Macromolecular Nanocrystal Structural Analysis with Electron and X-Rays: A Comparative Review
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, přehledy
PubMed
31561479
PubMed Central
PMC6804143
DOI
10.3390/molecules24193490
PII: molecules24193490
Knihovny.cz E-zdroje
- Klíčová slova
- X-ray free-electron laser, electron diffraction, nanocrystallography,
- MeSH
- elektrony * MeSH
- krystalografie rentgenová MeSH
- makromolekulární látky chemie MeSH
- molekulární modely * MeSH
- molekulární struktura MeSH
- nanočástice chemie MeSH
- rentgenové záření * MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
- Názvy látek
- makromolekulární látky MeSH
Crystallography has long been the unrivaled method that can provide the atomistic structural models of macromolecules, using either X-rays or electrons as probes. The methodology has gone through several revolutionary periods, driven by the development of new sources, detectors, and other instrumentation. Novel sources of both X-ray and electrons are constantly emerging. The increase in brightness of these sources, complemented by the advanced detection techniques, has relaxed the traditionally strict need for large, high quality, crystals. Recent reports suggest high-quality diffraction datasets from crystals as small as a few hundreds of nanometers can be routinely obtained. This has resulted in the genesis of a new field of macromolecular nanocrystal crystallography. Here we will make a brief comparative review of this growing field focusing on the use of X-rays and electrons sources.
Zobrazit více v PubMed
Drenth J. Principles of Protein X-Ray Crystallography. 3rd ed. Springer; New York, NY, USA: 2006.
Chapman H.N., Fromme P., Barty A., White T.A., Kirian R.A., Aquila A., Hunter M.S., Schulz J., DePonte D.P., Weierstall U., et al. Femtosecond x-ray protein nanocrystallography. Nature. 2011;470:73–77. doi: 10.1038/nature09750. PubMed DOI PMC
Clabbers M.T.B., Genderen E.V., Wan W., Wiegers E.L., Gruene T., Abrahams J.P. Protein structure determination by electron diffraction using a single three dimensional nanocrystal. Acta Cryst. Sect. D. 2017;73:738–748. doi: 10.1107/S2059798317010348. PubMed DOI PMC
Aquila A., Barty A., Bostedt C., Boutet S., Carini G., dePonte D., Drell P., Doniach S., Downing K.H., Earnest T., et al. The linac coherent light source single particle imaging road map. Struct. Dyn. 2015;2:041701. doi: 10.1063/1.4918726. PubMed DOI PMC
Bai X.C., McMullan G., Scheres S.H.W. How cryo-EM is revolutionizing structural biology. Trends Biochem. Sci. 2015;40:49–57. doi: 10.1016/j.tibs.2014.10.005. PubMed DOI
Duke E. Macromolecular crystallography at synchrotron radiation sources: Current status and future developments. Proc. R. Soc. A. 2010;466:3421–3452. doi: 10.1098/rspa.2010.0448. DOI
Cusack S., Belrhali H., Bram A., Burghammer M., Perrakis A., Riekel C. Small Is Beautiful: Protein Micro-Cryst. Nat. Struct. Biol. 1998;5:634–637. doi: 10.1038/1325. PubMed DOI
Hunter M.S., DePonte D.P., Shapiro D.A., Kirian R.A., Wang X., Starodub D., Marchesini S., Weierstall U., Doak R.B., Spence J.C., et al. X-ray diffraction from membrane protein nanocrystals. Biophys. J. 2011;100:198–206. doi: 10.1016/j.bpj.2010.10.049. PubMed DOI PMC
Laue M.V. Eine quantitative prüfung der theorie für die interferenz-erscheinungen bei Röntgenstrahlen. Ann. Phys. 1913;346:989–1002. doi: 10.1002/andp.19133461005. DOI
Watson J.D., Crick F.H.C. Molecular Structure of Nucleic Acids: A Structure for Deoxyribose Nucleic Acid. Nature. 1953;171:737–738. doi: 10.1038/171737a0. PubMed DOI
Perutz M.F., Rossman M.G., Cullis A.F., Muirhead H., Will G., North A.C. Structure of haemoglobin: A three-dimensional Fourier synthesis at 5.5-Å resolution, obtained by X-ray analysis. Nature. 1960;185:416–422. doi: 10.1038/185416a0. PubMed DOI
Kendrew J.C., Dickerson R.E., Strandberg B.E., Hart R.G., Davies D.R., Philips D.C., Shore V.C. Structure of myoglobin: A three-dimensional Fourier synthesis at 2 Å resolution. Nature. 1960;185:422–427. doi: 10.1038/185422a0. PubMed DOI
Dauter Z., Jaskolski M., Wlodawer A. Impact of synchrotron radiation on macromolecular crystallography: A personal view. J. Synchrotron Radiat. 2010;17:433–444. doi: 10.1107/S0909049510011611. PubMed DOI PMC
Emma P., Akre R., Arthur J., Bionta R., Bostedt C., Bozek J., Brachmann A., Bucksbaum P., Coffee R., Decker F.J., et al. First lasing and operation of an ångstrom-wavelength free-electron laser. Nat. Photon. 2010;4:641–647. doi: 10.1038/nphoton.2010.176. DOI
Yabashi M., Tanaka H., Ishikawa T. Overview of the SACLA facility. J. Synchrotron Radiat. 2015;22:477–484. doi: 10.1107/S1600577515004658. PubMed DOI PMC
Altarelli M., Brinkmann R., Chergui M., Decking W., Dobson B., Düsterer S., Grübel G., Graeff W., Graafsma H., Hajdu J., et al. The European X-Ray Free-Electron Laser Technical Design Report. DESY; Hamburg, Germany: 2007. DOI
Pechkova E., Nicolini C. Protein nanocrystallography: A new approach to structural proteomics. Trends Biotechnol. 2004;22:117–122. doi: 10.1016/j.tibtech.2004.01.011. PubMed DOI
Nicolini C., Pechkova E. Nanocrystallography: An emerging technology for structural proteomics. Expert Rev. Proteom. 2004;1:253–256. doi: 10.1586/14789450.1.3.253. PubMed DOI
Pechkova E., Nicolini C. Langmuir-Blodgett nanotemplates for protein crystallography. Nat Protoc. 2017;12:2570–2589. doi: 10.1038/nprot.2017.108. PubMed DOI
Neutze R., Wout R., van der Spoel D., Weckert E., Hajdu J. Potential for biomolecular imaging with femtosecond X-ray pulses. Nature. 2000;406:752–757. doi: 10.1038/35021099. PubMed DOI
Schlichting I. Serial femtosecond crystallography: The first five years. IUCrJ. 2015;2:246–255. doi: 10.1107/S205225251402702X. PubMed DOI PMC
Johansson L.C., Stauch B., Ishchenko A., Cherezov V. A Bright Future for Serial Femtosecond Crystallography with XFELs. Trends Biochem. Sci. 2017;42:749–762. doi: 10.1016/j.tibs.2017.06.007. PubMed DOI PMC
Nango E., Royant A., Kubo M., Nakane T., Wickstrand C., Kimura T., Tanaka T., Tono K., Song C.Y., Tanaka R., et al. A three-dimensional movie of structural changes in bacteriorhodopsin. Science. 2016;354:1552–1557. doi: 10.1126/science.aah3497. PubMed DOI
Boutet S., Lomb L., Williams G.J., Barends T.R., Aquila A., Doak R.B., Weierstall U., DePonte D.P., Steinbrener J., Shoeman R.L., et al. High-Resolution Protein Structure Determination by Serial Femtosecond Crystallography. Science. 2012;337:362–364. doi: 10.1126/science.1217737. PubMed DOI PMC
Suga M., Akita F., Hirata K., Ueno G., Murakami H., Nakajima Y., Shen J.-R. Native structure of photosystem II at 1.95A° resolution viewed by femtosecond X-ray pulses. Nature. 2015;517:99–103. doi: 10.1038/nature13991. PubMed DOI
Masuda T., Suzuki M., Inoue S., Song C., Nakane T., Nango E., Tanaka R., Tono K., Joti Y., Kameshima T., et al. Atomic resolution structure of serine protease proteinase K at ambient temperature. Sci. Rep. 2017;7:45604. doi: 10.1038/srep45604. PubMed DOI PMC
Koopmann R., Cupelli K., Reduce L., Nass K., Deponte D.P., White T.A., Stellato F., Rehders D., Liang M., Andreasson J., et al. In vivo protein crystallization opens new routes in structural biology. Nat. Methods. 2012;9:259–262. doi: 10.1038/nmeth.1859. PubMed DOI PMC
Liu W., Wacker D., Gati C., Han G.W., James D., Wang D., Nelson G., Weierstall U., Katritch V., Barty A., et al. Serial femtosecond crystallography of G protein-coupled receptors. Science. 2013;342:1521–1524. doi: 10.1126/science.1244142. PubMed DOI PMC
Weierstall U., James D., Wang C., White T.A., Wang D., Liu W., Spence J.C., Doak R.B., Nelson G., Fromme P., et al. Lipidic cubic phase injector facilitates membrane protein serial femtosecond crystallography. Nat. Commun. 2014;5:3309. doi: 10.1038/ncomms4309. PubMed DOI PMC
Johansson L.C., Arnlund D., Katona G., White T.A., Barty A., DePonte D.P., Shoeman R.L., Wickstrand C., Sharma A., Williams G.J., et al. Structure of a photosynthetic reaction centre determined by serial femtosecond crystallography. Nat. Commun. 2013;4:2911. doi: 10.1038/ncomms3911. PubMed DOI PMC
Barends T.R.M., Foucar L., Botha S., Doak R.B., Shoeman R.L., Nass K., Koglin J.E., Williams G.J., Boutet S., Messerschmidt M., et al. De novo protein crystal structure determination from X-ray free-electron laser data. Nature. 2014;505:244–247. doi: 10.1038/nature12773. PubMed DOI
Demirci H., Sierra R.G., Laksmono H., Shoeman R.L., Botha S., Barends T.R., Nass K., Schlichting I., Doak R.B., Gati C., et al. 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. Sect. F Struct. Biol. Cryst. Commun. 2013;69:1066–1069. doi: 10.1107/S174430911302099X. PubMed DOI PMC
Young I.D., Ibrahim M., Chatterjee R., Gul S., Fuller F., Koroidov S., Brewster A.S., Tran R., Alonso-Mori R., Kroll T., et al. Structure of photosystem II and substrate binding at room temperature. Nature. 2016;540:453–457. doi: 10.1038/nature20161. PubMed DOI PMC
Edlund P., Takala H., Claesson E., Henry L., Dods R., Lehtivuori H., Panman M., Pande K., White T., Nakane T., et al. The room temperature crystal structure of a bacterial phytochrome determined by serial femtosecond crystallography. Sci. Rep. 2016;6:35279. doi: 10.1038/srep35279. PubMed DOI PMC
Ishigami I., Zatsepin N.A., Hikita M., Conrad C.E., Nelson G., Coe J.D., Basu S., Grant T.D., Seaberg M.H., Sierra R.G., et al. Crystal structure of CO-bound cytochrome c oxidase determined by serial femtosecond X-ray crystallography at room temperature. Proc. Natl. Acad. Sci. USA. 2017;114:8011–8016. doi: 10.1073/pnas.1705628114. PubMed DOI PMC
Kang Y., Zhou X.E., Gao X., He Y., Liu W., Ishchenko A., Barty A., White T.A., Yefanov O., Han G.W., et al. Crystal structure of rhodopsin bound to arrestin by femtosecond X-ray laser. Nature. 2015;523:561–567. doi: 10.1038/nature14656. PubMed DOI PMC
Aquila A., Hunter M.S., Doak R.B., Kirian R.A., Fromme P., White T.A., Andreasson J., Arnlund D., Bajt S., Barends T.R., et al. Time-resolved protein nanocrystallography using an X-ray free-electron laser. Opt. Express. 2012;20:2706–2716. doi: 10.1364/OE.20.002706. PubMed DOI PMC
Tenboer J., Basu S., Zatsepin N., Pande K., Milathianaki D., Frank M., Hunter M., Boutet S., Williams G.J., Koglin J.E., et al. Time-resolved serial crystallography captures high-resolution intermediates of photoactive yellow protein. Science. 2014;346:1242–1246. doi: 10.1126/science.1259357. PubMed DOI PMC
Kupitz C., Basu S., Grotjohann I., Fromme R., Zatsepin N.A., Rendek K.N., Hunter M.S., Shoeman R.L., White T.A., Wang. D., et al. Serial time-resolved crystallography of photosystem II using a femtosecond X-ray laser. Nature. 2014;513:261–265. doi: 10.1038/nature13453. PubMed DOI PMC
Stagno J.R., Liu Y., Bhandari Y.R., Conrad C.E., Panja S., Swain M., Fan L., Nelson G., Li C., Wendel D.R., et al. Structures of riboswitch RNA reaction states by mix-and-inject XFEL serial crystallography. Nature. 2017;541:242–246. doi: 10.1038/nature20599. PubMed DOI PMC
Jakobi A.J., Passon D.M., Knoops K., Stellato F., Liang M., White T.A., Seine T., Messerschmidt M., Chapman H.N., Wilmanns M. In cellulo serial crystallography of alcohol oxidase crystals inside yeast cells. IUCrJ. 2016;3:88–95. doi: 10.1107/S2052252515022927. PubMed DOI PMC
Dilanian R.A., Streltsov V., Coughlan H.D., Quiney H.M., Martin A.V., Klonis N., Dogovski C., Boutet S., Messerschmidt M., Williams G.J., et al. Nanocrystallography measurements of early stage synthetic malaria pigment. J. Appl. Cryst. 2017;50:1533–1540. doi: 10.1107/S1600576717012663. PubMed DOI PMC
Redecke L., Nass K., DePonte D.P., White T.A., Rehders D., Barty A., Stellato F., Liang M., Barends T.R.M., Boutet S., et al. Natively inhibited Trypanosoma brucei cathepsin B structure determined by using an X-ray laser. Science. 2013;339:227–230. doi: 10.1126/science.1229663. PubMed DOI PMC
Colletier J.P., Sawaya M.R., Gingery M., Rodriguez J.A., Cascio D., Brewster A.S., Michels-Clark T., Hice R.H., Coquelle N., Boutet S., et al. De novo phasing with X-ray laser reveals mosquito larvicide BinAB structure. Nature. 2016;539:43–47. doi: 10.1038/nature19825. PubMed DOI PMC
Gati C., Oberthuer D., Yefanov O., Bunker R.D., Stellato F., Chiu E., Yeh S.M., Aquila A., Basu S., Bean R., et al. Atomic structure of granulin determined from native nanocrystalline granulovirus using an X-ray free-electron laser. Proc. Natl. Acad. Sci. USA. 2017;114:2247–2252. doi: 10.1073/pnas.1609243114. PubMed DOI PMC
Cohen A.E., Soltis S.M., González A., Aguila L., Alonso-Mori R., Barnes C.O., Baxter E.L., Brehmer W., Brewster A.S., Brunger A.T., et al. Goniometer-based femtosecond crystallography with X-ray free electron lasers. Proc. Natl. Acad. Sci. USA. 2014;111:17122–17127. doi: 10.1073/pnas.1418733111. PubMed DOI PMC
Pedrini B., Tsai C.J., Capitani G., Padeste C., Hunter M.S., Zatsepin N.A., Barty A., Benner W.H., Boutet S., Feld G.K., et al. 7 Å resolution in protein two-dimensional-crystal X-ray diffraction at Linac Coherent Light Source. Philos. Trans. R Soc. Lond. B Biol. Sci. 2014;369:20130500. doi: 10.1098/rstb.2013.0500. PubMed DOI PMC
Grünbein M.L., Nass Kovacs G. Sample delivery for serial crystallography at free-electron lasers and synchrotrons. Acta Cryst. D Struct. Biol. 2019;75:178–191. doi: 10.1107/S205979831801567X. PubMed DOI PMC
Liu H., Spence J.C.H. XFEL data analysis for structural biology. Quant Biol. 2016;4:159. doi: 10.1007/s40484-016-0076-z. DOI
Eriksson M., Friso J.V., Quitmann C. Diffraction-limited storage rings—A window to the science of tomorrow. J. Synchrotron Rad. 2014;21:837–842. doi: 10.1107/S1600577514019286. PubMed DOI
Kirian R.A., Wang X., Weierstall U., Schmidt K.E., Spence J.C.H., Hunter M., Fromme P., White T., Chapman H.N., Holton J. Femtosecond Protein Nanocrystallography-Data Anal. Methods. Opt. Express. 2010;18:5713–5723. doi: 10.1364/OE.18.005713. PubMed DOI PMC
De Rossier D.J., Klug A. Reconstruction of three dimensional structures from Electron Micrographs. Nature. 1968;217:130–134. doi: 10.1038/217130a0. PubMed DOI
Henderson R., Unwin P.N.T. Three-dimensional model of purple membrane obtained by electron microscopy. Nature. 1975;257:28–32. doi: 10.1038/257028a0. PubMed DOI
Gonen T., Cheng Y., Sliz P., Hiroaki Y., Fujiyoshi Y., Harrison S.C., Walz T. Lipid-protein interactions in double-layered two-dimensional AQP0 crystals. Nature. 2005;438:633–638. doi: 10.1038/nature04321. PubMed DOI PMC
Dorset D.L., Parsons D.F. Electron diffraction from single, fully-hydrated, ox-liver catalase microcrystals. Acta Cryst. A. 1975;31:210–215. doi: 10.1107/S0567739475000423. DOI
Nannenga B.L., Gonen T. MicroED: A versatile cryoEM method for structure determination. Emerg. Top. Life Sci. 2018;2:1–8. doi: 10.1042/ETLS20170082. PubMed DOI PMC
Shi D., Nannenga B.L., Iadanza M.G., Gonen T. Three-dimensional electron crystallography of protein microcrystals. Elife. 2013;2:e01345. doi: 10.7554/eLife.01345. PubMed DOI PMC
Duyvesteyn H.M.E., Kotecha A., Ginn H.M., Hecksel C.W., Beale E.V., de Haas F., Evans G., Zhang P., Chiu W., Stuart D.I. Machining protein microcrystals for structure determination by electron diffraction. Proc. Natl. Acad. Sci. USA. 2018;115:9569–9573. doi: 10.1073/pnas.1809978115. PubMed DOI PMC
Li X., Zhang S., Zhang J., Sun F. In situ protein micro-crystal fabrication by cryo-FIB for electron diffraction. Biophys. Rep. 2018;4:339–347. doi: 10.1007/s41048-018-0075-x. PubMed DOI PMC
Thompson R.F., Walker M., Siebert C.A., Muench S.P., Ranson N.A. An introduction to sample preparation and imaging by cryo-electron microscopy for structural biology. Methods. 2016;100:3–15. doi: 10.1016/j.ymeth.2016.02.017. PubMed DOI PMC
Nannenga B.L., Gonen T. MicroED opens a new era for biological structure determination. Curr. Opin. Struct. Biol. 2016;40:128–135. doi: 10.1016/j.sbi.2016.09.007. PubMed DOI PMC
Martynowycz M.W., Gonen T. From electron crystallography of 2D crystals to MicroED of 3D crystals. Curr. Opin. Colloid Interface Sci. 2018;34:9–16. doi: 10.1016/j.cocis.2018.01.010. PubMed DOI PMC
Nannenga B.L., Gonen T. The cryo-EM method microcrystal electron diffraction (MicroED) Nat. Methods. 2019;16:369–379. doi: 10.1038/s41592-019-0395-x. PubMed DOI PMC
Rodriguez J.A., Ivanova M.I., Sawaya M.R., Cascio D., Reyes F.E., Shi D., Sangwan S., Guenther E.L., Johnson L.M., Zhang M., et al. Structure of the toxic core of α-synuclein from invisible crystals. Nature. 2015;525:486–490. doi: 10.1038/nature15368. PubMed DOI PMC
Yonekura K., Kato K., Ogasawara M., Tomita M., Toyoshima C. Electron crystallography of ultrathin 3D protein crystals: Atomic model with charges. Proc. Natl. Acad. Sci. USA. 2015;112:3368–3373. doi: 10.1073/pnas.1500724112. PubMed DOI PMC
Purdy M.D., Shi D., Chrustowicz J., Hattne J., Gonen T., Yeager M. MicroED structures of HIV-1 Gag CTD-SP1 reveal binding interactions with the maturation inhibitor bevirimat. Proc. Natl. Acad. Sci. USA. 2018;115:13258–13263. doi: 10.1073/pnas.1806806115. PubMed DOI PMC
De la Cruz M.J., Hattne J., Shi D., Seidler P., Rodriguez J., Reyes F.E., Sawaya M.R., Cascio D., Weiss S.C., Kim S.K., et al. Atomic-resolution structures from fragmented protein crystals with the cryoEM method MicroED. Nat. Methods. 2017;14:399–402. doi: 10.1038/nmeth.4178. PubMed DOI PMC
Lanza A., Margheritis E., Mugnaioli E., Cappello V., Garau G., Gemmi M. Nanobeam precession-assisted 3D electron diffraction reveals a new polymorph of hen egg-white lysozyme. IUCrJ. 2019;6:178–188. doi: 10.1107/S2052252518017657. PubMed DOI PMC
Xu H., Lebrette H., Clabbers M., Zhao J., Griese J.J., Zou X., Högbom M. Solving a new R2lox protein structure by microcrystal electron diffraction. Sci. Adv. 2019;5:eaax4621. doi: 10.1126/sciadv.aax4621. PubMed DOI PMC
Zhu L., Bu G., Jing L., Shi D., Gonen T., Liu W., Nannenga B.L. Structure determination from lipidic cubic phase embedded microcrystals by MicroED. bioRxiv. 2019:724575. doi: 10.1101/724575. PubMed DOI PMC
Nederlof I., Li Y.W., Marin V.H., Abrahams J.P. Imaging protein three-dimensional nanocrystals with cryo-EM. Acta Cryst. 2013;D69:852–859. doi: 10.1107/S0907444913002734. PubMed DOI
Sawaya M.R., Rodriguez J., Cascio D., Collazo M.J., Shi D., Reyes F.E., Hattne J., Gonen T., Eisenberg D.S. Ab initio structure determination from prion nanocrystals at atomic resolution by MicroED. Proc. Natl. Acad. Sci. USA. 2016;113:11232–11236. doi: 10.1073/pnas.1606287113. PubMed DOI PMC
Kolb U., Mugnaioli E., Gorelik T.E. Automated electron diffraction tomography—A new tool for nano crystal structure analysis. Cryst. Res. Technol. 2011;46:542–554. doi: 10.1002/crat.201100036. DOI
Kolb U., Krysiak Y., Plana-Ruiz S. Automated electron diffraction tomography – development and applications. Acta Cryst. Sect. Bstruct. Sci. Cryst. Eng. Mater. 2019;75:463–474. doi: 10.1107/S2052520619006711. PubMed DOI PMC
Wan W., Sun J.L., Su J., Hovmoller S., Zou X.D. Three-dimensional rotation electron diffraction: Software RED for automated data collection and data processing. J. Appl. Cryst. 2013;46:1863–1873. doi: 10.1107/S0021889813027714. PubMed DOI PMC
Iadanza M.G., Gonen T. A suite of software for processing MicroED data of extremely small protein crystals. J. Appl. Cryst. 2014;47:1140–1145. doi: 10.1107/S1600576714008073. PubMed DOI PMC
Nannenga B.L., Shi D., Leslie A., Gonen T. High-resolution structure determination by continuous-rotation data collection in MicroED. Nat. Methods. 2014;11:927–930. doi: 10.1038/nmeth.3043. PubMed DOI PMC
Hattne J., Reyes F.E., Nannenga B.L., Shi D., de la Cruz M.J., Leslie A.G., Gonen T. MicroED data collection and processing. Acta Cryst. Sect. Afound. Adv. 2015;71:353–360. doi: 10.1107/S2053273315010669. PubMed DOI PMC
Leslie A.G.W., Powell H.R. Evolving Methods for Macromolecular Crystallography. Springer; Dordrecht, The Netherlands: 2007. Processing diffraction data with mosflm.
Clabbers M., Gruene T., Parkhurst J.M., Abrahams J.P., Waterman D.G. Electron diffraction data processing with DIALS. Acta Cryst. Sect. Dstruct. Biol. 2018;74:506–518. doi: 10.1107/S2059798318007726. PubMed DOI PMC
Kabsch W. XDS. Acta Cryst. Sect. Dbiol. Cryst. 2010;66:125–132. doi: 10.1107/S0907444909047337. PubMed DOI PMC
Dwyer J.R., Hebeisen C.T., Ernstorfer R., Harb M., Deyirmenjian B.V., Jordan R.E., Miller R.J.D. Femtosecond electron diffraction: Making the molecular movie. Philos. Trans. A Math Phys. Eng. Sci. 2006;364:741–778. doi: 10.1098/rsta.2005.1735. PubMed DOI
Ruan C.Y., Vigliotti F., Lobastov V.A., Chen S., Zewail A.H. Ultrafast electron crystallography: Transient structures of molecules, surfaces, and phase transitions. Proc. Natl. Acad. Sci. USA. 2004;101:1123–1128. doi: 10.1073/pnas.0307302101. PubMed DOI PMC
Yang D.S., Baum P., Zewail A.H. Ultrafast electron crystallography of the cooperative reaction path in vanadium dioxide. Struct. Dyn. 2016;3:034304. doi: 10.1063/1.4953370. PubMed DOI PMC
Chen S., Seidel M.T., Zewail A.H. Ultrafast Electron Crystallography of Phospholipids. Angew. Chem. Int. Ed. 2006;45:5154–5158. doi: 10.1002/anie.200601778. PubMed DOI
Spence J.C.H., Kirian R.R., Wang X., Weierstall U., Schmidt K.E., White T., Barty A., Chapman H.N., Marchesini S., Holton J. Phasing of coherent femtosecond X-ray diffraction from size-varying nanocrystals. Opt. Express. 2011;19:2866–2873. doi: 10.1364/OE.19.002866. PubMed DOI
Kirian R.A., Bean R.J., Beyerlein K.R., Yefanov O.M., White T.A., Barty A., Chapman H.N. Phasing coherently illuminated nanocrystals bounded by partial unit cells. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2014;369:20130331. doi: 10.1098/rstb.2013.0331. PubMed DOI PMC
Gallagher-Jons M., Ophus C., Bustillo K.C., Boyer D.R., Panova O., Glynn C., Zee C.T., Ciston J., Mancia K.C., Minor A.M., et al. Nanoscale mosaicity revealed in peptide microcrystals by scanning electron nanodiffraction. Commun. Biol. 2019;18:2–26. doi: 10.1038/s42003-018-0263-8. PubMed DOI PMC
Wiedorn M.O., Oberthür D., Bean R., Schubert R., Werner N., Abbey B., Aepfelbacher M., Adriano L., Allahgholi A., Al-Qudami N., et al. Megahertz serial crystallography. Nat. Commun. 2018;9:4025. doi: 10.1038/s41467-018-06156-7. PubMed DOI PMC
Weierstall U. Liquid sample delivery techniques for serial femtosecond crystallography. Phil. Trans. R. Soc. B. 2014;369 doi: 10.1098/rstb.2013.0337. PubMed DOI PMC
Jonsson H.O., Caleman C., Andreasson J., Tımneanu N. Hit detection in serial femtosecond crystallography using X-ray spectroscopy of plasma emission. IUCrJ. 2017;4:778–784. doi: 10.1107/S2052252517014154. PubMed DOI PMC
White T.A., Mariani V., Brehm W., Yefanov O., Barty A., Beyerlein K.R., Chervinskii F., Galli L., Gati C., Nakane T., et al. Recent developments in CrystFEL. J. Appl. Crystallogr. 2016;49:680–689. doi: 10.1107/S1600576716004751. PubMed DOI PMC
Kabsch W. Processing of X-ray snapshots from crystals in random orientations. Acta Cryst. Sect. Dbiol. Cryst. 2014;70:2204–2216. doi: 10.1107/S1399004714013534. PubMed DOI PMC
Ginn H.M., Brewster A.S., Hattne J., Evans G., Wagner A., Grimes J.M., Sauter N.K., Sutton G., Stuart D.I. A revised partiality model and post-refinement algorithm for X-ray free-electron laser data. Acta Crystallogr. Sect. D Biol. Crystallogr. 2015;71:1400–1410. doi: 10.1107/S1399004715006902. PubMed DOI PMC
Palatinus L., Brázda P., Boullay P., Perez O., Klementová M., Petit S., Eigner V., Zaarour M., Mintova S. Hydrogen positions in single nanocrystals revealed by electron diffraction. Science. 2017;355:6321. doi: 10.1126/science.aak9652. PubMed DOI
Palatinus L., Corrêa C.A., Steciuk G., Jacob D., Roussel P., Boullay P., Klementová M., Gemmi M., Kopeček J., Domeneghetti M.C. Structure refinement using precession electron diffraction tomography and dynamical diffraction: Tests on experimental data. Acta Cryst. A. 2013;69:171–188. doi: 10.1107/S010876731204946X. PubMed DOI
Jansen J., Tang D., Zandbergen H.W., Schenk H. MSLS, a Least-Squares Procedure for Accurate Crystal Structure Refinement from Dynamical Electron Diffraction Patterns. Actacrystallogr. A. 1998;54:91–101. doi: 10.1107/S0108767397010489. DOI
Henderson R. The potential and limitations of neutrons, electrons and X-rays for atomic resolution microscopy of unstained biological molecules. Q. Rev. Biophys. 1995;28:171–193. doi: 10.1017/S003358350000305X. PubMed DOI
Barty A., Caleman C., Aquila A., Timneanu N., Lomb L., White T.A., Andreasson J., Arnlund D., Bajt S., Barends T.R., et al. Self-terminating diffraction gates femtosecond X-ray nanocrystallography measurements. Nat. Photonics. 2012;6:35–40. doi: 10.1038/nphoton.2011.297. PubMed DOI PMC
On-the-fly resolution enhancement in X-ray protein crystallography using electric field