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Force-Induced Unravelling of DNA Origami

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Abstract

We present the forcible unravelling of some of the largest DNA nanostructures ever simulated with a nucleotide-level coarse-grained model and combine our results with experiments to shed light on the mechanical properties and unfolding pathways of DNA origami systems.

In my own stories I have found that violence is strangely capable of returning my characters to reality and preparing them to accept their moment of grace.

—Flannery O’Connor, from On Her Own Work (1963).

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References

  1. Engel MC, Smith DM, Jobst MA, Sajfutdinow M, Liedl T, Romano F, Rovigatti L, Louis AA, Doye JPK (2018) Force-induced unravelling of DNA origami. ACS Nano 12(7):6734–6747

    Article  Google Scholar 

  2. Smith SB, Cui Y, Bustamante C (1996) Overstretching B-DNA: the elastic response of individual double-stranded and sinle-stranded DNA molecules. Science 271:795–799

    Article  ADS  Google Scholar 

  3. Bosco A, Camunas-Soler J, Ritort F (2014) Elastic properties and secondary structure formation of single-stranded DNA at monovalent and divalent salt conditions. Nucleic Acids Res 42:2064–2074

    Article  Google Scholar 

  4. McIntosh DB, Ribeck N, Saleh OA (2009) Detailed scaling analysis of low-force polyelectrolyte elasticity. Phys Rev E 80:041803

    Article  ADS  Google Scholar 

  5. Essevaz-Roulet B, Bockelmann U, Heslot F (1997) Mechanical separation of the complementary strands of DNA. Proc Natl Acad Sci USA 94:11935–11940

    Article  ADS  Google Scholar 

  6. Strunz T, Oroszlan K, Schäfer R, Güntherodt H-J (1999) Dynamic force spectroscopy of single DNA molecules. Proc Natl Acad Sci USA 96:11277–11282

    Article  ADS  Google Scholar 

  7. Kühner F, Morfill J, Neher RA, Blank K, Gaub HE (2007) Force-induced DNA slippage. Biophys J 92:2491–2497

    Article  Google Scholar 

  8. van Mameren J, Gross P, Farge G, Hooijman P, Modesti M, Falkenberg M, Wuite GJL, Peterman EJG (2009) Unraveling the structure of DNA during overstretching by using multicolor, single-molecule fluorescence imaging. Proc Natl Acad Sci USA 106:18231–18236

    Article  ADS  Google Scholar 

  9. Gross P, Laurens N, Oddershede LB, Bockelmann U, Peterman EJG, Wuite GJL (2011) Quantifying how DNA stretches, melts and changes twist under tension. Nat Phys 7:731–736

    Article  Google Scholar 

  10. Romano F, Chakraborty D, Doye JPK, Ouldridge TE, Louis AA (2013) Coarse-grained simulations of DNA overstretching. J Chem Phys 138:085101

    Article  ADS  Google Scholar 

  11. Forth S, Deufel C, Sheinin MY, Daniels B, Sethna JP, Wang MD (2008) Abrupt buckling transition observed during the plectoneme formation of individual DNA molecules. Phys Rev Lett 100:148301

    Article  ADS  Google Scholar 

  12. Nomidis SK, Kriegel F, Vanderlinden W, Lipfert J, Carlon E (2017) Twist-bend coupling and the torsional response of double-stranded DNA. Phys Rev Lett 118:217801

    Article  ADS  Google Scholar 

  13. Zhang Y, McEwan A, Crothers D, Levene S (2006) Analysis of in-vivo LacR-mediated gene repression based on the mechanics of DNA looping. PLoS One 1:e136

    Article  ADS  Google Scholar 

  14. Goodman SD, Nash HA (1989) Functional replacement of a protein-induced bend in a DNA recombination site. Nature 341:251–254

    Article  ADS  Google Scholar 

  15. Bustamante C, Bryant Z, Smith SB (2003) Ten years of tension: single-molecule DNA mechanics. Nature 421:423–427

    Article  ADS  Google Scholar 

  16. Goktas M, Blank KG (2017) Molecular force sensors: from fundamental concepts toward applications in cell biology. Adv Mater Interfaces 4:1600441

    Article  Google Scholar 

  17. Wang X, Ha T (2013) Defining single molecular forces required to activate integrin and notch signaling. Science 340:991–994

    Article  ADS  Google Scholar 

  18. Blakely BL, Dumelin CE, Trappmann B, McGregor LM, Choi CK, Anthony PC, Duesterberg VK, Baker BM, Block SM, Liu DR, Chen CS (2014) A DNA-based molecular probe for optically reporting cellular traction forces. Nat Methods 11:1229–1232

    Article  Google Scholar 

  19. Cocco S, Monasson R, Marko JF (2001) Force and kinetic barriers to unzipping of the DNA double helix. Proc Natl Acad Sci USA 98:8608–8613

    Article  ADS  Google Scholar 

  20. Mosayebi M, Louis AA, Doye JPK, Ouldridge TE (2015) Force-induced rupture of a DNA duplex: from fundamentals to force sensors. ACS Nano 9:11993–12003

    Article  Google Scholar 

  21. Evans E, Ritchie K (1997) Dynamic strength of molecular adhesion bonds. Biophys J 72:1541–1555

    Article  Google Scholar 

  22. Hatch K, Danilowicz C, Coljee V, Prentiss M (2008) Demonstration that the shear force required to separate short double-stranded DNA does not increase significantly with sequence length for sequences longer than 25 base pairs. Phys Rev E 78:011920

    Article  ADS  Google Scholar 

  23. Neher RA, Gerland U (2005) DNA as a programmable viscoelastic nanoelement. Biophys J 89:3846–3855

    Article  Google Scholar 

  24. Williams MC, Wenner JR, Rouzina I, Bloomfield VA (2001) Entropy and heat capacity of DNA melting from temperature dependence of single molecule stretching. Biophys J 80:1932–1939

    Article  Google Scholar 

  25. Wenner JR, Williams MC, Rouzina I, Bloomfield VA (2002) Salt dependence of the elasticity and overstretching transition of single DNA molecules. Biophys J 82:3160–3169

    Article  Google Scholar 

  26. Fu H, Chen H, Koh CG, Lim CT (2009) Effects of magnesium salt concentrations on B-DNA overstretching transition. Eur Phys J E 29:45–49

    Article  Google Scholar 

  27. Huguet JM, Bizarro CV, Forns N, Smith SB, Bustamante C, Ritort F (2010) Single-molecule derivation of salt dependent base-pair free energies in DNA. Proc Natl Acad Sci USA 107:15431–15436

    Article  ADS  Google Scholar 

  28. Rief M, Clausen-Schaumann H, Gaub HE (1999) Sequence-dependent mechanics of single DNA molecules. Nat Struct Mol Biol 6:346–349

    Article  Google Scholar 

  29. Seeman NC (2010) Nanomaterials based on DNA. Annu Rev Biochem 79:65–87

    Article  Google Scholar 

  30. Jones MR, Seeman NC, Mirkin CA (2015) Programmable materials and the nature of the DNA bond. Science 347:1260901

    Article  Google Scholar 

  31. Fu TJ, Seeman NC (1993) DNA double-crossover molecules. Biochemistry 32:3211–3220

    Article  Google Scholar 

  32. Liu D, Wang M, Deng Z, Walulu R, Mao C (2004) Tensegrity: construction of rigid DNA triangles with flexible four-arm DNA junctions. J Am Chem Soc 126:2324–2325

    Article  Google Scholar 

  33. He Y, Ye T, Su M, Zhang C, Ribbe AE, Jiang W, Mao C (2008) Hierarchical self-assembly of DNA into symmetric supramolecular polyhedra. Nature 452:198

    Article  ADS  Google Scholar 

  34. Mathieu F, Liao S, Kopatsch J, Wang T, Mao C, Seeman NC (2005) Six-helix bundles designed from DNA. Nano Lett 5:661–665

    Article  ADS  Google Scholar 

  35. Rothemund PWK (2006) Folding DNA to create nanoscale shapes and patterns. Nature 440:297–302

    Article  ADS  Google Scholar 

  36. Bell NAW, Engst CR, Ablay M, Divitini G, Ducati C, Liedl T, Keyser UF (2012) DNA origami nanopores. Nano Lett 12:512–517

    Article  ADS  Google Scholar 

  37. Koirala D, Shrestha P, Emura T, Hidaka K, Mandal S, Endo M, Sugiyama H, Mao H (2014) Single-molecule mechanochemical sensing using DNA origami nanostructures. Angew Chem Int Ed 126:8275–8279

    Article  Google Scholar 

  38. Andersen ES, Dong M, Nielsen MM, Jahn K, Subramani R, Mamdouh W, Golas MM, Sander B, Stark H, Oliveira CLP, Pedersen JS, Birkedal V, Besenbacher F, Gothelf KV, Kjems J (2009) Self-assembly of a nanoscale DNA box with a controllable lid. Nature 459:73–76

    Article  ADS  Google Scholar 

  39. Pinheiro AV, Han D, Shih WM, Yan H (2011) Challenges and opportunities for structural DNA nanotechnology. Nat Nanotechnol 6:763–772

    Article  ADS  Google Scholar 

  40. Yin P, Hariadi RF, Sahu S, Choi HMT, Park SH, LaBean TH, Reif JH (2008) Programming DNA tube circumferences. Science 321:824–826

    Article  ADS  Google Scholar 

  41. Wei B, Dai M, Yin P (2012a) Complex shapes self-assembled from single-stranded DNA tiles. Nature 485:623

    Article  ADS  Google Scholar 

  42. Ke Y, Ong LL, Shih WM, Yin P (2012) Three-dimensional structures self-assembled from DNA bricks. Science 338:1177–1183

    Article  ADS  Google Scholar 

  43. Sa-Ardyen P, Vologodskii AV, Seeman NC (2003) The flexibility of DNA double crossover molecules. Biophys J 84:3829–3837

    Article  Google Scholar 

  44. Kauert DJ, Kurth T, Liedl T, Seidel R (2011) Direct mechanical measurements reveal the material properties of three-dimensional DNA origami. Nano Lett 11:5558–5563

    Article  ADS  Google Scholar 

  45. Wang T, Schiffels D, Martinez Cuesta S, Kuchnir Fygenson D, Seeman NC (2012) Design and characterization of 1D nanotubes and 2D periodic arrays self-assembled from DNA multi-helix bundles. J Am Chem Soc 134:1606–1616

    Article  Google Scholar 

  46. Schiffels D, Liedl T, Fygenson DK (2013) Nanoscale structure and microscale stiffness of DNA nanotubes. ACS Nano 7:6700–6710

    Article  Google Scholar 

  47. Yoo J, Aksimentiev A (2013) In situ structure and dynamics of DNA origami determined through molecular dynamics simulations. Proc Natl Acad Sci USA 110:20099–20104

    Article  ADS  Google Scholar 

  48. Slone SM, Li C-Y, Yoo J, Aksimentiev A (2016b) Molecular mechanics of DNA bricks: in situ structure, mechanical properties and ionic conductivity. New J Phys 18:055012

    Article  Google Scholar 

  49. Castro CE, Kilchherr F, Kim D-N, Shiao EL, Wauer T, Wortmann P, Bathe M, Dietz H (2011) A primer to scaffolded DNA origami. Nat Methods 8:221

    Article  Google Scholar 

  50. Kim D-N, Kilchherr F, Dietz H, Bathe M (2012) Quantitative prediction of 3D solution shape and flexibility of nucleic acid nanostructures. Nucleic Acids Res 40:2862–2868

    Article  Google Scholar 

  51. Reshetnikov RV, Stolyarova AV, Zalevsky AO, Panteleev DY, Pavlova GV, Klinov DV, Golovin AV, Protopopova AD (2018) A coarse-grained model for DNA origami. Nucleic Acids Res 46:1102–1112

    Article  Google Scholar 

  52. Schreck JS, Romano F, Zimmer MH, Louis AA, Doye JPK (2016) Characterizing DNA star-tile-based nanostructures using a coarse-grained model. ACS Nano 10:4236–4247

    Article  Google Scholar 

  53. Ke Y, Lindsay S, Chang Y, Liu Y, Yan H (2008) Self-assembled water-soluble nucleic acid probe tiles for label-free RNA hybridization assays. Science 319:180–183

    Article  ADS  Google Scholar 

  54. Gu H, Yang W, Seeman NC (2010) DNA scissors device used to measure muts binding to DNA mis-pairs. J Am Chem Soc 132:4352–4357 PMID: 20205420

    Article  Google Scholar 

  55. Iwaki M, Wickham SF, Ikezaki K, Yanagida T, Shih WM (2016) A programmable DNA origami nanospring that reveals force-induced adjacent binding of myosin VI heads. Nat Commun 7:13715

    Article  ADS  Google Scholar 

  56. Funke JJ, Ketterer P, Lieleg C, Schunter S, Korber P, Dietz H (2016) Uncovering the forces between nucleosomes using DNA origami. Sci Adv 2:1600974

    Article  ADS  Google Scholar 

  57. Nickels PC, Wünsch B, Holzmeister P, Bae W, Kneer LM, Grohmann D, Tinnefeld P, Liedl T (2016) Molecular force spectroscopy with a DNA origami-based nanoscopic force clamp. Science 354:305–307

    Article  ADS  Google Scholar 

  58. Liedl T, Hogberg B, Tytell J, Ingber DE, Shih WM (2010) Self-assembly of three-dimensional prestressed tensegrity structures from DNA. Nat Nanotechnol 5:520–524

    Article  ADS  Google Scholar 

  59. Simmel SS, Nickels PC, Liedl T (2014) Wireframe and tensegrity DNA nanostructures. Acc Chem Res 47:1691–1699

    Article  Google Scholar 

  60. Marras AE, Zhou L, Su H-J, Castro CE (2015) Programmable motion of DNA origami mechanisms. Proc Natl Acad Sci USA 112:713–718

    Article  ADS  Google Scholar 

  61. Wei R, Martin TG, Rant U, Dietz H (2012b) DNA origami gatekeepers for solid-state nanopores. Angew Chem Int Ed 51:4864–4867

    Article  Google Scholar 

  62. Schuldt C, Schnauß J, Händler T, Glaser M, Lorenz J, Golde T, Käs JA, Smith DM (2016) Tuning synthetic semiflexible networks by bending stiffness. Phys Rev Lett 117:197801

    Article  ADS  Google Scholar 

  63. Shrestha P, Emura T, Koirala D, Cui Y, Hidaka K, Maximuck WJ, Endo M, Sugiyama H, Mao H (2016) Mechanical properties of DNA origami nanoassemblies are determined by Holliday junction mechanophores. Nucleic Acids Res 44:6574–6582

    Article  Google Scholar 

  64. Bae W, Kim K, Min D, Ryu J-K, Hyeon C, Yoon T-Y (2014) Programmed folding of DNA origami structures through single-molecule force control. Nat Commun 5:5654

    Article  ADS  Google Scholar 

  65. Ouldridge TE, Louis AA, Doye JPK (2011) Structural, mechanical, and thermodynamic properties of a coarse-grained DNA model. J Comput Phys 134:085101

    Google Scholar 

  66. Šulc P, Romano F, Ouldridge TE, Rovigatti L, Doye JPK, Louis AA (2012) Sequence-dependent thermodynamics of a coarse-grained DNA model. J Comput Phys 137:135101

    Google Scholar 

  67. Snodin BEK, Randisi F, Mosayebi M, Šulc P, Schreck JS, Romano F, Ouldridge TE, Tsukanov R, Nir E, Louis AA, Doye JPK (2015) Introducing improved structural properties and salt dependence into a coarse-grained model of DNA. J Chem Phys 142:234901

    Article  ADS  Google Scholar 

  68. Sharma R, Schreck JS, Romano F, Louis AA, Doye JPK (2017) Characterizing the motion of jointed DNA nanostructures using a coarse-grained model. ACS Nano 11:12426–12435

    Article  Google Scholar 

  69. Matek C, Ouldridge TE, Doye JPK, Louis AA (2015) Plectoneme tip bubbles: coupled denaturation and writhing in supercoiled DNA. Sci Rep 5:7655

    Article  ADS  Google Scholar 

  70. Matek C, Ouldridge TE, Levy A, Doye JPK, Louis AA (2012) DNA cruciform arms nucleate through a correlated but asynchronous cooperative mechanism. J Phys Chem B 116:11616–11625

    Article  Google Scholar 

  71. Depa P, Chen C, Maranas JK (2011) Why are coarse-grained force fields too fast? A look at dynamics of four coarse-grained polymers. J Chem Phys 134:014903

    Article  ADS  Google Scholar 

  72. Padding JT, Louis AA (2006) Hydrodynamic interactions and Brownian forces in colloidal suspensions: coarse-graining over time and length scales. Phys Rev E 74:031402

    Article  ADS  Google Scholar 

  73. Russo J, Tartaglia P, Sciortino F (2009) Reversible gels of patchy particles: role of the valence. J Chem Phys 131:014504

    Article  ADS  Google Scholar 

  74. Jobst MA, Milles LF, Schoeler C, Ott W, Fried DB, Bayer EA, Gaub HE, Nash MA (2015) Resolving dual binding conformations of cellulosome cohesin-dockerin complexes using single-molecule force spectroscopy. eLIFE 4:180–183

    Google Scholar 

  75. Schoeler C, Verdorfer T, Gaub HE, Nash MA (2016) Biasing effects of receptor-ligand complexes on protein-unfolding statistics. Phys Rev E 94:042412

    Article  ADS  Google Scholar 

  76. Kramers H (1940) Brownian motion in a field of force and the diffusion model of chemical reactions. Physica 7:284–304

    Article  ADS  MathSciNet  MATH  Google Scholar 

  77. Ray C, Brown JR, Akhremitchev BB (2007) Correction of systematic errors in single-molecule force spectroscopy with polymeric tethers by atomic force microscopy. J Phys Chem B 111:1963–1974

    Article  Google Scholar 

  78. Neuert G, Albrecht C, Pamir E, Gaub H (2006) Dynamic force spectroscopy of the digoxigenin antibody complex. FEBS Lett 580:505–509

    Article  Google Scholar 

  79. Alemany A, Ritort F (2014) Determination of the elastic properties of short ssDNA molecules by mechanically folding and unfolding DNA hairpins. Biopolymers 101:1193–1199

    Article  Google Scholar 

  80. Woodside MT, Block SM (2014) Reconstructing Folding energy landscapes by single-molecule force spectroscopy. Annu Rev Biophys 43:19–39

    Article  Google Scholar 

  81. Dudko OK, Hummer G, Szabo A (2006) Intrinsic rates and activation free energies from single-molecule pulling experiments. Phys Rev Lett 96:108101

    Article  ADS  Google Scholar 

  82. Bullerjahn JT, Sturm S, Kroy K (2014) Theory of rapid force spectroscopy. Nat Commun 5:4463

    Article  ADS  Google Scholar 

  83. Bell G (1978) Models for the specific adhesion of cells to cells. Science 200:618–627

    Article  ADS  Google Scholar 

  84. Hummer G, Szabo A (2003) Kinetics from nonequilibrium single-molecule pulling experiments. Biophys J 85:5–15

    Article  Google Scholar 

  85. Getfert S, Reimann P (2012) Hidden multiple bond effects in dynamic force spectroscopy. Biophys J 102:1184–1193

    Article  Google Scholar 

  86. Ritchie DB, Foster DAN, Woodside MT (2012) Programmed \(-1\) frameshifting efficiency correlates with RNA pseudoknot conformational plasticity, not resistance to mechanical unfolding. Proc Natl Acad Sci USA 109:16167–16172

    Article  ADS  Google Scholar 

  87. Strackharn M, Stahl SW, Puchner EM, Gaub HE (2012) Functional assembly of aptamer binding sites by single-molecule cut-and-paste. Nano Lett 12:2425–2428

    Article  ADS  Google Scholar 

  88. Scargle JD (1982) Studies in astronomical time series analysis. II—statistical aspects of spectral analysis of unevenly spaced data. Astrophys J 263:835–853

    Article  ADS  Google Scholar 

  89. Fugmann S, Sokolov IM (2009) Scaling of the rupture dynamics of polymer chains pulled at one end at a constant rate. Phys Rev E 79:021803

    Article  ADS  Google Scholar 

  90. Puchner EM, Gaub HE (2012) Single-molecule mechanoenzymatics. Annu Rev Biophys 41:497–518

    Article  Google Scholar 

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Correspondence to Megan Clare Engel .

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Engel, M.C. (2019). Force-Induced Unravelling of DNA Origami. In: DNA Systems Under Internal and External Forcing. Springer Theses. Springer, Cham. https://doi.org/10.1007/978-3-030-25413-1_4

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