An Investigation of Cell Displacement in Direct and Indirect DNA Damage Induced by Photon Radiation: A Geant4-DNA Study
Abstract
Purpose: This study aimed to investigate the biological effects of photon radiation and its potential for cancer treatment through targeted radiation therapy by studying direct and indirect DNA damage induced by 15, 30, and 50 keV photon radiation using Geant4-DNA Monte Carlo simulations.
Materials and Methods: Two spherical cells (C and C2) and their cell nucleus were modeled in liquid water. An atomic DNA model constructed in the Geant4-DNA Monte Carlo simulation toolkit, containing 125,000 chromatin fibers, was placed inside the nucleus of the C2 cell. The number of direct and indirect single-strand breaks (SSBs), double-strand breaks (DSBs), and hybrid double-strand breaks (HDSB) in the C2 cell caused by 15, 30, and 50 keV photons were calculated for N2←CS, N2←Cy, N2←C, and N2←N Target←Source combinations, at the distances of 0, 2.5, and 5 μm between two cells.
Results: Low energy (15 keV) photons emitted within the cell surface and the cell cytoplasm resulted in the highest DNA damage, producing markedly higher SSBs, DSBs, and HDSBs compared to the whole cell and the nucleus sources across 0-5 μm target distances. Increasing the photon energy to 30 and 50 keV showed 81-96% reduced DNA damage. Additionally, the 2.5 μm target distance decreased DSBs up to 53%.
Conclusion: Based on the results, 15 keV photons are more effective for the inhibition or control of cancer cells.
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28- S. Siddique and J. C. Chow, “Recent advances in functionalized nanoparticles in cancer theranostics,” Nanomaterials, vol. 12, no. 16, p. 2826, (2022).
29- S. A. Zein et al., “Monte Carlo simulations of electron interactions with the DNA molecule: A complete set of physics models for Geant4-DNA simulation toolkit,” Nuclear Instruments and Methods in Physics Research Section B: Beam Interactions with Materials and Atoms, vol. 542, pp. 51-60, (2023).
30- N. Lampe, M. Karamitros, V. Breton, J. M. Brown, D. Sakata, D. Sarramia, and S. Incerti, “Mechanistic DNA damage simulations in Geant4-DNA Part 2: Electron and proton damage in a bacterial cell,” Physica Medica, vol. 48, pp. 146-155, (2018).
31- M. Bordage, J. Bordes, S. Edel, M. Terrissol, X. Franceries, M. Bardiès, N. Lampe, and S. Incerti, “Implementation of new physics models for low energy electrons in liquid water in Geant4-DNA,” Physica Medica, vol. 32, no. 12, pp. 1833-1840, (2016).
32- D. E. Cullen, J. H. Hubbell, and L. Kissel, “EPDL97: the Evaluated Photon Data Library, "97 Version, 1997,” University of California, Lawrence Livermore National Laboratory: Livermore, CA, (1997).
33- I. Kyriakou, D. Sakata, H. N. Tran, Y. Perrot, W.-G. Shin, N. Lampe, S. Zein, M. C. Bordage, S. Guatelli, and C. Villagrasa, “Review of the Geant4-DNA simulation toolkit for radiobiological applications at the cellular and DNA level,” Cancers, vol. 14, no. 1, pp. 35, (2021).
34- C. A. Santiago, and J. C. Chow, “Variations in Gold Nanoparticle Size on DNA Damage: A Monte Carlo Study Based on a Multiple-Particle Model Using Electron Beams,” Applied Sciences, vol. 13, no. 8, pp. 4916, (2023).
35- A. Azizi Ganjgah, and P. Taherparvar, “Evaluation of direct and indirect DNA Damage under the Photon Irradiation in the Presence of Gold, Gadolinium, and Silver Nanoparticles Using Geant4-DNA,” Radiation Physics and Engineering, vol. 5, no. 3, pp. 33-41, (2024).
2- P. Taherparvar, and A. Azizi Ganjgah, “Comparison of direct DNA damage by protons and oxygen, carbon, and helium ions using Geant4-DNA code,” Iranian Journal of Physics Research, vol. 23, no. 4, pp. 353-371, (2024).
3- R. Baskar, J. Dai, N. Wenlong, R. Yeo, and K.-W. Yeoh, “Biological response of cancer cells to radiation treatment,” Frontiers in molecular biosciences, vol. 1, p. 24, (2014).
4- S. Asadian et al., “β-radiating radionuclides in cancer treatment, novel insight into promising approach,” Pharmacological research, vol. 160, p. 105070, (2020).
5- M. S. Moradi and B. S. Bidabadi, “Micro-dosimetry calculation of Auger-electron-emitting radionuclides mostly used in nuclear medicine using GEANT4-DNA,” Applied Radiation and Isotopes, vol. 141, pp. 73-79, (2018).
6- J.-P. Pouget et al., “Cell membrane is a more sensitive target than cytoplasm to dense ionization produced by auger electrons,” Radiation research, vol. 170, no. 2, pp. 192-200, (2008).
7- H. Date, K. Sutherland, H. Hasegawa, and M. Shimozuma, “Ionization and excitation collision processes of electrons in liquid water,” Nuclear Instruments and Methods in Physics Research Section B: Beam Interactions with Materials and Atoms, vol. 265, no. 2, pp. 515-520, (2007).
8- P. Ahmadi, M. S. Zafarghandi, and A. Shokri, “Calculation of direct and indirect damages of Auger electron-emitting radionuclides based on the atomic geometric model: A simulation study using Geant4-DNA toolkit,” Nuclear Instruments and Methods in Physics Research Section B: Beam Interactions with Materials and Atoms, vol. 483, pp. 22-28, (2020).
9- L. H. Thompson, “Recognition, signaling, and repair of DNA double-strand breaks produced by ionizing radiation in mammalian cells: the molecular choreography,” Mutation Research/Reviews in Mutation Research, vol. 751, no. 2, pp. 158-246, (2012).
10- M. Frankenberg-Schwager and D. Frankenberg, “DNA double-strand breaks: their repair and relationship to cell killing in yeast,” International journal of radiation biology, vol. 58, no. 4, pp. 569-575, (1990).
11- M. A. Bernal et al., “Track structure modeling in liquid water: A review of the Geant4-DNA very low energy extension of the Geant4 Monte Carlo simulation toolkit,” Physica Medica, vol. 31, no. 8, pp. 861-874, (2015).
12- Z. Francis et al., “Molecular scale track structure simulations in liquid water using the Geant4-DNA Monte-Carlo processes,” Applied radiation and isotopes, vol. 69, no. 1, pp. 220-226, (2011).
13- J. Allison et al., “Recent developments in Geant4,” Nuclear instruments and methods in physics research section A: Accelerators, Spectrometers, Detectors and Associated Equipment, vol. 835, pp. 186-225, (2016).
14- R. Salim, and P. Taherparvar, “A Monte Carlo study on the effects of a static uniform magnetic field on micro-scale dosimetry of Auger-emitters using Geant4-DNA,” Radiation Physics and Chemistry, vol. 195, pp. 110063, 2022.
15- R. Salim, and P. Taherparvar, "Dosimetry assessment of theranostic Auger-emitting radionuclides in a micron-sized multicellular cluster model: a Monte Carlo study using Geant4-DNA simulations,” Applied Radiation and Isotopes, vol. 188, pp. 110380, 2022.
16- U. Titt, B. Bednarz, and H. Paganetti, “Comparison of MCNPX and Geant4 proton energy deposition predictions for clinical use,” Physics in Medicine & Biology, vol. 57, no. 20, p. 6381, (2012).
17- M. Bernal and J. Liendo, “An investigation on the capabilities of the PENELOPE MC code in nanodosimetry,” Medical physics, vol. 36, no. 2, pp. 620-625, (2009).
18- J. Baró, J. Sempau, J. Fernández-Varea, and F. Salvat, “PENELOPE: an algorithm for Monte Carlo simulation of the penetration and energy loss of electrons and positrons in matter,” Nuclear Instruments and Methods in Physics Research Section B: Beam Interactions with Materials and Atoms, vol. 100, no. 1, pp. 31-46, (1995).
19- W. Friedland, P. Jacob, and P. Kundrat, “Mechanistic simulation of radiation damage to DNA and its repair: on the track towards systems radiation biology modelling,” Radiation protection dosimetry, vol. 143, no. 2-4, pp. 542-548, (2011).
20- L. Lindborg and H. Nikjoo, “Microdosimetry and radiation quality determinations in radiation protection and radiation therapy,” Radiation protection dosimetry, vol. 143, no. 2-4, pp. 402-408, (2011).
21- G. Raisali, L. Mirzakhanian, S. F. Masoudi, and F. Semsarha, “Calculation of DNA strand breaks due to direct and indirect effects of Auger electrons from incorporated 123I and 125I radionuclides using the Geant4 computer code,” International journal of radiation biology, vol. 89, no. 1, pp. 57-64, (2013).
22- Z. A. Ganjeh, M. Eslami-Kalantari, M. E. Loushab, and A. A. Mowlavi, “Simulation of direct DNA damages caused by alpha particles versus protons,” Nuclear Instruments and Methods in Physics Research Section B: Beam Interactions with Materials and Atoms, vol. 473, pp. 10-15, 2020.
23- J. Chen, S. Yun, T. Dong, Z. Ren, and X. Zhang, “Investigate the radiation-induced damage on an atomistic DNA model by using Geant4-DNA toolkit,” Nuclear Instruments and Methods in Physics Research Section B: Beam Interactions with Materials and Atoms, vol. 494, pp. 59-67, (2021).
24- M. A. Bernal et al., “An atomistic geometrical model of the B-DNA configuration for DNA–radiation interaction simulations,” Computer Physics Communications, vol. 184, no. 12, pp. 2840-2847, (2013).
25- C. Bousis, D. Emfietzoglou, P. Hadjidoukas, and H. Nikjoo, “Monte Carlo single-cell dosimetry of Auger-electron emitting radionuclides,” Physics in Medicine & Biology, vol. 55, no. 9, p. 2555, (2010).
26- Y.-Y. Hsiao, F.-C. Tai, C.-C. Chan, and C.-C. Tsai, “A computational method to estimate the effect of gold nanoparticles on X-ray induced dose enhancement and double-strand break yields,” IEEE Access, vol. 9, pp. 62745-62751, (2021).
27- Z. A. Ganjeh, M. Eslami-Kalantari, M. E. Loushab, and A. A. Mowlavi, “Calculation of direct DNA damages by a new approach for carbon ions and protons using Geant4-DNA,” Radiation Physics and Chemistry, vol. 179, p. 109249, (2021).
28- S. Siddique and J. C. Chow, “Recent advances in functionalized nanoparticles in cancer theranostics,” Nanomaterials, vol. 12, no. 16, p. 2826, (2022).
29- S. A. Zein et al., “Monte Carlo simulations of electron interactions with the DNA molecule: A complete set of physics models for Geant4-DNA simulation toolkit,” Nuclear Instruments and Methods in Physics Research Section B: Beam Interactions with Materials and Atoms, vol. 542, pp. 51-60, (2023).
30- N. Lampe, M. Karamitros, V. Breton, J. M. Brown, D. Sakata, D. Sarramia, and S. Incerti, “Mechanistic DNA damage simulations in Geant4-DNA Part 2: Electron and proton damage in a bacterial cell,” Physica Medica, vol. 48, pp. 146-155, (2018).
31- M. Bordage, J. Bordes, S. Edel, M. Terrissol, X. Franceries, M. Bardiès, N. Lampe, and S. Incerti, “Implementation of new physics models for low energy electrons in liquid water in Geant4-DNA,” Physica Medica, vol. 32, no. 12, pp. 1833-1840, (2016).
32- D. E. Cullen, J. H. Hubbell, and L. Kissel, “EPDL97: the Evaluated Photon Data Library, "97 Version, 1997,” University of California, Lawrence Livermore National Laboratory: Livermore, CA, (1997).
33- I. Kyriakou, D. Sakata, H. N. Tran, Y. Perrot, W.-G. Shin, N. Lampe, S. Zein, M. C. Bordage, S. Guatelli, and C. Villagrasa, “Review of the Geant4-DNA simulation toolkit for radiobiological applications at the cellular and DNA level,” Cancers, vol. 14, no. 1, pp. 35, (2021).
34- C. A. Santiago, and J. C. Chow, “Variations in Gold Nanoparticle Size on DNA Damage: A Monte Carlo Study Based on a Multiple-Particle Model Using Electron Beams,” Applied Sciences, vol. 13, no. 8, pp. 4916, (2023).
35- A. Azizi Ganjgah, and P. Taherparvar, “Evaluation of direct and indirect DNA Damage under the Photon Irradiation in the Presence of Gold, Gadolinium, and Silver Nanoparticles Using Geant4-DNA,” Radiation Physics and Engineering, vol. 5, no. 3, pp. 33-41, (2024).
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How to Cite
1.
Azizi Ganjgah A, Taherparvar P. An Investigation of Cell Displacement in Direct and Indirect DNA Damage Induced by Photon Radiation: A Geant4-DNA Study. Frontiers Biomed Technol. 2024;.
