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Lipidic cubic phase injector is a viable crystal delivery system for time-resolved serial crystallography.

Nogly P, Panneels V, Nelson G, Gati C, Kimura T, Milne C, Milathianaki D, Kubo M, Wu W, Conrad C, Coe J, Bean R, Zhao Y, Båth P, Dods R, Harimoorthy R, Beyerlein KR, Rheinberger J, James D, DePonte D, Li C, Sala L, Williams GJ, Hunter MS, Koglin JE, Berntsen P, Nango E, Iwata S, Chapman HN, Fromme P, Frank M, Abela R, Boutet S, Barty A, White TA, Weierstall U, Spence J, Neutze R, Schertler G, Standfuss J
Nat Commun 7 12314 (2016)
Related entries: 4x31, 4x32

Cited: 27 times
EuropePMC logo PMID: 27545823

Abstract

Serial femtosecond crystallography (SFX) using X-ray free-electron laser sources is an emerging method with considerable potential for time-resolved pump-probe experiments. Here we present a lipidic cubic phase SFX structure of the light-driven proton pump bacteriorhodopsin (bR) to 2.3 Å resolution and a method to investigate protein dynamics with modest sample requirement. Time-resolved SFX (TR-SFX) with a pump-probe delay of 1 ms yields difference Fourier maps compatible with the dark to M state transition of bR. Importantly, the method is very sample efficient and reduces sample consumption to about 1 mg per collected time point. Accumulation of M intermediate within the crystal lattice is confirmed by time-resolved visible absorption spectroscopy. This study provides an important step towards characterizing the complete photocycle dynamics of retinal proteins and demonstrates the feasibility of a sample efficient viscous medium jet for TR-SFX.

Articles - 5j7a mentioned but not cited (1)

  1. Lipidic cubic phase injector is a viable crystal delivery system for time-resolved serial crystallography. Nogly P, Panneels V, Nelson G, Gati C, Kimura T, Milne C, Milathianaki D, Kubo M, Wu W, Conrad C, Coe J, Bean R, Zhao Y, Båth P, Dods R, Harimoorthy R, Beyerlein KR, Rheinberger J, James D, DePonte D, Li C, Sala L, Williams GJ, Hunter MS, Koglin JE, Berntsen P, Nango E, Iwata S, Chapman HN, Fromme P, Frank M, Abela R, Boutet S, Barty A, White TA, Weierstall U, Spence J, Neutze R, Schertler G, Standfuss J. Nat Commun 7 12314 (2016)


Reviews citing this publication (4)

  1. A Bright Future for Serial Femtosecond Crystallography with XFELs. Johansson LC, Stauch B, Ishchenko A, Cherezov V. Trends Biochem Sci 42 749-762 (2017)
  2. Bacteriorhodopsin: Structural Insights Revealed Using X-Ray Lasers and Synchrotron Radiation. Wickstrand C, Nogly P, Nango E, Iwata S, Standfuss J, Neutze R. Annu Rev Biochem 88 59-83 (2019)
  3. The complementarity of serial femtosecond crystallography and MicroED for structure determination from microcrystals. Zatsepin NA, Li C, Colasurd P, Nannenga BL. Curr Opin Struct Biol 58 286-293 (2019)
  4. Dynamic Structural Biology Experiments at XFEL or Synchrotron Sources. Aller P, Orville AM. Methods Mol Biol 2305 203-228 (2021)

Articles citing this publication (22)

  1. A three-dimensional movie of structural changes in bacteriorhodopsin. Nango E, Royant A, Kubo M, Nakane T, Wickstrand C, Kimura T, Tanaka T, Tono K, Song C, Tanaka R, Arima T, Yamashita A, Kobayashi J, Hosaka T, Mizohata E, Nogly P, Sugahara M, Nam D, Nomura T, Shimamura T, Im D, Fujiwara T, Yamanaka Y, Jeon B, Nishizawa T, Oda K, Fukuda M, Andersson R, Båth P, Dods R, Davidsson J, Matsuoka S, Kawatake S, Murata M, Nureki O, Owada S, Kameshima T, Hatsui T, Joti Y, Schertler G, Yabashi M, Bondar AN, Standfuss J, Neutze R, Iwata S. Science 354 1552-1557 (2016)
  2. Retinal isomerization in bacteriorhodopsin captured by a femtosecond x-ray laser. Nogly P, Weinert T, James D, Carbajo S, Ozerov D, Furrer A, Gashi D, Borin V, Skopintsev P, Jaeger K, Nass K, Båth P, Bosman R, Koglin J, Seaberg M, Lane T, Kekilli D, Brünle S, Tanaka T, Wu W, Milne C, White T, Barty A, Weierstall U, Panneels V, Nango E, Iwata S, Hunter M, Schapiro I, Schertler G, Neutze R, Standfuss J. Science 361 eaat0094 (2018)
  3. Serial millisecond crystallography for routine room-temperature structure determination at synchrotrons. Weinert T, Olieric N, Cheng R, Brünle S, James D, Ozerov D, Gashi D, Vera L, Marsh M, Jaeger K, Dworkowski F, Panepucci E, Basu S, Skopintsev P, Doré AS, Geng T, Cooke RM, Liang M, Prota AE, Panneels V, Nogly P, Ermler U, Schertler G, Hennig M, Steinmetz MO, Wang M, Standfuss J. Nat Commun 8 542 (2017)
  4. Hydroxyethyl cellulose matrix applied to serial crystallography. Sugahara M, Nakane T, Masuda T, Suzuki M, Inoue S, Song C, Tanaka R, Nakatsu T, Mizohata E, Yumoto F, Tono K, Joti Y, Kameshima T, Hatsui T, Yabashi M, Nureki O, Numata K, Nango E, Iwata S. Sci Rep 7 703 (2017)
  5. Capturing an initial intermediate during the P450nor enzymatic reaction using time-resolved XFEL crystallography and caged-substrate. Tosha T, Nomura T, Nishida T, Saeki N, Okubayashi K, Yamagiwa R, Sugahara M, Nakane T, Yamashita K, Hirata K, Ueno G, Kimura T, Hisano T, Muramoto K, Sawai H, Takeda H, Mizohata E, Yamashita A, Kanematsu Y, Takano Y, Nango E, Tanaka R, Nureki O, Shoji O, Ikemoto Y, Murakami H, Owada S, Tono K, Yabashi M, Yamamoto M, Ago H, Iwata S, Sugimoto H, Shiro Y, Kubo M. Nat Commun 8 1585 (2017)
  6. Photoswitching mechanism of a fluorescent protein revealed by time-resolved crystallography and transient absorption spectroscopy. Woodhouse J, Nass Kovacs G, Coquelle N, Uriarte LM, Adam V, Barends TRM, Byrdin M, de la Mora E, Bruce Doak R, Feliks M, Field M, Fieschi F, Guillon V, Jakobs S, Joti Y, Macheboeuf P, Motomura K, Nass K, Owada S, Roome CM, Ruckebusch C, Schirò G, Shoeman RL, Thepaut M, Togashi T, Tono K, Yabashi M, Cammarata M, Foucar L, Bourgeois D, Sliwa M, Colletier JP, Schlichting I, Weik M. Nat Commun 11 741 (2020)
  7. On-chip crystallization for serial crystallography experiments and on-chip ligand-binding studies. Lieske J, Cerv M, Kreida S, Komadina D, Fischer J, Barthelmess M, Fischer P, Pakendorf T, Yefanov O, Mariani V, Seine T, Ross BH, Crosas E, Lorbeer O, Burkhardt A, Lane TJ, Guenther S, Bergtholdt J, Schoen S, Törnroth-Horsefield S, Chapman HN, Meents A. IUCrJ 6 714-728 (2019)
  8. Short-wavelength free-electron laser sources and science: a review. Seddon EA, Clarke JA, Dunning DJ, Masciovecchio C, Milne CJ, Parmigiani F, Rugg D, Spence JCH, Thompson NR, Ueda K, Vinko SM, Wark JS, Wurth W. Rep Prog Phys 80 115901 (2017)
  9. a-ARM: Automatic Rhodopsin Modeling with Chromophore Cavity Generation, Ionization State Selection, and External Counterion Placement. Pedraza-González L, De Vico L, Marı N MADC, Fanelli F, Olivucci M. J Chem Theory Comput 15 3134-3152 (2019)
  10. Perspective: Opportunities for ultrafast science at SwissFEL. Abela R, Beaud P, van Bokhoven JA, Chergui M, Feurer T, Haase J, Ingold G, Johnson SL, Knopp G, Lemke H, Milne CJ, Pedrini B, Radi P, Schertler G, Standfuss J, Staub U, Patthey L. Struct Dyn 4 061602 (2017)
  11. 3D printed devices and infrastructure for liquid sample delivery at the European XFEL. Vakili M, Bielecki J, Knoška J, Otte F, Han H, Kloos M, Schubert R, Delmas E, Mills G, de Wijn R, Letrun R, Dold S, Bean R, Round A, Kim Y, Lima FA, Dörner K, Valerio J, Heymann M, Mancuso AP, Schulz J. J Synchrotron Radiat 29 331-346 (2022)
  12. Orientation of non-spherical protonated water clusters revealed by infrared absorption dichroism. Daldrop JO, Saita M, Heyden M, Lorenz-Fonfria VA, Heberle J, Netz RR. Nat Commun 9 311 (2018)
  13. The role of water molecules in phototransduction of retinal proteins and G protein-coupled receptors. Lesca E, Panneels V, Schertler GFX. Faraday Discuss 207 27-37 (2018)
  14. Temperature dependence of protein-water interactions in a gated yeast aquaporin. Aponte-Santamaría C, Fischer G, Båth P, Neutze R, de Groot BL. Sci Rep 7 4016 (2017)
  15. Time-resolved x-ray crystallography capture of a slow reaction tetrahydrofolate intermediate. Cao H, Skolnick J. Struct Dyn 6 024701 (2019)
  16. X-ray transparent microfluidic chips for high-throughput screening and optimization of in meso membrane protein crystallization. Schieferstein JM, Pawate AS, Sun C, Wan F, Sheraden PN, Broecker J, Ernst OP, Gennis RB, Kenis PJA. Biomicrofluidics 11 024118 (2017)
  17. Crystal structure of CmABCB1 multi-drug exporter in lipidic mesophase revealed by LCP-SFX. Pan D, Oyama R, Sato T, Nakane T, Mizunuma R, Matsuoka K, Joti Y, Tono K, Nango E, Iwata S, Nakatsu T, Kato H. IUCrJ 9 134-145 (2022)
  18. High-throughput in situ experimental phasing. Lawrence JM, Orlans J, Evans G, Orville AM, Foadi J, Aller P. Acta Crystallogr D Struct Biol 76 790-801 (2020)
  19. Correction of rhodopsin serial crystallography diffraction intensities for a lattice-translocation defect. Rodrigues MJ, Casadei CM, Weinert T, Panneels V, Schertler GFX. Acta Crystallogr D Struct Biol 79 224-233 (2023)
  20. Observations of phase changes in monoolein during high viscous injection. Wells DJ, Berntsen P, Balaur E, Kewish CM, Adams P, Aquila A, Binns J, Boutet S, Broomhall H, Caleman C, Christofferson A, Conn CE, Dahlqvist C, Flueckiger L, Gian Roque F, Greaves TL, Hejazian M, Hunter M, Hadian Jazi M, Jönsson HO, Pathirannahalage SK, Kirian RA, Kozlov A, Kurta RP, Marman H, Mendez D, Morgan A, Nugent K, Oberthuer D, Quiney H, Reinhardt J, Saha S, Sellberg JA, Sierra R, Wiedorn M, Abbey B, Martin AV, Darmanin C. J Synchrotron Radiat 29 602-614 (2022)
  21. A multi-reservoir extruder for time-resolved serial protein crystallography and compound screening at X-ray free-electron lasers. Wranik M, Kepa MW, Beale EV, James D, Bertrand Q, Weinert T, Furrer A, Glover H, Gashi D, Carrillo M, Kondo Y, Stipp RT, Khusainov G, Nass K, Ozerov D, Cirelli C, Johnson PJM, Dworkowski F, Beale JH, Stubbs S, Zamofing T, Schneider M, Krauskopf K, Gao L, Thorn-Seshold O, Bostedt C, Bacellar C, Steinmetz MO, Milne C, Standfuss J. Nat Commun 14 7956 (2023)
  22. A versatile approach to high-density microcrystals in lipidic cubic phase for room-temperature serial crystallography. Birch J, Kwan TOC, Judge PJ, Axford D, Aller P, Butryn A, Reis RI, Bada Juarez JF, Vinals J, Owen RL, Nango E, Tanaka R, Tono K, Joti Y, Tanaka T, Owada S, Sugahara M, Iwata S, Orville AM, Watts A, Moraes I. J Appl Crystallogr 56 1361-1370 (2023)


Related citations provided by authors (1)

  1. Lipidic cubic phase serial millisecond crystallography using synchrotron radiation.. Nogly P, James D, Wang D, White TA, Zatsepin N, Shilova A, Nelson G, Liu H, Johansson L, Heymann M, Jaeger K, Metz M, Wickstrand C, Wu W, Båth P, Berntsen P, Oberthuer D, Panneels V, Cherezov V, Chapman H, Schertler G, Neutze R, Spence J, Moraes I, Burghammer M, Standfuss J, Weierstall U IUCrJ 2 168-76 (2015)

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