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Title: Structural enzymology using X-ray free electron lasers

Abstract

Mix-and-inject serial crystallography (MISC) is a technique designed to image enzyme catalyzed reactions in which small protein crystals are mixed with a substrate just prior to being probed by an X-ray pulse. This approach offers several advantages over flow cell studies. It provides (i) room temperature structures at near atomic resolution, (ii) time resolution ranging from microseconds to seconds, and (iii) convenient reaction initiation. It outruns radiation damage by using femtosecond X-ray pulses allowing damage and chemistry to be separated. Here, we demonstrate that MISC is feasible at an X-ray free electron laser by studying the reaction of M. tuberculosis ß-lactamase microcrystals with ceftriaxone antibiotic solution. Electron density maps of the apo-ß-lactamase and of the ceftriaxone bound form were obtained at 2.8 Å and 2.4 Å resolution, respectively. Finally, these results pave the way to study cyclic and non-cyclic reactions and represent a new field of time-resolved structural dynamics for numerous substrate-triggered biological reactions.

Authors:
 [1];  [2];  [3];  [4];  [5];  [1];  [5];  [6];  [6];  [6];  [1];  [7];  [7];  [7];  [8];  [8];  [9];  [5];  [1];  [1] more »;  [10];  [2];  [2];  [8];  [8];  [8];  [11];  [11];  [11];  [11];  [11];  [11];  [11];  [11];  [12];  [8];  [8];  [8];  [8];  [5];  [3];  [3];  [3];  [3];  [1];  [7];  [11];  [1];  [2];  [1] « less
+ Show Author Affiliations
  1. Univ. of Wisconsin, Milwaukee, WI (United States). Dept. of Physics
  2. Rice Univ., Houston, TX (United States). Dept. of BioSciences
  3. Arizona State Univ., Tempe, AZ (United States). Dept. of Physics
  4. Marbles Inc., Westfield, IN (United States)
  5. Deutsches Elektronen-Synchrotron (DESY), Hamburg (Germany). Center for Free-Electron Laser Science; Univ. of Hamburg (Germany)
  6. SLAC National Accelerator Lab., Menlo Park, CA (United States). Linac Coherent Light Source (LCLS)
  7. Cornell Univ., Ithaca, NY (United States). Dept. of Applied and Engineering Physics
  8. Deutsches Elektronen-Synchrotron (DESY), Hamburg (Germany). Center for Free-Electron Laser Science
  9. Univ. of Hamburg (Germany)
  10. State Univ. of New York (SUNY), Buffalo, NY (United States). Hauptman-Woodward Inst.
  11. Arizona State Univ., Tempe, AZ (United States). School of Molecular Sciences and Biodesign Center for Applied Structural Discovery
  12. Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
Publication Date:
Research Org.:
Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States); SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH); National Science Foundation (NSF)
OSTI Identifier:
1395301
Alternate Identifier(s):
OSTI ID: 1369303; OSTI ID: 2229580
Report Number(s):
LLNL-JRNL-857682
Journal ID: ISSN 2329-7778; SDTYAE
Grant/Contract Number:  
AC52-07NA27344; AC02-76SF00515
Resource Type:
Accepted Manuscript
Journal Name:
Structural Dynamics
Additional Journal Information:
Journal Volume: 4; Journal Issue: 4; Journal ID: ISSN 2329-7778
Publisher:
American Crystallographic Association/AIP
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 59 BASIC BIOLOGICAL SCIENCES; Crystal structure; Electron densities of states; Enzymes; Enzyme kinetics; Biochemical reactions; crystal structure; electron densities of states; enzymes; enzyme kinetics; biochemical reactions

Citation Formats

Kupitz, Christopher, Olmos, Jose L., Holl, Mark, Tremblay, Lee, Pande, Kanupriya, Pandey, Suraj, Oberthür, Dominik, Hunter, Mark, Liang, Mengning, Aquila, Andrew, Tenboer, Jason, Calvey, George, Katz, Andrea, Chen, Yujie, Wiedorn, Max O., Knoska, Juraj, Meents, Alke, Majriani, Valerio, Norwood, Tyler, Poudyal, Ishwor, Grant, Thomas, Miller, Mitchell D., Xu, Weijun, Tolstikova, Aleksandra, Morgan, Andrew, Metz, Markus, Martin-Garcia, Jose M., Zook, James D., Roy-Chowdhury, Shatabdi, Coe, Jesse, Nagaratnam, Nirupa, Meza, Domingo, Fromme, Raimund, Basu, Shibom, Frank, Matthias, White, Thomas, Barty, Anton, Bajt, Sasa, Yefanov, Oleksandr, Chapman, Henry N., Zatsepin, Nadia, Nelson, Garrett, Weierstall, Uwe, Spence, John, Schwander, Peter, Pollack, Lois, Fromme, Petra, Ourmazd, Abbas, Phillips, George N., and Schmidt, Marius. Structural enzymology using X-ray free electron lasers. United States: N. p., 2016. Web. doi:10.1063/1.4972069.
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Kupitz, Christopher, Olmos, Jose L., Holl, Mark, Tremblay, Lee, Pande, Kanupriya, Pandey, Suraj, Oberthür, Dominik, Hunter, Mark, Liang, Mengning, Aquila, Andrew, Tenboer, Jason, Calvey, George, Katz, Andrea, Chen, Yujie, Wiedorn, Max O., Knoska, Juraj, Meents, Alke, Majriani, Valerio, Norwood, Tyler, Poudyal, Ishwor, Grant, Thomas, Miller, Mitchell D., Xu, Weijun, Tolstikova, Aleksandra, Morgan, Andrew, Metz, Markus, Martin-Garcia, Jose M., Zook, James D., Roy-Chowdhury, Shatabdi, Coe, Jesse, Nagaratnam, Nirupa, Meza, Domingo, Fromme, Raimund, Basu, Shibom, Frank, Matthias, White, Thomas, Barty, Anton, Bajt, Sasa, Yefanov, Oleksandr, Chapman, Henry N., Zatsepin, Nadia, Nelson, Garrett, Weierstall, Uwe, Spence, John, Schwander, Peter, Pollack, Lois, Fromme, Petra, Ourmazd, Abbas, Phillips, George N., & Schmidt, Marius. Structural enzymology using X-ray free electron lasers. United States. https://doi.org/10.1063/1.4972069
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Kupitz, Christopher, Olmos, Jose L., Holl, Mark, Tremblay, Lee, Pande, Kanupriya, Pandey, Suraj, Oberthür, Dominik, Hunter, Mark, Liang, Mengning, Aquila, Andrew, Tenboer, Jason, Calvey, George, Katz, Andrea, Chen, Yujie, Wiedorn, Max O., Knoska, Juraj, Meents, Alke, Majriani, Valerio, Norwood, Tyler, Poudyal, Ishwor, Grant, Thomas, Miller, Mitchell D., Xu, Weijun, Tolstikova, Aleksandra, Morgan, Andrew, Metz, Markus, Martin-Garcia, Jose M., Zook, James D., Roy-Chowdhury, Shatabdi, Coe, Jesse, Nagaratnam, Nirupa, Meza, Domingo, Fromme, Raimund, Basu, Shibom, Frank, Matthias, White, Thomas, Barty, Anton, Bajt, Sasa, Yefanov, Oleksandr, Chapman, Henry N., Zatsepin, Nadia, Nelson, Garrett, Weierstall, Uwe, Spence, John, Schwander, Peter, Pollack, Lois, Fromme, Petra, Ourmazd, Abbas, Phillips, George N., and Schmidt, Marius. Thu . "Structural enzymology using X-ray free electron lasers". United States. https://doi.org/10.1063/1.4972069. https://www.osti.gov/servlets/purl/1395301.
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@article{osti_1395301,
title = {Structural enzymology using X-ray free electron lasers},
author = {Kupitz, Christopher and Olmos, Jose L. and Holl, Mark and Tremblay, Lee and Pande, Kanupriya and Pandey, Suraj and Oberthür, Dominik and Hunter, Mark and Liang, Mengning and Aquila, Andrew and Tenboer, Jason and Calvey, George and Katz, Andrea and Chen, Yujie and Wiedorn, Max O. and Knoska, Juraj and Meents, Alke and Majriani, Valerio and Norwood, Tyler and Poudyal, Ishwor and Grant, Thomas and Miller, Mitchell D. and Xu, Weijun and Tolstikova, Aleksandra and Morgan, Andrew and Metz, Markus and Martin-Garcia, Jose M. and Zook, James D. and Roy-Chowdhury, Shatabdi and Coe, Jesse and Nagaratnam, Nirupa and Meza, Domingo and Fromme, Raimund and Basu, Shibom and Frank, Matthias and White, Thomas and Barty, Anton and Bajt, Sasa and Yefanov, Oleksandr and Chapman, Henry N. and Zatsepin, Nadia and Nelson, Garrett and Weierstall, Uwe and Spence, John and Schwander, Peter and Pollack, Lois and Fromme, Petra and Ourmazd, Abbas and Phillips, George N. and Schmidt, Marius},
abstractNote = {Mix-and-inject serial crystallography (MISC) is a technique designed to image enzyme catalyzed reactions in which small protein crystals are mixed with a substrate just prior to being probed by an X-ray pulse. This approach offers several advantages over flow cell studies. It provides (i) room temperature structures at near atomic resolution, (ii) time resolution ranging from microseconds to seconds, and (iii) convenient reaction initiation. It outruns radiation damage by using femtosecond X-ray pulses allowing damage and chemistry to be separated. Here, we demonstrate that MISC is feasible at an X-ray free electron laser by studying the reaction of M. tuberculosis ß-lactamase microcrystals with ceftriaxone antibiotic solution. Electron density maps of the apo-ß-lactamase and of the ceftriaxone bound form were obtained at 2.8 Å and 2.4 Å resolution, respectively. Finally, these results pave the way to study cyclic and non-cyclic reactions and represent a new field of time-resolved structural dynamics for numerous substrate-triggered biological reactions.},
doi = {10.1063/1.4972069},
journal = {Structural Dynamics},
number = 4,
volume = 4,
place = {United States},
year = {Thu Dec 15 00:00:00 EST 2016},
month = {Thu Dec 15 00:00:00 EST 2016}
}
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https://doi.org/10.1063/1.4972069
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Figures / Tables:

FIG. 1 FIG. 1: Data collection schematic showing the T-junction set-up used for a mixing time of about 2 s. The T-junction was placed outside of the nozzle rod in our experiment but could also be engineered to fit inside closer to the interaction region for shorter mixing times.
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    Rapid Sample Delivery for Megahertz Serial Crystallography at X-ray FELs
    text, January 2018

    • Wiedorn, Max O.; Awel, Salah; Morgan, Andrew J.
    • Deutsches Elektronen-Synchrotron, DESY, Hamburg
    • DOI: 10.3204/pubdb-2018-02209

    Short-wavelength free-electron laser sources and science: a review
    text, January 2017

    • Seddon, E. A.; Clarke, J. A.; Dunning, D. J.
    • Deutsches Elektronen-Synchrotron, DESY, Hamburg
    • DOI: 10.3204/pubdb-2018-00596

    Ultracompact 3D microfluidics for time-resolved structural biology
    journal, January 2020

    Molecular dynamics simulations of macromolecular crystals
    journal, November 2018

    • Cerutti, David S.; Case, David A.
    • Wiley Interdisciplinary Reviews: Computational Molecular Science, Vol. 9, Issue 4
    • DOI: 10.1002/wcms.1402

    Mix-and-inject XFEL crystallography reveals gated conformational dynamics during enzyme catalysis
    journal, December 2019

    • Dasgupta, Medhanjali; Budday, Dominik; de Oliveira, Saulo H. P.
    • Proceedings of the National Academy of Sciences, Vol. 116, Issue 51
    • DOI: 10.1073/pnas.1901864116

    Time-resolved serial femtosecond crystallography at the European XFEL
    journal, November 2019

    Ultracompact 3D microfluidics for time-resolved structural biology
    journal, January 2020

    Membrane protein megahertz crystallography at the European XFEL
    text, January 2019

    • Gisriel, Chris; Coe, Jesse; Letrun, Romain
    • Deutsches Elektronen-Synchrotron, DESY, Hamburg
    • DOI: 10.3204/pubdb-2019-03909

    Rapid sample delivery for megahertz serial crystallography at X-ray FELs
    journal, July 2018

    Ultracompact 3D microfluidics for time-resolved structural biology
    text, January 2020

    • Knoška, Juraj; Adriano, Luigi; Awel, Salah
    • Deutsches Elektronen-Synchrotron, DESY, Hamburg
    • DOI: 10.3204/pubdb-2020-00687
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