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Occurrence and stability of anion–π interactions between phosphate and nucleobases in functional RNA molecules

We present a systematic structural and energetic characterization of phosphate(OP)–nucleobase anion…π stacking interactions in RNAs. We observed OP–nucleobase stacking contacts in a variety of structural motifs other than regular helices and spanning broadly diverse sequence distances. Apart from th...

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Autores principales: Chawla, Mohit, Kalra, Kanav, Cao, Zhen, Cavallo, Luigi, Oliva, Romina
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9723503/
https://www.ncbi.nlm.nih.gov/pubmed/36416268
http://dx.doi.org/10.1093/nar/gkac1081
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author Chawla, Mohit
Kalra, Kanav
Cao, Zhen
Cavallo, Luigi
Oliva, Romina
author_facet Chawla, Mohit
Kalra, Kanav
Cao, Zhen
Cavallo, Luigi
Oliva, Romina
author_sort Chawla, Mohit
collection PubMed
description We present a systematic structural and energetic characterization of phosphate(OP)–nucleobase anion…π stacking interactions in RNAs. We observed OP–nucleobase stacking contacts in a variety of structural motifs other than regular helices and spanning broadly diverse sequence distances. Apart from the stacking between a phosphate and a guanine or a uracil two-residue upstream in specific U-turns, such interactions in RNA have been scarcely characterized to date. Our QM calculations showed an energy minimum at a distance between the OP atom and the nucleobase plane centroid slightly below 3 Å for all the nucleobases. By sliding the OP atom over the nucleobase plane we localized the optimal mutual positioning of the stacked moieties, corresponding to an energy minimum below -6 kcal•mol(−1), for all the nucleobases, consistently with the projections of the OP atoms over the different π-rings we observed in experimental occurrences. We also found that the strength of the interaction clearly correlates with its electrostatic component, pointing to it as the most relevant contribution. Finally, as OP–uracil and OP–guanine interactions represent together 86% of the instances we detected, we also proved their stability under dynamic conditions in model systems simulated by state-of-the art DFT-MD calculations.
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spelling pubmed-97235032022-12-07 Occurrence and stability of anion–π interactions between phosphate and nucleobases in functional RNA molecules Chawla, Mohit Kalra, Kanav Cao, Zhen Cavallo, Luigi Oliva, Romina Nucleic Acids Res Computational Biology We present a systematic structural and energetic characterization of phosphate(OP)–nucleobase anion…π stacking interactions in RNAs. We observed OP–nucleobase stacking contacts in a variety of structural motifs other than regular helices and spanning broadly diverse sequence distances. Apart from the stacking between a phosphate and a guanine or a uracil two-residue upstream in specific U-turns, such interactions in RNA have been scarcely characterized to date. Our QM calculations showed an energy minimum at a distance between the OP atom and the nucleobase plane centroid slightly below 3 Å for all the nucleobases. By sliding the OP atom over the nucleobase plane we localized the optimal mutual positioning of the stacked moieties, corresponding to an energy minimum below -6 kcal•mol(−1), for all the nucleobases, consistently with the projections of the OP atoms over the different π-rings we observed in experimental occurrences. We also found that the strength of the interaction clearly correlates with its electrostatic component, pointing to it as the most relevant contribution. Finally, as OP–uracil and OP–guanine interactions represent together 86% of the instances we detected, we also proved their stability under dynamic conditions in model systems simulated by state-of-the art DFT-MD calculations. Oxford University Press 2022-11-23 /pmc/articles/PMC9723503/ /pubmed/36416268 http://dx.doi.org/10.1093/nar/gkac1081 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of Nucleic Acids Research. https://creativecommons.org/licenses/by-nc/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Computational Biology
Chawla, Mohit
Kalra, Kanav
Cao, Zhen
Cavallo, Luigi
Oliva, Romina
Occurrence and stability of anion–π interactions between phosphate and nucleobases in functional RNA molecules
title Occurrence and stability of anion–π interactions between phosphate and nucleobases in functional RNA molecules
title_full Occurrence and stability of anion–π interactions between phosphate and nucleobases in functional RNA molecules
title_fullStr Occurrence and stability of anion–π interactions between phosphate and nucleobases in functional RNA molecules
title_full_unstemmed Occurrence and stability of anion–π interactions between phosphate and nucleobases in functional RNA molecules
title_short Occurrence and stability of anion–π interactions between phosphate and nucleobases in functional RNA molecules
title_sort occurrence and stability of anion–π interactions between phosphate and nucleobases in functional rna molecules
topic Computational Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9723503/
https://www.ncbi.nlm.nih.gov/pubmed/36416268
http://dx.doi.org/10.1093/nar/gkac1081
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