Perspectives in radiation biophysics: From radiation track structure simulation to mechanistic models of DNA damage and repair

Abstract In radiation targeted therapy and genetic risk estimation of low dose radiation protection there is a crucial need for full description of DNA damage response and repair (DDR) leading to cell death and cell mutation. We propose such a description can be arrived through realistic track-structure simulations together with mechanistic mathematical formulation of DDR and the availability of experimental data for testing the proof of principle. In this paper we review briefly first the state of the art in DNA damage and repair, and then the recent advances in the physics of track structure which represents an essential tool in radiation biophysics.

[1]  H. Nikjoo,et al.  Nanodosimetry in a 12C ion beam using Monte Carlo simulations , 2010 .

[2]  Qi Ding,et al.  Non-homologous End Joining Requires That the DNA-PK Complex Undergo an Autophosphorylation-dependent Rearrangement at DNA Ends* , 2004, Journal of Biological Chemistry.

[3]  P. Calsou,et al.  Effect of double-strand break DNA sequence on the PARP-1 NHEJ pathway. , 2008, Biochemical and biophysical research communications.

[4]  C. Champion,et al.  Electron and positron elastic scattering in gaseous and liquid water: A comparative study , 2008 .

[5]  U. Landman,et al.  Excess electron transport in water , 1990 .

[6]  Dimitris Emfietzoglou,et al.  Energy Loss of Hydrogen- and Helium-Ion Beams in DNA: Calculations Based on a Realistic Energy-Loss Function of the Target , 2011, Radiation research.

[7]  J. E. Turner,et al.  Radiation Interactions and Energy Transport in the Condensed Phase , 1991 .

[8]  Francis A Cucinotta,et al.  A Complete Dielectric Response Model for Liquid Water: A Solution of the Bethe Ridge Problem , 2005, Radiation research.

[9]  Hooshang Nikjoo,et al.  Response to the letter of Bodgi and Foray: on the coherence between mathematical models of DSB repair and physiological reality. , 2014, Mutation research. Genetic toxicology and environmental mutagenesis.

[10]  P. Jeggo,et al.  The Heterochromatic Barrier to DNA Double Strand Break Repair: How to Get the Entry Visa , 2012, International journal of molecular sciences.

[11]  Hooshang Nikjoo,et al.  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. , 2015, Mutation research. Genetic toxicology and environmental mutagenesis.

[12]  Herwig G. Paretzke,et al.  Electron inelastic-scattering cross sections in liquid water , 1999 .

[13]  G. Olivera,et al.  Theoretical calculation of electronic stopping power of water vapor by proton impact. , 1995, Radiation research.

[14]  P. Jeggo,et al.  The impact of heterochromatin on DSB repair. , 2009, Biochemical Society transactions.

[15]  Mitio Inokuti,et al.  Inelastic Collisions of Fast Charged Particles with Atoms and Molecules-The Bethe Theory Revisited , 1971 .

[16]  H. Nikjoo,et al.  Repair of the double-strand breaks induced by low energy electrons: A modelling approach , 2012, International journal of radiation biology.

[17]  B. Stenerlöw,et al.  Induction and Rejoining of DNA Double-Strand Breaks in Normal Human Skin Fibroblasts after Exposure to Radiation of Different Linear Energy Transfer: Possible Roles of Track Structure and Chromatin Organization , 2001, Radiation research.

[18]  M. E. Rudd,et al.  Electron production in proton collisions with atoms and molecules: energy distributions , 1992 .

[19]  George Iliakis,et al.  Efficient rejoining of radiation-induced DNA double-strand breaks in vertebrate cells deficient in genes of the RAD52 epistasis group , 2001, Oncogene.

[20]  J. D. Vries,et al.  Cq+-induced excitation and fragmentation of uracil : effects of the projectile electronic structure , 2002 .

[21]  T. Liamsuwan,et al.  Physical and biophysical properties of proton tracks of energies 1 keV to 300 MeV in water , 2011, International journal of radiation biology.

[22]  J. Fulford,et al.  Quantitative analysis of the energetics of DNA damage. , 2002, Radiation protection dosimetry.

[23]  M. Löbrich,et al.  Joining of correct and incorrect DNA ends at double-strand breaks produced by high-linear energy transfer radiation in human fibroblasts. , 1998, Radiation research.

[24]  Stephens,et al.  Slow electrons in condensed matter. , 1986, Physical Review B (Condensed Matter).

[25]  B. Pons,et al.  Classical treatment of ion-H 2 O collisions with a three-center model potential , 2011 .

[26]  W. Dynan,et al.  Geometry of a complex formed by double strand break repair proteins at a single DNA end: recruitment of DNA-PKcs induces inward translocation of Ku protein. , 1999, Nucleic acids research.

[27]  Simon M. Pimblott,et al.  Effect of Elastic Collisions on Energy Deposition by Electrons in Water , 1997 .

[28]  D. T. Goodhead,et al.  Quantitative modelling of DNA damage using Monte Carlo track structure method , 1999, Radiation and environmental biophysics.

[29]  P O'Neill,et al.  Computational Approach for Determining the Spectrum of DNA Damage Induced by Ionizing Radiation , 2001, Radiation research.

[30]  David Liljequist,et al.  On the sampling of step length in Monte Carlo simulation of trajectories with very small mean free path , 2012 .

[31]  S. Incerti,et al.  A free-parameter theoretical model for describing the electron elastic scattering in water in the Geant4 toolkit , 2009 .

[32]  R. Baskin,et al.  Visualization of Rad54, a chromatin remodeling protein, translocating on single DNA molecules. , 2006, Molecular cell.

[33]  S. Jackson,et al.  XLF Interacts with the XRCC4-DNA Ligase IV Complex to Promote DNA Nonhomologous End-Joining , 2006, Cell.

[34]  R. H. Ritchie,et al.  Comparisons of Calculations with PARTRAC and NOREC: Transport of Electrons in Liquid Water , 2008, Radiation research.

[35]  D. Emfietzoglou,et al.  Inelastic Cross Sections for Low-Energy Electrons in Liquid Water: Exchange and Correlation Effects , 2013, Radiation research.

[36]  Markus Löbrich,et al.  ATM and Artemis promote homologous recombination of radiation-induced DNA double-strand breaks in G2 , 2009, The EMBO journal.

[37]  T Liamsuwan,et al.  Radiation track, DNA damage and response—a review , 2016, Reports on progress in physics. Physical Society.

[38]  G. Iliakis,et al.  Kinetics of DNA double-strand break repair throughout the cell cycle as assayed by pulsed field gel electrophoresis in CHO cells. , 1991, International journal of radiation biology.

[39]  C. Champion,et al.  Total cross sections for ionizing processes induced by proton impact on molecules of biological interest: A classical trajectory Monte Carlo approach , 2008 .

[40]  Markus Löbrich,et al.  Factors determining DNA double‐strand break repair pathway choice in G2 phase , 2011, The EMBO journal.

[41]  L. Sanche,et al.  Adapting gas-phase electron scattering R -matrix calculations to a condensed-matter environment , 2007 .

[42]  J. Ganachaud,et al.  Theoretical study of the secondary electron emission of insulating targets , 1995 .

[43]  H. Nikjoo,et al.  Spectrum of Radiation-Induced Clustered Non-DSB Damage – A Monte Carlo Track Structure Modeling and Calculations , 2015, Radiation research.

[44]  M. Weinfeld,et al.  Involvement of polynucleotide kinase in a poly(ADP-ribose) polymerase-1-dependent DNA double-strand breaks rejoining pathway. , 2006, Journal of molecular biology.

[45]  S. L. McLawhorn,et al.  Electron Emission from Amorphous Solid Water Induced by Passage of Energetic Protons and Fluorine Ions , 2010, Radiation research.

[46]  M. Quinto,et al.  Water versus DNA: new insights into proton track-structure modelling in radiobiology and radiotherapy , 2015, Physics in medicine and biology.

[47]  Hooshang Nikjoo,et al.  The Non-homologous End-Joining (NHEJ) Pathway for the Repair of DNA Double-Strand Breaks: I. A Mathematical Model , 2013, Radiation research.

[48]  T. Liamsuwan,et al.  A Monte Carlo track structure simulation code for the full-slowing-down carbon projectiles of energies 1 keV u–1–10 MeV u–1 in water , 2013, Physics in medicine and biology.

[49]  R. N. Hamm,et al.  Collective oscillation in liquid water , 1974 .

[50]  D. Liljequist Contribution from inelastic scattering to the validity of trajectory methods , 2013 .

[51]  Toshinori Suzuki,et al.  Effective attenuation length of an electron in liquid water between 10 and 600 eV. , 2014, Physical review. E, Statistical, nonlinear, and soft matter physics.

[52]  S. Uehara,et al.  Energy spectra of secondary electrons in water vapour , 1996, Radiation and environmental biophysics.

[53]  H. Nikjoo,et al.  Radiation induced base excision repair (BER): a mechanistic mathematical approach. , 2014, DNA repair.

[54]  T Hyslop,et al.  DNA-dependent protein kinase stimulates an independently active, nonhomologous, end-joining apparatus. , 2000, Cancer research.

[55]  T. Liamsuwan,et al.  Cross sections for bare and dressed carbon ions in water and neon , 2013, Physics in medicine and biology.

[56]  F. Salvat,et al.  Simple method for the simulation of multiple elastic scattering of electrons , 1989 .

[57]  G. Moschini,et al.  DNA DSB induction and rejoining in V79 cells irradiated with light ions: a constant field gel electrophoresis study. , 2000, International journal of radiation biology.

[58]  Lennart Lindborg,et al.  RBE of low energy electrons and photons , 2010, Physics in medicine and biology.

[59]  M. Dingfelder Track-structure simulations for charged particles. , 2012, Health physics.

[60]  Michael Dingfelder,et al.  Updated model for dielectric response function of liquid water. , 2014, Applied radiation and isotopes : including data, instrumentation and methods for use in agriculture, industry and medicine.

[61]  Francis A. Cucinotta,et al.  Track-structure codes in radiation research , 2006 .

[62]  David J. Chen,et al.  Phosphorylation of Ku dictates DNA double-strand break (DSB) repair pathway choice in S phase , 2015, Nucleic acids research.

[63]  Francesc Salvat,et al.  Optical-model potential for electron and positron elastic scattering by atoms , 2003 .

[64]  J. H. Miller,et al.  Proton energy degradation in water vapor. , 1973, Radiation research.

[65]  N. Arista,et al.  Dielectric description of wakes and stopping powers in solids , 1998 .

[66]  Hooshang Nikjoo,et al.  Biochemical DSB-repair model for mammalian cells in G1 and early S phases of the cell cycle. , 2013, Mutation research.

[67]  C. Kao,et al.  The complete optical spectrum of liquid water measured by inelastic x-ray scattering. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[68]  Å. Carlsson Tedgren,et al.  Nanodosimetry and RBE values in radiotherapy. , 2015, Radiation protection dosimetry.

[69]  D. Liljequist Coherent elastic scattering trajectory simulation , 2012 .

[70]  A. Itoh,et al.  Absolute doubly differential cross sections for ionization of adenine by 1.0-MeV protons , 2011 .

[71]  K. Schwarz,et al.  DNA-PKcs regulates a single-stranded DNA endonuclease activity of Artemis. , 2010, DNA repair.

[72]  A. Padellec,et al.  Electron spectroscopy in proton collisions with dry gas-phase uracil base , 2006 .

[73]  L. Sihver,et al.  Applications of the microdosimetric function implemented in the macroscopic particle transport simulation code PHITS , 2012, International journal of radiation biology.

[74]  L. Sanche,et al.  Cross Sections for Low-Energy (1–100 eV) Electron Elastic and Inelastic Scattering in Amorphous Ice , 2003, Radiation research.

[75]  T. Liamsuwan,et al.  Microdosimetry of the full slowing down of protons using Monte Carlo track structure simulations. , 2015, Radiation protection dosimetry.

[76]  J. D. Bourke,et al.  Electron inelastic mean free path theory and density functional theory resolving discrepancies for low-energy electrons in copper. , 2014, The journal of physical chemistry. A.

[77]  P. Jeggo,et al.  DNA‐PK autophosphorylation facilitates Artemis endonuclease activity , 2006, The EMBO journal.

[78]  Hooshang Nikjoo,et al.  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 , 2013, Radiation research.

[79]  T. Liamsuwan,et al.  Microdosimetry of proton and carbon ions. , 2014, Medical physics.

[80]  E. Crespan,et al.  Microhomology-mediated DNA strand annealing and elongation by human DNA polymerases λ and β on normal and repetitive DNA sequences , 2012, Nucleic acids research.

[81]  Hooshang Nikjoo,et al.  A model of the cell nucleus for DNA damage calculations , 2012, International journal of radiation biology.

[82]  M. Faubel,et al.  Photoelectron spectroscopy of liquid water and aqueous solution: Electron effective attenuation lengths and emission-angle anisotropy , 2010 .

[83]  N. Hiraoka,et al.  Accurate Measurements of Dielectric and Optical Functions of Liquid Water and Liquid Benzene in the VUV Region (1-100 eV) Using Small-Angle Inelastic X-ray Scattering. , 2015, The journal of physical chemistry. B.

[84]  A. Rosenfeld,et al.  Electron emission from amorphous solid water after proton impact: Benchmarking PTra and Geant4 track structure Monte Carlo simulations , 2012 .