• This record comes from PubMed

Breaking the DNA by soft X-rays in the water window reveals the scavenging and temporal behaviour of ·OH radicals

. 2024 Nov 18 ; 14 (1) : 28515. [epub] 20241118

Language English Country Great Britain, England Media electronic

Document type Journal Article

Grant support
L100102051 Akademie Věd České Republiky
RVO: 61389005 Akademie Věd České Republiky
PPI/PRO/2019/1/00001/U/00001 Narodowa Agencja Wymiany Akademickiej
871124 Laserlab-Europe
LM2023068 Ministerstvo Školství, Mládeže a Tělovýchovy

Links

PubMed 39557928
PubMed Central PMC11574138
DOI 10.1038/s41598-024-79328-9
PII: 10.1038/s41598-024-79328-9
Knihovny.cz E-resources

A laser-plasma source emitting photons with energies in the water window spectral range has been used to reveal the radiation chemical yields of single-strand breaks in plasmid DNA as a function of ·OH radical scavenger concentration. Direct and indirect effects were investigated separately using DNA samples with various levels of hydration. We experimentally determined the value of the efficiency factor for strand cleavage in DNA caused by the reaction with ·OH radicals at 0.11, which was previously found in the theoretical studies. Additionally, the radiation chemical yield of ·OH radicals specific to the water window radiation emission of the source was determined by comparison with the gamma radiation-induced strand break yields. The ·OH radical yield determined using the plasmid DNA samples as a model was similar to the yield found using sensitive fluorescent dosimeters in previous experiments.

See more in PubMed

Hieda, K. DNA damage induced by vacuum and soft X-ray photons from synchrotron radiation. Int. J. Radiat. Biol.66, 561–567. 10.1080/09553009414551631 (1994). PubMed

Hieda, K., Suzuki, K., Hirono, T., Suzuki, M. & Furusawa, Y. Single- and double-strand breaks in pBR322 DNA by vacuum-UV from 8.3 to 20.7eV. J. Radiat. Res.35, 104–111. 10.1269/jrr.35.104 (1994). PubMed

Hieda, K., Hirono, T. & Azami, A. Single- and double-strand breaks in pBR322 plasmid DNA by monochromatic X-rays on and off the K-absorption peak of phosphorus. Int. J. Radiat. Biol.70, 437–445. 10.1080/095530096144914 (1996). PubMed

Yokoya, A., Watanabe, R. & Hara, T. Single- and double-strand breaks in solid pBR322 DNA induced by ultrasoft X-rays at photon energies of 388, 435 and 573 eV. J. Radiat. Res.40, 145–158. 10.1269/jrr.40.145 (1999). PubMed

Prise, M. et al. Critical energies for SSB and DSB induction in plasmid DNA by low-energy photons: Action spectra for strand-break induction in plasmid DNA irradiated in vacuum. Int. J. Radiat. Biol.76, 881–890. 10.1080/09553000050050891 (2000). PubMed

Yokoya, A., Cunniffe, S. M. T., Watanabe, R., Kobayashi, K. & O’Neill, P. Induction of DNA strand breaks, base lesions and clustered damage sites in hydrated plasmid DNA films by ultrasoft X-rays around the phosphorus K-edge. Radiat. Res.172, 296–305. 10.1667/RR1609.1 (2009). PubMed

Meesungnoen, J., Jay-Gerin, J., Filali-Mouhim, A. & Mankhetkorn, S. Low-energy electron penetration range in liquid Water. Radiat. Res.158, 657–660. 10.1667/0033-7587(2002)158[0657:LEEPRI]2.0.CO;2 (2002). PubMed

Pimblott, S. M. & LaVerne, J. A. Production of low-energy electrons by ionizing radiation. Radiat. Phys. Chem.76, 1244–1247. 10.1016/j.radphyschem.2007.02.012 (2007).

Favaudon, V. et al. Ultrahigh dose-rate FLASH irradiation increases the differential response between normal and tumor tissue in mice. Sci. Transl. Med.6, 10.1126/scitranslmed.3008973 (2014). PubMed

Kusumoto, T., Kitamura, H., Hojo, S., Konishi, T. & Kodaira, S. Significant changes in yields of 7-hydroxy-coumarin-3-carboxylic acid produced under FLASH radiotherapy conditions. RSC Adv.10, 38709–38714. 10.1039/D0RA07999E (2020). PubMed PMC

Kusumoto, T. et al. Radiation Chemical yields of 7-hydroxy-coumarin-3-carboxylic acid for proton- and carbon-ion beams at ultra-high dose rates: Potential roles in FLASH effects. Radiat. Res.198, 10.1667/RADE-21-00.230.1 (2022). PubMed

Blain, G. et al. Proton irradiations at ultra-high dose rate vs. conventional dose rate: Strong impact on hydrogen peroxide yield. Radiat. Res.198, 10.1667/RADE-22-00021.1 (2022). PubMed

Montay-Gruel, P. et al. Long-term neurocognitive benefits of FLASH radiotherapy driven by reduced reactive oxygen species. Proc. Natl. Acad. Sci.116, 10943–10951. 10.1073/pnas.1901777116 (2019). PubMed PMC

Labarbe, R., Hotoiu, L., Barbier, J. & Favaudon, V. A physicochemical model of reaction kinetics supports peroxyl radical recombination as the main determinant of the FLASH effect. Radiother. Oncol.153, 303–310. 10.1016/j.radonc.2020.06.001 (2020). PubMed

Alanazi, A., Meesungnoen, J. & Jay-Gerin, J.-P. A computer modeling study of water radiolysis at high dose rates. Relevance to FLASH radiotherapy. Radiat. Res.195, 10.1667/RADE-20-00168.1 (2020). PubMed

Kusumoto, T. et al. Dose rate effects on hydrated electrons, hydrogen peroxide, and a OH radical molecular probe under clinical energy protons. Radiat. Res.201, 10.1667/RADE-23-00244.1 (2024). PubMed

Wolter, H. Spiegelsysteme streifenden Einfalls als abbildende Optiken für Röntgenstrahlen. Annalen der Physik445, 94–114. 10.1002/andp.19524450108 (1952).

Wachulak, P. et al. “Water window’’ compact, table-top laser plasma soft X-ray sources based on a gas puff target. Nucl. Instrum. Methods Phys. Res. Sect. B Beam Interact. Mater. Atoms268, 1692–1700. 10.1016/j.nimb.2010.02.002 (2010).

Davídková, M. et al. A high-power laser-driven source of sub-nanosecond soft X-ray pulses for single-shot radiobiology experiments. Radiat. Res.168, 382–387. 10.1667/RR0676.1 (2007). PubMed

Zielbauer, B. et al. Strand breaks in DNA samples induced with LASERIX. In X-Ray Lasers 2008, Proceedings (eds. Lewis, C. L. S. & Riley, D.), vol. 130, 409–411, 10.1007/978-1-4020-9924-3_47 (Springer, 2009).

Ayele, M. et al. Development and characterization of a laser-plasma soft X-ray source for contact microscopy. Nucl. Instrum. Methods Phys. Res. Sect. B Beam Interact. Mater. Atoms411, 35–43. 10.1016/j.nimb.2017.03.082 (2017).

Vyšín, L. et al. Chemical dosimetry in the “Water Window’’: Ferric ions and hydroxyl radicals produced by intense soft X-rays. Radiat. Res.193, 372. 10.1667/RR15520.1 (2020). PubMed

Hicks, M. & Gebicki, J. M. Rate constants for reaction of hydroxyl radicals with Tris, Tricine and Hepes buffers. FEBS Lett.199, 92–94. 10.1016/0014-5793(86)81230-3 (1986).

Buxton, G. V., Greenstock, C. L., Helman, W. P. & Ross, A. B. Critical review of rate constants for reactions of hydrated electrons, hydrogen atoms and hydroxyl radicals (·OH/·O - in aqueous solution). J. Phys. Chem. Ref. Data17, 513–886. 10.1063/1.555805 (1988).

Jomova, K. et al. Reactive oxygen species, toxicity, oxidative stress, and antioxidants: Chronic diseases and aging. Arch. Toxicol.97, 2499–2574. 10.1007/s00204-023-03562-9 (2023). PubMed PMC

Tullius, T. D. & Greenbaum, J. A. Mapping nucleic acid structure by hydroxyl radical cleavage. Curr. Opin. Chem. Biol.9, 127–134. 10.1016/j.cbpa.2005.02.009 (2005). PubMed

Halliwell, B. & Gutteridge, J. M. C. Free Radicals in Biology and Medicine (Oxford University Press, 2015).

Cheng, F.-C., Jen, J.-F. & Tsai, T.-H. Hydroxyl radical in living systems and its separation methods. J. Chromatogr. B781, 481–496. 10.1016/S1570-0232(02)00620-7 (2002). PubMed

Zhao, Z. Hydroxyl radical generations form the physiologically relevant Fenton-like reactions. Free Radic. Biol. Med.208, 510–515. 10.1016/j.freeradbiomed.2023.09.013 (2023). PubMed

Fleming, A. M. & Burrows, C. J. On the irrelevancy of hydroxyl radical to DNA damage from oxidative stress and implications for epigenetics. Chemical Society Reviews49, 6524–6528. 10.1039/D0CS00579G (2020). PubMed PMC

Vyšín, L. et al. Dose-rate effects in breaking DNA strands by short pulses of extreme ultraviolet radiation. Radiat. Res.189, 466–476. 10.1667/RR14825.1 (2018). PubMed

Henke, B., Gullikson, E. & Davis, J. X-Ray interactions: Photoabsorption, scattering, transmission, and reflection at E = 50–30,000 eV, Z = 1–92. Atomic Data Nucl. Data Tables54, 181–342. 10.1006/adnd.1993.1013 (1993).

Adjei, D. et al. DNA strand breaks induced by soft X-ray pulses from a compact laser plasma source. Radiat. Phys. Chem.120, 17–25. 10.1016/j.radphyschem.2015.11.021 (2016).

LaVerne, J. A. & Pimblott, S. M. Yields of hydroxyl radical and hydrated electron scavenging reactions in aqueous solutions of biological interest. Radiat. Res.135, 16. 10.2307/3578391 (1993). PubMed

Milligan, J. R., Aguilera, J. A. & Ward, J. F. Variation of single-strand break yield with scavenger concentration for plasmid DNA irradiated in aqueous solution. Radiat. Res.133, 151. 10.2307/3578350 (1993). PubMed

Klimczak, U., Ludwig, D., Mark, F., Rettberg, P. & Schulte-Frohlinde, D. Irradiation of plasmid and phage DNA in water-alcohol mixtures: Strand breaks and lethal damage as a function of scavenger concentration. Int. J. Radiat. Biol.64, 497–510. 10.1080/09553009314551711 (1993). PubMed

LaVerne, J. A. & Pimblott, S. M. Diffusion-kinetic modelling of the cooperative effect of scavengers on the scavenged yield of the hydroxyl radical. J. Chem. Soc. Faraday Trans.89, 3527. 10.1039/ft9938903527 (1993).

Mark, F., Becker, U., Herak, J. N. & Schulte-Frohlinde, D. Radiolysis of DNA in aqueous solution in the presence of a scavenger: A kinetic model based on a nonhomogeneous reaction of OH radicals with DNA molecules of spherical or cylindrical shape. Radiat. Environ. Biophys.28, 81–99. 10.1007/BF01210293 (1989). PubMed

Espenson, J. H. Chemical Kinetics and Reaction Mechanisms 2nd edn. (McGraw-Hill, Inc., 1995).

Latulippe, D. R. & Zydney, A. L. Radius of gyration of plasmid DNA isoforms from static light scattering. Biotechnol. Bioeng.107, 134–142. 10.1002/bit.22787 (2010). PubMed

Prazeres, D. M. F. Prediction of diffusion coefficients of plasmids. Biotechnol. Bioeng.99, 1040–1044. 10.1002/bit.21626 (2008). PubMed

Debije, M. G., Strickler, M. D. & Bernhard, W. A. On the efficiency of hole and electron transfer from the hydration layer to DNA: An EPR study of crystalline DNA X-irradiated at 4 K. Radiat. Res.154, 163–70. 10.1667/0033-7587(2000)154[0163:oteoha]2.0.co;2 (2000). PubMed PMC

Becker, D., Adhikary, A. & Sevilla, M. D. The role of charge and spin migration in DNA radiation damage. In Charge Migration in DNA (ed. Chakraborty, T.), chap. 7, 1st edn, 139–175. 10.1007/978-3-540-72494-0_7 (Springer, 2007).

Souici, M. et al. DNA strand break dependence on Tris and arginine scavenger concentrations under ultra-soft X-ray irradiation: The contribution of secondary arginine radicals. Radiat. Environ. Biophys.55, 215–228. 10.1007/s00411-016-0642-9 (2016). PubMed

LaVerne, J. A. OH radicals and oxidizing products in the gamma radiolysis of water. Radiat. Res.153, 196–200. 10.1667/0033-7587(2000)153[0196:oraopi]2.0.co;2 (2000). PubMed

Pimblott, S. M. & LaVerne, J. A. Effect of electron energy on the radiation chemistry of liquid water. Radiat. Res.150, 159. 10.2307/3579851 (1998). PubMed

Pimblott, S. M. & LaVerne, J. A. Diffusion-kinetic theories for LET effects on the radiolysis of Water. J. Phys. Chem.98, 6136–6143. 10.1021/j100075a016 (1994).

Fulford, J., Nikjoo, H., Goodhead, D. T. & O’Neill, P. Yields of SSB and DSB induced in DNA by Al K ultrasoft X-rays and α-particles: Comparison of experimental and simulated yields. Int. J. Radiat. Biol.77, 1053–1066. 10.1080/09553000110069308 (2001). PubMed

Fromm, M. & Boulanouar, O. Low energy electrons and ultra-soft X-rays irradiation of plasmid DNA. Tech. Innov. Radiat. Phys. Chem.128, 44–53. 10.1016/j.radphyschem.2016.05.025 (2016).

Hervé du Penhoat, M.-A. et al. Lethal effect of carbon K-shell photoionizations in Chinese hamster V79 cell nuclei: Experimental method and theoretical analysis. Radiat. Res.151, 649. 10.2307/3580203 (1999). PubMed

Fayard, B. et al. Cell inactivation and double-strand breaks: The role of core ionizations, as probed by ultrasoft X-rays. Radiat. Res.157, 128–40. 10.1667/0033-7587(2002)157[0128:ciadsb]2.0.co;2 (2002). PubMed

Gobert, F. N. et al. Chromosome aberrations and cell inactivation induced in mammalian cells by ultrasoft X-rays: Correlation with the core ionizations in DNA. Int. J. Radiat. Biol.80, 135–45. 10.1080/09553000310001654710 (2004). PubMed

Hervé du Penhoat, M.-A. et al. Double-strand break induction and repair in V79-4 hamster cells: The role of core ionisations, as probed by ultrasoft X-rays. Int. J. Radiat. Biol.86, 205–219. 10.3109/09553000903419296 (2010). PubMed

Fulford, J., Bonner, P., Goodhead, D. T., Hill, M. A. & O’Neill,. Experimental determination of the dependence of OH radical yield on photon energy: A comparison with theoretical simulations. J. Phys. Chem. A103, 11345–11349. 10.1021/jp993087n (1999).

Milligan, J., Aguilera, J. A., Paglinawan, R. A., Ward, J. F. & Limoli, C. L. DNA strand break yields after post-high LET irradiation incubation with endonuclease-III and evidence for hydroxyl radical clustering. Int. J. Radiat. Biol.77, 155–164. 10.1080/09553000010013445 (2001). PubMed

Goodhead, D. T. & Nikjoo, H. Track structure analysis of ultrasoft X-rays compared to high- and low-LET radiations. Int. J. Radiat. Biol.55, 513–529. 10.1080/09553008914550571 (1989). PubMed

Kreipl, M. S., Friedland, W. & Paretzke, H. G. Interaction of ion tracks in spatial and temporal proximity. Radiat. Environ. Biophys.48, 349–359. 10.1007/s00411-009-0234-z (2009). PubMed

LaVerne, J. A. & Pimblott, S. M. Scavenger and time dependences of radicals and molecular products in the electron radiolysis of water: Examination of experiments and models. J. Phys. Chem.95, 3196–3206. 10.1021/j100161a044 (1991).

Gonzalez, D. H., Kuang, X. M., Scott, J. A., Rocha, G. O. & Paulson, S. E. Terephthalate probe for hydroxyl radicals: Yield of 2-hydroxyterephthalic acid and transition metal interference. Anal. Lett.51, 2488–2497. 10.1080/00032719.2018.1431246 (2018).

Find record

Citation metrics

Loading data ...

Archiving options

Loading data ...