Blind Predictions of DNA and RNA Tweezers Experiments with Force and Torque

PLoS Computational Biology

Volumn 10, Issue 8, 2014, Pages

  Chou, Fang Chieh ^a   Lipfert, Jan ^b,c   Das, Rhiju ^a  

^a STANFORD UNIVERSITY   (United States)

^b DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^c UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMOLECULES; FORECASTING; TORQUE;

BASE PAIRS; BLIND PREDICTIONS; FORCE AND TORQUES; LEVEL MODEL; MEASUREMENTS OF; PERSISTENCE LENGTH; RANDOM SEQUENCE; SINGLE MOLECULE; THREE FOLDS; TOPOISOMERASES;

NUCLEIC ACIDS;

DNA TOPOISOMERASE; DNA Z; DOUBLE STRANDED DNA; DOUBLE STRANDED RNA; POLYADENYLIC ACID; POLYTHYMIDYLIC ACID; DNA; RNA;

ARTICLE; CALCULATION; COMPUTER PROGRAM; CONTROLLED STUDY; CRYSTALLOGRAPHY; FORCE; MECHANICAL STRESS; NUCLEOSOME; OPTICAL TWEEZERS; PREDICTION; RNA CONFORMATION; SIMULATION; TORQUE; TORSION; VIRUS CAPSID; ALGORITHM; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; CONFORMATION; NANOTECHNOLOGY; PROCEDURES; YOUNG MODULUS;

ALGORITHMS; COMPUTER SIMULATION; DNA; ELASTIC MODULUS; MODELS, MOLECULAR; NANOTECHNOLOGY; NUCLEIC ACID CONFORMATION; RNA; TORQUE;

EID: 84908586687     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003756     Document Type: Article

References (93)

1. Bloomfield VA, Crothers DM, Tinoco I, Jr. (2000) Nucleic Acids: Structures, Properties, and Functions: University Science Books.
2. Gesteland RF, Cech T, Atkins JF (2006) The RNA world: the nature of modern RNA suggests a prebiotic RNA world. Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory Press.
3. Rohs R, Jin X, West SM, Joshi R, Honig B, et al. (2010) Origins of Specificity in Protein-DNA Recognition. Annual Review of Biochemistry 79: 233–269.
4. Lee G, Bratkowski MA, Ding F, Ke A, Ha T, (2012) Elastic coupling between RNA degradation and unwinding by an exoribonuclease. Science 336: 1726–1729.
5. Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ, (1997) Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389: 251–260.
6. Earnshaw WC, Casjens SR, (1980) DNA packaging by the double-stranded DNA bacteriophages. Cell 21: 319–331.
7. Smith DE, Tans SJ, Smith SB, Grimes S, Anderson DL, et al. (2001) The bacteriophage φ29 portal motor can package DNA against a large internal force. Nature 413: 748–752.
8. Smith SB, Finzi L, Bustamante C, (1992) Direct mechanical measurements of the elasticity of single DNA molecules by using magnetic beads. Science 258: 1122–1126.
9. Strick TR, Allemand JF, Bensimon D, Bensimon A, Croquette V, (1996) The elasticity of a single supercoiled DNA molecule. Science 271: 1835–1837.
10. Strick TR, Dessinges MN, Charvin G, Dekker NH, Allemand JF, et al. (2003) Stretching of macromolecules and proteins. Reports on Progress in Physics 66: 1.
11. Bustamante C, Bryant Z, Smith SB, (2003) Ten years of tension: single-molecule DNA mechanics. Nature 421: 423–427.
12. Bryant Z, Stone MD, Gore J, Smith SB, Cozzarelli NR, et al. (2003) Structural transitions and elasticity from torque measurements on DNA. Nature 424: 338–341.
13. Abels JA, Moreno-Herrero F, van der Heijden T, Dekker C, Dekker NH, (2005) Single-Molecule Measurements of the Persistence Length of Double-Stranded RNA. Biophysical Journal 88: 2737–2744.
14. Gore J, Bryant Z, Nöllmann M, Le MU, Cozzarelli NR, et al. (2006) DNA overwinds when stretched. Nature 442: 836–839.
15. Lionnet T, Joubaud S, Lavery R, Bensimon D, Croquette V, (2006) Wringing Out DNA. Physical Review Letters 96: 178102.
16. Lipfert J, Kerssemakers JW, Jager T, Dekker NH, (2010) Magnetic torque tweezers: measuring torsional stiffness in DNA and RecA-DNA filaments. Nature Methods 7: 977–980.
17. Lipfert J, Wiggin M, Kerssemakers JWJ, Pedaci F, Dekker NH, (2011) Freely orbiting magnetic tweezers to directly monitor changes in the twist of nucleic acids. Nature Communications 2: 439.
18. Bryant Z, Oberstrass FC, Basu A, (2012) Recent developments in single-molecule DNA mechanics. Current Opinion in Structural Biology 22: 304–312.
19. Forth S, Sheinin MY, Inman J, Wang MD, (2013) Torque Measurement at the Single-Molecule Level. Annual Review of Biophysics 42: 583–604.
20. Herrero-Galán E, Fuentes-Perez ME, Carrasco C, Valpuesta JM, Carrascosa JL, et al. (2013) Mechanical Identities of RNA and DNA Double Helices Unveiled at the Single-Molecule Level. Journal of the American Chemical Society 135: 122–131.
21. Moroz JD, Nelson P, (1997) Torsional directed walks, entropic elasticity, and DNA twist stiffness. Proceedings of the National Academy of Sciences 94: 14418–14422.
22. Moroz JD, Nelson P, (1998) Entropic Elasticity of Twist-Storing Polymers. Macromolecules 31: 6333–6347.
23. Bouchiat C, Wang MD, Allemand J, Strick T, Block SM, et al. (1999) Estimating the persistence length of a worm-like chain molecule from force-extension measurements. Biophysical Journal 76: 409–413.
24. Bouchiat C, Mézard M, (2000) Elastic rod model of a supercoiled DNA molecule. The European Physical Journal E 2: 377–402.
25. Cheatham IIIKollma PA, (1996) Observation of the A-DNA to B-DNA Transition During Unrestrained Molecular Dynamics in Aqueous Solution. Journal of Molecular Biology 259: 434–444.
26. Sherer EC, Harris SA, Soliva R, Orozco M, Laughton CA, (1999) Molecular Dynamics Studies of DNA A-Tract Structure and Flexibility. Journal of the American Chemical Society 121: 5981–5991.
27. Cheatham TE, Iii (2004) Simulation and modeling of nucleic acid structure, dynamics and interactions. Current Opinion in Structural Biology 14: 360–367.
28. Araúzo-Bravo MJ, Fujii S, Kono H, Ahmad S, Sarai A, (2005) Sequence-Dependent Conformational Energy of DNA Derived from Molecular Dynamics Simulations: Toward Understanding the Indirect Readout Mechanism in Protein−DNA Recognition. Journal of the American Chemical Society 127: 16074–16089.
29. Lionnet T, Lankaš F, (2007) Sequence-Dependent Twist-Stretch Coupling in DNA. Biophysical Journal 92: L30–L32.
30. Das R, Karanicolas J, Baker D, (2010) Atomic accuracy in predicting and designing noncanonical RNA structure. Nature Methods 7: 291–294.
31. Sripakdeevong P, Kladwang W, Das R, (2011) An enumerative stepwise ansatz enables atomic-accuracy RNA loop modeling. Proceedings of the National Academy of Sciences 108: 20573–20578.
32. Pérez A, Luque FJ, Orozco M, (2012) Frontiers in Molecular Dynamics Simulations of DNA. Accounts of Chemical Research 45: 196–205.
33. Olson WK, Colasanti AV, Czapla L, Zheng G (2008) Insights into the Sequence-Dependent Macromolecular Properties of DNA from Base-Pair Level Modeling. In: Voth GA, editor. Coarse-Graining of Condensed Phase and Biomolecular Systems: CRC Press. pp. 205–223.
34. de Pablo JJ, (2011) Coarse-grained simulations of macromolecules: from DNA to nanocomposites. Annual review of physical chemistry 62: 555–574.
35. Doye JPK, Ouldridge TE, Louis AA, Romano F, Šulc P, et al. (2013) Coarse-graining DNA for simulations of DNA nanotechnology. Physical Chemistry Chemical Physics 15: 20395–20414.
36. Potoyan DA, Savelyev A, Papoian GA, (2013) Recent successes in coarse-grained modeling of DNA. Wiley Interdisciplinary Reviews: Computational Molecular Science 3: 69–83.
37. Olson WK, Marky NL, Jernigan RL, Zhurkin VB, (1993) Influence of Fluctuations on DNA Curvature: A Comparison of Flexible and Static Wedge Models of Intrinsically Bent DNA. Journal of Molecular Biology 232: 530–554.
38. Marky NL, Olson WK, (1994) Configurational statistics of the DNA duplex: Extended generator matrices to treat the rotations and translations of adjacent residues. Biopolymers 34: 109–120.
39. Gorin AA, Zhurkin VB, Olson WK, (1995) B-DNA Twisting Correlates with Base-pair Morphology. Journal of Molecular Biology 247: 34–48.
40. Olson WK, Gorin AA, Lu X-J, Hock LM, Zhurkin VB, (1998) DNA sequence-dependent deformability deduced from protein–DNA crystal complexes. Proceedings of the National Academy of Sciences 95: 11163–11168.
41. Olson WK, Zhurkin VB, (2000) Modeling DNA deformations. Current Opinion in Structural Biology 10: 286–297.
42. Olson WK, Bansal M, Burley SK, Dickerson RE, Gerstein M, et al. (2001) A standard reference frame for the description of nucleic acid base-pair geometry. Journal of Molecular Biology 313: 229–237.
43. Matsumoto A, Olson WK, (2002) Sequence-dependent motions of DNA: a normal mode analysis at the base-pair level. Biophysical Journal 83: 22–41.
44. Matsumoto A, Olson WK, (2006) Predicted Effects of Local Conformational Coupling and External Restraints on the Torsional Properties of Single DNA Molecules. Multiscale Modeling & Simulation 5: 1227–1247.
45. Czapla L, Swigon D, Olson WK, (2006) Sequence-Dependent Effects in the Cyclization of Short DNA. Journal of Chemical Theory and Computation 2: 685–695.
46. Zheng G, Czapla L, Srinivasan AR, Olson WK, (2010) How stiff is DNA? Physical Chemistry Chemical Physics 12: 1399–1406.
47. Shi X, Herschlag D, Harbury PAB, (2013) Structural ensemble and microscopic elasticity of freely diffusing DNA by direct measurement of fluctuations. Proceedings of the National Academy of Sciences 110: E1444–E1451.
48. Trovato F, Tozzini V, (2008) Supercoiling and local denaturation of plasmids with a minimalist DNA model. The journal of physical chemistry B 112: 13197–13200.
49. Niewieczerzał S, Cieplak M, (2009) Stretching and twisting of the DNA duplexes in coarse-grained dynamical models. Journal of Physics: Condensed Matter 21: 474221.
50. Matek C, Ouldridge TE, Levy A, Doye JPK, Louis AA, (2012) DNA Cruciform Arms Nucleate through a Correlated but Asynchronous Cooperative Mechanism. The Journal of Physical Chemistry B 116: 11616–11625.
51. Romano F, Chakraborty D, Doye JPK, Ouldridge TE, Louis AA, (2013) Coarse-grained simulations of DNA overstretching. The Journal of Chemical Physics 138: 085101.
52. Lankas F, Gonzalez O, Heffler LM, Stoll G, Moakher M, et al. (2009) On the parameterization of rigid base and basepair models of DNA from molecular dynamics simulations. Physical chemistry chemical physics: PCCP 11: 10565–10588.
53. Klenin K, Langowski J, (2000) Computation of writhe in modeling of supercoiled DNA. Biopolymers 54: 307–317.
54. Rossetto V, Maggs AC, (2003) Writhing geometry of open DNA. The Journal of Chemical Physics 118: 9864–9874.
55. Starostin EL (2005) On the writhe of non-closed curves. Physical and Numerical Models in Knot Theory Including Applications to the Life Sciences: World Scientific. pp. 525–545.
56. Britton LA, Olson WK, Tobias I, (2009) Two perspectives on the twist of DNA. The Journal of Chemical Physics 131: 245101–245108.
57. Odijk T, (1995) Stiff Chains and Filaments under Tension. Macromolecules 28: 7016–7018.
58. 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.
59. Forth S, Deufel C, Sheinin MY, Daniels B, Sethna JP, et al. (2008) Abrupt Buckling Transition Observed during the Plectoneme Formation of Individual DNA Molecules. Physical Review Letters 100: 148301.
60. Smith SB, Cui Y, Bustamante C, (1996) Overstretching B-DNA: the elastic response of individual double-stranded and single-stranded DNA molecules. Science 271: 795–799.
61. Baumann CG, Smith SB, Bloomfield VA, Bustamante C, (1997) Ionic effects on the elasticity of single DNA molecules. Proc Natl Acad Sci U S A 94: 6185–6190.
62. Celedon A, Nodelman IM, Wildt B, Dewan R, Searson P, et al. (2009) Magnetic tweezers measurement of single molecule torque. Nano Letters 9: 1720–1725.
63. Kauert DJ, Kurth T, Liedl T, Seidel R, (2011) Direct mechanical measurements reveal the material properties of three-dimensional DNA origami. Nano Letters 11: 5558–5563.
64. Mosconi F, Allemand JF, Croquette V, (2011) Soft magnetic tweezers: a proof of principle. Review of scientific instruments 82: 034302.
65. Shore D, Baldwin RL, (1983) Energetics of DNA twisting. I. Relation between twist and cyclization probability. Journal of molecular biology 170: 957–981.
66. Horowitz DS, Wang JC, (1984) Torsional rigidity of DNA and length dependence of the free energy of DNA supercoiling. Journal of Molecular Biology 173: 75–91.
67. Taylor WH, Hagerman PJ, (1990) Application of the method of phage T4 DNA ligase-catalyzed ring-closure to the study of DNA structure: II. NaCl-dependence of DNA flexibility and helical repeat. Journal of Molecular Biology 212: 363–376.
68. Fujimoto BS, Brewood GP, Schurr JM, (2006) Torsional Rigidities of Weakly Strained DNAs. Biophysical Journal 91: 4166–4179.
69. Lebel P, Basu A, Oberstrass FC, Tretter EM, Bryant Z, (2014) Gold rotor bead tracking for high-speed measurements of DNA twist, torque and extension. Nat Methods 11: 456–462.
70. Segal E, Widom J, (2009) Poly(dA:dT) tracts: major determinants of nucleosome organization. Current Opinion in Structural Biology 19: 65–71.
71. Wu H-M, Crothers DM, (1984) The locus of sequence-directed and protein-induced DNA bending. Nature 308: 509–513.
72. Rich A, Zhang S, (2003) Z-DNA: the long road to biological function. Nat Rev Genet 4: 566–572.
73. Thomas TJ, Bloomfield VA, (1983) Chain flexibility and hydrodynamics of the B and Z forms of poly(dG-dC).poly(dG-dC). Nucleic Acids Research 11: 1919–1930.
74. Revet B, Malinge JM, Delain E, Bret ML, Leng M, (1984) Electron microscopic measurement of chain flexibility of polydG-dC.poly(dG-dC) modified by cis-diamminedichloroplatinum(II). Nucleic Acids Research 12: 8349–8362.
75. Ashikawa I, Kinosita K, JrIkegami A, (1984) Dynamics of Z-form DNA. Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression 782: 87–93.
76. Nikolova EN, Kim E, Wise AA, O/'Brien PJ, Andricioaei I, et al. (2011) Transient Hoogsteen base pairs in canonical duplex DNA. Nature 470: 498–502.
77. Mathew-Fenn RS, Das R, Harbury PA, (2008) Remeasuring the double helix. Science 322: 446–449.
78. Shroff H, Reinhard BM, Siu M, Agarwal H, Spakowitz A, et al. (2005) Biocompatible Force Sensor with Optical Readout and Dimensions of 6 nm3. Nano Letters 5: 1509–1514.
79. Diekmann S, (1989) Definitions and nomenclature of nucleic acid structure parameters. Journal of Molecular Biology 205: 787–791.
80. El Hassan MA, Calladine CR, (1995) The Assessment of the Geometry of Dinucleotide Steps in Double-Helical DNA; a New Local Calculation Scheme. Journal of Molecular Biology 251: 648–664.
81. Lu X-J, Olson WK, (2003) 3DNA: a software package for the analysis, rebuilding and visualization of three-dimensional nucleic acid structures. Nucleic Acids Research 31: 5108–5121.
82. Lu X-J, Olson WK, (2008) 3DNA: a versatile, integrated software system for the analysis, rebuilding and visualization of three-dimensional nucleic-acid structures. Nature Protocols 3: 1213–1227.
83. Metropolis N, Rosenbluth AW, Rosenbluth MN, Teller AH, Teller E, (1953) Equation of State Calculations by Fast Computing Machines. The Journal of Chemical Physics 21: 1087–1092.
84. Gosse C, Croquette V, (2002) Magnetic Tweezers: Micromanipulation and Force Measurement at the Molecular Level. Biophysical Journal 82: 3314–3329.
85. Greenleaf WJ, Woodside MT, Abbondanzieri EA, Block SM, (2005) Passive All-Optical Force Clamp for High-Resolution Laser Trapping. Physical Review Letters 95: 208102.
86. Neuman KC, Nagy A, (2008) Single-molecule force spectroscopy: optical tweezers, magnetic tweezers and atomic force microscopy. Nature Methods 5: 491–505.
87. Călugăreanu G, (1959) L'intégrale de Gauss et l'analyse des noeuds tridimensionnels. Rev Math Pures Appl 4: 5–20.
88. Călugăreanu G, (1961) Sur les classes d'isotopie des noeuds tridimensionnels et leurs invariants. Czechoslovak Mathematical Journal 11: 588–625.
89. White JH, (1969) Self-linking and the Gauss integral in higher dimensions. American Journal of Mathematics 91: 693–728.
90. Fuller FB, (1971) The writhing number of a space curve. Proceedings of the National Academy of Sciences 68: 815–819.
91. Fuller FB, (1978) Decomposition of the linking number of a closed ribbon: A problem from molecular biology. Proceedings of the National Academy of Sciences 75: 3557–3561.
92. Neukirch S, Starostin EL, (2008) Writhe formulas and antipodal points in plectonemic DNA configurations. Physical Review E 78: 041912.
93. Agarwal PK, Edelsbrunner H, Wang Y, (2004) Computing the Writhing Number of a Polygonal Knot. Discrete & Computational Geometry 32: 37–53.