Ultrafast Dynamics of a Nucleobase Analogue Illuminated by a Short Intense X-ray Free Electron Laser Pulse
Abstract
Understanding x-ray radiation damage is a crucial issue for both medical applications of x rays and x-ray free-electron-laser (XFEL) science aimed at molecular imaging. Decrypting the charge and fragmentation dynamics of nucleobases, the smallest units of a macro-biomolecule, contributes to a bottom-up understanding of the damage via cascades of phenomena following x-ray exposure. We investigate experimentally and by numerical simulations the ultrafast radiation damage induced on a nucleobase analogue (5-iodouracil) by an ultrashort (10 fs) high-intensity radiation pulse generated by XFEL at SPring-8 Angstrom Compact free electron Laser (SACLA). The present study elucidates a plausible underlying radiosensitizing mechanism of 5-iodouracil. This mechanism is independent of the exact composition of 5-iodouracil and thus relevant to other such radiosensitizers. Furthermore, we found that despite a rapid increase of the net molecular charge in the presence of iodine, and of the ultrafast release of hydrogen, the other atoms are almost frozen within the 10-fs duration of the exposure. Finally, this validates single-shot molecular imaging as a consistent approach, provided the radiation pulse used is brief enough.
- Authors:
- more »
- Publication Date:
- Research Org.:
- Kansas State Univ., Manhattan, KS (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1257647
- Alternate Identifier(s):
- OSTI ID: 1286132
- Grant/Contract Number:
- FG02-86ER1349; FG02-86ER13491
- Resource Type:
- Published Article
- Journal Name:
- Physical Review. X
- Additional Journal Information:
- Journal Name: Physical Review. X Journal Volume: 6 Journal Issue: 2; Journal ID: ISSN 2160-3308
- Publisher:
- American Physical Society
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 73 NUCLEAR PHYSICS AND RADIATION PHYSICS; ionization; charge; molecules; operation; region; atoms
Citation Formats
Nagaya, K., Motomura, K., Kukk, E., Fukuzawa, H., Wada, S., Tachibana, T., Ito, Y., Mondal, S., Sakai, T., Matsunami, K., Koga, R., Ohmura, S., Takahashi, Y., Kanno, M., Rudenko, A., Nicolas, C., Liu, X. -J., Zhang, Y., Chen, J., Anand, M., Jiang, Y. H., Kim, D. -E., Tono, K., Yabashi, M., Kono, H., Miron, C., Yao, M., and Ueda, K. Ultrafast Dynamics of a Nucleobase Analogue Illuminated by a Short Intense X-ray Free Electron Laser Pulse. United States: N. p., 2016.
Web. doi:10.1103/PhysRevX.6.021035.
Nagaya, K., Motomura, K., Kukk, E., Fukuzawa, H., Wada, S., Tachibana, T., Ito, Y., Mondal, S., Sakai, T., Matsunami, K., Koga, R., Ohmura, S., Takahashi, Y., Kanno, M., Rudenko, A., Nicolas, C., Liu, X. -J., Zhang, Y., Chen, J., Anand, M., Jiang, Y. H., Kim, D. -E., Tono, K., Yabashi, M., Kono, H., Miron, C., Yao, M., & Ueda, K. Ultrafast Dynamics of a Nucleobase Analogue Illuminated by a Short Intense X-ray Free Electron Laser Pulse. United States. https://doi.org/10.1103/PhysRevX.6.021035
Nagaya, K., Motomura, K., Kukk, E., Fukuzawa, H., Wada, S., Tachibana, T., Ito, Y., Mondal, S., Sakai, T., Matsunami, K., Koga, R., Ohmura, S., Takahashi, Y., Kanno, M., Rudenko, A., Nicolas, C., Liu, X. -J., Zhang, Y., Chen, J., Anand, M., Jiang, Y. H., Kim, D. -E., Tono, K., Yabashi, M., Kono, H., Miron, C., Yao, M., and Ueda, K. Thu .
"Ultrafast Dynamics of a Nucleobase Analogue Illuminated by a Short Intense X-ray Free Electron Laser Pulse". United States. https://doi.org/10.1103/PhysRevX.6.021035.
@article{osti_1257647,
title = {Ultrafast Dynamics of a Nucleobase Analogue Illuminated by a Short Intense X-ray Free Electron Laser Pulse},
author = {Nagaya, K. and Motomura, K. and Kukk, E. and Fukuzawa, H. and Wada, S. and Tachibana, T. and Ito, Y. and Mondal, S. and Sakai, T. and Matsunami, K. and Koga, R. and Ohmura, S. and Takahashi, Y. and Kanno, M. and Rudenko, A. and Nicolas, C. and Liu, X. -J. and Zhang, Y. and Chen, J. and Anand, M. and Jiang, Y. H. and Kim, D. -E. and Tono, K. and Yabashi, M. and Kono, H. and Miron, C. and Yao, M. and Ueda, K.},
abstractNote = {Understanding x-ray radiation damage is a crucial issue for both medical applications of x rays and x-ray free-electron-laser (XFEL) science aimed at molecular imaging. Decrypting the charge and fragmentation dynamics of nucleobases, the smallest units of a macro-biomolecule, contributes to a bottom-up understanding of the damage via cascades of phenomena following x-ray exposure. We investigate experimentally and by numerical simulations the ultrafast radiation damage induced on a nucleobase analogue (5-iodouracil) by an ultrashort (10 fs) high-intensity radiation pulse generated by XFEL at SPring-8 Angstrom Compact free electron Laser (SACLA). The present study elucidates a plausible underlying radiosensitizing mechanism of 5-iodouracil. This mechanism is independent of the exact composition of 5-iodouracil and thus relevant to other such radiosensitizers. Furthermore, we found that despite a rapid increase of the net molecular charge in the presence of iodine, and of the ultrafast release of hydrogen, the other atoms are almost frozen within the 10-fs duration of the exposure. Finally, this validates single-shot molecular imaging as a consistent approach, provided the radiation pulse used is brief enough.},
doi = {10.1103/PhysRevX.6.021035},
journal = {Physical Review. X},
number = 2,
volume = 6,
place = {United States},
year = {2016},
month = {6}
}
https://doi.org/10.1103/PhysRevX.6.021035
Web of Science
Works referenced in this record:
Single mimivirus particles intercepted and imaged with an X-ray laser
journal, February 2011
- Seibert, M. Marvin; Ekeberg, Tomas; Maia, Filipe R. N. C.
- Nature, Vol. 470, Issue 7332
Monte Carlo calculation of ion, electron, and photon spectra of xenon atoms in x-ray free-electron laser pulses
journal, June 2012
- Son, Sang-Kil; Santra, Robin
- Physical Review A, Vol. 85, Issue 6
The Effect of 5-Halogenated Deoxyuridines on the Frequency of X-Ray-Induced Chromosomal Aberrations in Vicia faba
journal, June 1963
- Kihlman, B. A.
- Hereditas, Vol. 49, Issue 3
Crystal structure of rhodopsin bound to arrestin by femtosecond X-ray laser
journal, July 2015
- Kang, Yanyong; Zhou, X. Edward; Gao, Xiang
- Nature, Vol. 523, Issue 7562
Study on the Structure and Vibrational Dynamics of Functional Molecules and Molecular Clusters by Double Resonance Vibrational Spectroscopy
journal, February 2009
- Ebata, Takayuki
- Bulletin of the Chemical Society of Japan, Vol. 82, Issue 2
Is Coulomb explosion a damaging mechanism for 125 IUdR?
journal, January 2004
- Pomplun, Ekkehard; Sutmann, Godehard
- International Journal of Radiation Biology, Vol. 80, Issue 11-12
Nanoplasma Formation by High Intensity Hard X-rays
journal, June 2015
- Tachibana, T.; Jurek, Z.; Fukuzawa, H.
- Scientific Reports, Vol. 5, Issue 1
Beamline, experimental stations and photon beam diagnostics for the hard x-ray free electron laser of SACLA
journal, August 2013
- Tono, K.; Togashi, T.; Inubushi, Y.
- New Journal of Physics, Vol. 15, Issue 8
Shapes and vorticities of superfluid helium nanodroplets
journal, August 2014
- Gomez, L. F.; Ferguson, K. R.; Cryan, J. P.
- Science, Vol. 345, Issue 6199
Dynamics of Photoelectrons and Structural Changes of Tungsten Trioxide Observed by Femtosecond Transient XAFS
journal, December 2015
- Uemura, Yohei; Kido, Daiki; Wakisaka, Yuki
- Angewandte Chemie International Edition, Vol. 55, Issue 4
Visualizing the non-equilibrium dynamics of photoinduced intramolecular electron transfer with femtosecond X-ray pulses
journal, March 2015
- Canton, Sophie E.; Kjær, Kasper S.; Vankó, György
- Nature Communications, Vol. 6, Issue 1
Charge and Nuclear Dynamics Induced by Deep Inner-Shell Multiphoton Ionization of CH 3 I Molecules by Intense X-ray Free-Electron Laser Pulses
journal, July 2015
- Motomura, Koji; Kukk, Edwin; Fukuzawa, Hironobu
- The Journal of Physical Chemistry Letters, Vol. 6, Issue 15
Single-shot beam-position monitor for x-ray free electron laser
journal, February 2011
- Tono, Kensuke; Kudo, Togo; Yabashi, Makina
- Review of Scientific Instruments, Vol. 82, Issue 2
Fluorinated Pyrimidines, A New Class of Tumour-Inhibitory Compounds
journal, March 1957
- Heidelberger, Charles; Chaudhuri, N. K.; Danneberg, Peter
- Nature, Vol. 179, Issue 4561
Nonlinear Atomic Response to Intense Ultrashort X Rays
journal, February 2011
- Doumy, G.; Roedig, C.; Son, S. -K.
- Physical Review Letters, Vol. 106, Issue 8
Determination of the Pulse Duration of an X-Ray Free Electron Laser Using Highly Resolved Single-Shot Spectra
journal, October 2012
- Inubushi, Yuichi; Tono, Kensuke; Togashi, Tadashi
- Physical Review Letters, Vol. 109, Issue 14
Ultrafast isomerization initiated by X-ray core ionization
journal, September 2015
- Liekhus-Schmaltz, Chelsea E.; Tenney, Ian; Osipov, Timur
- Nature Communications, Vol. 6, Issue 1
Resonant Auger decay driving intermolecular Coulombic decay in molecular dimers
journal, December 2013
- Trinter, F.; Schöffler, M. S.; Kim, H. -K.
- Nature, Vol. 505, Issue 7485
Imaging charge transfer in iodomethane upon x-ray photoabsorption
journal, July 2014
- Erk, B.; Boll, R.; Trippel, S.
- Science, Vol. 345, Issue 6194
Transient lattice contraction in the solid-to-plasma transition
journal, January 2016
- Ferguson, Ken R.; Bucher, Maximilian; Gorkhover, Tais
- Science Advances, Vol. 2, Issue 1
Probing the transition state region in catalytic CO oxidation on Ru
journal, February 2015
- Öström, H.; Öberg, H.; Xin, H.
- Science, Vol. 347, Issue 6225
Potential for biomolecular imaging with femtosecond X-ray pulses
journal, August 2000
- Neutze, Richard; Wouts, Remco; van der Spoel, David
- Nature, Vol. 406, Issue 6797
Ultrafast Charge Rearrangement and Nuclear Dynamics upon Inner-Shell Multiple Ionization of Small Polyatomic Molecules
journal, January 2013
- Erk, B.; Rolles, D.; Foucar, L.
- Physical Review Letters, Vol. 110, Issue 5
Charge build-up during decay of DNA-incorporated 123/125 I: Consequences for labeled molecular structures
journal, March 2012
- Kümmerle, Eberhard A.; Pomplun, Ekkehard
- International Journal of Radiation Biology, Vol. 88, Issue 12
Site- and energy-selective slow-electron production through intermolecular Coulombic decay
journal, December 2013
- Gokhberg, Kirill; Kolorenč, Přemysl; Kuleff, Alexander I.
- Nature, Vol. 505, Issue 7485
Operation of a free-electron laser from the extreme ultraviolet to the water window
journal, June 2007
- Ackermann, W.; Asova, G.; Ayvazyan, V.
- Nature Photonics, Vol. 1, Issue 6
Focusing of X-ray free-electron laser pulses with reflective optics
journal, December 2012
- Yumoto, Hirokatsu; Mimura, Hidekazu; Koyama, Takahisa
- Nature Photonics, Vol. 7, Issue 1
A compact X-ray free-electron laser emitting in the sub-ångström region
journal, June 2012
- Ishikawa, Tetsuya; Aoyagi, Hideki; Asaka, Takao
- Nature Photonics, Vol. 6, Issue 8
Nanoplasma Dynamics of Single Large Xenon Clusters Irradiated with Superintense X-Ray Pulses from the Linac Coherent Light Source Free-Electron Laser
journal, June 2012
- Gorkhover, T.; Adolph, M.; Rupp, D.
- Physical Review Letters, Vol. 108, Issue 24
Deep Inner-Shell Multiphoton Ionization by Intense X-Ray Free-Electron Laser Pulses
journal, April 2013
- Fukuzawa, H.; Son, S. -K.; Motomura, K.
- Physical Review Letters, Vol. 110, Issue 17
Ultra-efficient ionization of heavy atoms by intense X-ray free-electron laser pulses
journal, November 2012
- Rudek, Benedikt; Son, Sang-Kil; Foucar, Lutz
- Nature Photonics, Vol. 6, Issue 12
First lasing and operation of an ångstrom-wavelength free-electron laser
journal, August 2010
- Emma, P.; Akre, R.; Arthur, J.
- Nature Photonics, Vol. 4, Issue 9
General atomic and molecular electronic structure system
journal, November 1993
- Schmidt, Michael W.; Baldridge, Kim K.; Boatz, Jerry A.
- Journal of Computational Chemistry, Vol. 14, Issue 11, p. 1347-1363
Multiple hit readout of a microchannel plate detector with a three-layer delay-line anode
journal, October 2002
- Jagutzki, O.; Cerezo, A.; Czasch, A.
- IEEE Transactions on Nuclear Science, Vol. 49, Issue 5
Direct observation of bond formation in solution with femtosecond X-ray scattering
journal, February 2015
- Kim, Kyung Hwan; Kim, Jong Goo; Nozawa, Shunsuke
- Nature, Vol. 518, Issue 7539
Femtosecond electronic response of atoms to ultra-intense X-rays
journal, July 2010
- Young, L.; Kanter, E. P.; Krässig, B.
- Nature, Vol. 466, Issue 7302
The role of metal ions in X-ray-induced photochemistry
journal, January 2016
- Stumpf, V.; Gokhberg, K.; Cederbaum, L. S.
- Nature Chemistry, Vol. 8, Issue 3
Electron spectroscopy of rare-gas clusters irradiated by x-ray free-electron laser pulses from SACLA
journal, January 2016
- Fukuzawa, H.; Tachibana, T.; Motomura, K.
- Journal of Physics B: Atomic, Molecular and Optical Physics, Vol. 49, Issue 3
Pulse energy measurement at the hard x-ray laser in Japan
journal, July 2012
- Kato, M.; Tanaka, T.; Kurosawa, T.
- Applied Physics Letters, Vol. 101, Issue 2
Auger processes in the 21st century
journal, January 2008
- Howell, Roger W.
- International Journal of Radiation Biology, Vol. 84, Issue 12
Nonlinear lattice dynamics as a basis for enhanced superconductivity in YBa2Cu3O6.5
journal, December 2014
- Mankowsky, R.; Subedi, A.; Först, M.
- Nature, Vol. 516, Issue 7529
Orbital-specific mapping of the ligand exchange dynamics of Fe(CO)5 in solution
journal, April 2015
- Wernet, Ph.; Kunnus, K.; Josefsson, I.
- Nature, Vol. 520, Issue 7545
A time-dependent order parameter for ultrafast photoinduced phase transitions
journal, August 2014
- Beaud, P.; Caviezel, A.; Mariager, S. O.
- Nature Materials, Vol. 13, Issue 10
Macromolecular diffractive imaging using imperfect crystals
text, January 2016
- Ayyer, Kartik; Yefanov, Oleksandr; Oberthür, Dominik
- Deutsches Elektronen-Synchrotron, DESY, Hamburg
Direct observation of ultrafast collective motions in CO myoglobin upon ligand dissociation
journal, September 2015
- Barends, T. R. M.; Foucar, L.; Ardevol, A.
- Science, Vol. 350, Issue 6259
Imaging live cell in micro-liquid enclosure by X-ray laser diffraction
journal, January 2014
- Kimura, Takashi; Joti, Yasumasa; Shibuya, Akemi
- Nature Communications, Vol. 5, Issue 1
Macromolecular diffractive imaging using imperfect crystals
journal, February 2016
- Ayyer, Kartik; Yefanov, Oleksandr M.; Oberthür, Dominik
- Nature, Vol. 530, Issue 7589, p. 202-206
Nonlinear Atomic Response to Intense Ultrashort X Rays
journal, February 2011
- Doumy, G.; Roedig, C.; Son, S. -K.
- Physical Review Letters, Vol. 106, Issue 8
Deep Inner-Shell Multiphoton Ionization by Intense X-Ray Free-Electron Laser Pulses
journal, April 2013
- Fukuzawa, H.; Son, S. -K.; Motomura, K.
- Physical Review Letters, Vol. 110, Issue 17
Nanoplasma Dynamics of Single Large Xenon Clusters Irradiated with Superintense X-Ray Pulses from the Linac Coherent Light Source Free-Electron Laser
journal, June 2012
- Gorkhover, T.; Adolph, M.; Rupp, D.
- Physical Review Letters, Vol. 108, Issue 24
Ultrafast Charge Rearrangement and Nuclear Dynamics upon Inner-Shell Multiple Ionization of Small Polyatomic Molecules
journal, January 2013
- Erk, B.; Rolles, D.; Foucar, L.
- Physical Review Letters, Vol. 110, Issue 5
Multiple hit readout of a microchannel plate detector with a three-layer delay-line anode
journal, October 2002
- Jagutzki, O.; Cerezo, A.; Czasch, A.
- IEEE Transactions on Nuclear Science, Vol. 49, Issue 5
Monte Carlo calculation of ion, electron, and photon spectra of xenon atoms in x-ray free-electron laser pulses
journal, June 2012
- Son, Sang-Kil; Santra, Robin
- Physical Review A, Vol. 85, Issue 6
Determination of the Pulse Duration of an X-Ray Free Electron Laser Using Highly Resolved Single-Shot Spectra
journal, October 2012
- Inubushi, Yuichi; Tono, Kensuke; Togashi, Tadashi
- Physical Review Letters, Vol. 109, Issue 14
Works referencing / citing this record:
Capturing the photo-induced dynamics of nano-molecules by X-ray free electron laser induced Coulomb explosion
journal, September 2019
- Yamazaki, Kaoru; Niitsu, Naoyuki; Kanno, Manabu
- The Journal of Chemical Physics, Vol. 151, Issue 12
Roadmap of ultrafast x-ray atomic and molecular physics
journal, January 2018
- Young, Linda; Ueda, Kiyoshi; Gühr, Markus
- Journal of Physics B: Atomic, Molecular and Optical Physics, Vol. 51, Issue 3
Radiation-Induced Chemical Dynamics in Ar Clusters Exposed to Strong X-Ray Pulses
journal, May 2018
- Kumagai, Yoshiaki; Jurek, Zoltan; Xu, Weiqing
- Physical Review Letters, Vol. 120, Issue 22
An efficient approximate algorithm for nonadiabatic molecular dynamics
journal, December 2018
- Hanasaki, Kota; Kanno, Manabu; Niehaus, Thomas A.
- The Journal of Chemical Physics, Vol. 149, Issue 24
Time-resolved electron spectroscopy for chemical analysis of photodissociation: Photoelectron spectra of Fe(CO) 5 , Fe(CO) 4 , and Fe(CO) 3
journal, July 2018
- Leitner, T.; Josefsson, I.; Mazza, T.
- The Journal of Chemical Physics, Vol. 149, Issue 4
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
Fragmentation dynamics of nitrogen trifluoride induced by electron collision
journal, October 2019
- Wang, Enliang; Shan, Xu; Shen, Zhenjie
- The Journal of Chemical Physics, Vol. 151, Issue 13
Stimulated resonant inelastic x-ray scattering with chirped, broadband pulses
text, January 2019
- Hollstein, Maximilian; Rohringer, Nina
- Deutsches Elektronen-Synchrotron, DESY, Hamburg