Bringing diffuse X-ray scattering into focus

Current Opinion in Structural Biology

Volumn 50, Issue , 2018, Pages 109-116

  Wall, Michael E ^a   Wolff, Alexander M ^b   Fraser, James S ^b  

^a LOS ALAMOS NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRYSTAL STRUCTURE; ELECTRON BEAM; GENE PROBE; LIGHT INTENSITY; MACROMOLECULE; MOLECULAR DYNAMICS; PRIORITY JOURNAL; RADIATION SCATTERING; REVIEW; ROOM TEMPERATURE; SIGNAL NOISE RATIO; SOLVATION; STRUCTURAL MODEL; X RAY CRYSTALLOGRAPHY; X RAY DIFFRACTION; CHEMISTRY; MOLECULAR MODEL; PROCEDURES; PROTEIN CONFORMATION; X RAY;

PROTEIN;

MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; PROTEIN CONFORMATION; PROTEINS; SCATTERING, RADIATION; X-RAY DIFFRACTION; X-RAYS;

EID: 85042198958     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2018.01.009     Document Type: Review

References (68)

1. Burley, S.K., Berman, H.M., Kleywegt, G.J., Markley, J.L., Nakamura, H., Velankar, S., Protein Data Bank (PDB): the single global macromolecular structure archive. Methods Mol Biol 1607 (2017), 627–641.
2. Welberry, T.R., Diffuse X-Ray Scattering and Models of Disorder. 2004, Oxford University Press, Oxford.
3. Keen, D.A., Goodwin, A.L., The crystallography of correlated disorder. Nature 521 (2015), 303–309.
4. Caspar, D.L., Clarage, J., Salunke, D.M., Clarage, M., Liquid-like movements in crystalline insulin. Nature 332 (1988), 659–662.
5. Chacko, S., Phillips, G.N. Jr., Diffuse X-ray scattering from tropomyosin crystals. Biophys J 61 (1992), 1256–1266.
6. Clarage, J.B., Clarage, M.S., Phillips, W.C., Sweet, R.M., Caspar, D.L., Correlations of atomic movements in lysozyme crystals. Proteins 12 (1992), 145–157.
7. Clarage, J.B., Romo, T., Andrews, B.K., Pettitt, B.M., Phillips, G.N. Jr., A sampling problem in molecular dynamics simulations of macromolecules. Proc Natl Acad Sci U S A 92 (1995), 3288–3292.
8. Doucet, J., Benoit, J.P., Molecular dynamics studied by analysis of the X-ray diffuse scattering from lysozyme crystals. Nature 325 (1987), 643–646.
9. Faure, P., Micu, A., Pérahia, D., Doucet, J., Smith, J.C., Benoit, J.P., Correlated intramolecular motions and diffuse X-ray scattering in lysozyme. Nat Struct Biol 1 (1994), 124–128.
10. Glover, I.D., Harris, G.W., Helliwell, J.R., Moss, D.S., The variety of X-ray diffuse-scattering from macromolecular crystals and its respective components. Acta Crystallogr B 47 (1991), 960–968.
11. Helliwell, J.R., Glover, I.D., Jones, A., Pantos, E., Moss, D.S., Protein dynamics — use of computer-graphics and protein crystal diffuse-scattering recorded with synchrotron X-radiation. Biochem Soc Transact 14 (1986), 653–655.
12. Kolatkar, A.R., Clarage, J.B., Phillips, G.N. Jr., Analysis of diffuse scattering from yeast initiator tRNA crystals. Acta Crystallogr D 50 (1994), 210–218.
13. Mizuguchi, K., Kidera, A., Gō, N., Collective motions in proteins investigated by X-ray diffuse scattering. Proteins 18 (1994), 34–48.
14. Perez, J., Faure, P., Benoit, J.P., Molecular rigid-body displacements in a tetragonal lysozyme crystal confirmed by X-ray diffuse scattering. Acta Crystallogr D: Biol Crystallogr 52 (1996), 722–729.
15. Phillips, G.N. Jr., Fillers, J.P., Cohen, C., Motions of tropomyosin. Crystal as metaphor. Biophys J 32 (1980), 485–502.
16. Polikanov, Y.S., Moore, P.B., Acoustic vibrations contribute to the diffuse scatter produced by ribosome crystals. Acta Crystallogr D: Biol Crystallogr 71 (2015), 2021–2031 Careful analysis of the diffuse scattering present in 70S ribosome crystals revealed that lattice vibrations may explain a significant portion of the diffuse signal, highlighting the importance of models that account for correlated variations across unit cell boundaries.
17. Wall, M.E., Clarage, J.B., Phillips, G.N., Motions of calmodulin characterized using both Bragg and diffuse X-ray scattering. Structure 5 (1997), 1599–1612.
18. Wall, M.E., Ealick, S.E., Gruner, S.M., Three-dimensional diffuse X-ray scattering from crystals of staphylococcal nuclease. Proc Natl Acad Sci U S A 94 (1997), 6180–6184.
19. Van Benschoten, A.H., Liu, L., Gonzalez, A., Brewster, A.S., Sauter, N.K., Fraser, J.S., Wall, M.E., Measuring and modeling diffuse scattering in protein X-ray crystallography. Proc Natl Acad Sci U S A 113 (2016), 4069–4074 Diffuse data is extracted from data collected under optimal conditions for Bragg analysis, revealing that modern PAD detectors and fine phi slicing can make diffuse data widely available. Also, LLM and normal modes models of disorder account for a substantial portion of the diffuse signal isolated from cypa and trypsin.
20. Wall, M.E., Adams, P.D., Fraser, J.S., Sauter, N.K., Diffuse X-ray scattering to model protein motions. Structure 22 (2014), 182–184.
21. Meinhold, L., Smith, J.C., Correlated dynamics determining X-ray diffuse scattering from a crystalline protein revealed by molecular dynamics simulation. Phys Rev Lett, 95, 2005, 218103.
22. Wall, M.E., Van Benschoten, A.H., Sauter, N.K., Adams, P.D., Fraser, J.S., Terwilliger, T.C., Conformational dynamics of a crystalline protein from microsecond-scale molecular dynamics simulations and diffuse X-ray scattering. Proc Natl Acad Sci U S A 111 (2014), 17887–17892 In this study, the authors demonstrate the importance of long time-scale simulations to accurately sample a protein's correlated motions. The improvement is most evident when examining the anisotropic portion of the diffuse signal attributed to protein dynamics alone.
23. Holton, J.M., Classen, S., Frankel, K.A., Tainer, J.A., The R-factor gap in macromolecular crystallography: an untapped potential for insights on accurate structures. FEBS J 281 (2014), 4046–4060.
24. Fraser, J.S., van den Bedem, H., Samelson, A.J., Lang, P.T., Holton, J.M., Echols, N., Alber, T., Accessing protein conformational ensembles using room-temperature X-ray crystallography. Proc Natl Acad Sci U S A 108 (2011), 16247–16252.
25. Wall, M.E., Sweet, R.M., Ando, N., Fraser, J.S., Phillips, G.N., Measurement and Interpretation of Diffuse Scattering in X-Ray Diffraction for Macromolecular Crystallography. 2017 https://www.osti.gov/scitech/biblio/1400134.
26. Meisburger, S.P., Thomas, W.C., Watkins, M.B., Ando, N., X-ray scattering studies of protein structural dynamics. Chem Rev 117 (2017), 7615–7672 This excellent review thoroughly lays out the connection between diffuse scattering, solution scattering, and crystallography. The assumptions and limitations of various approaches to analyzing diffuse data are clearly explained, and several disorder models are explored using case studies of biochemical interest.
27. Wall, M.E., Diffuse features in X-ray diffraction from protein crystals. (Ph.D.) Physics, 1996, Princeton University.
28. Ayyer, K., Yefanov, O.M., Oberthur, D., Roy-Chowdhury, S., Galli, L., Mariani, V., Basu, S., Coe, J., Conrad, C.E., Fromme, R., et al. Macromolecular diffractive imaging using imperfect crystals. Nature 530 (2016), 202–206 This work extends the analysis of diffuse X-ray scattering into the realm of XFELS and serial crystallography, while also advocating for the use of diffuse scattering for phasing and resolution extension. Rigid body translations of the PSII dimer are the proposed source of the diffuse signal.
29. Sui, S., Wang, Y., Kolewe, K.W., Srajer, V., Henning, R., Schiffman, J.D., Dimitrakopoulos, C., Perry, S.L., Graphene-based microfluidics for serial crystallography. Lab Chip 16 (2016), 3082–3096 Graphene coated microfluidic chips enable collection of diffraction data with very high signal-to-noise, and may provide an alternative to jet based delivery systems for SFX experiments.
30. Estermann, M.A., Steurer, W., Diffuse scattering data acquisition techniques. Phase Transit 67 (1998), 165–195.
31. Peck, A., Poitevin, F., Lane, T.J., Intermolecular correlations are necessary to explain diffuse scattering from protein crystals. IUCrJ, 5, 2018 in press The authors approach diffuse scattering from a modelling perspective, and rigorously test current disorder models against a series of experimental datasets. Quantitative tests allow them to discern that most disorder models explain a limited portion of the diffuse signal, and that a LLM model is the best option, especially when correlations across unit cell boundaries are included.
32. Wall, M.E., Methods and software for diffuse X-ray scattering from protein crystals. Methods Mol Biol 544 (2009), 269–279.
33. Wall, M.E., Internal protein motions in molecular dynamics simulations of Bragg and diffuse X-ray scattering. IUCrJ, 5, 2017, 10.1107/S2052252518000519 A molecular dynamics simulation of diffuse X-ray scattering from staphylococcal nuclease crystals is greatly improved when the unit cell model is expanded to a 2 × 2 × 2 layout of eight unit cells. The dynamics are dominated by internal protein motions rather than rigid packing interactions.
34. Winter, G., Lobley, C.M., Prince, S.M., Decision making in xia2. Acta Crystallogr D: Biol Crystallogr 69 (2013), 1260–1273.
35. Grosse-Kunstleve, R.W., Sauter, N.K., Moriarty, N.W., Adams, P.D., The Computational Crystallography Toolbox: crystallographic algorithms in a reusable software framework. J Appl Crystallogr 35 (2002), 126–136.
36. Haliloglu, T., Bahar, I., Adaptability of protein structures to enable functional interactions and evolutionary implications. Curr Opin Struct Biol 35 (2015), 17–23.
37. Riccardi, D., Cui, Q., Phillips, G.N. Jr., Evaluating elastic network models of crystalline biological molecules with temperature factors, correlated motions, and diffuse X-ray scattering. Biophys J 99 (2010), 2616–2625.
38. Meinhold, L., Merzel, F., Smith, J.C., Lattice dynamics of a protein crystal. Phys Rev Lett, 99, 2007, 138101.
39. James, R., The Optical Principles of the Diffraction of X-Rays. 1948, Bell, London.
40. Suhre, K., Sanejouand, Y.H., ElNemo: a normal mode web server for protein movement analysis and the generation of templates for molecular replacement. Nucleic Acids Res 32 (2004), W610–W614.
41. Schilbach, S., Hantsche, M., Tegunov, D., Dienemann, C., Wigge, C., Urlaub, H., Cramer, P., Structures of transcription pre-initiation complex with TFIIH and Mediator. Nature 551 (2017), 204–209.
42. Van Benschoten, A.H., Afonine, P.V., Terwilliger, T.C., Wall, M.E., Jackson, C.J., Sauter, N.K., Adams, P.D., Urzhumtsev, A., Fraser, J.S., Predicting X-ray diffuse scattering from translation-libration-screw structural ensembles. Acta Crystallogr D: Biol Crystallogr 71 (2015), 1657–1667 Predicted diffuse scattering patterns differ substantially across different TLS models derived from the same data. This provides an important proof of principle for the use of diffuse scattering in refinement of macromolecular models.
43. Burnley, B.T., Afonine, P.V., Adams, P.D., Gros, P., Modelling dynamics in protein crystal structures by ensemble refinement. Elife, 1, 2012, e00311.
44. Levin, E.J., Kondrashov, D.A., Wesenberg, G.E., Phillips, G.N. Jr., Ensemble refinement of protein crystal structures: validation and application. Structure 15 (2007), 1040–1052.
45. Héry, S., Genest, D., Smith, J.C., X-ray diffuse scattering and rigid-body motion in crystalline lysozyme probed by molecular dynamics simulation. J Mol Biol 279 (1998), 303–319.
46. Meinhold, L., Smith, J.C., Fluctuations and correlations in crystalline protein dynamics: a simulation analysis of Staphylococcal nuclease. Biophys J 88 (2005), 2554–2563.
47. Meinhold, L., Smith, J.C., Protein dynamics from X-ray crystallography: anisotropic, global motion in diffuse scattering patterns. Proteins 66 (2007), 941–953.
48. Janowski, P.A., Cerutti, D.S., Holton, J., Case, D.A., Peptide crystal simulations reveal hidden dynamics. J Am Chem Soc 135 (2013), 7938–7948.
49. Janowski, P.A., Liu, C., Deckman, J., Case, D.A., Molecular dynamics simulation of triclinic lysozyme in a crystal lattice. Protein Sci 25 (2016), 87–102 MD simulations of lysozyme in a crystalline lattice reveal enhanced agreement with structural models derived from Bragg data. Nonetheless, convergence is slow, the lattice becomes disordered, and fluctuations of residues involved in crystal contacts are too high, indicating the need for improved MD force fields.
50. Kurauskas, V., Izmailov, S.A., Rogacheva, O.N., Hessel, A., Ayala, I., Woodhouse, J., Shilova, A., Xue, Y., Yuwen, T., Coquelle, N., et al. Slow conformational exchange and overall rocking motion in ubiquitin protein crystals. Nat Commun, 8, 2017, 145.
51. Ma, P., Xue, Y., Coquelle, N., Haller, J.D., Yuwen, T., Ayala, I., Mikhailovskii, O., Willbold, D., Colletier, J.P., Skrynnikov, N.R., et al. Observing the overall rocking motion of a protein in a crystal. Nat Commun, 6, 2015, 8361.
52. Mollica, L., Baias, M., Lewandowski, J.R., Wylie, B.J., Sperling, L.J., Rienstra, C.M., Emsley, L., Blackledge, M., Atomic-resolution structural dynamics in crystalline proteins from NMR and molecular simulation. J Phys Chem Lett 3 (2012), 3657–3662.
53. Elser, V., Millane, R.P., Reconstruction of an object from its symmetry-averaged diffraction pattern. Acta Crystallogr Sect A 64 (2008), 273–279.
54. Stroud, R.M., Agard, D.A., Structure determination of asymmetric membrane profiles using an iterative Fourier method. Biophys J 25 (1979), 495–512.
55. Makowski, L., The use of continuous diffraction data as a phase constraint. 1. One-dimensional theory. J Appl Crystallogr 14 (1981), 160–168.
56. Chapman, H.N., Yefanov, O.M., Ayyer, K., White, T.A., Barty, A., Morgan, A., Mariani, V., Oberthuer, D., Pande, K., Continuous diffraction of molecules and disordered molecular crystals. J Appl Crystallogr 50 (2017), 1084–1103.
57. Caliandro, R., Carrozzini, B., Cascarano, G.L., De Caro, L., Giacovazzo, C., Siliqi, D., Phasing at resolution higher than the experimental resolution. Acta Crystallogr D: Biol Crystallogr 61 (2005), 556–565.
58. Wang, B.C., Resolution of phase ambiguity in macromolecular crystallography. Methods Enzymol 115 (1985), 90–112.
59. Fischer, N., Neumann, P., Konevega, A.L., Bock, L.V., Ficner, R., Rodnina, M.V., Stark, H., Structure of the E. coli ribosome-EF-Tu complex at <3 A resolution by Cs-corrected cryo-EM. Nature 520 (2015), 567–570.
60. Bhat, T.N., Cohen, G.H., OMITMAP: an electron density map suitable for the examination of errors in a macromolecular model. J Appl Cryst 17 (1984), 244–248.
61. Moore, P.B., On the relationship between diffraction patterns and motions in macromolecular crystals. Structure 17 (2009), 1307–1315.
62. Guinier, A., X-Ray Diffraction in Crystals, Imperfect Crystals, and Amorphous Bodies. 1963, W. H. Freeman and Company, San Francisco.
63. Clarage, J.B., Phillips, G.N. Jr., Analysis of diffuse scattering and relation to molecular motion. Methods Enzymol 277 (1997), 407–432.
64. Chaudhry, C., Horwich, A.L., Brunger, A.T., Adams, P.D., Exploring the structural dynamics of the E. coli chaperonin GroEL using translation-libration-screw crystallographic refinement of intermediate states. J Mol Biol 342 (2004), 229–245.
65. Meyer, P.A., Socias, S., Key, J., Ransey, E., Tjon, E.C., Buschiazzo, A., Lei, M., Botka, C., Withrow, J., Neau, D., et al. Data publication with the structural biology data grid supports live analysis. Nat Commun, 7, 2016, 10882.
66. Maia, F.R., The coherent X-ray imaging data bank. Nat Methods 9 (2012), 854–855.
67. Kroon-Batenburg, L.M., Helliwell, J.R., McMahon, B., Terwilliger, T.C., Raw diffraction data preservation and reuse: overview, update on practicalities and metadata requirements. IUCrJ 4 (2017), 87–99.
68. Shoemaker, S., Ando, N., X-rays in the cryo-EM era: structural biology's dynamic future. Biochemistry 57 (2017), 277–285.