Computational modeling and a Geant4-DNA study of the rejoining of direct and indirect DNA damage induced by low energy electrons and carbon ions

References

• Anderson RM, Stevens DL, Sumption ND, Townsend KM, Goodhead DT, Hill MA. 2007. Effect of linear energy transfer (LET) on the complexity of alpha-particle-induced chromosome aberrations in human CD34þ cells. Radiat Res. 167(5):541–550.
   PubMed Web of Science ®Google Scholar
• Antonelli F, Campa A, Esposito G, Giardullo P, Belli M, Dini V, Meschini S, Simone G, Sorrentino E, Gerardi S, et al. 2015. Induction and repair of DNA DSB as revealed by H2AX phosphorylation foci in human fibroblasts exposed to low and high-let radiation: relationship with early and delayed reproductive cell death. Radiat Res. 183(4):417–431.
   PubMed Web of Science ®Google Scholar
• Asaithamby A, Uematsu N, Chatterjee A, Story MD, Burma S, Chen JD. 2008. Repair of HZE-particle-induced DNA double-strand breaks in normal human fibroblasts. Radiat Res. 169(4):437–446.
   PubMed Web of Science ®Google Scholar
• Baiocco G, Barbieri S, Babini G, Morini J, Alloni D, Friedland W, Kundrát P, Schmitt E, Puchalska M, Sihver L, et al. 2016. The origin of neutron biological effectiveness as a function of energy. Sci Rep. 6:34033.
   PubMed Web of Science ®Google Scholar
• Belli M, Cherubini R, Dalla Vecchia M, Dini V, Moschini G, Signoretti C, Simone G, Tabocchini MA, Tiveron P. 2000. DNA DSB induction and rejoining in V79 cells irradiated with light ions: a constant field gel electrophoresis study. Int J Radiat Biol. 76(8):1095–1104.
   PubMed Web of Science ®Google Scholar
• Beucher A, Birraux J, Tchouandong L, Barton O, Shibata A, Conrad S, Goodarzi AA, Krempler A, Jeggo PA, Löbrich M, et al. 2009. ATM and Artemis promote homologous recombination of radiation-induced DNA double-strand breaks in G2. Embo J. 28(21):3413–3427.
   PubMed Web of Science ®Google Scholar
• Bordage MC, Bordes J, Edel S, Terrissol M, Franceries X, Bardiès M, Lampe N, Incerti S. 2016. Implementation of new physics models for low energy electrons in liquid water in Geant4-DNA. Phys Med. 32(12):1833–1840.
   PubMed Web of Science ®Google Scholar
• Buxton G, Greenstock C, Helman W, Ross AA. 1988. Critical review of rate constants for reactions of hydrated electrons, hydrogen atoms and hydroxyl radicals (·OH/·O−) in aqueous solution. J Phys Chem Ref Data. 17(2):513–886.
   Web of Science ®Google Scholar
• Carante M, Aime C, Cajiao J, Ballarini F. 2018. BIANCA, a biophysical model of cell survival and chromosome damage by protons, C-ions and He-ions at energies and doses used in hadrontherapy. Phys Med Biol. 63(7):075007.
   PubMed Web of Science ®Google Scholar
• Charlton DE, Nikjoo H, Humm JL. 1989. Calculation of initial yields of single and double-strand breaks in cell nuclei from electrons, protons and alpha particles. Int J Radiat Biol. 56(1):1–19.
   PubMed Web of Science ®Google Scholar
• Crespan E, Czabany T, Maga G, Hubscher U. 2012. Microhomology-mediated DNAstrand annealing and elongation by human DNA polymerases lambda andbeta on normal and repetitive DNA sequences. Nucleic Acids Res. 40(12):5577–5590.
   PubMed Web of Science ®Google Scholar
• Cucinotta FA, Nikjoo H, O’Neill P, Goodhead DT. 2000. Kinetics of DSB rejoiningand formation of simple chromosome exchange aberrations. Int J Radiat Biol. 76(11):1463–1474.
   PubMed Web of Science ®Google Scholar
• Cucinotta FA, Pluth JM, Anderson JA, Harper JV, O'Neill P. 2008. Biochemicalkinetics model of DSB repair and induction of gamma-H2AX foci by non-homologous end joining. Radiat Res. 169(2):214–222.
   PubMed Web of Science ®Google Scholar
• de la Fuente Rosales L, Incerti S, Francis Z, Bernal MA. 2018. Accounting for radiation-induced indirect damage on DNA with the Geant4-DNA code. Phys Med. 51:108–116.
   PubMed Web of Science ®Google Scholar
• de Lara CM, Hill MA, Jenner TJ, Papworth D, O'Neill P. 2001. Dependence of the yield of DNA double-strand breaks in Chinese Hamster V79–4 Cells on the Photon energy of Ultrasoft X Rays. Radiat Res. 155(3):440–448.
   PubMed Web of Science ®Google Scholar
• Drouet J, Frit P, Delteil C, de Villartay JP, Salles B, Calsou P. 2006. Interplay between Ku, Artemis, and the DNA-dependent protein kinase catalytic subunit at DNA ends. J Biol Chem. 281(38):27784–27793.
   PubMed Web of Science ®Google Scholar
• Famulari G, Pater P, Enger S. 2017. Microdosimetry calculations for monoenergetic electrons using Geant4-DNA combined with a weighted track sampling algorithm. Phys Med Biol. 62(13):5495–5508.
   PubMed Web of Science ®Google Scholar
• Franken NAP, Hovingh S, Ten Cate R, Krawczyk P, Stap J, Hoebe R, Aten J, Barendsen GW. 2012. Relative biological effectiveness of high linear energy transfer α-particles for the induction of DNA-double-strand breaks, chromosome aberrations and reproductive cell death in SW-1573 lung tumour cells. Oncol Rep. 27(3):769–774.
   PubMed Web of Science ®Google Scholar
• Friedland W, Jacob P, Kundrat P. 2010. Stochastic simulation of DNA double-strand break repair by non-homologous end joining based on track structure calculations. Radiat Res. 173(5):677–688.
   PubMed Web of Science ®Google Scholar
• Friedland W, Jacob P, Kundrat P. 2011. Mechanistic simulation of radiation damage to DNA and its repair: on the track towards systems radiation biology modelling. Radiat Prot Dosimetry. 143(2–4):542–548.
   PubMed Web of Science ®Google Scholar
• Friedland W, Kundrat P, Jacob P. 2012. Stochastic modelling of DSB repair afterphoton and ion irradiation. Int J Radiat Biol. 88(1–2):129–136.
   PubMed Web of Science ®Google Scholar
• Friedland W, Kundrát P. 2013. Track structure based modelling of chromosome aberrations after photon and alpha-particle irradiation. Mutat Res. 756(1–2):213–223.
   PubMed Web of Science ®Google Scholar
• Friedland W, Schmitt E, Kundrat P, Dingfelder M, Baiocco G, Barbieri S, Ottolenghi A. 2017. Comprehensive track-structure based evaluation of DNA damage by light ions from radiotherapy relevant energies down to stopping. Sci Rep. 7:45161.
   PubMed Web of Science ®Google Scholar
• Gallego C, Gonçalves MAFV, Wijnholds J. 2020. Novel therapeutic approaches for the treatment of retinal degenerative diseases: focus on CRISPR/Cas-based gene editing. Front Neurosci. 14:838.
   PubMed Web of Science ®Google Scholar
• Geuting V, Reul C, Löbrich M. 2013. ATM release at resected double-strand breaks provides heterochromatin reconstitution to facilitate homologous recombination. PLoS Genet. 9(8):e1003667.
   PubMed Web of Science ®Google Scholar
• Goodarzi AA, Jeggo P, Lobrich M. 2010. The influence of heterochromatin on DNA double strand break repair: getting the strong, silent type to relax. DNA Repair. 9(12):1273–1282.
   PubMed Web of Science ®Google Scholar
• Goodhead DT. 1994. Initial events in the cellular effects of ionizing radiations: clustered damage in DNA. Int J Radiat Biol. 65(1):7–17.
   PubMed Web of Science ®Google Scholar
• Goodhead DT, Thacker J. 1977. Inactivation and mutation of cultured mammalian cells by aluminium characteristic ultrasoft X-rays I properties of aluminium X-rays and preliminary experiments with Chinese hamster cells. Int J Radiat Biol Relat Stud Phys Chem Med. 31(6):541–559.
   PubMed Web of Science ®Google Scholar
• Hartlerode AJ, Morgan MJ, Wu Y, Buis J, Ferguson DO. 2015. Recruitment and activation of the ATM kinase in the absence of DNA-damage sensors. Nat Struct Mol Biol. 22(9):736–743.
   PubMed Web of Science ®Google Scholar
• Henthorn NT, Warmenhoven JW, Sotiropoulos M, Mackay RI, Kirkby NF, Kirkby KJ, Merchant MJ. 2018. In Silico non-homologous end joining following ion induced DNA double strand breaks predicts that repair fidelity depends on break density. Sci Rep. 8(1):2654.
   PubMedGoogle Scholar
• Heyer WD, Ehmsen KT, Liu J. 2010. Regulation of homologous recombination ineukaryotes. Annu Rev Genet. 44:113–139.
   PubMed Web of Science ®Google Scholar
• Hirayama R, Uzawa A, Obara M, Takase N, Koda K, Ozaki M, Noguchi M, Matsumoto Y, Li H, Yamashita K, et al. 2015. Determination of the relative biological effectiveness and oxygen enhancement ratio for micronuclei formation using high-LET radiation in solid tumor cells: an in vitro and in vivo study. Mutat Res Genet Toxicol Environ Mutagen. 793:41–47.
   PubMed Web of Science ®Google Scholar
• Ingram SP, Warmenhoven JW, Henthorn NT, Smith EAK, Chadwick AL, Burnet NG, Mackay RI, Kirkby NF, Kirkby KJ, Merchant MJ. 2019. Mechanistic modelling supports entwined rather than exclusively competitive DNA double-strand break repair pathway. Sci Rep. 9(1):6359.
   PubMed Web of Science ®Google Scholar
• Jeggo P, Lobrich M. 2006. Radiation-induced DNA damage responses. Radiat Prot Dosimetry. 122(1–4):124–127.
   PubMed Web of Science ®Google Scholar
• Kandaiya S, Lobachevsky PN, D’cunha G, Martin RF. 1996. DNA strand breakage by 125I decay in synthetic oligodeoxynucleotide:1 Fragment distribution and DMSO protection effect. Acta Oncol. 35(7):803–808.
   PubMed Web of Science ®Google Scholar
• Karamitros M, Luan S, Bernal M, Allison J, Baldacchino G, Davidkova M. 2014. Diffusion-controlled reactions modeling in Geant4-DNA. J. Comp. Phys. 274:841–882.
   Web of Science ®Google Scholar
• Kellerer AM. 1975. Fandamental of microdosimetry. In: Kase KR, Bjarngaard BE, Attix FH, editors, The dosimetry of ionizing radiation, vol 1. Cambridge: Academic Press.
   Google Scholar
• Liang L, Deng L, Chen YP, Li GC, Shao CS, Tischfield JA. 2005. Modulation of DNA end joining by nuclear proteins. J Biol Chem. 280(36):31442–31449.
   PubMed Web of Science ®Google Scholar
• Lobrich M, Cooper P, Rydberg B. 1998. Joining of correct and incorrect DNA ends at double-strand breaks produced by high-linear energy transfer radiation in human fibroblasts. Radiat Res. 150(6):619–626.
   PubMed Web of Science ®Google Scholar
• Lowe SW, Schmitt EM, Smith SW, Osborne BA, Jacks T. 1993. P53 is required for radiation-induced apoptosis in mouse thymocytes. Nature. 362(6423):847–849.
   PubMed Web of Science ®Google Scholar
• Lieber MR. 2010. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu Rev Biochem. 79:181–211.
   PubMed Web of Science ®Google Scholar
• Mahaney B, Meek K, Lees-Miller S. 2009. Repair of ionizing radiation-induced DNA double-strand breaks by non-homologous end-joining. Biochem J. 417(3):639–650.
   PubMedGoogle Scholar
• Martin RF, Haseltine WA. 1981. Range of radiochemical damage to DNA with decay of iodine-125. Science. 213(4510):896–898.
   PubMed Web of Science ®Google Scholar
• McVey M, Lee SE. 2008. MMEJ repair of double-strand breaks (director’s cut): deleted sequences and alternative endings. Trends Genet. 24(11):529–538.
   PubMed Web of Science ®Google Scholar
• Meek K, Dang V, Lees-Miller SP. 2008. DNA-PK: the means to justify the ends? Adv Immunol. 99:33–58.
   PubMed Web of Science ®Google Scholar
• Metzger L, Iliakis G. 1991. Kinetics of DNA double-strand break repair throughoutthe cell-cycle as assayed by pulsed field gel-electrophoresis in cho cells. Int J Radiat Biol. 59(6):1325–1339.
   PubMed Web of Science ®Google Scholar
• Moeini H, Mokari M, Alamatsaz MH, Taleei R. 2020. Calculation of the initial DNA damage induced by alpha particles in comparison with protons and electrons using Geant4-DNA. Int J Radiat Biol. 96(6):767–778.
   PubMed Web of Science ®Google Scholar
• Moeini H, Mokari M. 2022. DNA damage and microdosimetry for carbon ions: track structure simulations as the key to quantitative modeling of radiation-induced damage. Med Phys. 49(7):4823–4836.
   PubMed Web of Science ®Google Scholar
• Mokari M, Alamatsaz MH, Moeini H, Taleei R. 2018. A simulation approach for determining the spectrum of DNA damage induced by protons. Phys Med Biol. 63(17):175003.
   PubMed Web of Science ®Google Scholar
• Mokari M, Moeini H, Soleimani M, Fereidouni E. 2020. Calculation and comparison of the direct and indirect DNA damage induced by low energy electrons using default and CPA100 cross section models within Geant4-DNA. Nuc Instrum Methods Phys Res B. 480:56–66.
   Web of Science ®Google Scholar
• Mokari M, Moeini H, Soleimani M. 2021. Calculation of microdosimetric spectra for protons using Geant4-DNA and a μ-randomness sampling algorithm for the nanometric structures. Int J Radiat Biol. 97(2):208–218.
   PubMed Web of Science ®Google Scholar
• Mladenov E, Iliakis G. 2011. The pathways of double-strand break repair. In: DNA repair – on the pathways to fixing DNA damage and errors, Storici F. editor. London: IntechOpen.
   Google Scholar
• Milligan JR, Wu CCL, Ng JNN, Aguiler JA, Ward JF. 1996. Characterization of the reaction rate coefficient of DNA with the hydroxyl radical. Radiat Res. 146(5):510–513.
   PubMed Web of Science ®Google Scholar
• Neal J, Meek K. 2011. Choosing the right path: does DNA-PK help make the deci-sion? Mutat Res. 711(1–2):73–86.
   PubMed Web of Science ®Google Scholar
• Nikjoo H, O’Neill P, Wilson WE, Goodhead DT. 2001. Computational approach for determining the spectrum of DNA damage induced by ionizing radiation. Radiat Res. 156(5 Pt 2):577–583.
   PubMed Web of Science ®Google Scholar
• Nikjoo H. Uehara S. 2004. Track structure studies of biological systems. In: Charged particle and photon interactions with matter: chemical, physiochemical, and biological consequences with applications, Mozumder A. and Hatano Y, editors., New York: Marcel Dekker.
   Google Scholar
• Nikjoo H, Emfietzoglou D, Liamsuwan T, Taleei R, Liljequist D, Uehara S. 2016. Radiation track, DNA damage and response – a review. Rep Prog Phys. 79(11):116601.
   PubMed Web of Science ®Google Scholar
• Nikitaki Z, Nikolov V, Mavragani I, Mladenov E, Mangelis A, Laskaratou D. 2016. Measurement of complex DNA damage induction and repair in human cellular systems after exposure to ionizing radiations of varying linear energy transfer (LET). Free Radic. Res. 1:S64–S78.
   Google Scholar
• Oeck S, Szymonowicz K, Wiel G. 2018. Relating linear energy transfer to the formation and resolution of DNA repair Foci after irradiation with equal doses of X-ray photons, plateau, or bragg-peak protons. Int J Mol Sci. 19:3779.
   PubMed Web of Science ®Google Scholar
• Pardo B, Gómez-González B, Aguilera A. 2009. DNA repair in mammalian cells. Cell Mol Life Sci. 66(6):1039–1056.
   PubMedGoogle Scholar
• Particle Therapy Co-Operative Group. Particle therapy facilities in clinical operation, particle therapy co-operative group, December 2022. accessed https://www.ptcog.ch/index.php/facilities-in-operation-restricted.
   Google Scholar
• Reynolds P, Anderson JA, Harper JV, Hill MA, Botchway SW, Parker AW, O’Neill P. 2012. The dynamics of Ku70/80 and DNA-PKcs at DSBs induced by ionizingradiation is dependent on the complexity of damage. Nucleic Acids Res. 40(21):10821–10831.,.
   PubMed Web of Science ®Google Scholar
• Riballo E, Kühne M, Rief N, Doherty A, Smith GCM, Recio M-J, Reis C, Dahm K, Fricke A, Krempler A, et al. 2004. A pathway of double-strand break rejoining dependent uponATM, Artemis, and proteins locating to gamma-H2AX foci. Mol Cell. 16(5):715–724.,.
   PubMed Web of Science ®Google Scholar
• Rogakou EP, Pilch DR, Orr HA, Ivanova SV, Bonner MW. 1998. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem. 273(10):5858–5868.
   PubMed Web of Science ®Google Scholar
• Simsek D, Brunet E, Wong SYW, Katyal S, Gao Y, McKinnon PJ. 2011. DNA ligaseIII promotes alternative nonhomologous end-joining during chromosomaltranslocation formation. PLoS Genet. 7:1002080.
   PubMed Web of Science ®Google Scholar
• Shibata A, Conrad S, Birraux J, Geuting V, Barton O, Ismail A, Kakarougkas A, Meek K, Taucher-Scholz G, Löbrich M, et al. 2011. Factors determining DNAdouble-strand break repair pathway choice in G2 phase. Embo J. 30(6):1079–1092.
   PubMed Web of Science ®Google Scholar
• Stenerlow B, Hoglund E, Carlsson J, Blomquist E. 2000. Rejoining of DNA fragmentsproduced by radiations of different linear energy transfer. Int J Radiat Biol. 76:549–557.
   PubMed Web of Science ®Google Scholar
• Symington LS, Gautier J. 2011. Double-strand break end resection and repair path-way choice. Annu Rev Genet. 45:247–271.
   PubMed Web of Science ®Google Scholar
• Taleei R, Hultqvist M, Gudowska I, Nikjoo H. 2012. A Monte Carlo evaluation of carbon and lithium ions dose distributions in water. Int J Radiat Biol. 88(1–2):189–194.
   PubMed Web of Science ®Google Scholar
• Taleei R, Nikjoo H. 2013a. The non-homologous end-joining (NHEJ) pathway for the repair of DNA double-strand breaks: I A mathematical model. Radiat Res. 179(5):530–539.
   PubMed Web of Science ®Google Scholar
• Taleei R, Nikjoo H. 2013b. Biochemical DSB-repair model for mammalian cells in G1 and early S phases of the cell cycle. Mutat Res. 756(1–2):206–212.
   PubMed Web of Science ®Google Scholar
• Terrissol M. 1994. Modelling of radiation damage by 125I on a nucleosome. Int J Radiat Biol. 66(5):447–451.
   PubMed Web of Science ®Google Scholar
• Uematsu N, Weterings E, Yano K-i, Morotomi-Yano K, Jakob B, Taucher-Scholz G, Mari P-O, van Gent DC, Chen BPC, Chen DJ. 2007. Autophosphorylation of DNA-PKCS regulates its dynamics at DNA double-strand breaks. J Cell Biol. 177(2):219–229.
   PubMed Web of Science ®Google Scholar
• Wang M, Wu W, Wu W, Rosidi B, Zhang L, Wang H, Iliakis G. 2006. PARP-1 and Ku compete for repair of DNA double strand breaks by distinct NHEJ pathways. Nucleic Acids Res. 34(21):6170–6182.
   PubMed Web of Science ®Google Scholar
• Ward JF. 1994. The complexity of DNA damage – relevance to biological consequences. Int J Radiat Biol. 66(5):427–432.
   PubMed Web of Science ®Google Scholar
• Wang J, Pluth JM, Cooper PK, Cowan MJ, Chen DJ, Yannone SM. 2005. Artemis phosphorylation and function in response to damage. DNA Repair. 4(5):556–570.
   PubMedGoogle Scholar
• Warmenhoven JW, Henthorn NT, Ingram SP, Chadwick AL, Sotiropoulos M, Korabel N, Fedotov S, Mackay RI, Kirkby KJ, Merchant MJ.,. 2020. Insights into the non-homologous end joining pathway and double strand break end mobility provided by mechanistic in silico modelling. DNA Repair. 85:102743.
   PubMed Web of Science ®Google Scholar
• Watanabe R, Rahmanian S, Nikjoo H. 2015. Spectrum of radiation-induced clustered Non-DSB damage – a Monte Carlo track structure modeling and calculations. Radiat Res. 183(5):525–540.
   PubMed Web of Science ®Google Scholar
• Yeh CD, Richardson CD, Corn JE. 2019. Advances in genome editing through control of DNA repair pathways. Nat Cell Biol. 21(12):1468–1478.
   PubMed Web of Science ®Google Scholar
• Zhao L, Bao C, Shang Y. 2020. The determinant of DNA repair pathway choices in ionising radiation-induced DNA double-strand breaks. Bio Med Res Int. 2020:4834965.
   Google Scholar