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A multi-reservoir extruder for time-resolved serial protein crystallography and compound screening at X-ray free-electron lasers

Author

Listed:
  • Maximilian Wranik

    (Division of Biology and Chemistry, Paul Scherrer Institut, Villigen-PSI)

  • Michal W. Kepa

    (Division of Biology and Chemistry, Paul Scherrer Institut, Villigen-PSI)

  • Emma V. Beale

    (Photon Science Division, Paul Scherrer Institut, Villigen-PSI)

  • Daniel James

    (Division of Biology and Chemistry, Paul Scherrer Institut, Villigen-PSI)

  • Quentin Bertrand

    (Division of Biology and Chemistry, Paul Scherrer Institut, Villigen-PSI)

  • Tobias Weinert

    (Division of Biology and Chemistry, Paul Scherrer Institut, Villigen-PSI)

  • Antonia Furrer

    (Division of Biology and Chemistry, Paul Scherrer Institut, Villigen-PSI)

  • Hannah Glover

    (Division of Biology and Chemistry, Paul Scherrer Institut, Villigen-PSI)

  • Dardan Gashi

    (Photon Science Division, Paul Scherrer Institut, Villigen-PSI)

  • Melissa Carrillo

    (Photon Science Division, Paul Scherrer Institut, Villigen-PSI)

  • Yasushi Kondo

    (Division of Biology and Chemistry, Paul Scherrer Institut, Villigen-PSI)

  • Robin T. Stipp

    (Division of Biology and Chemistry, Paul Scherrer Institut, Villigen-PSI)

  • Georgii Khusainov

    (Division of Biology and Chemistry, Paul Scherrer Institut, Villigen-PSI)

  • Karol Nass

    (Photon Science Division, Paul Scherrer Institut, Villigen-PSI)

  • Dmitry Ozerov

    (Theory and Data Division, Paul Scherrer Institut, Villigen-PSI)

  • Claudio Cirelli

    (Photon Science Division, Paul Scherrer Institut, Villigen-PSI)

  • Philip J. M. Johnson

    (Photon Science Division, Paul Scherrer Institut, Villigen-PSI)

  • Florian Dworkowski

    (Photon Science Division, Paul Scherrer Institut, Villigen-PSI)

  • John H. Beale

    (Photon Science Division, Paul Scherrer Institut, Villigen-PSI)

  • Scott Stubbs

    (Paul Scherrer Institut, Villigen-PSI)

  • Thierry Zamofing

    (Paul Scherrer Institut, Villigen-PSI)

  • Marco Schneider

    (Paul Scherrer Institut, Villigen-PSI)

  • Kristina Krauskopf

    (Ludwig-Maximilians University of Munich)

  • Li Gao

    (Ludwig-Maximilians University of Munich)

  • Oliver Thorn-Seshold

    (Ludwig-Maximilians University of Munich)

  • Christoph Bostedt

    (Photon Science Division, Paul Scherrer Institut, Villigen-PSI
    Institute of Chemical Sciences and Engineering, École Polytechnique Fédérale de Lausanne (EPFL))

  • Camila Bacellar

    (Photon Science Division, Paul Scherrer Institut, Villigen-PSI)

  • Michel O. Steinmetz

    (Division of Biology and Chemistry, Paul Scherrer Institut, Villigen-PSI
    University of Basel)

  • Christopher Milne

    (Femtosecond X-ray Experiments Instrument, European XFEL GmbH)

  • Jörg Standfuss

    (Division of Biology and Chemistry, Paul Scherrer Institut, Villigen-PSI)

Abstract

Serial crystallography at X-ray free-electron lasers (XFELs) permits the determination of radiation-damage free static as well as time-resolved protein structures at room temperature. Efficient sample delivery is a key factor for such experiments. Here, we describe a multi-reservoir, high viscosity extruder as a step towards automation of sample delivery at XFELs. Compared to a standard single extruder, sample exchange time was halved and the workload of users was greatly reduced. In-built temperature control of samples facilitated optimal extrusion and supported sample stability. After commissioning the device with lysozyme crystals, we collected time-resolved data using crystals of a membrane-bound, light-driven sodium pump. Static data were also collected from the soluble protein tubulin that was soaked with a series of small molecule drugs. Using these data, we identify low occupancy (as little as 30%) ligands using a minimal amount of data from a serial crystallography experiment, a result that could be exploited for structure-based drug design.

Suggested Citation

  • Maximilian Wranik & Michal W. Kepa & Emma V. Beale & Daniel James & Quentin Bertrand & Tobias Weinert & Antonia Furrer & Hannah Glover & Dardan Gashi & Melissa Carrillo & Yasushi Kondo & Robin T. Stip, 2023. "A multi-reservoir extruder for time-resolved serial protein crystallography and compound screening at X-ray free-electron lasers," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43523-5
    DOI: 10.1038/s41467-023-43523-5
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    References listed on IDEAS

    as
    1. Przemyslaw Nogly & Valerie Panneels & Garrett Nelson & Cornelius Gati & Tetsunari Kimura & Christopher Milne & Despina Milathianaki & Minoru Kubo & Wenting Wu & Chelsie Conrad & Jesse Coe & Richard Be, 2016. "Lipidic cubic phase injector is a viable crystal delivery system for time-resolved serial crystallography," Nature Communications, Nature, vol. 7(1), pages 1-9, November.
    2. Tobias Weinert & Natacha Olieric & Robert Cheng & Steffen Brünle & Daniel James & Dmitry Ozerov & Dardan Gashi & Laura Vera & May Marsh & Kathrin Jaeger & Florian Dworkowski & Ezequiel Panepucci & Shi, 2017. "Serial millisecond crystallography for routine room-temperature structure determination at synchrotrons," Nature Communications, Nature, vol. 8(1), pages 1-11, December.
    3. John Jumper & Richard Evans & Alexander Pritzel & Tim Green & Michael Figurnov & Olaf Ronneberger & Kathryn Tunyasuvunakool & Russ Bates & Augustin Žídek & Anna Potapenko & Alex Bridgland & Clemens Me, 2021. "Highly accurate protein structure prediction with AlphaFold," Nature, Nature, vol. 596(7873), pages 583-589, August.
    4. Henry N. Chapman & Petra Fromme & Anton Barty & Thomas A. White & Richard A. Kirian & Andrew Aquila & Mark S. Hunter & Joachim Schulz & Daniel P. DePonte & Uwe Weierstall & R. Bruce Doak & Filipe R. N, 2011. "Femtosecond X-ray protein nanocrystallography," Nature, Nature, vol. 470(7332), pages 73-77, February.
    5. Karol Nass & Alexander Gorel & Malik M. Abdullah & Andrew V. Martin & Marco Kloos & Agostino Marinelli & Andrew Aquila & Thomas R. M. Barends & Franz-Josef Decker & R. Bruce Doak & Lutz Foucar & Elisa, 2020. "Structural dynamics in proteins induced by and probed with X-ray free-electron laser pulses," Nature Communications, Nature, vol. 11(1), pages 1-9, December.
    6. Maximilian Wranik & Tobias Weinert & Chavdar Slavov & Tiziana Masini & Antonia Furrer & Natacha Gaillard & Dario Gioia & Marco Ferrarotti & Daniel James & Hannah Glover & Melissa Carrillo & Demet Keki, 2023. "Watching the release of a photopharmacological drug from tubulin using time-resolved serial crystallography," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    7. Richard Neutze & Remco Wouts & David van der Spoel & Edgar Weckert & Janos Hajdu, 2000. "Potential for biomolecular imaging with femtosecond X-ray pulses," Nature, Nature, vol. 406(6797), pages 752-757, August.
    8. Uwe Weierstall & Daniel James & Chong Wang & Thomas A. White & Dingjie Wang & Wei Liu & John C. H. Spence & R. Bruce Doak & Garrett Nelson & Petra Fromme & Raimund Fromme & Ingo Grotjohann & Christoph, 2014. "Lipidic cubic phase injector facilitates membrane protein serial femtosecond crystallography," Nature Communications, Nature, vol. 5(1), pages 1-6, May.
    9. Petr Skopintsev & David Ehrenberg & Tobias Weinert & Daniel James & Rajiv K. Kar & Philip J. M. Johnson & Dmitry Ozerov & Antonia Furrer & Isabelle Martiel & Florian Dworkowski & Karol Nass & Gregor K, 2020. "Femtosecond-to-millisecond structural changes in a light-driven sodium pump," Nature, Nature, vol. 583(7815), pages 314-318, July.
    10. Thomas R. M. Barends & Lutz Foucar & Sabine Botha & R. Bruce Doak & Robert L. Shoeman & Karol Nass & Jason E. Koglin & Garth J. Williams & Sébastien Boutet & Marc Messerschmidt & Ilme Schlichting, 2014. "De novo protein crystal structure determination from X-ray free-electron laser data," Nature, Nature, vol. 505(7482), pages 244-247, January.
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