Low energy secondary electron induced damage of condensed nucleotides

McKee, A. D.; Schaible, M. J.; Rosenberg, R. A.; Kundu, S.; Orlando, Thomas M.

doi:10.1063/1.5090491

Low energy secondary electron induced damage of condensed nucleotides

Journal Article · Tue May 28 00:00:00 EDT 2019 · Journal of Chemical Physics

DOI:https://doi.org/10.1063/1.5090491· OSTI ID:1559940

^[1]; Schaible, M. J. ^[1]; Rosenberg, R. A. ^[2]; Kundu, S. ^[1]; ^[1]

Georgia Inst. of Technology, Atlanta, GA (United States)
Argonne National Lab. (ANL), Lemont, IL (United States)

Radiation damage and stimulated desorption of nucleotides 2'-deoxyadenosine 5'-monophosphate (dAMP), adenosine 5'-monophosphate (rAMP), 2'-deoxycytidine 5'-monophosphate (dCMP), and cytidine 5'-monophosphate (rCMP) deposited on Au have been measured using x-rays as both the probe and source of low energy secondary electrons. The fluence dependent behavior of the O-1s, C-1s, and N-1s photoelectron transitions was analyzed to obtain phosphate, sugar, and nucleobase damage cross sections. Although x-ray induced reactions in nucleotides involve both direct ionization and excitation, the observed bonding changes were likely dominated by the inelastic energy-loss channels associated with secondary electron capture and transient negative ion decay. Growth of the integrated peak area for the O-1s component at 531.3 eV, corresponding to cleavage of the C—O—P phosphodiester bond, yielded effective damage cross sections of about 23 Mb and 32 Mb (1 Mb = 10^–18 cm²) for AMP and CMP molecules, respectively. The cross sections for sugar damage, as determined from the decay of the C-1s component at 286.4 eV and the glycosidic carbon at 289.0 eV, were slightly lower (about 20 Mb) and statistically similar for the r- and d- forms of the nucleotides. Here, the C-1s component at 287.6 eV, corresponding to carbons in the nucleobase ring, showed a small initial increase and then decayed slowly, yielding a low damage cross section (~5 Mb). Although there is no statistical difference between the sugar forms, changing the nucleobase from adenine to cytidine has a slight effect on the damage cross section, possibly due to differing electron capture and transfer probabilities.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Lab. (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1559940

Alternate ID(s):: OSTI ID: 1523698

Journal Information:: Journal of Chemical Physics, Journal Name: Journal of Chemical Physics Journal Issue: 20 Vol. 150; ISSN 0021-9606

Publisher:: American Institute of Physics (AIP)Copyright Statement

Country of Publication:: United States

Language:: English

References (62)

Low‐Energy Electron‐Induced Strand Breaks in Telomere‐Derived DNA Sequences—Influence of DNA Sequence and Topology Rackwitz, Jenny; Bald, Ilko Chemistry – A European Journal, Vol. 24, Issue 18 https://doi.org/10.1002/chem.201705889	journal	February 2018
How Do Low-Energy (0.1—2 eV) Electrons Cause DNA-Strand Breaks? Simons, Jack ChemInform, Vol. 38, Issue 1 https://doi.org/10.1002/chin.200701262	journal	January 2007
Low-Energy Electron Transmission Through Thin-Film Molecular and Biomolecular Solids Naaman, R.; Sanche, L. ChemInform, Vol. 38, Issue 31 https://doi.org/10.1002/chin.200731257	journal	July 2007
Quantitative analysis of saccharides by X-ray photoelectron spectroscopy Stevens, Joanna S.; Schroeder, Sven L. M. Surface and Interface Analysis, Vol. 41, Issue 6 https://doi.org/10.1002/sia.3047	journal	June 2009
Quantitative analysis of complex amino acids and RGD peptides by X-ray photoelectron spectroscopy (XPS): Quantitative XPS analysis of amino acids and RGD peptides Stevens, Joanna S.; de Luca, Alba C.; Pelendritis, Michalis Surface and Interface Analysis, Vol. 45, Issue 8 https://doi.org/10.1002/sia.5261	journal	April 2013
Electron stopping power and inelastic mean free path in amino acids and protein over the energy range of 20–20,000 eV Tan, Zhenyu; Xia, Yueyuan; Zhao, Mingwen Radiation and Environmental Biophysics, Vol. 45, Issue 2 https://doi.org/10.1007/s00411-006-0049-0	journal	May 2006
Adsorption of carbonyl compounds on clean and modified Cu(110) surfaces: A combined eels-ups study Prabhakaran, K.; Rao, C. N. R. Applied Surface Science, Vol. 44, Issue 3 https://doi.org/10.1016/0169-4332(90)90051-z	journal	May 1990
The interaction of a protein–DNA surface complex with low-energy electrons Solomun, T.; Skalický, T. Chemical Physics Letters, Vol. 453, Issue 1-3 https://doi.org/10.1016/j.cplett.2007.12.078	journal	February 2008
Probing low-energy electron induced DNA damage using single photon ionization mass spectrometry Chen, Yanfeng; Aleksandrov, Alexandr; Orlando, Thomas M. International Journal of Mass Spectrometry, Vol. 277, Issue 1-3 https://doi.org/10.1016/j.ijms.2008.07.003	journal	November 2008
Spur energy distributions in liquid water using a generalized oscillator strength from inelastic X-ray scattering measurements Karamitros, Mathieu; Mozumder, Asokendu Radiation Physics and Chemistry, Vol. 141 https://doi.org/10.1016/j.radphyschem.2016.11.014	journal	December 2017
The measurement of molecular fragments from DNA components using synchrotron radiation Fujii, K.; Akamatsu, K.; Yokoya, A. Surface Science, Vol. 528, Issue 1-3 https://doi.org/10.1016/s0039-6028(02)02640-7	journal	March 2003
Image Contrast in Energy-Filtered BSE Images at Ultra-Low Accelerating Voltages Hashimoto, Yoichiro; Muto, Atsushi; Woods, Eric Microscopy Today, Vol. 24, Issue 3 https://doi.org/10.1017/s1551929516000390	journal	April 2016
Energy Thresholds of DNA Damage Induced by UV Radiation: An XPS Study Gomes, P. J.; Ferraria, A. M.; Botelho do Rego, A. M. The Journal of Physical Chemistry B, Vol. 119, Issue 17 https://doi.org/10.1021/acs.jpcb.5b01439	journal	April 2015
Electron Attachment to Microhydrated Deoxycytidine Monophosphate Kočišek, Jaroslav; Sedmidubská, Barbora; Indrajith, Suvasthika The Journal of Physical Chemistry B, Vol. 122, Issue 20 https://doi.org/10.1021/acs.jpcb.8b03033	journal	April 2018
Unified Mechanism for the Generation of Isolated and Clustered DNA Damages by a Single Low Energy (5–10 eV) Electron Shao, Yu; Dong, Yanfang; Hunting, Darel The Journal of Physical Chemistry C, Vol. 121, Issue 4 https://doi.org/10.1021/acs.jpcc.6b12110	journal	January 2017
Understanding the Interaction between Low-Energy Electrons and DNA Nucleotides in Aqueous Solution McAllister, Maeve; Smyth, Maeve; Gu, Bin The Journal of Physical Chemistry Letters, Vol. 6, Issue 15 https://doi.org/10.1021/acs.jpclett.5b01011	journal	July 2015
How Do Low-Energy (0.1−2 eV) Electrons Cause DNA-Strand Breaks? Simons, Jack Accounts of Chemical Research, Vol. 39, Issue 10 https://doi.org/10.1021/ar0680769	journal	October 2006
Low-Energy Electron Transmission through Thin-Film Molecular and Biomolecular Solids Naaman, R.; Sanche, L. Chemical Reviews, Vol. 107, Issue 5 https://doi.org/10.1021/cr040200j	journal	May 2007
Precursors of Solvated Electrons in Radiobiological Physics and Chemistry Alizadeh, Elahe; Sanche, Léon Chemical Reviews, Vol. 112, Issue 11 https://doi.org/10.1021/cr300063r	journal	June 2012
Low-energy (0-10 eV) electron transmission spectra of multilayer tryptophan films Leclerc, G.; Goulet, T.; Cloutier, P. The Journal of Physical Chemistry, Vol. 91, Issue 19 https://doi.org/10.1021/j100303a020	journal	September 1987
Single, Double, and Multiple Double Strand Breaks Induced in DNA by 3−100 eV Electrons Huels, Michael A.; Boudaïffa, Badia; Cloutier, Pierre Journal of the American Chemical Society, Vol. 125, Issue 15 https://doi.org/10.1021/ja029527x	journal	April 2003
Damage to Model DNA Fragments from Very Low-Energy (<1 eV) Electrons Berdys, Joanna; Anusiewicz, Iwona; Skurski, Piotr Journal of the American Chemical Society, Vol. 126, Issue 20 https://doi.org/10.1021/ja049876m	journal	May 2004
Chemical Basis of DNA Sugar−Phosphate Cleavage by Low-Energy Electrons Zheng, Yi; Cloutier, Pierre; Hunting, Darel J. Journal of the American Chemical Society, Vol. 127, Issue 47 https://doi.org/10.1021/ja054129q	journal	November 2005
On the Effect of Low-Energy Electron Induced DNA Strand Break in Aqueous Solution: A Theoretical Study Indicating Guanine as a Weak Link in DNA Schyman, Patric; Laaksonen, Aatto Journal of the American Chemical Society, Vol. 130, Issue 37 https://doi.org/10.1021/ja805000g	journal	September 2008
Low-Energy Electron-Induced DNA Damage: Effect of Base Sequence in Oligonucleotide Trimers Li, Zejun; Cloutier, Pierre; Sanche, Léon Journal of the American Chemical Society, Vol. 132, Issue 15 https://doi.org/10.1021/ja9099505	journal	April 2010
Electron-Stimulated Desorption of H ^- from Condensed-Phase Deoxyribose Analogues: Dissociative Electron Attachment versus Resonance Decay into Dipolar Dissociation Antic, D.; Parenteau, L.; Sanche, L. The Journal of Physical Chemistry B, Vol. 104, Issue 19 https://doi.org/10.1021/jp000206m	journal	May 2000
Mechanism for Damage to DNA by Low-Energy Electrons ^† Barrios, Robyn; Skurski, Piotr; Simons, Jack The Journal of Physical Chemistry B, Vol. 106, Issue 33 https://doi.org/10.1021/jp013861i	journal	August 2002
Bringing Electrons and Microarray Technology Together Solomun, T.; Sturm, H. The Journal of Physical Chemistry B, Vol. 111, Issue 36 https://doi.org/10.1021/jp075338v	journal	September 2007
Electronic Structure of Genomic DNA: A Photoemission and X-ray Absorption Study Kummer, Kurt; Vyalikh, Denis V.; Gavrila, Gianina The Journal of Physical Chemistry B, Vol. 114, Issue 29 https://doi.org/10.1021/jp1013237	journal	July 2010
Soft X-ray and Low Energy Electron-Induced Damage to DNA under N ₂ and O ₂ Atmospheres Alizadeh, Elahe; Cloutier, Pierre; Hunting, Darel The Journal of Physical Chemistry B, Vol. 115, Issue 15 https://doi.org/10.1021/jp200947g	journal	April 2011
Cleavage Enhancement of Specific Chemical Bonds in DNA by Cisplatin Radiosensitization Xiao, Fangxing; Luo, Xinglan; Fu, Xianzhi The Journal of Physical Chemistry B, Vol. 117, Issue 17 https://doi.org/10.1021/jp400852p	journal	April 2013
Side-by-Side Comparison of DNA Damage Induced by Low-Energy Electrons and High-Energy Photons with Solid TpTpT Trinucleotide Park, Yeunsoo; Peoples, Anita R.; Madugundu, Guru S. The Journal of Physical Chemistry B, Vol. 117, Issue 35 https://doi.org/10.1021/jp405397m	journal	August 2013
Interaction of Self-Assembled Monolayers of DNA with Electrons: HREELS and XPS Studies Vilar, Manuel Rei; Botelho do Rego, Ana M.; Ferraria, Ana M. The Journal of Physical Chemistry B, Vol. 112, Issue 23 https://doi.org/10.1021/jp8008207	journal	June 2008
Thermal Stability and Reducibility of Oxygen-Containing Functional Groups on Multiwalled Carbon Nanotube Surfaces: A Quantitative High-Resolution XPS and TPD/TPR Study Kundu, Shankhamala; Wang, Yuemin; Xia, Wei The Journal of Physical Chemistry C, Vol. 112, Issue 43 https://doi.org/10.1021/jp804413a	journal	October 2008
Damage Induced to DNA by Low-Energy (0−30 eV) Electrons under Vacuum and Atmospheric Conditions Brun, Émilie; Cloutier, Pierre; Sicard-Roselli, Cécile The Journal of Physical Chemistry B, Vol. 113, Issue 29 https://doi.org/10.1021/jp902540k	journal	July 2009
Sequence dependence of electron-induced DNA strand breakage revealed by DNA nanoarrays Keller, Adrian; Rackwitz, Jenny; Cauët, Emilie Scientific Reports, Vol. 4, Issue 1 https://doi.org/10.1038/srep07391	journal	December 2014
Damage to amino acid–nucleotide pairs induced by 1 eV electrons Ptasińska, Sylwia; Li, Zejun; Mason, Nigel J. Physical Chemistry Chemical Physics, Vol. 12, Issue 32 https://doi.org/10.1039/b926267a	journal	January 2010
Low energy electron attachment to the nucleotide deoxycytidine monophosphate: direct evidence for the molecular mechanisms of electron-induced DNA strand breaks Kopyra, Janina Physical Chemistry Chemical Physics, Vol. 14, Issue 23 https://doi.org/10.1039/c2cp40847c	journal	January 2012
The relationship between interfacial bonding and radiation damage in adsorbed DNA Rosenberg, R. A.; Symonds, J. M.; Vijayalakshmi, K. Phys. Chem. Chem. Phys., Vol. 16, Issue 29 https://doi.org/10.1039/c4cp01649a	journal	January 2014
Inelastic electron interaction (attachment/ionization) with deoxyribose Ptasińska, S.; Denifl, S.; Scheier, P. The Journal of Chemical Physics, Vol. 120, Issue 18 https://doi.org/10.1063/1.1690231	journal	May 2004
On the mechanism of anion desorption from DNA induced by low energy electrons Ptasińska, Sylwia; Sanche, Léon The Journal of Chemical Physics, Vol. 125, Issue 14 https://doi.org/10.1063/1.2338320	journal	October 2006
Low-energy electron diffraction and induced damage in hydrated DNA Orlando, Thomas M.; Oh, Doogie; Chen, Yanfeng The Journal of Chemical Physics, Vol. 128, Issue 19 https://doi.org/10.1063/1.2907722	journal	May 2008
X-ray induced damage in DNA monitored by X-ray photoelectron spectroscopy Ptasińska, Sylwia; Stypczyńska, Agnieszka; Nixon, Tony The Journal of Chemical Physics, Vol. 129, Issue 6 https://doi.org/10.1063/1.2961027	journal	August 2008
Lack of proportionality of total electron yield and soft x-ray absorption coefficient Henneken, H.; Scholze, F.; Ulm, G. Journal of Applied Physics, Vol. 87, Issue 1 https://doi.org/10.1063/1.371854	journal	January 2000
Resonant dissociation of DNA bases by subionization electrons Huels, Michael A.; Hahndorf, Ina; Illenberger, Eugen The Journal of Chemical Physics, Vol. 108, Issue 4 https://doi.org/10.1063/1.475503	journal	January 1998
Adenine adlayers on Cu(111): XPS and NEXAFS study Tsud, Nataliya; Bercha, Sofiia; Ševčíková, Klára The Journal of Chemical Physics, Vol. 143, Issue 17 https://doi.org/10.1063/1.4935055	journal	November 2015
Secondary electron energy distributions for gold as excited by C K _α (277 eV) and Al K _α (1487 eV) x rays Henke, Burton L.; Smith, Jerel A.; Attwood, David T. Applied Physics Letters, Vol. 29, Issue 9 https://doi.org/10.1063/1.89176	journal	November 1976
Damage of DNA by Low Energy Electrons (< 3 eV) Bald, Ilko; Illenberger, Eugen; Kopyra, Janina Journal of Physics: Conference Series, Vol. 373 https://doi.org/10.1088/1742-6596/373/1/012008	journal	July 2012
Detection of energy-selected secondary electrons in coincidence with energy-loss events in thin carbon foils Pijper, Folbert J.; Kruit, Pieter Physical Review B, Vol. 44, Issue 17 https://doi.org/10.1103/physrevb.44.9192	journal	November 1991
High-Resolution X-Ray Photoemission Spectrum of the Valence Bands of Gold Shirley, D. A. Physical Review B, Vol. 5, Issue 12 https://doi.org/10.1103/physrevb.5.4709	journal	June 1972
Dissociative electron attachment to hydrated single DNA strands Ptasińska, Sylwia; Sanche, Léon Physical Review E, Vol. 75, Issue 3 https://doi.org/10.1103/physreve.75.031915	journal	March 2007
Absolute cross section for low-energy-electron damage to condensed macromolecules: A case study of DNA Rezaee, Mohammad; Cloutier, Pierre; Bass, Andrew D. Physical Review E, Vol. 86, Issue 3 https://doi.org/10.1103/physreve.86.031913	journal	September 2012
Mechanism and Site of Attack for Direct Damage to DNA by Low-Energy Electrons Pan, X.; Sanche, L. Physical Review Letters, Vol. 94, Issue 19 https://doi.org/10.1103/physrevlett.94.198104	journal	May 2005
DNA Damage Induced by Low-Energy Electrons: Electron Transfer and Diffraction Zheng, Yi; Wagner, J. Richard; Sanche, Léon Physical Review Letters, Vol. 96, Issue 20 https://doi.org/10.1103/physrevlett.96.208101	journal	May 2006
Resonant Formation of DNA Strand Breaks by Low-Energy (3 to 20 eV) Electrons Boudaïffa, B. Science, Vol. 287, Issue 5458 https://doi.org/10.1126/science.287.5458.1658	journal	March 2000
Low energy electron-driven damage in biomolecules Sanche, L. The European Physical Journal D, Vol. 35, Issue 2 https://doi.org/10.1140/epjd/e2005-00206-6	journal	August 2005
Transport of secondary electrons through coatings of ion-irradiated metallic nanoparticles Haume, Kaspar; de Vera, Pablo; Verkhovtsev, Alexey The European Physical Journal D, Vol. 72, Issue 6 https://doi.org/10.1140/epjd/e2018-90050-x	journal	June 2018
Biomolecular Damage Induced by Ionizing Radiation: The Direct and Indirect Effects of Low-Energy Electrons on DNA Alizadeh, Elahe; Orlando, Thomas M.; Sanche, Léon Annual Review of Physical Chemistry, Vol. 66, Issue 1 https://doi.org/10.1146/annurev-physchem-040513-103605	journal	April 2015
DNA Damage Induced by Low-Energy Electrons: Conversion of Thymine to 5,6-Dihydrothymine in the Oligonucleotide Trimer TpTpT Park, Yeunsoo; Li, Zejun; Cloutier, Pierre Radiation Research, Vol. 175, Issue 2 https://doi.org/10.1667/rr2381.1	journal	February 2011
Halogen Anion Formation in 5-Halouracil Films: X Rays Compared to Subionization Electrons Klyachko, Dimitri V.; Huels, Michael A.; Sanche, Léon Radiation Research, Vol. 151, Issue 2 https://doi.org/10.2307/3579768	journal	February 1999
Measurement of inelastic cross sections for low-energy electron scattering from DNA bases Michaud, Marc; Bazin, Marc; Sanche, Le´on International Journal of Radiation Biology, Vol. 88, Issue 1-2 https://doi.org/10.3109/09553002.2011.577505	journal	May 2011
Transport of secondary electrons through coatings of ion-irradiated metallic nanoparticles Haume, Kaspar; de Vera, Pablo; Verkhovtsev, Alexey arXiv https://doi.org/10.48550/arxiv.1801.06894	text	January 2018

Cited By (2)

Clustered DNA Damages induced by 0.5 to 30 eV Electrons Zheng, Yi; Sanche, Léon International Journal of Molecular Sciences, Vol. 20, Issue 15 https://doi.org/10.3390/ijms20153749	journal	July 2019
Electron scattering from tin tetrachloride (SnCl ₄ ) molecules Możejko, Paweł; Stefanowska-Tur, Sylwia; Ptasińska-Denga, Elżbieta The Journal of Chemical Physics, Vol. 151, Issue 6 https://doi.org/10.1063/1.5116307	journal	August 2019

Similar Records

Vacuum ultraviolet photoionization of carbohydrates and nucleotides

Journal Article · Mon Jan 27 23:00:00 EST 2014 · Journal of Chemical Physics · OSTI ID:22255181

Controlling DNA fragmentation in MALDI-MS by chemical modification

Journal Article · Fri Jan 31 23:00:00 EST 1997 · Analytical Chemistry (Washington) · OSTI ID:501935

Nitrogen K-edge x-ray absorption near edge structure of pyrimidine-containing nucleotides in aqueous solution

Journal Article · Thu May 07 00:00:00 EDT 2015 · Journal of Chemical Physics · OSTI ID:22415755

Related Subjects

74 ATOMIC AND MOLECULAR PHYSICS
XPS
electrons
nucleotides
radiation damage

Low energy secondary electron induced damage of condensed nucleotides

Citation Formats

References (62)

Cited By (2)

Similar Records

Related Subjects