Biophysical Reviews

, Volume 8, Issue 2, pp 139–149 | Cite as

Protein–DNA and ion–DNA interactions revealed through contrast variation SAXS

  • Joshua M. Tokuda
  • Suzette A. Pabit
  • Lois Pollack


Understanding how DNA carries out its biological roles requires knowledge of its interactions with biological partners. Since DNA is a polyanionic polymer, electrostatic interactions contribute significantly. These interactions are mediated by positively charged protein residues or charge compensating cations. Direct detection of these partners and/or their effect on DNA conformation poses challenges, especially for monitoring conformational dynamics in real time. Small-angle x-ray scattering (SAXS) is uniquely sensitive to both the conformation and local environment (i.e. protein partner and associated ions) of the DNA. The primary challenge of studying multi-component systems with SAXS lies in resolving how each component contributes to the measured scattering. Here, we review two contrast variation (CV) strategies that enable targeted studies of the structures of DNA or its associated partners. First, solution contrast variation enables measurement of DNA conformation within a protein–DNA complex by masking out the protein contribution to the scattering profile. We review a specific example, in which the real-time unwrapping of DNA from a nucleosome core particle is measured during salt-induced disassembly. The second method, heavy atom isomorphous replacement, reports the spatial distribution of the cation cloud around duplex DNA by exploiting changes in the scattering strength of cations with varying atomic numbers. We demonstrate the application of this approach to provide the spatial distribution of monovalent cations (Na+, K+, Rb+, Cs+) around a standard 25-base pair DNA. The CV strategies presented here are valuable tools for understanding DNA interactions with its biological partners.


SAXS Contrast variation NCP DNA Ions Heavy atom isomorphous replacement 



The work was supported by National Institutes of Health grants (EUREKA R01-GM088645) and (R01-GM085062). J.M.T. was supported by National Institutes of Health Training Grant (T32GM008267).

Compliance with ethical standards

Conflict of interest

Joshua M. Tokuda declares that he has no conflict of interest.

Suzette A. Pabit declares that she has no conflict of interest.

Lois Pollack declares that she has no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.


  1. Anderson CF (1995) Salt-nucleic acid interactions. Annu Rev Phys Chem 46:657–700CrossRefPubMedGoogle Scholar
  2. Andresen K, Das R, Park HY et al (2004) Spatial distribution of competing ions around DNA in solution. Phys Rev Lett 93:248103. doi: 10.1103/PhysRevLett.93.248103 CrossRefPubMedGoogle Scholar
  3. Andresen K, Qiu X, Pabit SA et al (2008) Mono- and trivalent ions around DNA: a small-angle scattering study of competition and interactions. Biophys J 95:287–295. doi: 10.1529/biophysj.107.123174 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Andrews AJ, Luger K (2011) Nucleosome structure(s) and stability: variations on a theme. Annu Rev Biophys 40:99–117. doi: 10.1146/annurev-biophys-042910-155329 CrossRefPubMedGoogle Scholar
  5. Bai Y, Greenfeld M, Travers KJ et al (2007) Quantitative and comprehensive decomposition of the ion atmosphere around nucleic acids. J Am Chem Soc 129:14981–14988. doi: 10.1021/ja075020g CrossRefPubMedPubMedCentralGoogle Scholar
  6. Baldwin JP, Boseley PG, Bradbury EM, Ibel K (1975) The subunit structure of the eukaryotic chromosome. Nature 256:245–249CrossRefGoogle Scholar
  7. Ballauff M, Jusufi A (2006) Anomalous small-angle X-ray scattering: analyzing correlations and fluctuations in polyelectrolytes. Colloid Polym Sci 284:1303–1311. doi: 10.1007/s00396-006-1516-5 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bardhan JP (2012) Biomolecular electrostatics—I want your solvation (model). Comput Sci Discovery 5:013001. doi: 10.1088/1749-4699/5/1/013001 CrossRefGoogle Scholar
  9. Bernadó P, Svergun DI (2012) Structural analysis of intrinsically disordered proteins by small-angle x-ray scattering. Mol BioSyst 8:151–167. doi: 10.1039/C1MB05275F CrossRefPubMedGoogle Scholar
  10. Bernadó P, Mylonas E, Petoukhov MV et al (2007) Structural characterization of flexible proteins using small-angle x-ray scattering. J Am Chem Soc 129:5656–5664. doi: 10.1021/ja069124n CrossRefPubMedGoogle Scholar
  11. Bloomfield VA, Crothers DM, Tinoco JI (2001) Nucleic acids: structures, properties and functions. University Science Book, SausalitoGoogle Scholar
  12. Bradley DA, Hugtenburg RP, Yusoff AL (2006a) Near-edge elastic photon scattering from dilute aqueous ions. Radiat Phys Chem 75:2129–2135. doi: 10.1016/j.radphyschem.2005.12.033 CrossRefGoogle Scholar
  13. Bradley DA, Hugtenburg RP, Yusoff AL (2006b) At-edge minima in elastic photon scattering amplitudes for dilute aqueous ions. Radiat Phys Chem 75:1676–1682. doi: 10.1016/j.radphyschem.2005.11.029 CrossRefGoogle Scholar
  14. Bram S, Butler-Browne G, Baudy P, Ibel K (1975) Quaternary structure of chromatin. Proc Natl Acad Sci U S A 72:1043–1045. doi: 10.1073/pnas.72.3.1043 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Buning R, Van Noort J (2010) Single-pair FRET experiments on nucleosome conformational dynamics. Biochimie 92:1729–1740. doi: 10.1016/j.biochi.2010.08.010 CrossRefPubMedGoogle Scholar
  16. Chang SL, Chen SH, Rill RL, Lin JS (1990) Measurements of monovalent and divalent counterion distributions around persistence length DNA fragments in solution. J Phys Chem 94:8025–8028. doi: 10.1021/J100384a010 CrossRefGoogle Scholar
  17. Chaudhuri BN (2015) Emerging applications of small angle solution scattering in structural biology. Protein Sci 24:267–276. doi: 10.1002/pro.2624 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Chen Y, Tokuda JM, Topping T et al (2014) Revealing transient structures of nucleosomes as DNA unwinds. Nucleic Acids Res 42:8767–8776. doi: 10.1093/nar/gku562 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Chin K, Sharp KA, Honig B, Pyle AM (1999) Calculating the electrostatic properties of RNA provides new insights into molecular interactions and function. Nat Struct Biol 6:1055–1061Google Scholar
  20. Chu VB, Bai Y, Lipfert J et al (2007) Evaluation of ion binding to DNA duplexes using a size-modified Poisson-Boltzmann theory. Biophys J 93:3202–3209. doi: 10.1529/biophysj.106.099168 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Clark DJ, Kimura T (1990) Electrostatic mechanism of chromatin folding. J Mol Biol 211:883–896. doi: 10.1016/0022-2836(90)90081-V CrossRefPubMedGoogle Scholar
  22. Curry S (2015) Structural biology: a century-long journey into an unseen world. Interdiscip Sci Rev 40:1–10. doi: 10.1179/0308018815Z.000000000120 CrossRefGoogle Scholar
  23. Das R, Mills TT, Kwok LW et al (2003) Counterion distribution around DNA probed by solution x-ray scattering. Phys Rev Lett 90:188103CrossRefPubMedGoogle Scholar
  24. Draper DE (2004) A guide to ions and RNA structure. RNA 10:335–343. doi: 10.1261/rna.5205404.and CrossRefPubMedPubMedCentralGoogle Scholar
  25. Gansen A, Tóth K, Schwarz N, Langowski J (2009a) Structural variability of nucleosomes detected by single-pair Förster resonance energy transfer: Histone acetylation, sequence variation, and salt effects. J Phys Chem B 113:2604–2613. doi: 10.1021/jp7114737 CrossRefPubMedGoogle Scholar
  26. Gansen A, Valeri A, Hauger F et al (2009b) Nucleosome disassembly intermediates characterized by single-molecule FRET. Proc Natl Acad Sci U S A 106:15308–15313. doi: 10.1073/pnas.0903005106 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Gansen A, Toth K, Schwarz N, Langowski J (2015) Opposing roles of H3- and H4-acetylation in the regulation of nucleosome structure--a FRET study. Nucleic Acids Res 43:1433–1443. doi: 10.1093/nar/gku1354 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Giambaşu GM, Luchko T, Herschlag D et al (2014) Ion counting from explicit-solvent simulations and 3D-RISM. Biophys J 106:883–894. doi: 10.1016/j.bpj.2014.01.021 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Glatter O, Kratky O (1982) Small angle x-ray scattering. Academic, LondonGoogle Scholar
  30. Gopal A, Zhou ZH, Knobler CM, Gelbart WM (2012) Visualizing large RNA molecules in solution. RNA 18:284–299. doi: 10.1261/rna.027557.111 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Graewert MA, Svergun DI (2013) Impact and progress in small and wide angle x-ray scattering (SAXS and WAXS). Curr Opin Struct Biol 23:748–754. doi: 10.1016/ CrossRefPubMedGoogle Scholar
  32. Grochowski P, Trylska J (2007) Continuum molecular electrostatics, salt effects, and counterion binding--a review of the Poisson-Boltzmann Theory and its modifications. Biopolymers 89:93–113. doi: 10.1002/bip CrossRefGoogle Scholar
  33. Guinier A, Fournet G (1955) Small-angle scattering of x-rays. Wiley, New YorkGoogle Scholar
  34. Hagerman P (1988) Flexibility of DNA. Annu Rev Biophys Biomol Struct 17:265–286. doi: 10.1146/annurev.biophys.17.1.265 CrossRefGoogle Scholar
  35. Hansen JC (2002) Conformational dynamics of the chromatin fiber in solution: determinants, mechanisms, and functions. Annu Rev Biophys Biomol Struct 31:361–392. doi: 10.1146/annurev.biophys.31.101101.140858 CrossRefPubMedGoogle Scholar
  36. Hernan GG, Grayson P, Lin H et al (2007) Biological consequences of tightly bent DNA: the other life biological of a macromolecular celebrity. Biopolymers 85:115–130. doi: 10.1002/bip.20627.Biological CrossRefGoogle Scholar
  37. Hjelm RP, Kneale GG, Suau P et al (1977) Small angle neutron scattering studies of chromatin subunits in solution. Cell 10:139–151. doi: 10.1016/0092-8674(77)90148-9 CrossRefPubMedGoogle Scholar
  38. Hoch DA, Stratton JJ, Gloss LM (2007) Protein-protein förster resonance energy transfer analysis of nucleosome core particles containing H2A and H2A.Z. J Mol Biol 371:971–988. doi: 10.1016/j.jmb.2007.05.075 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Holst M, Baker N, Wang F (2000) Adaptive multilevel finite element solution of the Poisson-Boltzmann equation I. Algorithms and examples. J Comput Chem 21:1319–1342. doi: 10.1002/1096-987X(20001130)21:15<1319::AID-JCC1>3.0.CO;2-8 CrossRefGoogle Scholar
  40. Ibel K, Stuhrmann HB (1975) Comparison of neutron and x-ray scattering of dilute myoglobin solutions. J Mol Biol 93:255–265. doi: 10.1016/0022-2836(75)90131-X CrossRefPubMedGoogle Scholar
  41. Inoko Y, Yamamoto M, Satoru F, Ueki T (1992) X-ray scattering study of the shape of the DNA region core particle with synchrotron radiation in nucleosome Yoji Inoko’, Masaki Yamamoto, 2 Satoru Fujiwara, and Tatzuo Ueki2 of Biophysical Engineering, Faculty of Engineering Science, Osaka Received. Structure 316:310–316Google Scholar
  42. Jacques DA, Trewhella J (2010) Small-angle scattering for structural biology-expanding the frontier while avoiding the pitfalls. Protein Sci 19:642–657. doi: 10.1002/pro.351 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Kazantsev AV, Rambo RP, Karimpour S et al (2011) Solution structure of RNase P RNA. RNA 17:1159–1171. doi: 10.1261/rna.2563511 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Koch MH, Vachette P, Svergun DI (2003) Small-angle scattering: a view on the properties, structures and structural changes of biological macromolecules in solution. Q Rev Biophys 36:147–227Google Scholar
  45. Kornberg RD, Lorch Y (1999) Twenty-five years of the nucleosome, fundmamental particle of the eukaryotic chromosome. Cell 98:285–294CrossRefPubMedGoogle Scholar
  46. Korolev N, Vorontsova OV, Nordenskiöld L (2007) Physicochemical analysis of electrostatic foundation for DNA-protein interactions in chromatin transformations. Prog Biophys Mol Biol 95:23–49. doi: 10.1016/j.pbiomolbio.2006.11.003 CrossRefPubMedGoogle Scholar
  47. Korolev N, Allahverdi A, Yang Y et al (2010) Electrostatic origin of salt-induced nucleosome array compaction. Biophys J 99:1896–1905. doi: 10.1016/j.bpj.2010.07.017 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Li M, Wang MD (2012) Unzipping single DNA molecules to study nucleosome structure and dynamics. In: Wu C, Allis CD (eds) Methods in Enzymology, vol. 513. Academic, Burlington, pp. 29-58Google Scholar
  49. Li G, Widom J (2004) Nucleosomes facilitate their own invasion. Nat Struct Mol Biol 11:763–769. doi: 10.1038/nsmb801 CrossRefPubMedGoogle Scholar
  50. Lipfert J, Doniach S (2007) Small-angle x-ray scattering from RNA, proteins, and protein complexes. Annu Rev Biophys Biomol Struct 36:307–327. doi: 10.1146/annurev.biophys.36.040306.132655 CrossRefPubMedGoogle Scholar
  51. Lipfert J, Doniach S, Das R, Herschlag D (2014) Understanding nucleic acid-ion interactions. Annu Rev Biochem 83:813–841. doi: 10.1146/annurev-biochem-060409-092720 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Liu HB, Shi YM, Chen XS, Warshel A (2009) Simulating the electrostatic guidance of the vectorial translocations in hexameric helicases and translocases. Proc Natl Acad Sci U S A 106:7449–7454. doi: 10.1073/pnas.0900532106 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Lohman TM, Overman LB (1985) 2 Binding modes in escherichia-coli single-strand binding protein-single stranded DNA complexes - modulation by nacl concentration. J Biol Chem 260:3594–3603PubMedGoogle Scholar
  54. Luger K, Phillips SE (2010) Rise of the molecular machines. Curr Opin Struct Biol 20:70–72. doi: 10.1016/ CrossRefPubMedPubMedCentralGoogle Scholar
  55. Luger K, Mäder AW, Richmond RK et al (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389:251–260. doi: 10.1038/38444 CrossRefPubMedGoogle Scholar
  56. Luscombe NM, Austin SE, Berman HM, Thornton JM (2000) An overview of the structures of protein-DNA complexes. Genome Biol:11–37Google Scholar
  57. Luzzati V, Masson F, Mathis A (1967) X-ray scattering study of rigid polyelectrolyte solution. lithium, sodium, and cesium salts of DNA. Biopolymers 5:491–508CrossRefGoogle Scholar
  58. Manning GS (1969) Limiting laws and counterion condensation in polyelectrolyte solutions I. Colligative Properties. J Chem Phys 51:924. doi: 10.1063/1.1672157 CrossRefGoogle Scholar
  59. Marko JF, Siggia ED (1995) Stretching DNA. Macromolecules 28:8759–8770. doi: 10.1021/ma00130a008 CrossRefGoogle Scholar
  60. Martin E, Saenger W (2013) Principles of nucleic acid structure. Springer, New YorkGoogle Scholar
  61. Meisburger SP, Pabit SA, Pollack L (2015) Determining the locations of ions and water around DNA from X-ray scattering measurements. Biophys J 108:2886–2895. doi: 10.1016/j.bpj.2015.05.006 CrossRefPubMedGoogle Scholar
  62. Mihardja S, Spakowitz AJ, Zhang Y, Bustamante C (2006) Effect of force on mononucleosomal dynamics. Proc Natl Acad Sci U S A 103:15871–15876. doi: 10.1073/pnas.0607526103 CrossRefPubMedPubMedCentralGoogle Scholar
  63. Morfin I, Horkay F, Basser PJ et al (2004) Adsorption of divalent cations on DNA. Biophys J 87:2897–2904. doi: 10.1529/biophysj.104.045542 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Mouat MF, Manchester KL (1998) The intracellular ionic strength of red cells and the influence of complex formation. Comp Haematol Int 8:58–60CrossRefGoogle Scholar
  65. Ngo TTM, Ha T (2015) Nucleosomes undergo slow spontaneous gaping. Nucleic Acids Res 43:1–8. doi: 10.1093/nar/gkv276 CrossRefGoogle Scholar
  66. Ngo TTM, Zhang Q, Zhou R et al (2015) asymmetric unwrapping of nucleosomes under tension directed by DNA Local Flexibility. Cell 160:1135–1144. doi: 10.1016/j.cell.2015.02.001 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Nguyen HT, Pabit SA, Meisburger SP et al (2014) Accurate small and wide angle x-ray scattering profiles from atomic models of proteins and nucleic acids. J Chem Phys 141:22D508. doi: 10.1063/1.4896220 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Orthaber D, Bergmann A, Glatter O (2000) SAXS experiments on absolute scale with Kratky systems using water as a secondary standard. J Appl Crystallogr 33:218–225. doi: 10.1107/S0021889899015216 CrossRefGoogle Scholar
  69. Pabit SA, Finkelstein KD, Pollack L (2009) Using anomalous small angle X-ray scattering to probe the ion atmosphere around nucleic acids. Methods Enzymol 37:3887–3896Google Scholar
  70. Pabit SA, Qiu X, Lamb JS et al (2009b) Both helix topology and counterion distribution contribute to the more effective charge screening in dsRNA compared with dsDNA. Nucleic Acids Res 37:3887–3896. doi: 10.1093/nar/gkp257 CrossRefPubMedPubMedCentralGoogle Scholar
  71. Pabit SA, Meisburger SP, Li L et al (2010) Counting ions around DNA with anomalous small-angle x-ray scattering. J Am Chem Soc 132:16334–16336. doi: 10.1021/ja107259y CrossRefPubMedPubMedCentralGoogle Scholar
  72. Pardon JF, Worcester DL, Wooley JC et al (1975) Low-angle neutron scattering from chromatin subunit particles. J Chem Inf Model 2:2163–2176. doi: 10.1017/CBO9781107415324.004 Google Scholar
  73. Park S, Bardhan JP, Roux B, Makowski L (2009) Simulated x-ray scattering of protein solutions using explicit-solvent models. J Chem Phys 130:1–8. doi: 10.1063/1.3099611 Google Scholar
  74. Pérez J, Nishino Y (2012) Advances in x-ray scattering: from solution SAXS to achievements with coherent beams. Curr Opin Struct Biol 22:670–678. doi: 10.1016/ CrossRefPubMedGoogle Scholar
  75. Pollack L (2011) SAXS studies of ion-nucleic acid interactions. Annu Rev Biophys 40:225–242. doi: 10.1146/annurev-biophys-042910-155349 CrossRefPubMedGoogle Scholar
  76. Prinsen P, Schiessel H (2010) Nucleosome stability and accessibility of its DNA to proteins. Biochimie 92:1722–1728. doi: 10.1016/j.biochi.2010.08.008 CrossRefPubMedGoogle Scholar
  77. Richmond TJ, Davey CA (2003) The structure of DNA in the nucleosome core. Nature 423:145–150. doi: 10.1038/nature01595 CrossRefPubMedGoogle Scholar
  78. Rocchia W, Alexov E, Honig B (2001) Extending the applicability of the nonlinear Poisson-Boltzmann equation: multiple dielectric constants and multivalent ions. J Phys Chem B 105:6507–6514. doi: 10.1021/jp010454y CrossRefGoogle Scholar
  79. Rohs R, Jin X, West SM et al (2010) Origins of specificity in protein-DNA recognition. Annu Rev Biochem 79:233–269. doi: 10.1146/annurev-biochem-060408-091030 CrossRefPubMedPubMedCentralGoogle Scholar
  80. Sardet C, Tardieu A, Luzzati V (1976) Shape and size of bovine rhodopsin: a small-angle x-ray scattering study of a rhodopsin-detergent complex. J Mol Biol 105:383–407. doi: 10.1016/0022-2836(76)90100-5 CrossRefPubMedGoogle Scholar
  81. Shlyakhtenko LS, Lushnikov AY, Lyubchenko YL (2009) Dynamics of nucleosomes revealed by time-lapse atomic force microscopy. Biochemistry 48:7842–7848. doi: 10.1021/bi900977t CrossRefPubMedPubMedCentralGoogle Scholar
  82. Skou S, Gillilan RE, Ando N (2014) Synchrotron-based small-angle x-ray scattering of proteins in solution. Nat Protoc 9:1727–1739. doi: 10.1038/nprot.2014.116 CrossRefPubMedPubMedCentralGoogle Scholar
  83. Stoddard CD, Montange RK, Hennelly SP et al (2010) Free state conformational sampling of the SAM-I riboswitch aptamer domain. Structure 18:787–797. doi: 10.1016/j.str.2010.04.006.Free CrossRefPubMedPubMedCentralGoogle Scholar
  84. Stuhrmann HB (1974) Neutron small-angle scattering of biological macromolecules in solution. J Appl Crystallogr 7:173–178. doi: 10.1107/S0021889874009071 CrossRefGoogle Scholar
  85. Stuhrmann HB, Kirste RG (1965) Elimination Der Intrapartikularen Untergrundstreuung Bei Der Rontgenkleinwinkelstreuung an Kompakten Teilchen (Proteinen). Z Phys Chem-Frankfurt 46:247CrossRefGoogle Scholar
  86. Stuhrmann HB, Miller A (1978) Small-angle scattering of biological structures. J Appl Crystallogr 11:325–345. doi: 10.1107/S0021889878013473 CrossRefGoogle Scholar
  87. Svergun DI (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J Appl Crystallogr 25:495–503. doi: 10.1107/S0021889892001663 CrossRefGoogle Scholar
  88. Svergun DI, Koch MHJ (1994) Structural model of the 50 S subunit of escherichia coli ribosomes from solution scattering. J Mol Biol 240:66–77CrossRefPubMedGoogle Scholar
  89. Svergun DI, Koch MHJ (2003) Small-angle scattering studies of biological macromolecules in solution. Rep Prog Phys 66:1735–1782. doi: 10.1088/0034-4885/66/10/R05 CrossRefGoogle Scholar
  90. Svergun DI, Pedersen JS, Serdyuk IN, Koch MHJ (1994) Solution scattering from 50S ribosomal subunit resolves inconsistency between electron microscopic models. Proc Natl Acad Sci U S A 91:11826–11830CrossRefPubMedPubMedCentralGoogle Scholar
  91. Svergun DI, Koch MHJ, Timmins PA, May RP (2013) Small angle x-ray and neutron scattering from solutions of biological macromolecules. Oxford University Press, OxfordGoogle Scholar
  92. Sztucki M, Di Cola E, Narayanan T (2012) Anomalous small-angle x-ray scattering from charged soft matter. Eur Phys J Spec Top 208:319–331. doi: 10.1140/epjst/e2012-01627-x CrossRefGoogle Scholar
  93. Tang C, Loeliger E, Luncsford P et al (2004) Entropic switch regulates myristate exposure in the HIV-1 matrix protein. Proc Natl Acad Sci U S A 101:517–522. doi: 10.1073/pnas.0305665101 CrossRefPubMedPubMedCentralGoogle Scholar
  94. Tardieu A, Mateu L, Sardet C et al (1976) Structure of human serum lipoproteins in solution. II. Small-angle x-ray scattering study of HDL3 and LDL. J Mol Biol 101:129–153. doi: 10.1016/0022-2836(76)90368-5 CrossRefPubMedGoogle Scholar
  95. Thommes P, Hubscher U (1992) Review: eukaryotic DNA helicases: essential enzymes for DNA transactions. Chromosoma 101:467–473. doi: 10.1007/BF00352468 CrossRefPubMedGoogle Scholar
  96. Tims HS, Gurunathan K, Levitus M, Widom J (2011) Dynamics of nucleosome invasion by DNA binding proteins. J Mol Biol 411:430–448. doi: 10.1016/j.jmb.2011.05.044 CrossRefPubMedPubMedCentralGoogle Scholar
  97. Ueki T, Inoko Y, Kataoka M et al (1986) X-ray scattering study on hemoglobin solution with synchrotron radiation: a simple analysis of scattering profile at moderate angles in terms of arrangement of subunits. J Biochem 99:1127–1136PubMedGoogle Scholar
  98. Vestergaard B, Sayers Z (2014) Investigating increasingly complex macromolecular systems with small-angle x-ray scattering. IUCrJ 1:523–529. doi: 10.1107/S2052252514020843 CrossRefPubMedPubMedCentralGoogle Scholar
  99. Vlijm R, Lee M, Lipfert J et al (2015) Nucleosome assembly dynamics involve spontaneous fluctuations in the handedness of tetrasomes. Cell Rep 10:216–225. doi: 10.1016/j.celrep.2014.12.022 CrossRefPubMedGoogle Scholar
  100. Widom J (1998) Structure, dynamics, and function of chromatin in vitro. Annu Rev Biophys Biomol Struct 27:285–327. doi: 10.1146/Annurev.Biophys.27.1.285 CrossRefPubMedGoogle Scholar
  101. Wong GCL, Pollack L (2010) Electrostatics of strongly charged biological polymers: ion-mediated interactions and self-organization in nucleic acids and proteins. Annu Rev Phys Chem 61:171–189. doi: 10.1146/annurev.physchem.58.032806.104436 CrossRefPubMedGoogle Scholar
  102. Yager TD, McMurray CT, van Holde KE (1989) Salt-induced release of DNA from nucleosome core particles. Biochemistry 28:2271–2281. doi: 10.1021/bi00431a045 CrossRefPubMedGoogle Scholar
  103. You H, Iino R, Watanabe R, Noji H (2012) Winding single-molecule double-stranded DNA on a nanometer-sized reel. Nucleic Acids Res 1–6. doi:  10.1093/nar/gks651
  104. Zlatanova J, Bishop TC, Victor JM et al (2009) The nucleosome family: dynamic and growing. Structure 17:160–171. doi: 10.1016/j.str.2008.12.016 CrossRefPubMedGoogle Scholar
  105. Zuo X, Cui G, Merz KM et al (2006) X-ray diffraction “fingerprinting” of DNA structure in solution for quantitative evaluation of molecular dynamics simulation. Proc Natl Acad Sci U S A 103:3534–3539. doi: 10.1073/pnas.0600022103 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© International Union for Pure and Applied Biophysics (IUPAB) and Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Joshua M. Tokuda
    • 1
  • Suzette A. Pabit
    • 1
  • Lois Pollack
    • 1
  1. 1.School of Applied and Engineering PhysicsCornell UniversityIthacaUSA

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