Biostructural Science Inspired by Next-Generation X-Ray Sources

Annual Review of Biophysics

Volumn 44, Issue , 2015, Pages 33-51

  Gruner, Sol M ^a,b,c   Lattman, Eaton E ^d,e,f  

^a Department of Physics ^*  (United States)

^b Department of Molecular Biology and Genetics   (United States)

^c School of Chemical and Molecular Engineering   (United States)

^d HAUPTMAN WOODWARD MEDICAL RESEARCH INSTITUTE   (United States)

^e UNIVERSITY AT BUFFALO   (United States)

^f BioXFEL Science and Technology Center   (United States)

Author keywords

Biomolecular solution scattering; Bright storage ring sources; Energy recovery linac; Microcrystallography; Nanocrystallography; Synchrotron radiation sources; X ray free electron laser

Indexed keywords

ETHINYLESTRADIOL PLUS MEGESTROL ACETATE; PROTEIN;

ARTICLE; COMPTON EFFECT; ENERGY RECOVERY; LIGHT ABSORPTION; LINEAR ACCELERATOR; MOLECULAR DYNAMICS; PRIORITY JOURNAL; SYNCHROTRON RADIATION; X RAY CRYSTALLOGRAPHY; CHEMISTRY; CRYSTALLOGRAPHY; DEVICES; PROCEDURES; SYNCHROTRON; TRENDS;

CRYSTALLOGRAPHY; CRYSTALLOGRAPHY, X-RAY; PROTEINS; SYNCHROTRONS;

EID: 84937398926     PISSN: 1936122X     EISSN: 19361238     Source Type: Book Series    
DOI: 10.1146/annurev-biophys-060414-033813     Document Type: Article

References (112)

1. Amunts A, Brown A, Bai XC, Llácer JL, Hussain T, et al. 2014. Structure of the yeast mitochondrial large ribosomal subunit. Science 343: 1485-89
2. Ansari A, Berendzen J, Bowne SF, FrauenfelderH, Iben IET, et al. 1985. Protein states and proteinquakes. PNAS 82: 5000-4
3. Aquila A, Hunter MS, Doak RB, Kirian RA, Fromme P, et al. 2012. Time-resolved protein nanocrystallography using an X-ray free-electron laser. Opt. Express 20: 2706-16
4. Arnlund D, Johansson LC, Wickstrand C, Barty A, Williams GJ, et al. 2014. Visualizing a protein quake with time-resolved X-ray scattering at a free-electron laser. Nat. Methods 11: 923-26
5. Ayyer K. 2014. Reconstructing images from sparse data. PhD Thesis, Cornell Univ. Press
6. Ayyer K, PhilippHT, Tate MW, Elser V, Gruner SM. 2014. Real-space X-ray tomographic reconstruction of randomly oriented objects with sparse data frames. Opt. Express 22: 2403-13
7. Ayyer K, Philipp HT, Tate MW, Wierman JL, Elser V, Gruner SM. 2014. Determination of crystallographic intensities from sparse data. IUCrJ 2: 29-34
8. Ballabriga R, Alozy J, Campbell M, Fiederle M, Fröjdh E, et al. 2013. TheMedipix3RX: A high resolution, zero dead-time pixel detector readout chip allowing spectroscopic imaging. J. Instrum. 8: 2
9. Barends TRM, Foucar L, Botha S, Doak RB, Shoeman RL, et al. 2014. De novo protein crystal structure determination from X-ray free-electron laser data. Nature 505: 244-47
10. Barty A, Caleman C, Aquila A, Timneanu N, Lomb L, et al. 2012. Self-terminating diffraction gates femtosecond X-ray nanocrystallography measurements. Nat. Photonics 6: 35-40
11. Barty A, Küpper J, Chapman HN. 2013. Molecular imaging using X-ray free-electron lasers. Annu. Rev. Phys. Chem. 64: 415-35
12. Bass M, ed. 2001. Handbook of Optics. Volume III: Classical Optics, Vision Optics, X-Ray Optics. New York: McGraw-Hill
13. Bei M, Borland M, Cai Y, Elleaume P, Gerig R, et al. 2010. The potential of an ultimate storage ring for future light sources. Nuclear Instrum. Methods Phys. Res. A 622: 518-35
14. Bilderback DH, Brock JD, Dale DS, Finkelstein KD, Pfeifer MA, Gruner SM. 2010. Energy recovery linac (ERL) coherent hard X-ray sources. New J. Phys. 12: 035011
15. Blanchet CE, Svergun DI. 2013. Small-angle X-ray scattering on biological macromolecules and nanocomposites in solution. Annu. Rev. Phys. Chem. 64: 37-54
16. Bogan MJ. 2013. X-ray free electron lasers motivate bioanalytical characterization of protein nanocrystals: serial femtosecond crystallography. Anal. Chem. 85: 3464-71
17. Boutet S, Lomb L, Williams GJ, Barends TRM, Aquila A, et al. 2012. High-resolution protein structure determination by serial femtosecond crystallography. Science 337: 362-64
18. BrehmW, DiederichsK. 2014. Breaking the indexing ambiguity in serial crystallography. Acta Crystallogr. D 70: 101-9
19. Bunch JS, Verbridge SS, Alden JS, van der Zande AM, Parpia JM, et al. 2008. Impermeable atomic membranes from graphene sheets. Nano Lett. 8: 2458-62
20. Chapman HN, Fromme P, Barty A, White TA, Kirian RA, et al. 2011. Femtosecond X-ray protein nanocrystallography. Nature 470: 73-77
21. Cho HS, Schotte F, Dashdorj N, Kyndt J, Anfinrud PA. 2013. Probing anisotropic structure changes in proteins with picosecond time-resolved small-angle X-ray scattering. J. Phys. Chem. B 117: 15825-32
22. Cogdell RJ, Gall A, Köhler J. 2006. The architecture and function of the light-harvesting apparatus of purple bacteria: from single molecules to in vivo membranes. Q. Rev. Biophys. 39: 227-324
23. Deisenhofer J, Epp O, Sinning I, Michel H. 1995. Crystallographic refinement at 2. 3A? Resolution and refined model of the photosynthetic reaction centre from Rhodopseudomonas viridis. J. Mol. Biol. 246: 429-57
24. Demirci H, Sierra RG, Laksmono H, Shoeman RL, Botha S, et al. 2013. Serial femtosecond X-ray diffraction of 30S ribosomal subunit microcrystals in liquid suspension at ambient temperature using an X-ray free-electron laser. Acta Crystallogr. F 69: 1066-69
25. Donatelli JJ, Sethian JA. 2014. Algorithmic framework for X-ray nanocrystallographic reconstruction in the presence of the indexing ambiguity. PNAS 111: 593-98
26. Elser V. 2003. Phase retrieval by iterated projections. J. Opt. Soc. Am. A 20: 40-55
27. Elser V. 2009. Noise limits on reconstructing diffraction signals from random tomographs. IEEE Trans. Inf. Theory 55: 4715-22
28. ElserV. 2011. Strategies for processing diffraction data from randomly oriented particles. Ultramicroscopy 111: 788-92
29. Elser V. 2011. Three-dimensional structure from intensity correlations. New J. Phys. 13: 123014
30. Falcone R, Jacobsen C, Kirz J, Marchesini S, Shapiro D, Spence J. 2011. New directions in X-ray microscopy. Contemp. Phys. 52: 293-318
31. Foucar L, Barty A, Coppola N, Hartmann R, Holl P, et al. 2012. CASS-CFEL-ASG software suite. Comput. Phys. Commun. 183: 2207-13
32. Garman EF, Nave C. 2009. Radiation damage in protein crystals examined under various conditions by different methods. J. Synchrotron Radiat. 16: 129-32
33. Gasbarro A, Bazarov I. 2014. Reduced forms of the Wigner distribution function for the numerical analysis of rotationally symmetric synchrotron radiation. J. Synchrotron Radiat. 21: 289-99
34. Gati C, Bourenkov G, Klinge M, Rehders D, Stellato F, et al. 2014. Serial crystallography on in vivo grown microcrystals using synchrotron radiation. IUCrJ 1: 87-94
35. GimenezEN, Ballabriga R, CampbellM, Horswell I, Dolbnya I, et al. 2011. Characterization ofMedipix3 with synchrotron radiation. IEEE Trans. Nuclear Sci. 58: 323-32
36. Gimenez EN, Ballabriga R, Campbell M, Horswell I, Llopart X, et al. 2011. Study of charge-sharing in MEDIPIX3 using a micro-focused synchrotron beam. J. Instrum. 6: C01031
37. Glatter O, Kratky O. 1982. Small Angle X-Ray Scattering. New York: Academic
38. Greber BJ, Boehringer D, Leitner A, Bieri P, Voigts-Hoffmann F, et al. 2014. Architecture of the large subunit of the mammalian mitochondrial ribosome. Nature 505: 515-19
39. Hau-Riege SP. 2012. Photoelectron dynamics in X-ray free-electron-laser diffractive imaging of biological samples. Phys. Rev. Lett. 108: 238101
40. Hau-Riege SP. 2013. Nonequilibrium electron dynamics in materials driven by high-intensity X-ray pulses. Phys. Rev. E 87: 053102
41. HeymannM, Opthalage A, Wierman JL, Akella S, Szebenyi DME, et al. 2014. Room-temperature serial crystallography using a kinetically optimized microfluidic device for protein crystallization and on-chip X-ray diffraction. IUCrJ 1: 349-60
42. Holton JM. 2009. A beginner's guide to radiation damage. J. Synchrotron Radiat. 16: 133-42
43. Holton JM, Frankel KA. 2010. Theminimum crystal size needed for a complete diffraction data set. Acta Crystallogr. D 66: 393-408
44. Hosseinizadeh A, Schwander P, Dashti A, Fung R, D'Souza RM, Ourmazd A. 2014. High-resolution structure of viruses from random diffraction snapshots. Philos. Trans. R. Soc. B 369: 20130326
45. Howells MR, Beetz T, Chapman HN, Cui C, Holton JM, et al. 2009. An assessment of the resolution limitation due to radiation-damage in X-ray diffraction microscopy. J. Electron Spectrosc. Relat. Phenom. 170: 4-12
46. Hunter MS, Fromme P. 2011. Toward structure determination using membrane-protein nanocrystals and microcrystals. Methods 55: 387-404
47. Hura GL, Menon AL, Hammel M, Rambo RP, Poole FL 2nd, et al. 2009. Robust, high-throughput solution structural analyses by small angle X-ray scattering (SAXS). Nat. Methods 6: 606-12
48. Johansson LC, Arnlund D, Katona G, White TA, Barty A, et al. 2013. Structure of a photosynthetic reaction centre determined by serial femtosecond crystallography. Nat. Commun. 4: 2911
49. Johansson LC, Arnlund D, White TA, Katona G, DePonte DP, et al. 2012. Lipidic phase membrane protein serial femtosecond crystallography. Nat. Methods 9: 263-65
50. Kam Z. 1977. Determination of macromolecular structure in solution by spatial correlation of scattering fluctuations. Macromolecules 10: 927-34
51. Kam Z, Gafni I. 1985. Three-dimensional reconstruction of the shape of human wart virus using spatial correlations. Ultramicroscopy 17: 251-62
52. Kam Z, Koch MHJ, Bordas J. 1981. Fluctuation X-ray-scattering from biological particles in frozen solution by using synchrotron radiation. PNAS 78: 3559-62
53. Kang HJ, Lee C, Drew D. 2013. Breaking the barriers in membrane protein crystallography. Int. J. Biochem. Cell Biol. 45: 636-44
54. Kim KJ. 1986. Brightness, coherence and propagation characteristics of synchrotron radiation. Nuclear Instrum. Methods Phys. Res. A 246: 71-76
55. Kirian RA. 2012. Structure determination through correlated fluctuations in X-ray scattering. J. Phys. B 45: 223001
56. Kirian RA, Schmidt KE, Wang X, Doak RB, Spence JC. 2011. Signal, noise, and resolution in correlated fluctuations from snapshot small-angle X-ray scattering. Phys. Rev. E 84: 011921
57. Koch MHJ, 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: 147-227
58. Kuhlbrandt W. 2014. The resolution revolution. Science 343: 1443-44
59. LiuHG, Poon BK, Saldin DK, Spence JCH, Zwart PH. 2013. Three-dimensional single-particle imaging using angular correlations from X-ray laser data. Acta Crystallogr. A 69: 365-73
60. Liu W, Wacker D, Gati C, Han GW, James D, et al. 2013. Serial femtosecond crystallography of G protein-coupled receptors. Science 342: 1521-24
61. Loh ND. 2014. A minimal view of single-particle imaging with X-ray lasers. Philos. Trans. R. Soc. B 369: 20130328
62. Loh ND, Bogan MJ, Elser V, Barty A, Boutet S, et al. 2010. Cryptotomography: reconstructing 3D Fourier intensities from randomly oriented single-shot diffraction patterns. Phys. Rev. Lett. 104: 225501
63. Loh NTD, Elser V. 2009. Reconstruction algorithm for single-particle diffraction imaging experiments. Phys. Rev. E 80: 026705
64. McNeil BWJ, Thompson NR. 2010. X-ray free-electron lasers. Nat. Photonics 4: 814-21
65. Mendez D, Lane TJ, Sung J, Sellberg J, Levard C, et al. 2014. Observation of correlated X-ray scattering at atomic resolution. Philos. Trans. R. Soc. B 369: 20130315
66. Nave C, Garman EF. 2005. Towards an understanding of radiation damage in cryocooled macromolecular crystals. J. Synchrotron Radiat. 12: 257-60
67. Nave C, Hill MA. 2005. Will reduced radiation damage occur with very small crystals? J. Synchrotron Radiat. 12: 299-303
68. Nederlof I, Li YW, van Heel M, Abrahams JP. 2013. Imaging protein three-dimensional nanocrystals with cryo-EM. Acta Crystallogr. D 69: 852-59
69. Nederlof I, van Genderen E, Li YW, Abrahams JP. 2013. A Medipix quantum area detector allows rotation electron diffraction data collection from submicrometre three-dimensional protein crystals. Acta Crystallogr. D 69: 1223-30
70. Neutze R, Moffat K. 2012. Time-resolved structural studies at synchrotrons and X-ray free electron lasers: opportunities and challenges. Curr. Opin. Struct. Biol. 22: 651-59
71. Neutze R, Wouts R, van der Spoel D, Weckert E, Hajdu J. 2000. Potential for biomolecular imaging with femtosecond X-ray pulses. Nature 406: 752-57
72. Ohashi H, Yamazaki H, Yumoto H, Koyama T, Senba Y, et al. 2013. Stable delivery of nano-beams for advanced nano-scale analyses. J. Phys. 425: 052018
73. Perry SL, Guha S, Pawate AS, Bhaskarla A, Agarwal V, et al. 2013. A microfluidic approach for protein structure determination at room temperature via on-chip anomalous diffraction. Lab Chip 13: 3183-87
74. Philipp HT, Ayyer K, Tate MW, Elser V, Gruner SM. 2012. Solving structure with sparse, randomlyoriented X-ray data. Opt. Express 20: 13129-37
75. Philipp HT, Ayyer K, Tate MW, Elser V, Gruner SM. 2013. Recovering structure from many lowinformation 2-D images of randomly selected samples. J. Phys. 425: 192016
76. Pollack L. 2011. SAXS studies of ion-nucleic acid interactions. Annu. Rev. Biophys. 40: 225-42
77. Poon HC, Saldin DK. 2011. Beyond the crystallization paradigm: structure determination from diffraction patterns from ensembles of randomly oriented particles. Ultramicroscopy 111: 798-806
78. Putnam CD, Hammel M, Hura GL, Tainer JA. 2007. X-ray solution scattering (SAXS) combined with crystallography and computation: defining accurate macromolecular structures, conformations and assemblies in solution. Q. Rev. Biophys. 40: 191-285
79. Quevillon-Cheruel S, Dominique L, Leulliot N, Graille M, Poupon A, et al. 2004. The Paris-Sud yeast structural genomics pilot-project: from structure to function. Biochimie 86: 617-23
80. Ravelli RBG, Garman EF. 2006. Radiation damage in macromolecular cryocrystallography. Curr. Opin. Struct. Biol. 16: 624-29
81. Redecke L, Nass K, DePonte DP, White TA, Rehders D, et al. 2013. Natively inhibited Trypanosoma brucei cathepsin B structure determined by using an X-ray laser. Science 339: 227-30
82. Saldin DK, Poon HC, Bogan MJ, Marchesini S, Shapiro DA, et al. 2011. New light on disordered ensembles: Ab initio structure determination of one particle from scattering fluctuations of many copies. Phys. Rev. Lett. 106: 115501
83. Saldin DK, Poon HC, Schwander P, Uddin M, Schmidt M. 2011. Reconstructing an icosahedral virus from single-particle diffraction experiments. Opt. Express 19: 17318-35
84. Sanishvili R, Yoder DW, Pothineni SB, Rosenbaum G, Xu SL, et al. 2011. Radiation damage in protein crystals is reduced with a micron-sized X-ray beam. PNAS 108: 6127-32
85. Sauter NK, Hattne J, Grosse-Kunstleve RW, Echols N. 2013. New Python-based methods for data processing. Acta Crystallogr. D 69: 1274-82
86. Schlichting I, Miao J. 2012. Emerging opportunities in structural biology with X-ray free-electron lasers. Curr. Opin. Struct. Biol. 22: 613-26
87. Schmidt M. 2013. Mix and inject: reaction initiation by diffusion for time-resolved macromolecular crystallography. Adv. Condens. Matter Phys. http: //dx. doi. org/10. 1155/2013/167276
88. Schmidt-Krey I, ChengY, eds. 2013. Electron Crystallography of Soluble and Membrane Proteins. Heidelberg, Ger. : Springer
89. Schotte F, Cho HS, Kaila VRI, Kamikubo H, Dashdorj N, et al. 2012. Watching a signaling protein function in real time via 100-ps time-resolved Laue crystallography. PNAS 109: 19256-61
90. Shi D, Nannenga BL, Iadanza MG, Gonen T. 2013. Three-dimensional electron crystallography of protein microcrystals. Elife 2: e0 1345: 1-17
91. Shim JU, CristobalG, LinkDR, Thorsen T, Fraden S. 2007. Using microfluidics to decouple nucleation and growth of protein crystals. Crystal Growth Design 7: 2192-94
92. Shim JU, Cristobal G, Link DR, Thorsen T, Jia YW, et al. 2007. Control and measurement of the phase behavior of aqueous solutions using microfluidics. J. Am. Chem. Soc. 129: 8825-35
93. Shneerson VL, Saldin DK. 2009. Molecular shapes from small-angle X-ray scattering: extension of the theory to higher scattering angles. Acta Crystallogr. A 65: 128-34
94. Sliz P, Harrison SC, Rosenbaum G. 2003. How does radiation damage in protein crystals depend on X-ray dose? Structure 11: 13-19
95. Snell EH, Helliwell JR. 2005. Macromolecular crystallization in microgravity. Rep. Prog. Phys. 68: 799-853
96. Spence JCH, Weierstall U, Chapman HN. 2012. X-ray lasers for structural and dynamic biology. Rep. Prog. Phys. 75: 102601
97. Starodub D, Aquila A, Bajt S, BarthelmessM, Barty A, et al. 2012. Single-particle structure determination by correlations of snapshot X-ray diffraction patterns. Nat. Commun. 3: 1276
98. Stellato F, Oberth ür D, LiangM, Bean R, Gati C, et al. 2014. Room-temperature macromolecular serial crystallography using synchrotron radiation. IUCrJ 1: 204-12
99. Svergun DI, Koch MHJ. 2002. Advances in structure analysis using small-angle scattering in solution. Curr. Opin. Struct. Biol. 12: 654-60
100. Thibault P, Elser V. 2010. X-ray diffraction microscopy. Annu. Rev. Condens. Matter Phys. 1: 237-55
101. Warkentin M, Badeau R, Hopkins J, Thorne RE. 2011. Dark progression reveals slow timescales for radiation damage between T = 180 and 240 K. Acta Crystallogr. D 67: 792-803
102. Weierstall U, James D, Wang C, White TA, Wang D, et al. 2014. Lipidic cubic phase injector facilitates membrane protein serial femtosecond crystallography. Nat. Commun. 5: 3309
103. Weierstall U, Spence JCH, Doak RB. 2012. Injector for scattering measurements on fully solvated biospecies. Rev. Sci. Instrum. 83: 035108
104. White TA, Barty A, Stellato F, Holton JM, Kirian RA, et al. 2013. Crystallographic data processing for free-electron laser sources. Acta Crystallogr. D 69: 1231-40
105. White TA, Kirian RA, Martin AV, Aquila A, Nass K, et al. 2012. CrystFEL: A software suite for snapshot serial crystallography. J. Appl. Crystallogr. 45: 335-41
106. Wierman JL, Alden JS, KimCU, McEuen PL, Gruner SM. 2013. Graphene as a protein crystalmounting material to reduce background scatter. J. Appl. Crystallogr. 46: 1501-7
107. Woodson SA. 2010. Compact intermediates in RNA folding. Annu. Rev. Biophys. 39: 61-77
108. Woodson SA. 2011. RNA folding pathways and the self-assembly of ribosomes. Acc. Chem. Res. 44: 1312-19
109. Yuk JM, Kim K, Aleman B, Regan W, Ryu JH, et al. 2011. Graphene veils and sandwiches. Nano Lett. 11: 3290-94
110. Yuk JM, Park J, Ercius P, Kim K, Hellebusch DJ, et al. 2012. High-resolutionEMof colloidal nanocrystal growth using graphene liquid cells. Science 336: 61-64
111. Zang C, Stevens JA, Link JJ, Guo LJ, Wang LJ, Zhong DP. 2009. Ultrafast proteinquake dynamics in cytochrome c. J. Am. Chem. Soc. 131: 2846-52
112. Ziaja B, Chapman HN, Faustlin R, Hau-Riege S, Jurek Z, et al. 2012. Limitations of coherent diffractive imaging of single objects due to their damage by intense X-ray radiation. New J. Phys. 14: 114015