Literature DB >> 25313077

Double-stranded RNA under force and torque: similarities to and striking differences from double-stranded DNA.

Jan Lipfert1, Gary M Skinner2, Johannes M Keegstra2, Toivo Hensgens2, Tessa Jager2, David Dulin2, Mariana Köber2, Zhongbo Yu2, Serge P Donkers2, Fang-Chieh Chou3, Rhiju Das4, Nynke H Dekker5.   

Abstract

RNA plays myriad roles in the transmission and regulation of genetic information that are fundamentally constrained by its mechanical properties, including the elasticity and conformational transitions of the double-stranded (dsRNA) form. Although double-stranded DNA (dsDNA) mechanics have been dissected with exquisite precision, much less is known about dsRNA. Here we present a comprehensive characterization of dsRNA under external forces and torques using magnetic tweezers. We find that dsRNA has a force-torque phase diagram similar to that of dsDNA, including plectoneme formation, melting of the double helix induced by torque, a highly overwound state termed "P-RNA," and a highly underwound, left-handed state denoted "L-RNA." Beyond these similarities, our experiments reveal two unexpected behaviors of dsRNA: Unlike dsDNA, dsRNA shortens upon overwinding, and its characteristic transition rate at the plectonemic buckling transition is two orders of magnitude slower than for dsDNA. Our results challenge current models of nucleic acid mechanics, provide a baseline for modeling RNAs in biological contexts, and pave the way for new classes of magnetic tweezers experiments to dissect the role of twist and torque for RNA-protein interactions at the single-molecule level.

Keywords:  RNA; force; magnetic tweezers; nucleic acids; torque

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Year:  2014        PMID: 25313077      PMCID: PMC4217419          DOI: 10.1073/pnas.1407197111

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  52 in total

1.  Torque measurements reveal sequence-specific cooperative transitions in supercoiled DNA.

Authors:  Florian C Oberstrass; Louis E Fernandes; Zev Bryant
Journal:  Proc Natl Acad Sci U S A       Date:  2012-04-02       Impact factor: 11.205

2.  Energetics at the DNA supercoiling transition.

Authors:  Hergen Brutzer; Nicholas Luzzietti; Daniel Klaue; Ralf Seidel
Journal:  Biophys J       Date:  2010-04-07       Impact factor: 4.033

3.  Magnetic torque tweezers: measuring torsional stiffness in DNA and RecA-DNA filaments.

Authors:  Jan Lipfert; Jacob W J Kerssemakers; Tessa Jager; Nynke H Dekker
Journal:  Nat Methods       Date:  2010-10-17       Impact factor: 28.547

4.  Single-molecule measurements of the persistence length of double-stranded RNA.

Authors:  J A Abels; F Moreno-Herrero; T van der Heijden; C Dekker; N H Dekker
Journal:  Biophys J       Date:  2005-01-14       Impact factor: 4.033

5.  On structural transitions, thermodynamic equilibrium, and the phase diagram of DNA and RNA duplexes under torque and tension.

Authors:  Jeff Wereszczynski; Ioan Andricioaei
Journal:  Proc Natl Acad Sci U S A       Date:  2006-10-23       Impact factor: 11.205

6.  Magnetic tweezers measurement of single molecule torque.

Authors:  Alfredo Celedon; Ilana M Nodelman; Bridget Wildt; Rohit Dewan; Peter Searson; Denis Wirtz; Gregory D Bowman; Sean X Sun
Journal:  Nano Lett       Date:  2009-04       Impact factor: 11.189

7.  Multiplectoneme phase of double-stranded DNA under torsion.

Authors:  Marc Emanuel; Giovanni Lanzani; Helmut Schiessel
Journal:  Phys Rev E Stat Nonlin Soft Matter Phys       Date:  2013-08-12

8.  Torsional directed walks, entropic elasticity, and DNA twist stiffness.

Authors:  J D Moroz; P Nelson
Journal:  Proc Natl Acad Sci U S A       Date:  1997-12-23       Impact factor: 11.205

9.  DNA stretching and compression: large-scale simulations of double helical structures.

Authors:  K M Kosikov; A A Gorin; V B Zhurkin; W K Olson
Journal:  J Mol Biol       Date:  1999-06-25       Impact factor: 5.469

10.  Electrophoretic and hydrodynamic properties of duplex ribonucleic acid molecules transcribed in vitro: evidence that A-tracts do not generate curvature in RNA.

Authors:  F U Gast; P J Hagerman
Journal:  Biochemistry       Date:  1991-04-30       Impact factor: 3.162

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  50 in total

1.  High Spatiotemporal-Resolution Magnetic Tweezers: Calibration and Applications for DNA Dynamics.

Authors:  David Dulin; Tao Ju Cui; Jelmer Cnossen; Margreet W Docter; Jan Lipfert; Nynke H Dekker
Journal:  Biophys J       Date:  2015-11-17       Impact factor: 4.033

2.  Structural Flexibility of DNA-RNA Hybrid Duplex: Stretching and Twist-Stretch Coupling.

Authors:  Ju-Hui Liu; Kun Xi; Xi Zhang; Lei Bao; Xinghua Zhang; Zhi-Jie Tan
Journal:  Biophys J       Date:  2019-05-23       Impact factor: 4.033

3.  Sequence-dependent RNA helix conformational preferences predictably impact tertiary structure formation.

Authors:  Joseph D Yesselman; Sarah K Denny; Namita Bisaria; Daniel Herschlag; William J Greenleaf; Rhiju Das
Journal:  Proc Natl Acad Sci U S A       Date:  2019-08-02       Impact factor: 11.205

4.  Twist-bend coupling and the statistical mechanics of the twistable wormlike-chain model of DNA: Perturbation theory and beyond.

Authors:  Stefanos K Nomidis; Enrico Skoruppa; Enrico Carlon; John F Marko
Journal:  Phys Rev E       Date:  2019-03       Impact factor: 2.529

5.  Divalent Ion-Mediated DNA-DNA Interactions: A Comparative Study of Triplex and Duplex.

Authors:  Zhong-Liang Zhang; Yuan-Yan Wu; Kun Xi; Jian-Ping Sang; Zhi-Jie Tan
Journal:  Biophys J       Date:  2017-08-08       Impact factor: 4.033

6.  Understanding the Relative Flexibility of RNA and DNA Duplexes: Stretching and Twist-Stretch Coupling.

Authors:  Lei Bao; Xi Zhang; Ya-Zhou Shi; Yuan-Yan Wu; Zhi-Jie Tan
Journal:  Biophys J       Date:  2017-03-28       Impact factor: 4.033

7.  Understanding the mechanical response of double-stranded DNA and RNA under constant stretching forces using all-atom molecular dynamics.

Authors:  Alberto Marin-Gonzalez; J G Vilhena; Ruben Perez; Fernando Moreno-Herrero
Journal:  Proc Natl Acad Sci U S A       Date:  2017-06-20       Impact factor: 11.205

8.  DNA elasticity from coarse-grained simulations: The effect of groove asymmetry.

Authors:  Enrico Skoruppa; Michiel Laleman; Stefanos K Nomidis; Enrico Carlon
Journal:  J Chem Phys       Date:  2017-06-07       Impact factor: 3.488

9.  Kinetic Pathway of Torsional DNA Buckling.

Authors:  Andrew Dittmore; Jonathan Silver; Keir C Neuman
Journal:  J Phys Chem B       Date:  2018-10-31       Impact factor: 2.991

10.  Understanding the paradoxical mechanical response of in-phase A-tracts at different force regimes.

Authors:  Alberto Marin-Gonzalez; Cesar L Pastrana; Rebeca Bocanegra; Alejandro Martín-González; J G Vilhena; Rubén Pérez; Borja Ibarra; Clara Aicart-Ramos; Fernando Moreno-Herrero
Journal:  Nucleic Acids Res       Date:  2020-05-21       Impact factor: 16.971

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