1,235
Views
19
CrossRef citations to date
0
Altmetric
Review

An outlook on using serial femtosecond crystallography in drug discovery

, , , , & ORCID Icon
Pages 933-945 | Received 26 Feb 2019, Accepted 30 May 2019, Published online: 11 Jun 2019

References

  • Paul SM, Mytelka DS, Dunwiddie CT, et al. How to improve R&D productivity: the pharmaceutical industry’s grand challenge. Nat Rev Drug Discov. 2010;9:203–214.
  • Munos B. Lessons from 60 years of pharmaceutical innovation. Nat Rev Drug Discov. 2009;8:959–968.
  • Mullard A. 2018 FDA drug approvals. Nat Rev Drug Discov. 2019;18:85–89.
  • Smietana K, Siatkowski M, Møller M. Trends in clinical success rates. Nat Rev Drug Discov. 2016;15:379–380.
  • Van MRLM, Workman P. Structure-based drug design: aiming for a perfect fit. Essays Biochem. 2017;61:431–437.
  • Spence JCH. XFELs for structure and dynamics in biology. IUCrJ. 2017;4:322–339.
  • Johansson LC, Stauch B, Ishchenko A, et al. A bright future for serial femtosecond crystallography with XFELs. Trends Biochem Sci. 2017;42:749–762.
  • Bohacek RS, McMartin C, Guida WC, et al. Practice of structure-based drug design: a molecular modeling perspective. Med Res Rev. 1996;16:3–50.
  • Murray CW, Rees DC. The rise of fragment-based drug discovery. Nat Chem. 2009;1:187–192.
  • Peltason L, Bajorath J. SAR Index : quantifying the nature of structure - activity relationships. J Med Chem. 2007;50:5571–5578.
  • Ekins S, Mestres J, Testa B. In silico pharmacology for drug discovery : methods for virtual ligand screening and profiling. Br J Pharmacol. 2007;152:9–20.
  • Lyu J, Wang S, Balius TE, et al. Ultra-large library docking for discovering new chemotypes. Nature. 2019;566:224–229.
  • Sterling T, Irwin JJ. ZINC 15 - Ligand Discovery for Everyone. J Chem Inf Model. 2015;55:2324–2337.
  • Keserű GM, Erlanson DA, Ferenczy GG, et al. Design principles for fragment libraries: maximizing the value of learnings from pharma Fragment-Based Drug Discovery (FBDD) Programs for Use in Academia. J Med Chem. 2016;59:8189–8206.
  • Beddell CR, Goodford PJ, Norrington FE, et al. COMPOUNDS DESIGNED TO FIT A SITE OF KNOWN STRUCTURE IN HUMAN HAEMOGLOBIN. Br J Pharmacol. 1976;57:201–209.
  • Blundell T, Sibanda BL, Pearl L. Three-dimensional structure, specificity and catalytic mechanism of renin. Nature. 1983;304:273–275.
  • Dhanaraj V, Cg D, Frazao C, et al. X-ray analyses of peptide-inhibitor complexes define the structural basis of specificity for human and mouse renins. Nature. 1992;357:466–472.
  • Ma N, Pmd F, Bm M, et al. Three-dimensional structure of aspartyl protease from human immunodeficiency virus HIV-1. Nature. 1989;337:615–620.
  • Kim CU, Lew W, Williams MA, et al. Influenza neuraminidase inhibitors possessing a novel hydrophobic interaction in the enzyme active site : design, synthesis, and structural analysis of carbocyclic sialic acid analogues with potent anti-influenza activity. J Am Chem Soc. 1997;119:681–690.
  • Van Montfort RLM, Workman P. Structure-based design of molecular cancer therapeutics. Trends Biotechnol. 2009;27:315–328.
  • Borshell N, Papp T, Congreve M. Deal watch: valuation benefits of structure-enabled drug discovery. Nat Rev Drug Discov. 2011;10:166.
  • Cherezov V, Rosenbaum DM, Hanson MA, et al. High-resolution crystal structure of an engineered human b2-Adrenergic G Protein-Coupled Receptor. Science. 2007;318:1258–1266.
  • Pándy-Szekeres G, Munk C, Tsonkov TM, et al. GPCRdb in 2018: adding GPCR structure models and ligands. Nucleic Acids Res. 2018;46:440–446.
  • Katritch V, Cherezov V, Stevens RC. Structure-Function of the G Protein–coupled Receptor Superfamily. Annu Rev Pharmacol Toxicol. 2013;53:531–556.
  • Pellegrini C. The history of X-ray free-electron lasers. Eur Phys J H. 2012;37:659–708.
  • Ginzburg VL. On the radiation of microradiowaves and their absorbtion in the air. Izv Akad Nauk SSSR Ser Fiz. 1947;11:165.
  • Motz H. Applications of the radiation from fast electron beams. J Appl Phys. 1951;22:527–535.
  • Tiedtke K, Azima A, von Bargen N, et al. The soft x-ray free-electron laser FLASH at DESY: beamlines, diagnostics and end-stations. New J Phys. 2009;11:023029.
  • McNeil B. Free electron lasers: first light from hard X-ray laser. Nat Photonics. 2009;3:375–377.
  • Emma P, Akre R, Arthur J, et al. First lasing and operation of an ångstrom-wavelength free-electron laser. Nat Photonics. 2010;4:641–647.
  • McNeil BWJ, Thompson NR. X-ray free-electron lasers. Nat Photonics. 2010;4:814–821.
  • Neutze R, Wouts R, Van Der Spoel D, et al. Potential for biomolecular imaging with femtosecond X-ray pulses. Nature. 2000;406:752–757.
  • Miller RJD. Femtosecond crystallography with ultrabright electrons and X-rays: capturing chemistry in action. Science. 2014;343:1108–1117.
  • Kupitz C, Basu S, Grotjohann I, et al. Serial time-resolved crystallography of photosystem II using a femtosecond X-ray laser. Nature. 2014;513:261–265.
  • Bostedt C, Boutet S, Fritz DM, et al. Linac coherent light source: the first five years. Rev Mod Phys. 2016;88:015007.
  • Lv H, Leng Y, Yan Y, et al. The high level application architecture of the control system for SHINE. Nucl Instruments Methods Phys Res Sect A Accel Spectrometers Detect Assoc Equip. 2018;908:167–171.
  • Raubenheimer TO The LCLS-II-HE, A High Energy Upgrade of the LCLS-II. In: Chin YH, Zhao Z, Petit-Jean-Genaz C, et al., editors. Proceedings of the 60th ICFA Advanced Beam Dynamics Workshop on Future Light Sources; 2018 March 5-9; Shanghai, China. JACoW Publishing; p. 6–11. doi:10.18429/JACoW-FLS2018-MOP1WA02.
  • Chapman HN, Fromme P, Barty A, et al. Femtosecond X-ray protein nanocrystallography. Nature. 2011;470:73–77.
  • DePonte DP, Weierstall U, Schmidt K, et al. Gas dynamic virtual nozzle for generation of microscopic droplet streams. J Phys D Appl Phys. 2008;41:195505.
  • Oberthuer D, Knoška J, Wiedorn MO, et al. Double-flow focused liquid injector for efficient serial femtosecond crystallography. Sci Rep. 2017;7:44628.
  • Sierra RG, Laksmono H, Kern J, et al. Nanoflow electrospinning serial femtosecond crystallography. Acta Crystallogr Sect D Biol Crystallogr. 2012;68:1584–1587.
  • Sierra RG, Gati C, Laksmono H, et al. Concentric-flow electrokinetic injector enables serial crystallography of ribosome and photosystem II. Nat Methods. 2016;13:59–62.
  • Weierstall U, James D, Wang C, et al. Lipidic cubic phase injector facilitates membrane protein serial femtosecond crystallography. Nat Commun. 2014;5:3309.
  • Caffrey M, Cherezov V. Crystallizing membrane proteins using lipidic mesophases. Nat Protoc. 2009;4:706–731.
  • Stauch B, Cherezov V. Serial Femtosecond Crystallography of G Protein–coupled Receptors. Annu Rev Biophys. 2018;47:377–397.
  • Nango E, Royant A, Kubo M, et al. A three-dimensional movie of structural changes in bacteriorhodopsin. Science. 2016;354:1552–1557.
  • Fromme R, Ishchenko A, Metz M, et al. Serial femtosecond crystallography of soluble proteins in lipidic cubic phase. IUCrJ. 2015;2:545–551.
  • Hunter MS, Segelke B, Messerschmidt M, et al. Fixed-target protein serial microcrystallography with an x-ray free electron laser. Sci Rep. 2015;4:6026.
  • Roedig P, Ginn HM, Pakendorf T, et al. High-speed fixed-target serial virus crystallography. Nat Methods. 2017;14:805–810.
  • Fuller FD, Gul S, Chatterjee R, et al. Drop-on-demand sample delivery for studying biocatalysts in action at X-ray free-electron lasers. Nat Methods. 2017;14:443–449.
  • Tenboer J, Basu S, Zatsepin N, et al. Time-resolved serial crystallography captures high-resolution intermediates of photoactive yellow protein. Science. 2014;346:1242–1246.
  • Kupitz C, Grotjohann I, Conrad CE, et al. Microcrystallization techniques for serial femtosecond crystallography using photosystem II from Thermosynechococcus elongatus as a model system. Philos Trans R Soc B Biol Sci. 2014;369:20130316.
  • Dods R, Båth P, Arnlund D, et al. From macrocrystals to microcrystals: a strategy for membrane protein serial crystallography. Structure. 2017;25:1461–1468.
  • Redecke L, Nass K, DePonte DP, et al. Natively Inhibited Trypanosoma brucei Cathepsin B Structure Determined by Using an X-ray Laser. Science. 2013;339:227–230.
  • Jakobi AJ, Passon DM, Knoops K, et al. In cellulo serial crystallography of alcohol oxidase crystals inside yeast cells. IUCrJ. 2016;3:88–95.
  • Sawaya MR, Cascio D, Gingery M, et al. Protein crystal structure obtained at 2.9 A resolution from injecting bacterial cells into an X-ray free-electron laser beam. Proc Natl Acad Sci. 2014;111:12769–12774.
  • Duyvesteyn HME, Ginn HM, Pietilä MK, et al. Towards in cellulo virus crystallography. Sci Rep. 2018;8:3771.
  • Liu W, Ishchenko A, Cherezov V. Preparation of microcrystals in lipidic cubic phase for serial femtosecond crystallography. Nat Protoc. 2014;9:2123–2134.
  • Kissick DJ, Wanapun D, Simpson GJ. Second-order nonlinear optical imaging of chiral crystals. Annu Rev Anal Chem. 2011;4:419–437.
  • Brönnimann C, Trüb P. Hybrid pixel photon counting X-Ray detectors for synchrotron radiation. In: Jaeschke E, Khan S, Schneider J, et al., editors. Synchrotron light sources free-electron lasers. Cham: Springer; 2015. p. 1–29.
  • Hart P, Boutet S, Carini G, et al. The Cornell-SLAC pixel array detector at LCLS. IEEE Nucl Sci Symp Conf Rec. 2012 Oct 27 - Nov 3; Anaheim, CA, USA. IEEE; 2012. p. 538–541.
  • Henrich B, Becker J, Dinapoli R, et al. The adaptive gain integrating pixel detector AGIPD a detector for the European XFEL. Nucl Instruments Methods Phys Res Sect A Accel Spectrometers, Detect Assoc Equip. 2011;633:11–14.
  • Mozzanica A, Andrä M, Barten R, et al. The JUNGFRAU detector for applications at synchrotron light sources and XFELs. Synchrotron Radiat News. 2018;31:16–20.
  • Allahgholi A, Becker J, Delfs A, et al. The adaptive gain integrating pixel detector at the European XFEL. J Synchrotron Radiat. 2019;26:74–82.
  • Barty A, Kirian RA, Maia FRNC, et al. Cheetah : software for high-throughput reduction and analysis of serial femtosecond X-ray diffraction data. J Appl Crystallogr. 2014;47:1118–1131.
  • Coquelle N, Brewster AS, Kapp U, et al. Raster-scanning serial protein crystallography using micro- and nano-focused synchrotron beams. Acta Crystallogr Sect D Biol Crystallogr. 2015;71:1184–1196.
  • Ke TW, Brewster AS, Yu SX, et al. A convolutional neural network-based screening tool for X-ray serial crystallography. J Synchrotron Radiat. 2018;25:655–670.
  • Zaefferer S. New developments of computer-aided crystallographic analysis in transmission electron microscopy. J Appl Crystallogr. 2000;33:10–25.
  • Winter G, Waterman DG, Parkhurst JM, et al. DIALS : implementation and evaluation of a new integration package. Acta Crystallogr Sect D Struct Biol. 2018;74:85–97.
  • Kabsch W. Processing of X-ray snapshots from crystals in random orientations. Acta Crystallogr Sect D Biol Crystallogr. 2014;70:2204–2216.
  • Sauter NK, Hattne J, Grosse-Kunstleve RW, et al. New Python-based methods for data processing. Acta Crystallogr Sect D Biol Crystallogr. 2013;69:1274–1282.
  • Mariani V, Morgan A, Yoon CH, et al. OnDA : online data analysis and feedback for serial X-ray imaging. J Appl Crystallogr. 2016;49:1073–1080.
  • Nakane T, Joti Y, Tono K, et al. Data processing pipeline for serial femtosecond crystallography at SACLA. J Appl Crystallogr. 2016;49:1035–1041.
  • Foucar L. CFEL–ASG Software Suite (CASS): usage for free-electron laser experiments with biological focus. J Appl Crystallogr. 2016;49:1336–1346.
  • Park J, Kim S, Kim S, et al. Multifarious injection chamber for molecular structure study (MICOSS) system: development and application for serial femtosecond crystallography at Pohang Accelerator Laboratory X-ray Free-Electron Laser. J Synchrotron Radiat. 2018;25:323–328.
  • White TA, Kirian RA, Martin AV, et al. CrystFEL : a software suite for snapshot serial crystallography. J Appl Crystallogr. 2012;45:335–341.
  • Ginn HM, Evans G, Sauter NK, et al. On the release of cppxfel for processing X-ray free-electron laser images. J Appl Crystallogr. 2016;49:1065–1072.
  • Ginn HM, Roedig P, Kuo A, et al. TakeTwo : an indexing algorithm suited to still images with known crystal parameters. Acta Crystallogr Sect D Struct Biol. 2016;72:956–965.
  • Li C, Li X, Kirian R, et al. SPIND : a reference-based auto-indexing algorithm for sparse serial crystallography data. IUCrJ. 2019;6:72–84.
  • Gevorkov Y. xgandalf. 2019. Available from: https://stash.desy.de/users/gevorkov/repos/xgandalf/browse.
  • Beyerlein KR, White TA, Yefanov O, et al. FELIX: an algorithm for indexing multiple crystallites in X-ray free-electron laser snapshot diffraction images. J Appl Crystallogr. 2017;50:1075–1083.
  • White TA. Post-refinement method for snapshot serial crystallography. Philos Trans R Soc B Biol Sci. 2014;369:20130330.
  • Ginn HM, Brewster AS, Hattne J, et al. 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.
  • Sauter NK. XFEL diffraction: developing processing methods to optimize data quality. J Synchrotron Radiat. 2015;22:239–248.
  • Uervirojnangkoorn M, Zeldin OB, Lyubimov AY, et al. Enabling X-ray free electron laser crystallography for challenging biological systems from a limited number of crystals. Elife. 2015;4:e05421.
  • Kroon-Batenburg LMJ, Schreurs AMM, Ravelli RBG, et al. Accounting for partiality in serial crystallography using ray-tracing principles. Acta Crystallogr Sect D Biol Crystallogr. 2015;71:1799–1811.
  • Hattne J, Echols N, Tran R, et al. Accurate macromolecular structures using minimal measurements from X-ray free-electron lasers. Nat Methods. 2014;11:545–548.
  • Barends TRM, Foucar L, Botha S, et al. De novo protein crystal structure determination from X-ray free-electron laser data. Nature. 2014;505:244–247.
  • Yamashita K, Pan D, Okuda T, et al. An isomorphous replacement method for efficient de novo phasing for serial femtosecond crystallography. Sci Rep. 2015;5:14017.
  • Nakane T, Hanashima S, Suzuki M, et al. Membrane protein structure determination by SAD, SIR, or SIRAS phasing in serial femtosecond crystallography using an iododetergent. Proc Natl Acad Sci. 2016;113:13039–13044.
  • Colletier J-P, Sawaya MR, Gingery M, et al. De novo phasing with X-ray laser reveals mosquito larvicide BinAB structure. Nature. 2016;539:43–47.
  • Batyuk A, Galli L, Ishchenko A, et al. Native phasing of x-ray free-electron laser data for a G protein–coupled receptor. Sci Adv. 2016;2:e1600292.
  • Galli L, Son S-K, Barends TRM, et al. Towards phasing using high X-ray intensity. IUCrJ. 2015;2:627–634.
  • Millane RP, Chen JPJ. Aspects of direct phasing in femtosecond nanocrystallography. Philos Trans R Soc B Biol Sci. 2014;369:20130498.
  • Morgan AJ, Ayyer K, Barty A, et al. Ab initio phasing of the diffraction of crystals with translational disorder. Acta Crystallogr Sect A Found Adv. 2019;75:25–40.
  • Gorel A, Motomura K, Fukuzawa H, et al. Multi-wavelength anomalous diffraction de novo phasing using a two-colour X-ray free-electron laser with wide tunability. Nat Commun. 2017;8:1170.
  • Lomelino CL, Kim JK, Lee C, et al. Carbonic anhydrase II microcrystals suitable for XFEL studies. Acta Crystallogr Sect F Struct Biol Commun. 2018;74:327–330.
  • Ev M, Ay G, Ap L, et al. Successful GPCR structure determination using PAL XFEL. J Bioenerg Biomembr. 2018;50:467–603.
  • Liu W, Wacker D, Gati C, et al. Serial femtosecond crystallography of G protein-coupled receptors. Science. 2014;342:1521–1524.
  • Wang C, Wu H, Evron T, et al. Structural basis for Smoothened receptor modulation and chemoresistance to anticancer drugs. Nat Commun. 2014;5:4355.
  • Fenalti G, Zatsepin NA, Betti C, et al. Structural basis for bifunctional peptide recognition at human δ-opioid receptor. Nat Struct Mol Biol. 2015;22:265–268.
  • Kang Y, Zhou XE, Gao X, et al. Crystal structure of rhodopsin bound to arrestin by femtosecond X-ray laser. Nature. 2015;523:561–567.
  • Zhou XE, He Y, de Waal PW, et al. Identification of phosphorylation codes for arrestin recruitment by G protein-coupled receptors. Cell. 2017;170:457–469.
  • Zhang H, Qiao A, Yang D, et al. Structure of the full-length glucagon class B G-protein-coupled receptor. Nature. 2017;546:259–264.
  • Zhang X, Zhao F, Wu Y, et al. Crystal structure of a multi-domain human smoothened receptor in complex with a super stabilizing ligand. Nat Commun. 2017;8:15383.
  • Zhang H, Unal H, Gati C, et al. Structure of the angiotensin receptor revealed by serial femtosecond crystallography. Cell. 2015;161:833–844.
  • Zhang H, Han GW, Batyuk A, et al. Structural basis for selectivity and diversity in angiotensin II receptors. Nature. 2017;544:327–332.
  • Audet M, White KL, Breton B, et al. Crystal structure of misoprostol bound to the labor inducer prostaglandin E2 receptor. Nat Chem Biol. 2019;15:11–17.
  • Thomaston JL, Woldeyes RA, Nakane T, et al. XFEL structures of the influenza M2 proton channel: room temperature water networks and insights into proton conduction. Proc Natl Acad Sci. 2017;114:13357–13362.
  • O’Sullivan ME, Poitevin F, Sierra RG, et al. Aminoglycoside ribosome interactions reveal novel conformational states at ambient temperature. Nucleic Acids Res. 2018;46:9793–9804.
  • Mathews II, Allison K, Robbins T, et al. Conformational flexibility of the acyltransferase from the disorazole polyketide synthase is revealed by an x-ray free-electron laser using a room-temperature sample delivery method for serial crystallography. Biochemistry. 2017;56:4751–4756.
  • Aquila A, Hunter MS, Doak RB, et al. Time-resolved protein nanocrystallography using an X-ray free-electron laser. Opt Express. 2012;20:2706–2716.
  • Kern J, Tran R, Alonso-Mori R, et al. Taking snapshots of photosynthetic water oxidation using femtosecond X-ray diffraction and spectroscopy. Nat Commun. 2014;5:4371.
  • Barends TRM, Foucar L, Ardevol A, et al. Direct observation of ultrafast collective motions in CO myoglobin upon ligand dissociation. Science. 2015;350:445–450.
  • Pande K, Hutchison CDM, Groenhof G, et al. Femtosecond structural dynamics drives the trans/cis isomerization in photoactive yellow protein. Science. 2016;352:725–729.
  • Kern J, Chatterjee R, Young ID, et al. Structures of the intermediates of Kok’s photosynthetic water oxidation clock. Nature. 2018;563:421–425.
  • Coquelle N, Sliwa M, Woodhouse J, et al. Chromophore twisting in the excited state of a photoswitchable fluorescent protein captured by time-resolved serial femtosecond crystallography. Nat Chem. 2018;10:31–37.
  • Nogly P, Weinert T, James D, et al. Retinal isomerization in bacteriorhodopsin captured by a femtosecond x-ray laser. Science. 2018;361:eaat0094.
  • Tosha T, Nomura T, Nishida T, et al. Capturing an initial intermediate during the P450nor enzymatic reaction using time-resolved XFEL crystallography and caged-substrate. Nat Commun. 2017;8:1585.
  • Olmos JL, Pandey S, Martin-Garcia JM, et al. Enzyme intermediates captured “on the fly” by mix-and-inject serial crystallography. BMC Biol. 2018;16:59.
  • Wiedorn MO, Oberthür D, Bean R, et al. Megahertz serial crystallography. Nat Commun. 2018;9:4025.
  • Kuhlbrandt W. The Resolution Revolution. Science. 2014;343:1443–1444.
  • Martin-Garcia JM, Conrad CE, Coe J, et al. Serial femtosecond crystallography: A revolution in structural biology. Arch Biochem Biophys. 2016;602:32–47.
  • Renaud J-P, Chari A, Ciferri C, et al. Cryo-EM in drug discovery: achievements, limitations and prospects. Nat Rev Drug Discov. 2018;17:471–492.
  • Cheng RKY, Abela R, Hennig M. X-ray free electron laser: opportunities for drug discovery. Essays Biochem. 2017;61:529–542.
  • Spyrakis F, Ahmed MH, Bayden AS, et al. The roles of water in the protein matrix: a largely untapped resource for drug discovery. J Med Chem. 2017;60:6781–6827.
  • Grebner C, Iegre J, Ulander J, et al. Binding mode and induced fit predictions for prospective computational drug design. J Chem Inf Model. 2016;56:774–787.
  • Hauwert NJ, Mocking TAM, Da Costa Pereira D, et al. Synthesis and characterization of a bidirectional photoswitchable antagonist toolbox for real-time GPCR photopharmacology. J Am Chem Soc. 2018;140:4232–4243.
  • Kienzler MA, Isacoff EY. Precise modulation of neuronal activity with synthetic photoswitchable ligands. Curr Opin Neurobiol. 2017;45:202–209.
  • Dilanian RA, Streltsov V, Coughlan HD, et al. Nanocrystallography measurements of early stage synthetic malaria pigment. J Appl Crystallogr. 2017;50:1533–1540.
  • Seuring C, Ayyer K, Filippaki E, et al. Femtosecond X-ray coherent diffraction of aligned amyloid fibrils on low background graphene. Nat Commun. 2018;9:1836.
  • Huang C-F, Liang KS, Hsu T-L, et al. Free-electron-laser coherent diffraction images of individual drug-carrying liposome particles in solution. Nanoscale. 2018;10:2820–2824.
  • Barty A. Single molecule imaging using X-ray free electron lasers. Curr Opin Struct Biol. 2016;40:186–194.
  • MacArthur JP, Lutman AA, Krzywinski J, et al. Microbunch rotation and coherent undulator radiation from a kicked electron beam. Phys Rev X. 2018;8:04036.
  • Feng Y, Alonso-Mori R, Barends TRM, et al. Demonstration of simultaneous experiments using thin crystal multiplexing at the Linac Coherent Light Source. J Synchrotron Radiat. 2015;22:626–633.
  • Boutet S, Foucar L, Barends TRM, et al. Characterization and use of the spent beam for serial operation of LCLS. J Synchrotron Radiat. 2015;22:634–643.
  • Casanas A, Warshamanage R, Finke AD, et al. EIGER detector: application in macromolecular crystallography. Acta Crystallogr Sect D Struct Biol. 2016;72:1036–1048.
  • Graves WS, Berggren KK, Carbajo S, et al. Compact XFEL Light Source. Proc. FEL2013, New York, NY, USA. 2013:757–761.
  • Kartner FX. Terahertz driven linear accelerators and photon sources. 2016 41st Int. Conf. Infrared, Millimeter, Terahertz waves. IEEE; 2016 Sep 25-30; Copenhagen, Denmark.
  • Martin-Garcia JM, Conrad CE, Nelson G, et al. Serial millisecond crystallography of membrane and soluble protein microcrystals using synchrotron radiation. IUCrJ. 2017;4:439–454.
  • Eriksson M, van der Veen JF, Quitmann C. Diffraction-limited storage rings – a window to the science of tomorrow. J Synchrotron Radiat. 2014;21:837–842.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.