Supercoiled DNA Minicircles under Double-strand Breaks

Ye-Peng Qiao; Chun-Lai Ren

doi:10.1007/s10118-024-3106-8

Your Location：

Home >

Browse articles >

Supercoiled DNA Minicircles under Double-strand Breaks

RESEARCH ARTICLE | Updated：2024-08-27

- Supercoiled DNA Minicircles under Double-strand Breaks
- Supercoiled DNA Minicircles under Double-strand Breaks
- 高分子科学（英文版） 2024年42卷第9期页码：1353-1359
- Affiliations：
  
  National Laboratory of Solid State Microstructures and Department of Physics, Collaborative Innovation Center of Advanced Microstructures, Nanjing University, Nanjing 210093, China
- Author bio：
  
  chunlair@nju.edu.cn
- Funds：
  
  This work was financially supported by the National Natural Science Foundation of China (Nos. 12274212, 12347102 and 12174184). We are grateful to the High Performance Computing Center (HPCC) of Nanjing University for the numerical calculations in this study on its blade cluster system.;Electronic supplementary information (ESI) is available free of charge in the online version of this article at http://doi.org/10.1007/s10118-024-3106-8.
- DOI：10.1007/s10118-024-3106-8
  中图分类号：
- 收稿：2024-01-23，
  
  修回：2024-02-09，
  
  录用：2024-02-19，
  
  网络首发：2024-03-29，
  
  纸质出版：2024-09-01
- Accepted：
Scan QR Code
Qiao, Y. P.; Ren, C. L. Supercoiled DNA minicircles under double-strand breaks. Chinese J. Polym. Sci. 2024, 42, 1353–1359

Ye-Peng Qiao, Chun-Lai Ren. Supercoiled DNA Minicircles under Double-strand Breaks[J]. Chinese Journal of Polymer Science, 2024, 42(9): 1353-1359.
Qiao, Y. P.; Ren, C. L. Supercoiled DNA minicircles under double-strand breaks. Chinese J. Polym. Sci. 2024, 42, 1353–1359 DOI： 10.1007/s10118-024-3106-8.

Ye-Peng Qiao, Chun-Lai Ren. Supercoiled DNA Minicircles under Double-strand Breaks[J]. Chinese Journal of Polymer Science, 2024, 42(9): 1353-1359. DOI： 10.1007/s10118-024-3106-8.

摘要

Understanding how supercoiled DNA releases intramolecular stress is essential for its functional realization. We employed MD simulations based on the oxDNA2 model to investigate the dynamics of supercoiled minicircular DNA under double-strand breaks with two fixed endpoints

uncovering the molecular mechanism underlying the relaxation process.

Abstract

Understanding how supercoiled DNA releases intramolecular stress is essential for its functional realization. However

the molecular mechanism underlying the relaxation process remains insufficiently explored. Here we employed MD simulations based on the oxDNA2 model to investigate the relaxation process of a 336-base pair supercoiled minicircular DNA under double-strand breaks with two fixed endpoints. Our simulations show that the conformational changes in the DNA occur continuously

with intramolecular stress release happening abruptly only when the DNA chain traverses the breakage site. The relaxation process is influenced not only by the separation distance between the fixed ends but also their angle. Importantly

we observe an inhibitory effect on the relaxation characterized by small angles

where short terminal loops impede DNA conformational adjustments

preserving the supercoiled structure. These findings elucidate the intricate interplay between DNA conformational change

DNA motion and intramolecular stress release

shedding light on the mechanisms governing the relaxation of supercoiled DNA at the molecular level.

关键词

Keywords

references

Forth, S.; Sheinin, M. Y.; Inman, J.; Wang, M. D. Torque measurement at the single-molecule level. Annu. Rev. Biophys. 2013 , 42 , 583−604..

Kouzine, F.; Levens, D. The texture of chromatin. Cell 2019 , 179 , 579−581..

Ma, J.; Wang, M. D. DNA supercoiling during transcription. Biophys. Rev. 2016 , 8 , 75−87..

Dunaway, M.; Ostrander, E. A. Local domains of supercoiling activate a eukaryotic promoter in vivo. Nature 1993, 361 , 746-748..

Ding, Y.; Manzo, C.; Fulcrand, G.; Leng, F.; Dunlap, D.; Finzi, L. DNA supercoiling: a regulatory signal for the lambda repressor. Proc. Natl. Acad. Sci. U. S. A. 2014 , 111 , 15402−7..

Wang, G.; Vasquez, K. M. Effects of replication and transcription on DNA structure-related genetic instability. Genes 2017 , 8 , 17..

Sheinin, M. Y.; Forth, S.; Marko, J. F.; Wang, M. D. Underwound DNA under tension: structure, elasticity, and sequence-dependent behaviors. Phys. Rev. Lett. 2011 , 107 , 108102..

Seol, Y.; Neuman, K. C. The dynamic interplay between DNA topoisomerases and DNA topology. Biophys. Rev. 2016 , 8 , 101−111..

Bates, A. D.; Maxwell, A. DNA Topology . Oxford University Press: New York, USA, 2005 ..

Schvartzman, J. B.; Hernandez, P.; Krimer, D. B.; Dorier, J.; Stasiak, A. Closing the DNA replication cycle: from simple circular molecules to supercoiled and knotted DNA catenanes. Nucleic Acids Res. 2019 , 47 , 7182−7198..

Berger, J. M.; Gamblin, S. J.; Harrison, S. C.; Wang, J. C. Structure and mechanism of DNA topoisomerase II. Nature 1996 , 379 , 225−232..

Deweese, J. E.; Osheroff, N. The DNA cleavage reaction of topoisomerase II: wolf in sheep's clothing. Nucleic Acids Res. 2008 , 37 , 738−748..

Bates, A. D.; Noy, A.; Piperakis, M. M.; Harris, S. A.; Maxwell, A. Small DNA circles as probes of DNA topology. Biochem. Soc. Trans. 2013 , 41 , 565−570..

Gaspar, V. M.; Maia, C. J.; Queiroz, J. A.; Pichon, C.; Correia, I. J.; Sousa, F. Improved minicircle DNA biosynthesis for gene therapy applications. Hum. Gene Ther: Methods. 2014 , 25 , 93−105..

Crut, A.; Koster, D. A.; Seidel, R.; Wiggins, C. H.; Dekker, N. H. Fast dynamics of supercoiled DNA revealed by single-molecule experiments. Proc. Natl. Acad. Sci. U. S. A. 2007 , 104 , 11957−11962..

Galburt, E. A.; Tomko, E. J.; Stump, W. T.; Ruiz Manzano, A. Force-dependent melting of supercoiled DNA at thermophilic temperatures. Biophys. Chem . 2014, 187−188 , 23−28..

Qiao, Y. P.; Ren, C. L.; Ma, Y. Q. Two different ways of stress release in supercoiled DNA minicircles under DNA nick. J. Phys. Chem. B 2023 , 127 , 4015−4021..

Ouldridge, T. E.; Louis, A. A.; Doye, J. P. Structural, mechanical, and thermodynamic properties of a coarse-grained DNA model. J. Chem. Phys. 2011 , 134 , 085101..

Sulc, P.; Romano, F.; Ouldridge, T. E.; Rovigatti, L.; Doye, J. P.; Louis, A. A. Sequence-dependent thermodynamics of a coarse-grained DNA model. J. Chem. Phys. 2012 , 137 , 135101..

Snodin, B. E.; Randisi, F.; Mosayebi, M.; Sulc, P.; Schreck, J. S.; Romano, F.; Ouldridge, T. E.; Tsukanov, R.; Nir, E.; Louis, A. A.; Doye, J. P. Introducing improved structural properties and salt dependence into a coarse-grained model of DNA. J. Chem. Phys. 2015 , 142 , 234901..

Mosayebi, M.; Romano, F.; Ouldridge, T. E.; Louis, A. A.; Doye, J. P. The role of loop stacking in the dynamics of DNA hairpin formation. J. Phys. Chem. B 2014 , 118 , 14326−14335..

Li, L.; Wang, H.; Xiong, C.; Luo, D.; Chen, H.; Liu, Y. Quantify the combined effects of temperature and force on the stability of DNA hairpin. J. Phys.: Condens. Matter 2021 , 33 , 185102..

Schreck, J. S.; Ouldridge, T. E.; Romano, F.; Sulc, P.; Shaw, L. P.; Louis, A. A.; Doye, J. P. DNA hairpins destabilize duplexes primarily by promoting melting rather than by inhibiting hybridization. Nucleic Acids Res. 2015 , 43 , 6181−6190..

Matek, C.; Ouldridge, T. E.; Doye, J. P.; Louis, A. A. Plectoneme tip bubbles: coupled denaturation and writhing in supercoiled DNA. Sci. Rep. 2015 , 5 , 7655..

Coronel, L.; Suma, A.; Micheletti, C. Dynamics of supercoiled DNA with complex knots: large-scale rearrangements and persistent multi-strand interlocking. Nucleic Acids Res. 2018 , 46 , 7533−7541..

Kriegel, F.; Matek, C.; Drsata, T.; Kulenkampff, K.; Tschirpke, S.; Zacharias, M.; Lankas, F.; Lipfert, J. The temperature dependence of the helical twist of DNA. Nucleic Acids Res. 2018 , 46 , 7998−8009..

Desai, P. R.; Brahmachari, S.; Marko, J. F.; Das, S.; Neuman, K. C. Coarse-grained modelling of DNA plectoneme pinning in the presence of base-pair mismatches. Nucleic Acids Res. 2020 , 48 , 10713−10725..

Skoruppa, E.; Nomidis, S. K.; Marko, J. F.; Carlon, E. Bend-induced twist waves and the structure of nucleosomal DNA. Phys. Rev. Lett. 2018 , 121 , 088101..

Caraglio, M.; Skoruppa, E.; Carlon, E. Overtwisting induces polygonal shapes in bent DNA. J. Chem. Phys. 2019 , 150 , 135101..

Gutierrez Fosado, Y. A.; Landuzzi, F.; Sakaue, T. Twist dynamics and buckling instability of ring DNA: the effect of groove asymmetry and anisotropic bending. Soft Matter 2021 , 17 , 1530−1537..

Lim, W.; Randisi, F.; Doye, J. P. K.; Louis, A. A. The interplay of supercoiling and thymine dimers in DNA. Nucleic Acids Res. 2022 , 50 , 2480−2492..

Benson, E.; Lolaico, M.; Tarasov, Y.; Gadin, A.; Hogberg, B. Evolutionary refinement of DNA nanostructures using coarse-grained molecular dynamics simulations. ACS Nano 2019 , 13 , 12591−12598..

Schreck, J. S.; Romano, F.; Zimmer, M. H.; Louis, A. A.; Doye, J. P. Characterizing DNA star-tile-based nanostructures using a coarse-grained model. ACS Nano 2016 , 10 , 4236−4247..

Sharma, R.; Schreck, J. S.; Romano, F.; Louis, A. A.; Doye, J. P. K. Characterizing the motion of jointed DNA nanostructures using a coarse-grained model. ACS Nano 2017 , 11 , 12426−12435..

Chhabra, H.; Mishra, G.; Cao, Y.; Presern, D.; Skoruppa, E.; Tortora, M. M. C.; Doye, J. P. K. Computing the elastic mechanical properties of rodlike DNA nanostructures. J. Chem. Theory Comput. 2020 , 16 , 7748−7763..

Reinhardt, A.; Schreck, J. S.; Romano, F.; Doye, J. P. Self-assembly of two-dimensional binary quasicrystals: a possible route to a DNA quasicrystal. J. Phys.: Condens. Matter 2017 , 29 , 014006..

Naskar, S.; Maiti, P. K. Mechanical properties of DNA and DNA nanostructures: comparison of atomistic, Martini and oxDNA models. J. Mater. Chem. B 2021 , 9 , 5102−5113..

Ouldridge, T. E. DNA nanotechnology: understanding and optimisation through simulation. Mol. Phys. 2014 , 113 , 1−15..

Doye, J. P.; Ouldridge, T. E.; Louis, A. A.; Romano, F.; Sulc, P.; Matek, C.; Snodin, B. E.; Rovigatti, L.; Schreck, J. S.; Harrison, R. M.; Smith, W. P. Coarse-graining DNA for simulations of DNA nanotechnology. Phys. Chem. Chem. Phys. 2013 , 15 , 20395−20414..

Plimpton., S. Fast parallel algorithms for short-range molecular dynamics. J. Comput. Phys. 1995 , 117 , 1−19..

Henrich, O.; Gutierrez Fosado, Y. A.; Curk, T.; Ouldridge, T. E. Coarse-grained simulation of DNA using LAMMPS: an implementation of the oxDNA model and its applications. Eur. Phys. J. E: Soft Matter Biol. Phys. 2018 , 41 , 57..

Sengar, A.; Ouldridge, T. E.; Henri ch, O.; Rovigatti, L.; Sulc, P. A Primer on the oxDNA model of DNA: when to use it, how to simulate it and how to interpret the results. Front. Mol. Biosci. 2021 , 8 , 693710..

Davidchack, R. L.; Ouldridge, T. E.; Tretyakov, M. V. New Langevin and gradient thermostats for rigid body dynamics. J. Chem. Phys. 2015 , 142 , 144114..

Sayar, M.; Avsaroglu, B.; Kabakcioglu, A. Twist-writhe partitioning in a coarse-grained DNA minicircle model. Phys. Rev. E 2010 , 81 , 041916..

Stukowski, A. Visualization and analysis of atomistic simulation data with OVITO–the open visualization tool. Modell. Simul. Mater. Sci. Eng. 2010 , 18 , 015012..

Koster, D. A.; Croquette, V.; Dekker, C.; Shuman, S.; Dekker, N. H. Friction and torque govern the relaxation of DNA supercoils by eukaryotic topoisomerase IB. Nature 2005 , 434 , 671−674..

Strick, T. R.; Croquette, V.; Bensimon, D. Single-molecule analysis of DNA uncoiling by type II topoisomerase. Nature 2000 , 404 , 901−904..

Spakman, D.; Bakx, J. A. M.; Biebricher, A. S.; Peterman, E. J. G.; Wuite, G. J. L.; King, G. A. Unravelling the mechanisms of Type 1A topoisomerases using single-molecule approaches. Nucleic Acids Res. 2021 , 49 , 5470−5492..

Fathizadeh, A.; Schiessel, H.; Ejtehadi, M. R. Molecular dynamics simulation of supercoiled DNA rings. Macromolecules 2014 , 48 , 164−172..

浏览量

242

Downloads

CSCD

文章被引用时，请邮件提醒。

Submit

工具集

关联资源

Experimental Investigation of Graphene and TiO2 Reinforced Poly(vinyl alcohol)-based Fiber Metal Laminates

Tunable Circularly Polarized Luminescence of Helical Poly(phenylacetylene)s via Side-chain-to-Backbone Förster Resonance Energy Transfer

Two-way Shape Memory Effect of Polycaprolactone-based Polyurethane via Synergistic Role of Hydrogen Bonding and Crystallization Tuned by Malic Acid

Pyrimidoisoindigo-based Polymers for Ambipolar Charge Transport

Highly Regio- and trans-Selective Ring-opening Metathesis Polymerization of Chiral Aza-norbornene with a Simple Phenylimido-Tungsten Catalyst