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DNA supercoiling-induced shapes alter minicircle hydrodynamic properties

DNA in cells is organized in negatively supercoiled loops. The resulting torsional and bending strain allows DNA to adopt a surprisingly wide variety of 3-D shapes. This interplay between negative supercoiling, looping, and shape influences how DNA is stored, replicated, transcribed, repaired, and l...

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Autores principales: Waszkiewicz, Radost, Ranasinghe, Maduni, Fogg, Jonathan M, Catanese, Daniel J, Ekiel-Jeżewska, Maria L, Lisicki, Maciej, Demeler, Borries, Zechiedrich, Lynn, Szymczak, Piotr
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10164573/
https://www.ncbi.nlm.nih.gov/pubmed/36971110
http://dx.doi.org/10.1093/nar/gkad183
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author Waszkiewicz, Radost
Ranasinghe, Maduni
Fogg, Jonathan M
Catanese, Daniel J
Ekiel-Jeżewska, Maria L
Lisicki, Maciej
Demeler, Borries
Zechiedrich, Lynn
Szymczak, Piotr
author_facet Waszkiewicz, Radost
Ranasinghe, Maduni
Fogg, Jonathan M
Catanese, Daniel J
Ekiel-Jeżewska, Maria L
Lisicki, Maciej
Demeler, Borries
Zechiedrich, Lynn
Szymczak, Piotr
author_sort Waszkiewicz, Radost
collection PubMed
description DNA in cells is organized in negatively supercoiled loops. The resulting torsional and bending strain allows DNA to adopt a surprisingly wide variety of 3-D shapes. This interplay between negative supercoiling, looping, and shape influences how DNA is stored, replicated, transcribed, repaired, and likely every other aspect of DNA activity. To understand the consequences of negative supercoiling and curvature on the hydrodynamic properties of DNA, we submitted 336 bp and 672 bp DNA minicircles to analytical ultracentrifugation (AUC). We found that the diffusion coefficient, sedimentation coefficient, and the DNA hydrodynamic radius strongly depended on circularity, loop length, and degree of negative supercoiling. Because AUC cannot ascertain shape beyond degree of non-globularity, we applied linear elasticity theory to predict DNA shapes, and combined these with hydrodynamic calculations to interpret the AUC data, with reasonable agreement between theory and experiment. These complementary approaches, together with earlier electron cryotomography data, provide a framework for understanding and predicting the effects of supercoiling on the shape and hydrodynamic properties of DNA.
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spelling pubmed-101645732023-05-08 DNA supercoiling-induced shapes alter minicircle hydrodynamic properties Waszkiewicz, Radost Ranasinghe, Maduni Fogg, Jonathan M Catanese, Daniel J Ekiel-Jeżewska, Maria L Lisicki, Maciej Demeler, Borries Zechiedrich, Lynn Szymczak, Piotr Nucleic Acids Res Structural Biology DNA in cells is organized in negatively supercoiled loops. The resulting torsional and bending strain allows DNA to adopt a surprisingly wide variety of 3-D shapes. This interplay between negative supercoiling, looping, and shape influences how DNA is stored, replicated, transcribed, repaired, and likely every other aspect of DNA activity. To understand the consequences of negative supercoiling and curvature on the hydrodynamic properties of DNA, we submitted 336 bp and 672 bp DNA minicircles to analytical ultracentrifugation (AUC). We found that the diffusion coefficient, sedimentation coefficient, and the DNA hydrodynamic radius strongly depended on circularity, loop length, and degree of negative supercoiling. Because AUC cannot ascertain shape beyond degree of non-globularity, we applied linear elasticity theory to predict DNA shapes, and combined these with hydrodynamic calculations to interpret the AUC data, with reasonable agreement between theory and experiment. These complementary approaches, together with earlier electron cryotomography data, provide a framework for understanding and predicting the effects of supercoiling on the shape and hydrodynamic properties of DNA. Oxford University Press 2023-03-27 /pmc/articles/PMC10164573/ /pubmed/36971110 http://dx.doi.org/10.1093/nar/gkad183 Text en © The Author(s) 2023. Published by Oxford University Press on behalf of Nucleic Acids Research. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Structural Biology
Waszkiewicz, Radost
Ranasinghe, Maduni
Fogg, Jonathan M
Catanese, Daniel J
Ekiel-Jeżewska, Maria L
Lisicki, Maciej
Demeler, Borries
Zechiedrich, Lynn
Szymczak, Piotr
DNA supercoiling-induced shapes alter minicircle hydrodynamic properties
title DNA supercoiling-induced shapes alter minicircle hydrodynamic properties
title_full DNA supercoiling-induced shapes alter minicircle hydrodynamic properties
title_fullStr DNA supercoiling-induced shapes alter minicircle hydrodynamic properties
title_full_unstemmed DNA supercoiling-induced shapes alter minicircle hydrodynamic properties
title_short DNA supercoiling-induced shapes alter minicircle hydrodynamic properties
title_sort dna supercoiling-induced shapes alter minicircle hydrodynamic properties
topic Structural Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10164573/
https://www.ncbi.nlm.nih.gov/pubmed/36971110
http://dx.doi.org/10.1093/nar/gkad183
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