1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Physical Chemistry
  4. Volume 75, 2024
  5. Article

Annual Review of Physical Chemistry

Volume 75, 2024

3D Nanocrystallography and the Imperfect Molecular Lattice

Abstract

Crystallographic analysis relies on the scattering of quanta from arrays of atoms that populate a repeating lattice. While large crystals built of lattices that appear ideal are sought after by crystallographers, imperfections are the norm for molecular crystals. Additionally, advanced X-ray and electron diffraction techniques, used for crystallography, have opened the possibility of interrogating micro- and nanoscale crystals, with edges only millions or even thousands of molecules long. These crystals exist in a size regime that approximates the lower bounds for traditional models of crystal nonuniformity and imperfection. Accordingly, data generated by diffraction from both X-rays and electrons show increased complexity and are more challenging to conventionally model. New approaches in serial crystallography and spatially resolved electron diffraction mapping are changing this paradigm by better accounting for variability within and between crystals. The intersection of these methods presents an opportunity for a more comprehensive understanding of the structure and properties of nanocrystalline materials.

Keyword(s): 3DED, crystallography, MicroED, nanocrystal, SFX
Loading

Article metrics loading...

/content/journals/10.1146/annurev-physchem-083122-105226
2024-06-28
2024-10-10
Loading full text...

Full text loading...

/deliver/fulltext/physchem/75/1/annurev-physchem-083122-105226.html?itemId=/content/journals/10.1146/annurev-physchem-083122-105226&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Aroyo MI, ed. 2016.. International Tables for Crystallography: Space-Group Symmetry, Vol. A. Chester , UK:: Int. Union Crystallogr. , 2nd ed..
     [Google Scholar]
  2. 2.
    Karamertzanis PG, Pantelides CC. 2007.. Ab initio crystal structure prediction. II. Flexible molecules. . Mol. Phys. 105:(2–3):273–91
     [Crossref] [Google Scholar]
  3. 3.
    Lovelace JJ, Borgstahl GEO. 2020.. Characterizing pathological imperfections in macromolecular crystals: lattice disorders and modulations. . Crystallogr. Rev. 26:(1):3–50
     [Crossref] [Google Scholar]
  4. 4.
    Bragg WL. 1970.. Early days. . Acta Crystallogr. A 26:(2):171–72
     [Crossref] [Google Scholar]
  5. 5.
    Holton JM, Frankel KA. 2010.. The minimum crystal size needed for a complete diffraction data set. . Acta Crystallogr. D Biol. Crystallogr. 66:(Part 4):393–408
     [Crossref] [Google Scholar]
  6. 6.
    Shmueli U, ed. 2010.. International Tables for Crystallography: Reciprocal Space, Vol. B. Chester, UK:: Int. Union Crystallogr. , 2nd ed..
     [Google Scholar]
  7. 7.
    Schlichting I, Miao J. 2012.. Emerging opportunities in structural biology with X-ray free-electron lasers. . Curr. Opin. Struct. Biol. 22:(5):613–26
     [Crossref] [Google Scholar]
  8. 8.
    Pellegrini C, Reiche S. 2004.. The development of X-Ray free-electron lasers. . IEEE J. Sel. Top. Quantum Electron. 10:(6):1393–404
     [Crossref] [Google Scholar]
  9. 9.
    Emma P, Bane K, Cornacchia M, Huang Z, Schlarb H, et al. 2004.. Femtosecond and subfemtosecond X-ray pulses from a self-amplified spontaneous-emission-based free-electron laser. . Phys. Rev. Lett. 92:(7):074801
     [Crossref] [Google Scholar]
  10. 10.
    Glaeser RM. 1985.. Electron crystallography of biological macromolecules. . Annu. Rev. Phys. Chem. 36::243–75
     [Crossref] [Google Scholar]
  11. 11.
    Saha A, Nia SS, Rodríguez JA. 2022.. Electron diffraction of 3D molecular crystals. . Chem. Rev. 122:(17):13883–914
     [Crossref] [Google Scholar]
  12. 12.
    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:(12):839–43
     [Crossref] [Google Scholar]
  13. 13.
    Henderson R. 2018.. From electron crystallography to single particle cryoEM (Nobel lecture). . Angew. Chem. Int. Ed. 57:(34):10804–25
     [Crossref] [Google Scholar]
  14. 14.
    Zou X, Hovmöller S, Oleynikov P. 2011.. Electron Crystallography: Electron Microscopy and Electron Diffraction. Oxford, UK:: Oxford Univ. Press
     [Google Scholar]
  15. 15.
    Shi D, Nannenga BL, Iadanza MG, Gonen T. 2013.. Three-dimensional electron crystallography of protein microcrystals. . eLife 2::e01345
     [Crossref] [Google Scholar]
  16. 16.
    Åkerfeldt K. 2009.. Protein crystallography: a concise guide by Eaton E. Lattman and Patrick J. Loll. . Biochem. Mol. Biol. Educ. 37:(3):198
     [Crossref] [Google Scholar]
  17. 17.
    Cowley JM, Moodie AF. 1959.. The scattering of electrons by atoms and crystals. III. Single-crystal diffraction patterns. . Acta Crystallogr. 12:(5):360–67
     [Crossref] [Google Scholar]
  18. 18.
    Mendez D, Bolotovsky R, Bhowmick A, Brewster AS, Kern J, et al. 2020.. Beyond integration: modeling every pixel to obtain better structure factors from stills. . IUCrJ 7:(6):1151–67
     [Crossref] [Google Scholar]
  19. 19.
    Roedig P, Ginn HM, Pakendorf T, Sutton G, Harlos K, et al. 2017.. High-speed fixed-target serial virus crystallography. . Nat. Methods 14:(8):805–10
     [Crossref] [Google Scholar]
  20. 20.
    Neutze R, Wouts R, Van Der Spoel D, Weckert E, Hajdu J. 2000.. Potential for biomolecular imaging with femtosecond X-ray pulses. . Nature 406:(6797):752–57
     [Crossref] [Google Scholar]
  21. 21.
    Chapman HN, Fromme P, Barty A, White TA, Kirian RA, et al. 2011.. Femtosecond X-ray protein nanocrystallography. . Nature 470:(7332):73–77
     [Crossref] [Google Scholar]
  22. 22.
    Schriber EA, Paley DW, Bolotovsky R, Rosenberg DJ, Sierra RG, et al. 2022.. Chemical crystallography by serial femtosecond X-ray diffraction. . Nature 601:(7893):360–65
     [Crossref] [Google Scholar]
  23. 23.
    Brewster AS, Waterman DG, Parkhurst JM, Gildea RJ, Young ID, et al. 2018.. Improving signal strength in serial crystallography with DIALS geometry refinement. . Acta Crystallogr. D Struct. Biol. 74:(9):877–94
     [Crossref] [Google Scholar]
  24. 24.
    Kabsch W. 2014.. Processing of X-ray snapshots from crystals in random orientations. . Acta Crystallogr. D Biol. Crystallogr. 70:(8):2204–16
     [Crossref] [Google Scholar]
  25. 25.
    Sauter NK, Hattne J, Brewster AS, Echols N, Zwart PH, Adams PD. 2014.. Improved crystal orientation and physical properties from single-shot XFEL stills. . Acta Crystallogr. D Biol. Crystallogr. 70:(12):3299–309
     [Crossref] [Google Scholar]
  26. 26.
    White TA. 2014.. Post-refinement method for snapshot serial crystallography. . Philos. Trans. R. Soc. B 369:(1647):20130330
     [Crossref] [Google Scholar]
  27. 27.
    Sauter NK. 2015.. XFEL diffraction: developing processing methods to optimize data quality. . J. Synchrotron Radiat. 22:(2):239–48
     [Crossref] [Google Scholar]
  28. 28.
    Uervirojnangkoorn M, Zeldin OB, Lyubimov AY, Hattne J, Brewster AS, et al. 2015.. Enabling X-ray free electron laser crystallography for challenging biological systems from a limited number of crystals. . eLife 4::e05421
     [Crossref] [Google Scholar]
  29. 29.
    Ginn HM, Roedig P, Kuo A, Evans G, Sauter NK, et al. 2016.. TakeTwo: an indexing algorithm suited to still images with known crystal parameters. . Acta Crystallogr. D Struct. Biol. 72::956–65
     [Crossref] [Google Scholar]
  30. 30.
    Colletier J-P, Sawaya MR, Gingery M, Rodriguez JA, Cascio D, et al. 2016.. De novo phasing with X-ray laser reveals mosquito larvicide BinAB structure. . Nature 539:(7627):43–47
     [Crossref] [Google Scholar]
  31. 31.
    Brewster AS, Sawaya MR, Rodriguez J, Hattne J, Echols N, et al. 2015.. Indexing amyloid peptide diffraction from serial femtosecond crystallography: new algorithms for sparse patterns. . Acta Crystallogr. D Biol. Crystallogr. 71:(2):357–66
     [Crossref] [Google Scholar]
  32. 32.
    Maia FRNC, Yang C, Marchesini S. 2011.. Compressive auto-indexing in femtosecond nanocrystallography. . Ultramicroscopy 111:(7):807–11
     [Crossref] [Google Scholar]
  33. 33.
    Ayyer K, Philipp HT, Tate MW, Wierman JL, Elser V, Gruner SM. 2015.. Determination of crystallographic intensities from sparse data. . IUCrJ 2:(1):29–34
     [Crossref] [Google Scholar]
  34. 34.
    Ginn HM, Evans G, Sauter NK, Stuart DI. 2016.. On the release of cppxfel for processing X-ray free-electron laser images. . J. Appl. Crystallogr. 49:(3):1065–72
     [Crossref] [Google Scholar]
  35. 35.
    Li C, Li X, Kirian R, Spence JCH, Liu H, Zatsepin NA. 2019.. SPIND: a reference-based auto-indexing algorithm for sparse serial crystallography data. . IUCrJ 6:(1):72–84
     [Crossref] [Google Scholar]
  36. 36.
    Støckler LJ, Krause L, Svane B, Tolborg K, Richter B, et al. 2023.. Towards pump-probe single-crystal XFEL refinements for small-unit-cell systems. . IUCrJ 10:(1):103–17
     [Crossref] [Google Scholar]
  37. 37.
    Takaba K, Maki-Yonekura S, Inoue I, Tono K, Hamaguchi T, et al. 2023.. Structural resolution of a small organic molecule by serial X-ray free-electron laser and electron crystallography. . Nat. Chem. 15:(4):491–97
     [Crossref] [Google Scholar]
  38. 38.
    Kroon-Batenburg LMJ, Schreurs AMM, Ravelli RBG, Gros P. 2015.. Accounting for partiality in serial crystallography using ray-tracing principles. . Acta Crystallogr. D Biol. Crystallogr. 71:(9):1799–811
     [Crossref] [Google Scholar]
  39. 39.
    Holton JM, Classen S, Frankel KA, Tainer JA. 2014.. The R-factor gap in macromolecular crystallography: an untapped potential for insights on accurate structures. . FEBS J. 281:(18):4046–60
     [Crossref] [Google Scholar]
  40. 40.
    Lyubimov AY, Uervirojnangkoorn M, Zeldin OB, Zhou Q, Zhao M, et al. 2016.. Advances in X-ray free electron laser (XFEL) diffraction data processing applied to the crystal structure of the synaptotagmin-1/SNARE complex. . eLife 5::e18740
     [Crossref] [Google Scholar]
  41. 41.
    Nave C. 1998.. A description of imperfections in protein crystals. . Acta Crystallogr. D Biol. Crystallogr. 54:(5):848–53
     [Crossref] [Google Scholar]
  42. 42.
    White TA, Mariani V, Brehm W, Yefanov O, Barty A, et al. 2016.. Recent developments in CrystFEL. . J. Appl. Crystallogr. 49:(2):680–89
     [Crossref] [Google Scholar]
  43. 43.
    De Broglie L. 1924.. XXXV. A tentative theory of light quanta. . Lond. Edinb. Dublin Philos. Mag. J. Sci. 47:(278):446–58
     [Crossref] [Google Scholar]
  44. 44.
    Davisson C, Germer LH. 1927.. The scattering of electrons by a single crystal of nickel. . Nature 119::558–60
     [Crossref] [Google Scholar]
  45. 45.
    Thomson GP, Reid A. 1927.. Diffraction of cathode rays by a thin film. . Nature 119::890
     [Crossref] [Google Scholar]
  46. 46.
    Miyake S, Uyeda R. 1950.. An exception to Friedel's law in electron diffraction. . Acta Crystallogr. 3:(4):314
     [Crossref] [Google Scholar]
  47. 47.
    Kohra K. 1954.. Simultaneous reflexion in electron diffraction as a cause of the failure of Friedel's law. . J. Phys. Soc. Jpn. 9:(5):690–701
     [Crossref] [Google Scholar]
  48. 48.
    Cowley JM. 1953.. Structure analysis of single crystals by electron diffraction. I. Techniques. . Acta Crystallogr. 6:(6):516–21
     [Crossref] [Google Scholar]
  49. 49.
    Menter JW. 1956.. The direct study by electron microscopy of crystal lattices and their imperfections. . Philos. Mag. 86:(29–31):4529–52
     [Google Scholar]
  50. 50.
    Dorset DL, Hauptman HA. 1976.. Direct phase determination for quasi-kinematical electron diffraction intensity data from organic microcrystals. . Ultramicroscopy 1:(3–4):195–201
     [Crossref] [Google Scholar]
  51. 51.
    Kolb U, Gorelik T, Kübel C, Otten MT, Hubert D. 2007.. Towards automated diffraction tomography: part I—data acquisition. . Ultramicroscopy 107:(6–7):507–13
     [Crossref] [Google Scholar]
  52. 52.
    Mugnaioli E, Gorelik T, Kolb U. 2009.. “ Ab initio” structure solution from electron diffraction data obtained by a combination of automated diffraction tomography and precession technique. . Ultramicroscopy 109:(6):758–65
     [Crossref] [Google Scholar]
  53. 53.
    Palatinus L, Petříček V, Corrêa CA. 2015.. Structure refinement using precession electron diffraction tomography and dynamical diffraction: theory and implementation. . Acta Crystallogr. A Found. Adv. 71:(2):235–44
     [Crossref] [Google Scholar]
  54. 54.
    Brázda P, Palatinus L, Babor M. 2019.. Electron diffraction determines molecular absolute configuration in a pharmaceutical nanocrystal. . Science 364:(6441):667–69
     [Crossref] [Google Scholar]
  55. 55.
    Klar PB, Krysiak Y, Xu H, Steciuk G, Cho J, et al. 2023.. Accurate structure models and absolute configuration determination using dynamical effects in continuous-rotation 3D electron diffraction data. . Nat. Chem. 15:(6):848–55
     [Crossref] [Google Scholar]
  56. 56.
    Nederlof I, van Genderen E, Li Y-W, Abrahams JP. 2013.. A Medipix quantum area detector allows rotation electron diffraction data collection from submicrometre three-dimensional protein crystals. . Acta Crystallogr. D Biol. Crystallogr. 69:(7):1223–30
     [Crossref] [Google Scholar]
  57. 57.
    Nannenga BL, Shi D, Leslie AGW, Gonen T. 2014.. High-resolution structure determination by continuous-rotation data collection in MicroED. . Nat. Methods 11:(9):927–30
     [Crossref] [Google Scholar]
  58. 58.
    Rodriguez JA, Eisenberg DS, Gonen T. 2017.. Taking the measure of MicroED. . Curr. Opin. Struct. Biol. 46::79–86
     [Crossref] [Google Scholar]
  59. 59.
    De La Cruz MJ, Hattne J, Shi D, Seidler P, Rodriguez J, et al. 2017.. Atomic-resolution structures from fragmented protein crystals with the cryoEM method MicroED. . Nat. Methods 14:(4):399–402
     [Crossref] [Google Scholar]
  60. 60.
    Jones CG, Martynowycz MW, Hattne J, Fulton TJ, Stoltz BM, et al. 2018.. The cryoEM method MicroED as a powerful tool for small molecule structure determination. . ACS Cent. Sci. 4:(11):1587–92
     [Crossref] [Google Scholar]
  61. 61.
    Gruene T, Wennmacher JTC, Zaubitzer C, Holstein JJ, Heidler J, et al. 2018.. Rapid structure determination of microcrystalline molecular compounds using electron diffraction. . Angew. Chem. Int. Ed. 57:(50):16313–17
     [Crossref] [Google Scholar]
  62. 62.
    Richards LS, Millán C, Miao J, Martynowycz MW, Sawaya MR, et al. 2020.. Fragment-based determination of a proteinase K structure from MicroED data using ARCIMBOLDO_SHREDDER. . Acta Crystallogr. D Struct. Biol. 76:(8):703–12
     [Crossref] [Google Scholar]
  63. 63.
    Richards LS, Flores MD, Millán C, Glynn C, Zee C-T, et al. 2023.. Fragment-based ab initio phasing of peptidic nanocrystals by MicroED. . ACS Bio Med Chem Au 3:(2):201–10
     [Crossref] [Google Scholar]
  64. 64.
    Sawaya MR, Rodriguez J, Cascio D, Collazo MJ, Shi D, et al. 2016.. Ab initio structure determination from prion nanocrystals at atomic resolution by MicroED. . PNAS 113:(40):11232–36
     [Crossref] [Google Scholar]
  65. 65.
    Saha A, Evans M, Holton T, Rodriguez J. 2021.. Factors of atomic electron scattering (FAES): a resource for Gaussian parameterization of integral ionic, fractionally charged and neutral electron scattering factors. . Acta Crystallogr. A Found. Adv. 77::a50
     [Crossref] [Google Scholar]
  66. 66.
    Martynowycz MW, Clabbers MTB, Unge J, Hattne J, Gonen T. 2021.. Benchmarking the ideal sample thickness in cryo-EM. . PNAS 118:(49):e2108884118
     [Crossref] [Google Scholar]
  67. 67.
    Kim LJ, Ohashi M, Zhang Z, Tan D, Asay M, et al. 2021.. Prospecting for natural products by genome mining and microcrystal electron diffraction. . Nat. Chem. Biol. 17:(8):872–77
     [Crossref] [Google Scholar]
  68. 68.
    Latychevskaia T, Abrahams JP. 2019.. Inelastic scattering and solvent scattering reduce dynamical diffraction in biological crystals. . Acta Crystallogr. B Struct. Sci. Cryst. Eng. Mater. 75:(4):523–31
     [Crossref] [Google Scholar]
  69. 69.
    Yonekura K, Kato K, Ogasawara M, Tomita M, Toyoshima C. 2015.. Electron crystallography of ultrathin 3D protein crystals: atomic model with charges. . PNAS 112:(11):3368–73
     [Crossref] [Google Scholar]
  70. 70.
    Yonekura K, Ishikawa T, Maki-Yonekura S. 2019.. A new cryo-EM system for electron 3D crystallography by eEFD. . J. Struct. Biol. 206:(2):243–53
     [Crossref] [Google Scholar]
  71. 71.
    Ercius P, Boese M, Duden T, Dahmen U. 2012.. Operation of TEAM I in a user environment at NCEM. . Microsc. Microanal. 18:(4):676–83
     [Crossref] [Google Scholar]
  72. 72.
    McMullan G, Faruqi AR, Henderson R, Guerrini N, Turchetta R, et al. 2009.. Experimental observation of the improvement in MTF from backthinning a CMOS direct electron detector. . Ultramicroscopy 109:(9):1144–47
     [Crossref] [Google Scholar]
  73. 73.
    Ruskin AI, Yu Z, Grigorieff N. 2013.. Quantitative characterization of electron detectors for transmission electron microscopy. . J. Struct. Biol. 184:(3):385–93
     [Crossref] [Google Scholar]
  74. 74.
    Ciston J, Johnson IJ, Draney BR, Ercius P, Fong E, et al. 2019.. The 4D camera: very high speed electron counting for 4D-STEM. . Microsc. Microanal. 25:(Suppl. 2):1930–31
     [Crossref] [Google Scholar]
  75. 75.
    Fang S, Wen Y, Allen CS, Ophus C, Han GGD, et al. 2019.. Atomic electrostatic maps of 1D channels in 2D semiconductors using 4D scanning transmission electron microscopy. . Nat. Commun. 10:(1):1127
     [Crossref] [Google Scholar]
  76. 76.
    Varela M, Lupini AR, Benthem KV, Borisevich AY, Chisholm MF, et al. 2005.. Materials characterization in the aberration-corrected scanning transmission electron microscope. . Annu. Rev. Mater. Res. 35::539–69
     [Crossref] [Google Scholar]
  77. 77.
    Ophus C. 2019.. Four-dimensional scanning transmission electron microscopy (4D-STEM): from scanning nanodiffraction to ptychography and beyond. . Microsc. Microanal. 25:(3):563–82
     [Crossref] [Google Scholar]
  78. 78.
    Gallagher-Jones M, Bustillo KC, Ophus C, Richards LS, Ciston J, et al. 2020.. Atomic structures determined from digitally defined nanocrystalline regions. . IUCrJ 7:(3):490–99
     [Crossref] [Google Scholar]
  79. 79.
    Ercius P, Johnson IJ, Pelz P, Savitzky BH, Hughes L, et al. 2023.. The 4D Camera: an 87 kHz direct electron detector for scanning/transmission electron microscopy. . arXiv:2305.11961 [physics.ins-det]
  80. 80.
    Jones CG, Asay M, Kim LJ, Kleinsasser JF, Saha A, et al. 2019.. Characterization of reactive organometallic species via MicroED. . ACS Cent. Sci. 5:(9):1507–13
     [Crossref] [Google Scholar]
  81. 81.
    Ercius P, Alaidi O, Rames MJ, Ren G. 2015.. Electron tomography: a three-dimensional analytic tool for hard and soft materials research. . Adv. Mater. 27:(38):5638–63
     [Crossref] [Google Scholar]
  82. 82.
    Shi C, Cao MC, Rehn SM, Bae S-H, Kim J, et al. 2022.. Uncovering material deformations via machine learning combined with four-dimensional scanning transmission electron microscopy. . NPJ Comput. Mater. 8:(1):114
     [Crossref] [Google Scholar]
  83. 83.
    MacLaren I, Macgregor TA, Allen CS, Kirkland AI. 2020.. Detectors—The ongoing revolution in scanning transmission electron microscopy and why this important to material characterization. . APL Mater. 8:(11):110901
     [Crossref] [Google Scholar]
  84. 84.
    Jeong J, Cautaerts N, Dehm G, Liebscher CH. 2021.. Automated crystal orientation mapping by precession electron diffraction-assisted four-dimensional scanning transmission electron microscopy using a scintillator-based CMOS detector. . Microsc. Microanal. 27:(5):1102–12
     [Crossref] [Google Scholar]
  85. 85.
    Smeets S, Zou X, Wan W. 2018.. Serial electron crystallography for structure determination and phase analysis of nanocrystalline materials. . J. Appl. Crystallogr. 51:(5):1262–73
     [Crossref] [Google Scholar]
  86. 86.
    Bücker R, Hogan-Lamarre P, Mehrabi P, Schulz EC, Bultema LA, et al. 2020.. Serial protein crystallography in an electron microscope. . Nat. Commun. 11:(1):996
     [Crossref] [Google Scholar]
  87. 87.
    Wennmacher JTC, Zaubitzer C, Li T, Bahk YK, Wang J, et al. 2019.. 3D-structured supports create complete data sets for electron crystallography. . Nat. Commun. 10:(1):3316
     [Crossref] [Google Scholar]
  88. 88.
    Cheng Y. 2018.. Single-particle cryo-EM—How did it get here and where will it go. . Science 361:(6405):876–80
     [Crossref] [Google Scholar]
  89. 89.
    Castells-Graells R, Meador K, Arbing MA, Sawaya MR, Gee M, et al. 2023.. Cryo-EM structure determination of small therapeutic protein targets at 3 Å-resolution using a rigid imaging scaffold. . PNAS 120:(37):e2305494120
     [Crossref] [Google Scholar]
  90. 90.
    Hutchison CDM, Baxter JM, Fitzpatrick A, Dorlhiac G, Fadini A, et al. 2023.. Optical control of ultrafast structural dynamics in a fluorescent protein. . Nat. Chem. 15::1607–15
     [Crossref] [Google Scholar]
  91. 91.
    Martynowycz MW, Shiriaeva A, Clabbers MTB, Nicolas WJ, Weaver SJ, et al. 2023.. A robust approach for MicroED sample preparation of lipidic cubic phase embedded membrane protein crystals. . Nat. Commun. 14:(1):1086
     [Crossref] [Google Scholar]
  92. 92.
    Wolff AM, Young ID, Sierra RG, Brewster AS, Martynowycz MW, et al. 2020.. Comparing serial X-ray crystallography and microcrystal electron diffraction (MicroED) as methods for routine structure determination from small macromolecular crystals. . IUCrJ 7:(2):306–23
     [Crossref] [Google Scholar]
  93. 93.
    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:(9):2247–52
     [Crossref] [Google Scholar]
  94. 94.
    Nederlof I, Li YW, Van Heel M, Abrahams JP. 2013.. Imaging protein three-dimensional nanocrystals with cryo-EM. . Acta Crystallogr. D Biol. Crystallogr. 69:(5):852–59
     [Crossref] [Google Scholar]
  95. 95.
    Dorset DL. 1985.. Electron crystal structure analysis of small organic molecules. . J. Electron Microsc. Tech. 2:(2):89–128
     [Crossref] [Google Scholar]
  96. 96.
    Gallagher-Jones M, Ophus C, Bustillo KC, Boyer DR, Panova O, et al. 2019.. Nanoscale mosaicity revealed in peptide microcrystals by scanning electron nanodiffraction. . Commun. Biol. 2:(1):26
     [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-physchem-083122-105226
Loading
3D Nanocrystallography and the Imperfect Molecular Lattice
Annual Review of Physical Chemistry 75, 483 (2024); https://doi.org/10.1146/annurev-physchem-083122-105226
/content/journals/10.1146/annurev-physchem-083122-105226
/content/journals/10.1146/annurev-physchem-083122-105226
Loading

Data & Media loading...

Supplemental Materials

  • Supplemental Materials

file format pdf download PDF
  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error