Westhof 1990;OrtolevaDonnelly et al 1998;Strobel et al 1998). The GAAA/11-nt receptor interaction between L9 and the P5 region might, however, be replaced by other types of RNA-RNA contacts (e.g., Jaeger et al 1994;Lehnert et al 1996).…”

Section: Secondary Structure and Self-splicing Of Fungal S788 Intronsmentioning

confidence: 99%

Long-term evolution of the S788 fungal nuclear small subunit rRNA group I introns

Haugen¹,

Runge²,

Bhattacharya³

2004

RNA

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More than 1000 group I introns have been identified in fungal rDNA. Little is known, however, of the splicing and secondary structure evolution of these ribozymes. Here, we use a combination of comparative and biochemical methods to address the evolution and splicing of a vertically inherited group I intron found at position 788 in the fungal small subunit (S) rRNA. The ancestral state of the S788 intron contains a highly conserved core and an extended P5 domain typical of IC1 introns. In contrast, the more derived introns have lost most of P5, and have an accelerated divergence rate within the core region with three functionally important substitutions that unambiguously separate them from the ancestral pool. Of 14 S788 group I introns that were tested for splicing, five, all of the ancestral type, were able to self-splice and produced intron RNA circles in vitro. The more derived S788 introns did not self-splice, and potentially rely on fungal-specific factors to facilitate splicing. In summary, we demonstrate one possible fate of vertically inherited group I introns, the loss of secondary structure elements, lessened selective constraints in the intron core, and ultimately, dependence on host-mediated splicing.

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Complementary sets of noncanonical base pairs mediate RNA helix packing in the group I intron active site

Cited by 110 publications

References 38 publications

Stacking Effects on Local Structure in RNA: Changes in the Structure of Tandem GA Pairs when Flanking GC Pairs Are Replaced by isoG−isoC Pairs

Stacking Effects on Local Structure in RNA: Changes in the Structure of Tandem GA Pairs when Flanking GC Pairs Are Replaced by isoG−isoC Pairs

Mechanistic characterization of the HDV genomic ribozyme: The cleavage site base pair plays a structural role in facilitating catalysis

Long-term evolution of the S788 fungal nuclear small subunit rRNA group I introns

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