Track to the future: historical perspective on the importance of radiation track structure and DNA as a radiobiological target

References

• Anderson RM, Stevens DL, Goodhead DT. 2002. M-FISH analysis shows that complex chromosome aberrations induced by alpha-particle tracks are cumulative products of localized rearrangements. Proc Natl Acad Sci USA. 99:12167–12172.
   PubMed Web of Science ®Google Scholar
• 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 CD34+ cells. Radiat Res. 167:541–550.
   PubMed Web of Science ®Google Scholar
• Asaithamby A, Uematsu N, Chatterjee A, Story MD, Burma S, Chen DJ. 2008. Repair of HZE-particle-induced DNA double-strand breaks in normal human fibroblasts. Radiat Res. 169:437–446.
   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
• Barendsen GW. 1964. Impairment of the proliferative capacity of human cells in culture by alpha-particles with differing linear-energy transfer. Int J Radiat Biol. 8:453–466.
   Web of Science ®Google Scholar
• Barendsen GW, Walter HMD, Fowler JF, Bewley DK. 1963. Effects of different ionization radiations on human cells in tissue culture III. Experiments with cyclotron-accelerated alpha-particles and deuterons. Radiat Res. 18:106–119.
   Google Scholar
• Botchway SW, Stevens DL, Hill MA, Jenner TJ, O'Neill P. 1997. Induction and rejoining of DNA double-strand breaks in Chinese hamster V79-4 cells irradiated with characteristic aluminum K and copper L ultrasoft X rays. Radiat Res. 148:317–324.
   PubMed Web of Science ®Google Scholar
• Brustad T. 1962. Heavy ions and some aspects of their use in molecular and cellular radiobiology. Adv Biol Med Phys. 8:161–224.
   Google Scholar
• Butts JJ, Katz R. 1967. Theory of RBE for heavy ion bombardment of dry enzymes and viruses. Radiat Res. 30:855–871.
   PubMed Web of Science ®Google Scholar
• Charlton DE, Humm JL. 1988. A method of calculating initial DNA strand breakage following the decay of incorporated 125I. Int J Radiat Biol. 53:353–365.
   Web of Science ®Google Scholar
• Chudoba I, Plesch A, Lorch T, Lemke J, Claussen U, Senger G. 1999. High resolution multicolor-banding: a new technique for refined FISH analysis of human chromosomes. Cytogenet Cell Genet. 84:156–160.
   PubMedGoogle Scholar
• Cornforth MN. 2006. Perspectives on the formation of radiation-induced exchange aberrations. DNA Repair (Amst). 5:1182–1191.
   PubMed Web of Science ®Google Scholar
• Cucinotta FA, Pluth JM, Anderson JA, Harper JV, O'Neill P. 2008. Biochemical kinetics model of DSB repair and induction of gamma-H2AX foci by non-homologous end joining. Radiat Res. 169:214–222.
   PubMed Web of Science ®Google Scholar
• De Bont R, van Larebeke N. 2004. Endogenous DNA damage in humans: a review of quantitative data. Mutagenesis. 19:169–185.
   PubMed Web of Science ®Google Scholar
• Dickey JS, Baird BJ, Redon CE, Avdoshina V, Palchik G, Wu J, Kondratyev A, Bonner WM, Martin OA. 2012. Susceptibility to bystander DNA damage is influenced by replication and transcriptional activity. Nucleic Acids Res. 40:10274–10286.
   PubMed Web of Science ®Google Scholar
• Dobbs TA, Palmer P, Maniou Z, Lomax ME, O'Neill P. 2008. Interplay of two major repair pathways in the processing of complex double-strand DNA breaks. DNA Repair (Amst). 7:1372–1383.
   PubMed Web of Science ®Google Scholar
• Durante M, Pignalosa D, Jansen JA, Walboomers XF, Ritter S. 2010. Influence of nuclear geometry on the formation of genetic rearrangements in human cells. Radiat Res. 174:20–26.
   PubMed Web of Science ®Google Scholar
• Eccles LJ, O'Neill P, Lomax ME. 2011. Delayed repair of radiation induced clustered DNA damage: friend or foe? Mutat Res. 711:134–141.
   PubMed Web of Science ®Google Scholar
• Friedland W, Jacob P, Kundrát P. 2010. Stochastic simulation of DNA double-strand break repair by non-homologous end joining based on track structure calculations. Radiat Res. 173:677–688.
   PubMed Web of Science ®Google Scholar
• Friedland W, Kundrat P. 2013. Track structure based modelling of chromosome aberrations after photon and alpha-particle irradiation. Mutat Res. 756:213–223.
   PubMed Web of Science ®Google Scholar
• Friedland W, Paretzke HG, Ballarini F, Ottolenghi A, Kreth G, Cremer C. 2008. First steps towards systems radiation biology studies concerned with DNA and chromosome structure within living cells. Radiat Environ Biophys. 47:49–61.
   PubMed Web of Science ®Google Scholar
• Friedland W, Schmitt E, Kundrát 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
• Fulford J, Nikjoo H, Goodhead DT, O'Neill P. 2001. Yields of SSB and DSB induced in DNA by Al(K) ultrasoft X-rays and alpha-particles: comparison of experimental and simulated yields. Int J Radiat Biol. 77:1053–1066.
   PubMed Web of Science ®Google Scholar
• Georgakilas AG, O'Neill P, Stewart RD. 2013. Induction and repair of clustered DNA lesions: what do we know so far? Radiat Res. 180:100–109.
   PubMed Web of Science ®Google Scholar
• Goodhead DT, Brenner DJ. 1983. Estimation of a single property of low LET radiations which correlates with biological effectiveness. Phys Med Biol. 28:485–492.
   PubMed Web of Science ®Google Scholar
• Goodhead DT, Charlton DE. 1985. Analysis of high-let radiation effects in terms of local energy deposition. Radiat Prot Dosim. 13:253–258.
   Web of Science ®Google Scholar
• Goodhead DT, Munson RJ, Thacker J, Cox R. 1980. Mutation and inactivation of cultured mammalian cells exposed to beams of accelerated heavy ions. IV. Biophysical interpretation. Int J Radiat Biol. 37:135–167.
   Web of Science ®Google Scholar
• Goodhead DT, Nikjoo H. 1990. Current status of ultrasoft X-rays and track structure-analysis as tools for testing and developing biophysical models of radiation action. Radiat Prot Dosim. 31:343–350.
   Web of Science ®Google Scholar
• Goodhead DT, Thacker J, Cox R. 1993. Weiss Lecture. Effects of radiations of different qualities on cells: molecular mechanisms of damage and repair. Int J Radiat Biol. 63:543–556.
   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. 65:7–17.
   PubMed Web of Science ®Google Scholar
• Goodhead DT. 1999. Mechanisms for the biological effectiveness of high-LET radiations. J Radiat Res. 40 Suppl:1–13.
   PubMed Web of Science ®Google Scholar
• Goodhead DT. 2006. Energy deposition stochastics and track structure: what about the target? Radiat Prot Dosimetry. 122:3–15.
   PubMed Web of Science ®Google Scholar
• Gulston M, de Lara C, Jenner T, Davis E, O'Neill P. 2004. Processing of clustered DNA damage generates additional double-strand breaks in mammalian cells post-irradiation. Nucleic Acids Res. 32:1602–1609.
   PubMed Web of Science ®Google Scholar
• Gulston M, Fulford J, Jenner T, de Lara C, O'Neill P. 2002. Clustered DNA damage induced by gamma radiation in human fibroblasts (HF19), hamster (V79-4) cells and plasmid DNA is revealed as Fpg and Nth sensitive sites. Nucleic Acids Res. 30:3464–3472.
   PubMed Web of Science ®Google Scholar
• Hanahan D, Weinberg RA. 2011. Hallmarks of cancer: the next generation. Cell Mar. 144:646–674.
   PubMed Web of Science ®Google Scholar
• Hei TK, Zhou H, Ivanov VN, Hong M, Lieberman HB, Brenner DJ, Amundson SA, Geard CR. 2008. Mechanism of radiation-induced bystander effects: a unifying model. J Pharm Pharmacol. 60:943–950.
   PubMed Web of Science ®Google Scholar
• Hill MA. 2004. The variation in biological effectiveness of X-rays and gamma rays with energy. Radiat Prot Dosimetry. 112:471–481.
   PubMed Web of Science ®Google Scholar
• Hofer KG, Hughes WL. 1971. Radiotoxicity of intranuclear tritium, 125 iodine and 131 iodine. Radiat Res. 47:94–101.
   PubMed Web of Science ®Google Scholar
• Howard-Flanders P. 1958. Physical and chemical mechanisms in the injury of cells of ionizing radiations. Adv Biol Med Phys. 6:553–603.
   PubMedGoogle Scholar
• ICRP. 2003. Relative biological effectiveness (RBE), quality factor (Q), and radiation weighting factor (w(R)). ICRP Publication 92. Ann ICRP. 33:1–117.
   Google Scholar
• ICRP. 2007. The 2007 recommendations of the International Commission on Radiological Protection. ICRP Publication 103. Ann ICRP. 37:1–332.
   Google Scholar
• Jenner TJ, deLara CM, O'Neill P, Stevens DL. 1993. Induction and rejoining of DNA double-strand breaks in V79-4 mammalian cells following gamma- and alpha-irradiation. Int J Radiat Biol. 64:265–273.
   PubMed Web of Science ®Google Scholar
• Kadhim MA, Macdonald DA, Goodhead DT, Lorimore SA, Marsden SJ, Wright EG. 1992. Transmission of chromosomal instability after plutonium alpha-particle irradiation. Nature. 355:738–740.
   PubMed Web of Science ®Google Scholar
• Kaplan HS, Moses LE. 1964. Biological complexity and radiosensitivity. Radiation lethality in cells and viruses is correlated with nucleic acid content, structure, and ploidy. Science. 145:21–25.
   PubMed Web of Science ®Google Scholar
• Kassis AI, Fayad F, Kinsey BM, Sastry KS, Taube RA, Adelstein SJ. 1987. Radiotoxicity of 125I in mammalian cells. Radiat Res. 111:305–318.
   PubMed Web of Science ®Google Scholar
• Kinner A, Wu W, Staudt C, Iliakis G. 2008. Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res. 36:5678–5694.
   PubMed Web of Science ®Google Scholar
• Lea DE. 1962. Actions of radiation on living cells. Cambridge: Cambridge University Press.
   Google Scholar
• Li Y, Reynolds P, O'Neill P, Cucinotta FA. 2014. Modeling damage complexity-dependent non-homologous end-joining repair pathway. PLoS One. 9:e85816.
   PubMed Web of Science ®Google Scholar
• Magnander K, Hultborn R, Claesson K, Elmroth K. 2010. Clustered DNA damage in irradiated human diploid fibroblasts: influence of chromatin organization. Radiat Res. 173:272–282.
   PubMed Web of Science ®Google Scholar
• Malyarchuk S, Castore R, Harrison L. 2009. Apex1 can cleave complex clustered DNA lesions in cells. DNA Repair (Amst). 8:1343–1354.
   PubMed Web of Science ®Google Scholar
• Morgan GR, Mill AJ, Roberts CJ, Newman S, Holt PD. 1988. The radiobiology of 24 keV neutrons. Measurement of the relative biological effect free-in-air, survival and cytogenetic analysis of the biological effect at various depths in a polyethylene phantom and modification of the depth-dose profile by boron 10 for V79 Chinese hamster and HeLa cells. Br J Radiol. 61:1127–1135.
   PubMed Web of Science ®Google Scholar
• Morgan WF, Sowa MB. 2007. Non-targeted bystander effects induced by ionizing radiation. Mutat Res. 616:159–164.
   PubMed Web of Science ®Google Scholar
• Morgan WF. 2003a. Non-targeted and delayed effects of exposure to ionizing radiation: I. Radiation-induced genomic instability and bystander effects in vitro. Radiat Res. 159:567–580.
   PubMed Web of Science ®Google Scholar
• Morgan WF. 2003b. Non-targeted and delayed effects of exposure to ionizing radiation: II. Radiation-induced genomic instability and bystander effects in vivo, clastogenic factors and transgenerational effects. Radiat Res. 159:581–596.
   PubMed Web of Science ®Google Scholar
• Mozumder A, Magee JL. 1966. Model of tracks of ionizing radiations for radical reaction mechanisms. Radiat Res. 28:203–214.
   PubMed Web of Science ®Google Scholar
• Muller HJ. 1927. Artificial transmutation of the gene. Science. 66:84–87.
   PubMedGoogle Scholar
• Munro TR. 1970. The relative radiosensitivity of the nucleus and cytoplasm of Chinese hamster firbroblasts. Radiat Res. 42:451–480.
   PubMed Web of Science ®Google Scholar
• National Research Council (U.S.). 2006. Committee to assess health risks from exposure to low level of ionizing radiation. Health risks from exposure to low levels of ionizing radiation: BEIR VII Phase 2 Washington, DC: National Academies Press.
   Google Scholar
• Nikjoo H, Bolton CE, Watanabe R, Terrissol M, O'Neill P, Goodhead DT. 2002. Modelling of DNA damage induced by energetic electrons (100 eV to 100 keV). Radiat Prot Dosimetry. 99:77–80.
   PubMed Web of Science ®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. 79:116601.
   PubMed Web of Science ®Google Scholar
• Nikjoo H, Goodhead DT. 1991. Track structure analysis illustrating the prominent role of low-energy electrons in radiobiological effects of low-LET radiations. Phys Med Biol. 36:229–238.
   PubMed Web of Science ®Google Scholar
• Nikjoo H, O'Neill P, Goodhead DT, Terrissol M. 1997. Computational modelling of low-energy electron-induced DNA damage by early physical and chemical events. Int J Radiat Biol. 71:467–483.
   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. 156:577–583.
   PubMed Web of Science ®Google Scholar
• Ponomarev AL, George K, Cucinotta FA. 2012. Computational model of chromosome aberration yield induced by high- and low-LET radiation exposures. Radiat Res. 177:727–737.
   PubMed Web of Science ®Google Scholar
• Portess DI, Bauer G, Hill MA, O'Neill P. 2007. Low-dose irradiation of nontransformed cells stimulates the selective removal of precancerous cells via intercellular induction of apoptosis. Cancer Res. 67:1246–1253.
   PubMed Web of Science ®Google Scholar
• Prise KM, Folkard M, Newman HC, Michael BD. 1994. Effect of radiation quality on lesion complexity in cellular DNA. Int J Radiat Biol. 66:537–542.
   PubMed Web of Science ®Google Scholar
• Prise KM, O'Sullivan JM. 2009. Radiation-induced bystander signalling in cancer therapy. Nat Rev Cancer. 9:351–360.
   PubMed Web of Science ®Google Scholar
• Prise KM, Pinto M, Newman HC, Michael BD. 2001. A review of studies of ionizing radiation-induced double-strand break clustering. Radiat Res. 156:572–576.
   PubMed Web of Science ®Google Scholar
• Ray FA, Zimmerman E, Robinson B, Cornforth MN, Bedford JS, Goodwin EH, Bailey SM. 2013. Directional genomic hybridization for chromosomal inversion discovery and detection. Chromosome Res. 21:165–174.
   PubMed Web of Science ®Google Scholar
• Roots R, Okada S. 1975. Estimation of life times and diffusion distances of radicals involved in X-ray-induced DNA strand breaks of killing of mammalian cells. Radiat Res. 64:306–320.
   PubMed Web of Science ®Google Scholar
• Rothkamm K, Barnard S, Moquet J, Ellender M, Rana Z, Burdak-Rothkamm S. 2015. DNA damage foci: meaning and significance. Environ Mol Mutagen. 56:491–504.
   PubMed Web of Science ®Google Scholar
• Rothkamm K, Gunasekara K, Warda SA, Krempler A, Lobrich M. 2008. Radiation-induced HPRT mutations resulting from misrejoined DNA double-strand breaks. Radiat Res. 169:639–648.
   PubMed Web of Science ®Google Scholar
• Rydberg B, Holley WR, Mian IS, Chatterjee A. 1998. Chromatin conformation in living cells: support for a zig-zag model of the 30 nm chromatin fiber. J Mol Biol. 284:71–84.
   PubMed Web of Science ®Google Scholar
• Sax K. 1938. Chromosome aberrations induced by X-rays. Genetics. 23:494–516.
   PubMedGoogle Scholar
• Schmid TE, Greubel C, Hable V, Zlobinskaya O, Michalski D, Girst S, Siebenwirth C, Schmid E, Molls M, Multhoff G, et al. 2012. Low LET protons focused to submicrometer shows enhanced radiobiological effectiveness. Phys Med Biol. 57:5889–5907.
   PubMed Web of Science ®Google Scholar
• Schmidt P, Kiefer J. 1998. Deletion-pattern analysis of alpha-particle and X-ray induced mutations at the HPRT locus of V79 Chinese hamster cells. Mutat Res. 421:149–161.
   PubMed Web of Science ®Google Scholar
• Schwartz JL, Rotmensch J, Sun J, An J, Xu Z, Yu Y, Hsie AW. 1994. Multiplex polymerase chain reaction-based deletion analysis of spontaneous, gamma ray- and alpha-induced HPRT mutants of CHO-K1 cells. Mutagenesis. 9:537–540.
   PubMed Web of Science ®Google Scholar
• Singleton BK, Griffin CS, Thacker J. 2002. Clustered DNA damage leads to complex genetic changes in irradiated human cells. Cancer Res. 62:6263–6269.
   PubMed Web of Science ®Google Scholar
• Swenberg JA, Lu K, Moeller BC, Gao L, Upton PB, Nakamura J, Starr TB. 2011. Endogenous versus exogenous DNA adducts: their role in carcinogenesis, epidemiology, and risk assessment. Toxicol Sci. 120 Suppl 1:S130–S145.
   PubMed Web of Science ®Google Scholar
• Taleei R, Girard PM, Nikjoo H. 2015. DSB repair model for mammalian cells in early S and G1 phases of the cell cycle: application to damage induced by ionizing radiation of different quality. Mutat Res. 779:5–14.
   PubMed Web of Science ®Google Scholar
• Taleei R, Girard PM, Sankaranarayanan K, Nikjoo H. 2013. The non-homologous end-joining (NHEJ) mathematical model for the repair of double-strand breaks: II. Application to damage induced by ultrasoft X rays and low-energy electrons. Radiat Res. 179:540–548.
   PubMed Web of Science ®Google Scholar
• Taleei R, Nikjoo H. 2013. The non-homologous end-joining (NHEJ) pathway for the repair of DNA double-strand breaks: I. A mathematical model. Radiat Res. 179:530–539.
   PubMed Web of Science ®Google Scholar
• Thacker J, Wilkinson R, Ganesh A, North P. 1989. Mechanisms of resistance to ionising radiations: genetic and molecular studies on ataxia-telangiectasia and related radiation-sensitive mutants. In: DNA repair mechanisms and their biological implications in mammalian cells. New York: Plenum Press.
   Google Scholar
• Tsao D, Kalogerinis P, Tabrizi I, Dingfelder M, Stewart RD, Georgakilas AG. 2007. Induction and processing of oxidative clustered DNA lesions in 56Fe-ion-irradiated human monocytes. Radiat Res. 168:87–97.
   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. 183:525–540.
   PubMed Web of Science ®Google Scholar
• Zhu LX, Waldren CA, Vannias D, Hei TK. 1996. Cellular and molecular analysis of mutagenesis induced by charged particles of defined linear energy transfer. Radiat Res. 145:251–259.
   PubMed Web of Science ®Google Scholar
• Zirkle RE, Bloom W. 1953. Irradiation of parts of individual cells. Science. 117:487–493.
   PubMed Web of Science ®Google Scholar