Coarse-grained simulations of DNA overstretching.

We use a recently developed coarse-grained model to simulate the overstretching of duplex DNA. Overstretching at 23 °C occurs at 74 pN in the model, about 6-7 pN higher than the experimental value at equivalent salt conditions. Furthermore, the model reproduces the temperature dependence of the overstretching force well. The mechanism of overstretching is always force-induced melting by unpeeling from the free ends. That we never see S-DNA (overstretched duplex DNA), even though there is clear experimental evidence for this mode of overstretching under certain conditions, suggests that S-DNA is not simply an unstacked but hydrogen-bonded duplex, but instead probably has a more exotic structure.

[1]  Lorenzo Rovigatti,et al.  Coarse-graining DNA for simulations of DNA nanotechnology. , 2013, Physical chemistry chemical physics : PCCP.

[2]  O. Krichevsky.  DNA overstretched state: S-DNA form or force-induced melting? Comment on "Biophysical characterization of DNA binding from single molecule force measurements" by Mark C. Williams et al. , 2010, Physics of life reviews.

[3]  Núria Forns,et al.  Single-molecule derivation of salt dependent base-pair free energies in DNA , 2010, Proceedings of the National Academy of Sciences.

[4]  R. Metzler,et al.  Denaturation transition of stretched DNA. , 2007, Physical review letters.

[5]  Jie Yan,et al.  Two distinct overstretched DNA structures revealed by single-molecule thermodynamics measurements , 2012, Proceedings of the National Academy of Sciences.

[6]  P. Maiti,et al.  Structural rigidity of paranemic crossover and juxtapose DNA nanostructures. , 2011, Biophysical journal.

[7]  Kathy R. Chaurasiya,et al.  Biophysical characterization of DNA binding from single molecule force measurements. , 2010, Physics of life reviews.

[8]  I. Rouzina,et al.  Peeling back the mystery of DNA overstretching , 2009, Proceedings of the National Academy of Sciences.

[9]  J. Rudnick,et al.  Elasticity theory of the B-DNA to S-DNA transition. , 1998, Biophysical journal.

[10]  S. Wereley,et al.  Soft Matter , 2014 .

[11]  J. Doye,et al.  Sequence-dependent thermodynamics of a coarse-grained DNA model. , 2012, The Journal of chemical physics.

[12]  E. Siggia,et al.  Entropic elasticity of lambda-phage DNA. , 1994, Science.

[13]  Filip Lankaš.  Chapter 1:Modelling Nucleic Acid Structure and Flexibility: From Atomic to Mesoscopic Scale , 2012 .

[14]  T. Thundat,et al.  Stretched DNA structures observed with atomic force microscopy. , 1994, Nucleic acids research.

[15]  Christian Matek,et al.  DNA cruciform arms nucleate through a correlated but asynchronous cooperative mechanism. , 2012, The journal of physical chemistry. B.

[16]  Nancy Kleckner,et al.  The structure of DNA overstretched from the 5′5′ ends differs from the structure of DNA overstretched from the 3′3′ ends , 2009, Proceedings of the National Academy of Sciences.

[17]  P. Hobza,et al.  Stretched DNA investigated using molecular-dynamics and quantum-mechanical calculations. , 2010, Biophysical journal.

[18]  P. Maiti,et al.  Force induced DNA melting , 2008, Journal of physics. Condensed matter : an Institute of Physics journal.

[19]  S. Whitelam,et al.  There and (slowly) back again: entropy-driven hysteresis in a model of DNA overstretching. , 2006, Biophysical journal.

[20]  I. Rouzina,et al.  Force-induced melting of the DNA double helix. 2. Effect of solution conditions. , 2001, Biophysical journal.

[21]  Jeff Wereszczynski,et al.  On structural transitions, thermodynamic equilibrium, and the phase diagram of DNA and RNA duplexes under torque and tension , 2006, Proceedings of the National Academy of Sciences.

[22]  L. J. Maher,et al.  DNA curvature and flexibility in vitro and in vivo , 2010, Quarterly Reviews of Biophysics.

[23]  J. Doye,et al.  The effect of topology on the structure and free energy landscape of DNA kissing complexes. , 2012, The Journal of chemical physics.

[24]  A. Singh,et al.  Force induced melting of the constrained DNA. , 2009, The Journal of chemical physics.

[25]  Jonathan P. K. Doye,et al.  Simulating a burnt-bridges DNA motor with a coarse-grained DNA model , 2012, Natural Computing.

[26]  Juan J. de Pablo,et al.  Coarse-Grained Simulations of Macromolecules: From DNA to Nanocomposites , 2011 .

[27]  I. Rouzina,et al.  Force-induced melting of the DNA double helix 1. Thermodynamic analysis. , 2001, Biophysical journal.

[28]  Leandro Nunes de Castro,et al.  Natural Computing , 2005, Encyclopedia of Information Science and Technology.

[29]  Efthimios Kaxiras,et al.  Ab initio determination of coarse-grained interactions in double-stranded DNA. , 2012, The Journal of chemical physics.

[30]  Michael W Deem,et al.  Parallel tempering: theory, applications, and new perspectives. , 2005, Physical chemistry chemical physics : PCCP.

[31]  F. Sciortino,et al.  Self-assembly of short DNA duplexes: from a coarse-grained model to experiments through a theoretical link , 2012, 1204.0985.

[32]  P. Nelson,et al.  Theory of high-force DNA stretching and overstretching. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[33]  C. Bustamante,et al.  Tension induces a base-paired overstretched DNA conformation , 2012, Proceedings of the National Academy of Sciences.

[34]  Simona Cocco,et al.  Overstretching and force-driven strand separation of double-helix DNA. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

[35]  M. Elstner,et al.  On the structure and stretching of microhydrated DNA. , 2011, The journal of physical chemistry. A.

[36]  R. Lavery,et al.  DNA: An Extensible Molecule , 1996, Science.

[37]  S. Whitelam,et al.  Avoiding unphysical kinetic traps in Monte Carlo simulations of strongly attractive particles. , 2005, The Journal of chemical physics.

[38]  Aleksei Aksimentiev,et al.  Strain softening in stretched DNA. , 2008, Physical review letters.

[39]  A. A. Louis.  Coarse-grained modelling of DNA and DNA self-assembly , 2011 .

[40]  F. Seno,et al.  Different pulling modes in DNA overstretching: a theoretical analysis. , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[41]  A. Maritan,et al.  Phase diagrams for DNA denaturation under stretching forces , 2009 .

[42]  Molecular dynamics simulation of single DNA stretching reveals a novel structure , 2005 .

[43]  John Russo,et al.  Reversible gels of patchy particles: role of the valence. , 2009, The Journal of chemical physics.

[44]  I. Rouzina,et al.  Salt dependence of the elasticity and overstretching transition of single DNA molecules. , 2002, Biophysical journal.

[45]  J. Doye,et al.  Structural, mechanical, and thermodynamic properties of a coarse-grained DNA model. , 2010, The Journal of chemical physics.

[46]  D. Beratan,et al.  B-DNA to zip-DNA: simulating a DNA transition to a novel structure with enhanced charge-transport characteristics. , 2011, The journal of physical chemistry. A.

[47]  Joost van Mameren,et al.  Unraveling the structure of DNA during overstretching by using multicolor, single-molecule fluorescence imaging , 2009, Proceedings of the National Academy of Sciences.

[48]  S. Whitelam,et al.  Stretching chimeric DNA: a test for the putative S-form. , 2008, The Journal of chemical physics.

[49]  Christopher P Calderon,et al.  Quantifying DNA melting transitions using single-molecule force spectroscopy , 2009, Journal of physics. Condensed matter : an Institute of Physics journal.

[50]  A. Onufriev,et al.  Two-phase stretching of molecular chains , 2011, Proceedings of the National Academy of Sciences.

[51]  R Lavery,et al.  Modelling extreme stretching of DNA. , 1996, Nucleic acids research.

[52]  E. Peterman,et al.  Quantifying how DNA stretches, melts and changes twist under tension , 2011 .

[53]  Microscopic implications of S-DNA. , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[54]  N. Destainville,et al.  Mesoscopic models for DNA stretching under force: New results and comparison with experiments , 2012, The European physical journal. E, Soft matter.

[55]  J. Berger,et al.  DNA stretching by bacterial initiators promotes replication origin melting , 2011, Nature.

[56]  Jonathan Bath,et al.  Optimizing DNA nanotechnology through coarse-grained modeling: a two-footed DNA walker. , 2013, ACS nano.

[57]  A. Bishop,et al.  Thermomechanics of DNA: theory of thermal stability under load. , 2011, Physical review letters.

[58]  T. Ha,et al.  Recent advances in studying mechanical properties of DNA , 2012 .

[59]  C. Bustamante,et al.  Ten years of tension: single-molecule DNA mechanics , 2003, Nature.

[60]  I. Rouzina,et al.  Entropy and heat capacity of DNA melting from temperature dependence of single molecule stretching. , 2001, Biophysical journal.

[61]  Ioulia Rouzina,et al.  Thermodynamics of DNA interactions from single molecule stretching experiments. , 2002, Accounts of chemical research.

[62]  Jie Yan,et al.  Transition dynamics and selection of the distinct S-DNA and strand unpeeling modes of double helix overstretching , 2010, Nucleic acids research.

[63]  M. Cieplak,et al.  Stretching and twisting of the DNA duplexes in coarse-grained dynamical models , 2008, Journal of physics. Condensed matter : an Institute of Physics journal.

[64]  V. Subramaniam,et al.  Force spectroscopy and fluorescence microscopy of dsDNA–YOYO-1 complexes: implications for the structure of dsDNA in the overstretching region , 2010, Nucleic acids research.

[65]  C. Bustamante,et al.  Overstretching B-DNA: The Elastic Response of Individual Double-Stranded and Single-Stranded DNA Molecules , 1996, Science.

[66]  V. Lombardi,et al.  PicoNewton-millisecond force steps reveal the transition kinetics and mechanism of the double-stranded DNA elongation. , 2011, Biophysical journal.

[67]  T. Gisler,et al.  Overstretching of a 30 bp DNA duplex studied with steered molecular dynamics simulation: Effects of structural defects on structure and force-extension relation , 2009, The European physical journal. E, Soft matter.

[68]  C. Laughton,et al.  Molecular dynamics simulations of duplex stretching reveal the importance of entropy in determining the biomechanical properties of DNA. , 2005, Biophysical journal.

[69]  A. Fiasconaro,et al.  Dynamical model for the full stretching curve of DNA. , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[70]  I. Rouzina,et al.  Effect of pH on the overstretching transition of double-stranded DNA: evidence of force-induced DNA melting. , 2001, Biophysical journal.

[71]  T. Einert,et al.  A three-state model with loop entropy for the overstretching transition of DNA. , 2010, Biophysical journal.

[72]  D. Swigon,et al.  DNA stretching modeled at the base pair level: Overtwisting and shear instability in elastic linkages , 2012 .

[73]  Microscopic implications of competing pictures of DNA overstretching. Comment on "Biophysical characterization of DNA binding from single molecule force measurements" by Kathy R. Chaurasiya, Thayaparan Paramanathan, Micah J. McCauley and Mark C. Williams. , 2010, Physics of life reviews.

[74]  J. SantaLucia,et al.  The thermodynamics of DNA structural motifs. , 2004, Annual review of biophysics and biomolecular structure.

[75]  Jie Yan,et al.  Two distinct overstretched DNA states , 2010, Nucleic acids research.

[76]  J. Doye,et al.  DNA nanotweezers studied with a coarse-grained model of DNA. , 2009, Physical review letters.

[77]  P. Cizeau,et al.  Modeling extreme extension of DNA , 1997 .

[78]  R. Rosenfeld.  Nature , 2009, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.