Virus Structures by X-Ray Free-Electron Lasers

Literature Cited

1. 1. 

   Watson JD, Crick FHC. 1953. Molecular structure of nucleic acids: a structure for deoxyribose nucleic acid. Nature 171:737–38
   [Google Scholar]
2. 2. 

   Franklin RE. 1956. Structure of tobacco mosaic virus: location of the ribonucleic acid in the tobacco mosaic virus particle. Nature 177:928–30
   [Google Scholar]
3. 3. 

   Holmes KC, Stubbs GJ, Mandelkow E, Gallwitz U 1975. Structure of tobacco mosaic virus at 6.7 Å resolution. Nature 254:192–96
   [Google Scholar]
4. 4. 

   Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN et al. 2000. The Protein Data Bank. Nucleic Acids Res 28:235–42
   [Google Scholar]
5. 5. 

   Huang Z. 2013. Brightness and coherence of synchrotron radiation and FELs. Proceedings, 4th International Particle Accelerator Conference, IPAC 2013, May 13–17, 2013, Shanghai, China Z Dai, C Petit-Jean-Genaz, VRW Schaa, C Zhang 16–20 Geneva, Switz: JACoW
   [Google Scholar]
6. 6. 

   Weckert E. 2015. The potential of future light sources to explore the structure and function of matter. IUCrJ 2:230–45
   [Google Scholar]
7. 7. 

   Schmüser P, Dohlus M, Rossbach J, Behrens C 2014. X-ray free-electron lasers: technical realization and experimental results. Free-Electron Lasers in the Ultraviolet and X-Ray Regime165–82 Cham, Switz: Springer, 2nd ed..
   [Google Scholar]
8. 8. 

   Ackermann W, Asova G, Ayvazyan V, Azima A, Baboi N et al. 2007. Operation of a free-electron laser from the extreme ultraviolet to the water window. Nat. Photonics 1:336–42
   [Google Scholar]
9. 9. 

   Chapman HN, Barty A, Bogan MJ, Boutet S, Frank M et al. 2006. Femtosecond diffractive imaging with a soft-X-ray free-electron laser. Nat. Phys. 2:839–43
   [Google Scholar]
10. 10. 

    Bogan MJ, Benner WH, Boutet S, Rohner U, Frank M et al. 2008. Single particle X-ray diffractive imaging. Nano Lett 8:310–16
    [Google Scholar]
11. 11. 

    Emma P, Akre R, Arthur J, Bionta R, Bostedt C et al. 2010. First lasing and operation of an ångstrom-wavelength free-electron laser. Nat. Photonics 4:641–47
    [Google Scholar]
12. 12. 

    Bocchetta CJ, Abrami A, Allaria E, Andrian I, Bacescu D et al. 2007. FERMI@Elettra: Conceptual Design Report Trieste, Italy: Sincrotrone Trieste
13. 13. 

    Yabashi M, Tanaka H, Ishikawa T 2015. Overview of the SACLA facility. J. Synchrotron Radiat. 22:477–84
    [Google Scholar]
14. 14. 

    Altarelli M, Brinkmann R, Chergui M, Decking W, Dobson B et al. 2006. The European X-ray Free-Electron Laser: Technical Design Report Hamburg, Ger: DESY XFEL Proj. Group
15. 15. 

    Ganter R, Abela R, Braun HH, Garvey T, Patterson BD et al. 2010. SwissFEL Conceptual Design Report Villigen, Switz: Paul Scherrer Inst.
16. 16. 

    Kang H-S, Kim KW, Ko IS 2015. Status of the PAL-XFEL construction. Proceedings, 64th International Particle Accelerator Conference, IPAC 2015, May 3–8, 2015, Richmond, VA2439–43 Geneva, Switz: JACoW
    [Google Scholar]
17. 17. 

    Magdoff BS. 1953. Deterioration of the crystallinity of wet ribonuclease with exposure to X-radiation. Acta Crystallogr 6:801–2
    [Google Scholar]
18. 18. 

    Owen RL, Rudino-Pinera E, Garman EF 2006. Experimental determination of the radiation dose limit for cryocooled protein crystals. PNAS 103:4912–17
    [Google Scholar]
19. 19. 

    Meents A, Gutmann S, Wagner A, Schulze-Briese C 2010. Origin and temperature dependence of radiation damage in biological samples at cryogenic temperatures. PNAS 107:1094–99
    [Google Scholar]
20. 20. 

    Roedig P, Duman R, Sanchez-Weatherby J, Vartiainen I, Burkhardt A et al. 2016. Room-temperature macromolecular crystallography using a micro-patterned silicon chip with minimal background scattering. J. Appl. Crystallogr. 49:968–75
    [Google Scholar]
21. 21. 

    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
    [Google Scholar]
22. 22. 

    Gati C, Oberthuer D, Yefanov O, Bunker RD, Stellato F et al. 2017. Atomic structure of granulin determined from native nanocrystalline granulovirus using an X-ray free-electron laser. PNAS 114:2247–52
    [Google Scholar]
23. 23. 

    Kühlbrandt W. 2014. The resolution revolution. Science 343:1443–44
    [Google Scholar]
24. 24. 

    Seibert MM, Ekeberg T, Maia FR, Svenda M, Andreasson J et al. 2011. Single mimivirus particles intercepted and imaged with an X-ray laser. Nature 470:78–81
    [Google Scholar]
25. 25. 

    Gould EA. 1999. Methods for long-term virus preservation. Mol. Biotechnol. 13:57–66
    [Google Scholar]
26. 26. 

    Miao J, Charalambous P, Kirz J, Sayre D 1999. Extending the methodology of X-ray crystallography to allow imaging of micrometre-sized non-crystalline specimens. Nature 400:342–44
    [Google Scholar]
27. 27. 

    Miao J, Hodgson KO, Ishikawa T, Larabell CA, LeGros MA, Nishino Y 2003. Imaging whole Escherichia coli bacteria by using single-particle x-ray diffraction. PNAS 100:110–12
    [Google Scholar]
28. 28. 

    Song C, Jiang H, Mancuso A, Amirbekian B, Peng L et al. 2008. Quantitative imaging of single, unstained viruses with coherent x rays. Phys. Rev. Lett. 101:158101
    [Google Scholar]
29. 29. 

    Ekeberg T, Svenda M, Abergel C, Maia FR, Seltzer V et al. 2015. Three-dimensional reconstruction of the giant mimivirus particle with an x-ray free-electron laser. Phys. Rev. Lett. 114:098102
    [Google Scholar]
30. 30. 

    Hantke MF, Hasse D, Maia FRNC, Ekeberg T, John K et al. 2014. High-throughput imaging of heterogeneous cell organelles with an X-ray laser. Nat. Photonics 8:943–49
    [Google Scholar]
31. 31. 

    Aquila A, Barty A, Bostedt C, Boutet S, Carini G et al. 2015. The linac coherent light source single particle imaging road map. Struct. Dyn. 2:041701
    [Google Scholar]
32. 32. 

    Ferguson KR, Bucher M, Bozek JD, Carron S, Castagna JC et al. 2015. The Atomic, Molecular and Optical Science instrument at the Linac Coherent Light Source. J. Synchrotron Radiat. 22:492–97
    [Google Scholar]
33. 33. 

    Liang M, Williams GJ, Messerschmidt M, Seibert MM, Montanez PA et al. 2015. The Coherent X-ray Imaging instrument at the Linac Coherent Light Source. J. Synchrotron Radiat. 22:514–19
    [Google Scholar]
34. 34. 

    Holton JM, Frankel KA. 2010. The minimum crystal size needed for a complete diffraction data set. Acta Crystallogr. D Biol. Crystallogr. 66:393–408
    [Google Scholar]
35. 35. 

    Ayyer K, Geloni G, Kocharyan V, Saldin E, Serkez S et al. 2015. Perspectives for imaging single protein molecules with the present design of the European XFEL. Struct. Dyn. 2:041702
    [Google Scholar]
36. 36. 

    Daurer BJ, Okamoto K, Bielecki J, Maia FRNC, Mühlig K et al. 2017. Experimental strategies for imaging bioparticles with femtosecond hard X-ray pulses. IUCrJ 4:251–62
    [Google Scholar]
37. 37. 

    Siewert F, Buchheim J, Boutet S, Williams GJ, Montanez PA et al. 2012. Ultra-precise characterization of LCLS hard X-ray focusing mirrors by high resolution slope measuring deflectometry. Opt. Express 20:4525–36
    [Google Scholar]
38. 38. 

    Li Y, Beck R, Huang T, Choi MC, Divinagracia M 2008. Scatterless hybrid metal–single-crystal slit for small-angle X-ray scattering and high-resolution X-ray diffraction. J. Appl. Crystallogr. 41:1134–39
    [Google Scholar]
39. 39. 

    Dufresne EM, Dierker SB, Yin Z, Berman L 2009. Development of new apertures for coherent X-ray experiments. J. Synchrotron Radiat. 16:358–67
    [Google Scholar]
40. 40. 

    Wiedorn MO, Awel S, Morgan AJ, Barthelmess M, Bean R et al. 2017. Post-sample aperture for low background diffraction experiments at X-ray free-electron lasers. J. Synchrotron Radiat. 24:1296–98
    [Google Scholar]
41. 41. 

    Munke A, Andreasson J, Aquila A, Awel S, Ayyer K et al. 2016. Coherent diffraction of single Rice Dwarf virus particles using hard X-rays at the Linac Coherent Light Source. Sci. Data 3:160064
    [Google Scholar]
42. 42. 

    Marvin Seibert M, Boutet S, Svenda M, Ekeberg T, Maia FRNC et al. 2010. Femtosecond diffractive imaging of biological cells. J. Phys. B Atomic Mol. Opt. Phys. 43:194015
    [Google Scholar]
43. 43. 

    Seuring C, Ayyer K, Filippaki E, Barthelmess M, Longchamp JN et al. 2018. Femtosecond X-ray coherent diffraction of aligned amyloid fibrils on low background graphene. Nat. Commun. 9:1836
    [Google Scholar]
44. 44. 

    DePonte DP, Weierstall U, Schmidt K, Warner J, Starodub D et al. 2008. Gas dynamic virtual nozzle for generation of microscopic droplet streams. J. Phys. D Appl. Phys. 41:195505
    [Google Scholar]
45. 45. 

    Ganan-Calvo AM, DePonte DP, Herrada MA, Spence JC, Weierstall U, Doak RB 2010. Liquid capillary micro/nanojets in free-jet expansion. Small 6:822–24
    [Google Scholar]
46. 46. 

    Bielecki J, Hantke MF, Daurer BJ, Reddy HKN, Hasse D et al. 2018. Electrospray sample injection for single-particle imaging with X-ray lasers. bioRxiv 45345. https://doi.org/10.1101/453456
    [Crossref]
47. 47. 

    Hantke MF, Bielecki J, Kulyk O, Westphal D, Larsson DSD et al. 2018. Rayleigh-scattering microscopy for tracking and sizing nanoparticles in focused aerosol beams. IUCrJ 5:673–80
    [Google Scholar]
48. 48. 

    Kirian RA, Awel S, Eckerskorn N, Fleckenstein H, Wiedorn M et al. 2015. Simple convergent-nozzle aerosol injector for single-particle diffractive imaging with X-ray free-electron lasers. Struct. Dyn. 2:041717
    [Google Scholar]
49. 49. 

    Awel S, Kirian RA, Eckerskorn N, Wiedorn MO, Horke DA et al. 2016. Visualizing aerosol-particle injection for diffractive-imaging experiments. Opt. Express 24:6507–21
    [Google Scholar]
50. 50. 

    Awel S, Kirian RA, Wiedorn MO, Beyerlein KR, Roth N et al. 2018. Femtosecond X-ray diffraction from an aerosolized beam of protein nanocrystals. J. Appl. Crystallogr. 51:133–39
    [Google Scholar]
51. 51. 

    Roth N, Awel S, Horke DA, Küpper J 2018. Optimizing aerodynamic lenses for single-particle imaging. J. Aerosol Sci. 124:17–29
    [Google Scholar]
52. 52. 

    Hutchins DK, Holm J, Addison SR 1991. Electrodynamic focusing of charged aerosol particles. Aerosol Sci. Technol. 14:389–405
    [Google Scholar]
53. 53. 

    Eckerskorn N, Bowman R, Kirian RA, Awel S, Wiedorn M et al. 2015. Optically induced forces imposed in an optical funnel on a stream of particles in air or vacuum. Phys. Rev. Appl. 4:064001
    [Google Scholar]
54. 54. 

    Wiedorn MO, Awel S, Morgan AJ, Ayyer K, Gevorkov Y et al. 2018. Rapid sample delivery for megahertz serial crystallography at X-ray FELs. IUCrJ 5:574–84
    [Google Scholar]
55. 55. 

    Koralek JD, Kim JB, Bruza P, Curry CB, Chen Z et al. 2018. Generation and characterization of ultrathin free-flowing liquid sheets. Nat. Commun. 9:1353
    [Google Scholar]
56. 56. 

    Broennimann C, Eikenberry EF, Henrich B, Horisberger R, Huelsen G et al. 2006. The PILATUS 1M detector. J. Synchrotron Radiat. 13:120–30
    [Google Scholar]
57. 57. 

    Cohen AE, Soltis SM, Gonzalez A, Aguila L, Alonso-Mori R et al. 2014. Goniometer-based femtosecond crystallography with X-ray free electron lasers. PNAS 111:17122–27
    [Google Scholar]
58. 58. 

    Hartmann R, Epp S, Herrmann S, Holl P, Meidinger N et al. 2008. Large format pnCCDs as imaging detectors for X-ray free-electron-lasers. 2008 IEEE Nuclear Science Symposium Conference Record2590–95 New York: IEEE
    [Google Scholar]
59. 59. 

    Koerner LJ, Philipp HT, Hromalik MS, Tate MW, Gruner SM 2009. X-ray tests of a Pixel Array Detector for coherent x-ray imaging at the Linac Coherent Light Source. J. Instrum. 4:P03001
    [Google Scholar]
60. 60. 

    Mozzanica A, Bergamaschi A, Brueckner M, Cartier S, Dinapoli R et al. 2016. Characterization results of the JUNGFRAU full scale readout ASIC. J. Instrum. 11:C02047
    [Google Scholar]
61. 61. 

    Leonarski F, Redford S, Mozzanica A, Lopez-Cuenca C, Panepucci E et al. 2018. Fast and accurate data collection for macromolecular crystallography using the JUNGFRAU detector. Nat. Methods 15:799–804
    [Google Scholar]
62. 62. 

    Allahgholi A, Becker J, Bianco L, Delfs A, Dinapoli R et al. 2015. AGIPD, a high dynamic range fast detector for the European XFEL. J. Instrum. 10:C01023
    [Google Scholar]
63. 63. 

    Markovic B, Dragone A, Caragiulo P, Herbst R, Nishimura K et al. 2014. Design and characterization of the ePix100a: a low noise integrating pixel ASIC for LCLS detectors. 2014 IEEE Nuclear Science Symposium and Medical Imaging Conference (NSS/MIC): 8–15 Nov. 20141–3 Piscataway, NJ: IEEE
    [Google Scholar]
64. 64. 

    Mariani V, Morgan A, Yoon CH, Lane TJ, White TA et al. 2016. OnDA: online data analysis and feedback for serial X-ray imaging. J. Appl. Crystallogr. 49:1073–80
    [Google Scholar]
65. 65. 

    Daurer BJ, Hantke MF, Nettelblad C, Maia FR 2016. Hummingbird: monitoring and analyzing flash X-ray imaging experiments in real time. J. Appl. Crystallogr. 49:1042–47
    [Google Scholar]
66. 66. 

    Bobkov SA, Teslyuk AB, Kurta RP, Gorobtsov OY, Yefanov OM et al. 2015. Sorting algorithms for single-particle imaging experiments at X-ray free-electron lasers. J. Synchrotron Radiat. 22:1345–52
    [Google Scholar]
67. 67. 

    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 Biol. Sci. 369:20130326
    [Google Scholar]
68. 68. 

    Loh NT, Elser V. 2009. Reconstruction algorithm for single-particle diffraction imaging experiments. Phys. Rev. E 80:026705
    [Google Scholar]
69. 69. 

    Ayyer K, Lan TY, Elser V, Loh ND 2016. Dragonfly: an implementation of the expand-maximize-compress algorithm for single-particle imaging. J. Appl. Crystallogr. 49:1320–35
    [Google Scholar]
70. 70. 

    Chapman HN, Barty A, Marchesini S, Noy A, Hau-Riege SP et al. 2006. High-resolution ab initio three-dimensional x-ray diffraction microscopy. J. Opt. Soc. Am. A 23:1179
    [Google Scholar]
71. 71. 

    Shechtman Y, Eldar YC, Cohen O, Segev M 2013. Efficient coherent diffractive imaging for sparsely varying objects. Opt. Express 21:6327–38
    [Google Scholar]
72. 72. 

    Martin AV, Loh ND, Hampton CY, Sierra RG, Wang F et al. 2012. Femtosecond dark-field imaging with an X-ray free electron laser. Opt. Express 20:13501–12
    [Google Scholar]
73. 73. 

    Gorkhover T, Ulmer A, Ferguson K, Bucher M, Maia FRNC et al. 2018. Femtosecond X-ray Fourier holography imaging of free-flying nanoparticles. Nat. Photon. 12:150–53
    [Google Scholar]
74. 74. 

    Fox G, Stuart D, Acharya KR, Fry E, Rowlands D, Brown F 1987. Crystallization and preliminary X-ray diffraction analysis of foot-and-mouth disease virus. J. Mol. Biol. 196:591–97
    [Google Scholar]
75. 75. 

    Chapman HN, Fromme P, Barty A, White TA, Kirian RA et al. 2011. Femtosecond X-ray protein nanocrystallography. Nature 470:73–77
    [Google Scholar]
76. 76. 

    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
    [Google Scholar]
77. 77. 

    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
    [Google Scholar]
78. 78. 

    Stellato F, Oberthur D, Liang M, Bean R, Gati C et al. 2014. Room-temperature macromolecular serial crystallography using synchrotron radiation. IUCrJ 1:204–12
    [Google Scholar]
79. 79. 

    Wiedorn MO, Oberthur D, Bean R, Schubert R, Werner N et al. 2018. Megahertz serial crystallography. Nat. Commun. 9:4025
    [Google Scholar]
80. 80. 

    Grunbein ML, Bielecki J, Gorel A, Stricker M, Bean R et al. 2018. Megahertz data collection from protein microcrystals at an X-ray free-electron laser. Nat. Commun. 9:3487
    [Google Scholar]
81. 81. 

    Meents A, Wiedorn MO, Srajer V, Henning R, Sarrou I et al. 2017. Pink-beam serial crystallography. Nat. Commun. 8:1281
    [Google Scholar]
82. 82. 

    Lawrence RM, Conrad CE, Zatsepin NA, Grant TD, Liu H et al. 2015. Serial femtosecond X-ray diffraction of enveloped virus microcrystals. Struct. Dyn. 2:041720
    [Google Scholar]
83. 83. 

    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
    [Google Scholar]
84. 84. 

    Conrad CE, Basu S, James D, Wang D, Schaffer A et al. 2015. A novel inert crystal delivery medium for serial femtosecond crystallography. IUCrJ 2:421–30
    [Google Scholar]
85. 85. 

    Harrison SC, Strong RK, Schlesinger S, Schlesinger MJ 1992. Crystallization of Sindbis virus and its nucleocapsid. J. Mol. Biol. 226:277–80
    [Google Scholar]
86. 86. 

    Tang J, Jose J, Chipman P, Zhang W, Kuhn RJ, Baker TS 2011. Molecular links between the E2 envelope glycoprotein and nucleocapsid core in Sindbis virus. J. Mol. Biol. 414:442–59
    [Google Scholar]
87. 87. 

    Roedig P, Ginn HM, Pakendorf T, Sutton G, Harlos K et al. 2017. High-speed fixed-target serial virus crystallography. Nat. Methods 14:805–10
    [Google Scholar]
88. 88. 

    Smyth M, Tate J, Hoey E, Lyons C, Martin S, Stuart D 1995. Implications for viral uncoating from the structure of bovine enterovirus. Nat. Struct. Mol. Biol. 2:224–31
    [Google Scholar]
89. 89. 

    Goens SD, Botero S, Zemla A, Zhou CE, Perdue ML 2004. Bovine enterovirus 2: complete genomic sequence and molecular modelling of a reference strain and a wild-type isolate from endemically infected US cattle. J. Gen. Virol. 85:3195–203
    [Google Scholar]
90. 90. 

    Roedig P, Vartiainen I, Duman R, Panneerselvam S, Stube N et al. 2015. A micro-patterned silicon chip as sample holder for macromolecular crystallography experiments with minimal background scattering. Sci. Rep. 5:10451
    [Google Scholar]
91. 91. 

    Axford D, Owen RL, Aishima J, Foadi J, Morgan AW et al. 2012. In situ macromolecular crystallography using microbeams. Acta Crystallogr. D Biol. Crystallogr. 68:592–600
    [Google Scholar]
92. 92. 

    Trillo-Muyo S, Jasilionis A, Domagalski MJ, Chruszcz M, Minor W et al. 2013. Ultratight crystal packing of a 10 kDa protein. Acta Crystallogr. D Biol. Crystallogr. 69:464–70
    [Google Scholar]
93. 93. 

    Oberthuer D, Knoska J, Wiedorn MO, Beyerlein KR, Bushnell DA et al. 2017. Double-flow focused liquid injector for efficient serial femtosecond crystallography. Sci. Rep. 7:44628
    [Google Scholar]
94. 94. 

    Bartesaghi A, Aguerrebere C, Falconieri V, Banerjee S, Earl LA et al. 2018. Atomic resolution cryo-EM structure of β-galactosidase. Structure 26:848–56
    [Google Scholar]
95. 95. 

    Frank J. 2017. Advances in the field of single-particle cryo-electron microscopy over the last decade. Nat. Protoc. 12:209–12
    [Google Scholar]
96. 96. 

    Stagno JR, Liu Y, Bhandari YR, Conrad CE, Panja S et al. 2017. Structures of riboswitch RNA reaction states by mix-and-inject XFEL serial crystallography. Nature 541:242–46
    [Google Scholar]
97. 97. 

    Kupitz C, Olmos JL, Holl M, Tremblay L, Pande K et al. 2017. Structural enzymology using X-ray free electron lasers. Struct. Dyn. 4:044003
    [Google Scholar]
98. 98. 

    Beyerlein KR, Dierksmeyer D, Mariani V, Kuhn M, Sarrou I et al. 2017. Mix-and-diffuse serial synchrotron crystallography. IUCrJ 4:769–77
    [Google Scholar]
99. 99. 

    Olmos JL Jr, Pandey S, Martin-Garcia JM, Calvey G, Katz A et al. 2018. Enzyme intermediates captured “on the fly” by mix-and-inject serial crystallography. BMC Biol 16:59
    [Google Scholar]
100. 100. 

     Ahlberg Gagnér V, Lundholm I, Garcia-Bonete M-J, Rodilla H, Friedman R et al. 2019. A distributed lattice of aligned atoms exists in a protein structure: a hierarchical clustering study of displacement parameters in bovine trypsin. bioRxiv 475889. https://doi.org/10.1101/475889
     [Crossref]
101. 101. 

     Hekstra DR, White KI, Socolich MA, Henning RW, Srajer V, Ranganathan R 2016. Electric-field-stimulated protein mechanics. Nature 540:400–5
     [Google Scholar]
102. 102. 

     Fraser JS, van den Bedem H, Samelson AJ, Lang PT, Holton JM et al. 2011. Accessing protein conformational ensembles using room-temperature X-ray crystallography. PNAS 108:16247–52
     [Google Scholar]