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Secondary structure and domain architecture of the 23S and 5S rRNAs.

Petrov AS, Bernier CR, Hershkovits E, Xue Y, Waterbury CC, Hsiao C, Stepanov VG, Gaucher EA, Grover MA, Harvey SC, Hud NV, Wartell RM, Fox GE, Williams LD - Nucleic Acids Res. (2013)

Bottom Line: We partitioned the 23S rRNA into domains through analysis of molecular interactions, calculations of 2D folding propensities and compactness.The best domain model for the 23S rRNA contains seven domains, not six as previously ascribed.Domain 0 forms the core of the 23S rRNA, to which the other six domains are rooted.

View Article: PubMed Central - PubMed

Affiliation: School of Chemistry and Biochemistry, Georgia Institute of Technology, Atlanta, GA 30332, USA, Center for Ribosomal Origins and Evolution, Georgia Institute of Technology, Atlanta, GA 30332, USA, School of Chemical and Biomolecular Engineering, Georgia Institute of Technology, Atlanta, GA 30332, USA, Department of Biology and Biochemistry, University of Houston, Houston, TX 77204, USA and School of Biology, Georgia Institute of Technology, Atlanta, GA 30332, USA.

ABSTRACT
We present a de novo re-determination of the secondary (2°) structure and domain architecture of the 23S and 5S rRNAs, using 3D structures, determined by X-ray diffraction, as input. In the traditional 2° structure, the center of the 23S rRNA is an extended single strand, which in 3D is seen to be compact and double helical. Accurately assigning nucleotides to helices compels a revision of the 23S rRNA 2° structure. Unlike the traditional 2° structure, the revised 2° structure of the 23S rRNA shows architectural similarity with the 16S rRNA. The revised 2° structure also reveals a clear relationship with the 3D structure and is generalizable to rRNAs of other species from all three domains of life. The 2° structure revision required us to reconsider the domain architecture. We partitioned the 23S rRNA into domains through analysis of molecular interactions, calculations of 2D folding propensities and compactness. The best domain model for the 23S rRNA contains seven domains, not six as previously ascribed. Domain 0 forms the core of the 23S rRNA, to which the other six domains are rooted. Editable 2° structures mapped with various data are provided (http://apollo.chemistry.gatech.edu/RibosomeGallery).

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Loop E motifs: Helix 26a and Helix 95 of the 23S rRNA of E. coli. (a) The 2° structure and (b) the 3D structure of the rRNA that was traditionally represented as single-stranded, adapted from Leontis et al. (25,28). The symbols in the fragments of the 23S rRNA 2° structure represent non-Watson–Crick base pairs: circles correspond to the Watson–Crick edges, squares to the Hoogsteen edges, triangles to the sugar edges, the open symbols indicate trans basepairs and closed symbols, cis basepairs. (c) The 2° structure and (d) the 3D structure of the sarcin-ricin loop (Helix 95). A comparison the top and bottom panels illustrates the extent of 2° and 3D conservation of the loop E motif.
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gkt513-F3: Loop E motifs: Helix 26a and Helix 95 of the 23S rRNA of E. coli. (a) The 2° structure and (b) the 3D structure of the rRNA that was traditionally represented as single-stranded, adapted from Leontis et al. (25,28). The symbols in the fragments of the 23S rRNA 2° structure represent non-Watson–Crick base pairs: circles correspond to the Watson–Crick edges, squares to the Hoogsteen edges, triangles to the sugar edges, the open symbols indicate trans basepairs and closed symbols, cis basepairs. (c) The 2° structure and (d) the 3D structure of the sarcin-ricin loop (Helix 95). A comparison the top and bottom panels illustrates the extent of 2° and 3D conservation of the loop E motif.

Mentions: The projection of all base-pairing interactions onto 2° structurephylo (Figure 2) illustrates that the central single-stranded region is involved in an intense network of molecular interactions and is not single stranded. The two halves of the extended single-stranded region are seen to associate by contiguous base-pairing interactions. Nucleotides 1262–1270 are paired with nucleotides 2010–2017, to form what we call Helix 26a. Inspection of the 3D structure confirms Helix 26a (Figure 3a and b), which was inferred previously by Fox and Gutell (23,40) and by Leontis and Westhof (24). Mutational studies support the importance of Helix 26a in the 23S rRNA (41). The center of Helix 26a contains non-canonical base pairs (28) U1263-U1216 (Watson–Crick/Watson–Crick), A1264-A1215 (trans Sugar edge/Hoogsteen), A1265-A1214 (trans Hoogsteen/Hoogsteen); U1267-A1213 (trans Watson–Crick/Hoogsteen); A1268-G2012 (trans Hoogsteen/Sugar edge) and U1267-G1266 (cis Hoogsteen/Sugar edge) with G1266 forming a triple base pair with U1267 and A1213 (Figure 3a). The central non-canonical region is flanked by canonical Watson–Crick base pairs of A1262 with U2017, A1269 with U2011 and C1270 with G2010 (24,25).Figure 2.


Secondary structure and domain architecture of the 23S and 5S rRNAs.

Petrov AS, Bernier CR, Hershkovits E, Xue Y, Waterbury CC, Hsiao C, Stepanov VG, Gaucher EA, Grover MA, Harvey SC, Hud NV, Wartell RM, Fox GE, Williams LD - Nucleic Acids Res. (2013)

Loop E motifs: Helix 26a and Helix 95 of the 23S rRNA of E. coli. (a) The 2° structure and (b) the 3D structure of the rRNA that was traditionally represented as single-stranded, adapted from Leontis et al. (25,28). The symbols in the fragments of the 23S rRNA 2° structure represent non-Watson–Crick base pairs: circles correspond to the Watson–Crick edges, squares to the Hoogsteen edges, triangles to the sugar edges, the open symbols indicate trans basepairs and closed symbols, cis basepairs. (c) The 2° structure and (d) the 3D structure of the sarcin-ricin loop (Helix 95). A comparison the top and bottom panels illustrates the extent of 2° and 3D conservation of the loop E motif.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3753638&req=5

gkt513-F3: Loop E motifs: Helix 26a and Helix 95 of the 23S rRNA of E. coli. (a) The 2° structure and (b) the 3D structure of the rRNA that was traditionally represented as single-stranded, adapted from Leontis et al. (25,28). The symbols in the fragments of the 23S rRNA 2° structure represent non-Watson–Crick base pairs: circles correspond to the Watson–Crick edges, squares to the Hoogsteen edges, triangles to the sugar edges, the open symbols indicate trans basepairs and closed symbols, cis basepairs. (c) The 2° structure and (d) the 3D structure of the sarcin-ricin loop (Helix 95). A comparison the top and bottom panels illustrates the extent of 2° and 3D conservation of the loop E motif.
Mentions: The projection of all base-pairing interactions onto 2° structurephylo (Figure 2) illustrates that the central single-stranded region is involved in an intense network of molecular interactions and is not single stranded. The two halves of the extended single-stranded region are seen to associate by contiguous base-pairing interactions. Nucleotides 1262–1270 are paired with nucleotides 2010–2017, to form what we call Helix 26a. Inspection of the 3D structure confirms Helix 26a (Figure 3a and b), which was inferred previously by Fox and Gutell (23,40) and by Leontis and Westhof (24). Mutational studies support the importance of Helix 26a in the 23S rRNA (41). The center of Helix 26a contains non-canonical base pairs (28) U1263-U1216 (Watson–Crick/Watson–Crick), A1264-A1215 (trans Sugar edge/Hoogsteen), A1265-A1214 (trans Hoogsteen/Hoogsteen); U1267-A1213 (trans Watson–Crick/Hoogsteen); A1268-G2012 (trans Hoogsteen/Sugar edge) and U1267-G1266 (cis Hoogsteen/Sugar edge) with G1266 forming a triple base pair with U1267 and A1213 (Figure 3a). The central non-canonical region is flanked by canonical Watson–Crick base pairs of A1262 with U2017, A1269 with U2011 and C1270 with G2010 (24,25).Figure 2.

Bottom Line: We partitioned the 23S rRNA into domains through analysis of molecular interactions, calculations of 2D folding propensities and compactness.The best domain model for the 23S rRNA contains seven domains, not six as previously ascribed.Domain 0 forms the core of the 23S rRNA, to which the other six domains are rooted.

View Article: PubMed Central - PubMed

Affiliation: School of Chemistry and Biochemistry, Georgia Institute of Technology, Atlanta, GA 30332, USA, Center for Ribosomal Origins and Evolution, Georgia Institute of Technology, Atlanta, GA 30332, USA, School of Chemical and Biomolecular Engineering, Georgia Institute of Technology, Atlanta, GA 30332, USA, Department of Biology and Biochemistry, University of Houston, Houston, TX 77204, USA and School of Biology, Georgia Institute of Technology, Atlanta, GA 30332, USA.

ABSTRACT
We present a de novo re-determination of the secondary (2°) structure and domain architecture of the 23S and 5S rRNAs, using 3D structures, determined by X-ray diffraction, as input. In the traditional 2° structure, the center of the 23S rRNA is an extended single strand, which in 3D is seen to be compact and double helical. Accurately assigning nucleotides to helices compels a revision of the 23S rRNA 2° structure. Unlike the traditional 2° structure, the revised 2° structure of the 23S rRNA shows architectural similarity with the 16S rRNA. The revised 2° structure also reveals a clear relationship with the 3D structure and is generalizable to rRNAs of other species from all three domains of life. The 2° structure revision required us to reconsider the domain architecture. We partitioned the 23S rRNA into domains through analysis of molecular interactions, calculations of 2D folding propensities and compactness. The best domain model for the 23S rRNA contains seven domains, not six as previously ascribed. Domain 0 forms the core of the 23S rRNA, to which the other six domains are rooted. Editable 2° structures mapped with various data are provided (http://apollo.chemistry.gatech.edu/RibosomeGallery).

Show MeSH