Single, Double, and Multiple Double Strand Breaks Induced in DNA by 3−100 eV Electrons

Abstract

Nonthermal secondary electrons with initial kinetic energies below 100 eV are an abundant transient species created in irradiated cells and thermalize within picoseconds through successive multiple energy loss events. Here we show that below 15 eV such low-energy electrons induce single (SSB) and double (DSB) strand breaks in plasmid DNA exclusively via formation and decay of molecular resonances involving DNA components (base, sugar, hydration water, etc.). Furthermore, the strand break quantum yields (per incident electron) due to resonances occur with intensities similar to those that appear between 25 and 100 eV electron energy, where nonresonant mechanisms related to excitation/ionizations/dissociations are shown to dominate the yields, although with some contribution from multiple scattering electron energy loss events. We also present the first measurements of the electron energy dependence of multiple double strand breaks (MDSB) induced in DNA by electrons with energies below 100 eV. Unlike the SSB and DSB yields, which remain relatively constant above 25 eV, the MDSB yields show a strong monotonic increase above 30 eV, however with intensities at least 1 order of magnitude smaller than the combined SSB and DSB yields. The observation of MDSB above 30 eV is attributed to strand break clusters (nano-tracks) involving multiple successive interactions of one single electron at sites that are distant in primary sequence along the DNA double strand, but are in close contact; such regions exist in supercoiled DNA (as well as cellular DNA) where the double helix crosses itself or is in close proximity to another part of the same DNA molecule.

Induction of strand breaks in DNA films by low energy electrons and soft X-ray under nitrous oxide atmosphere

“…Additionally, electrons above about 15 eV which exist in the SE distribution emitted from tantalum substrate, possibly can contribute in the formation of multiple double strand breaks (MDSBs) via the direct interactions of a single incident electron with multiple sites in a single DNA molecule. The yield of MDSB can be determined from the integral of the entire broad feature representing the smear in the gel (Huels et al 2003).…”

The molecular origin of high DNA-repair efficiency by photolyase

“…The redox property at the active site is synergistically optimized to balance the FET and BET processes relative to the excited-state deactivation and the dimer splitting, respectively, to achieve the maximum outcome. After the complete dimer splitting, the third charge-recombination channel, the elector return to restore the active flavin cofactor and complete the repair photocycle, should not be too slow to avoid new damage of repaired DNA by the extra electron 29 . Any mutation as studied here that modulates the active-site reduction potentials and ET reorganization energies always breaks the dedicated synergy of the optimization for the main four elementary reactions in two competitions, and thus leads to lower repair efficiency than the WT enzyme.…”

Site- and energy-selective slow-electron production through intermolecular Coulombic decay

“…In the proposed RA-ICD cascade, in addition to the Auger and the above mentioned core-ICD electrons, highly damaging low-energy ICD electrons with controllable energies are emitted. For example, SSBs in DNA are produced favorably by electrons with energies between 0 and 4 eV [36], while DSBs are mostly induced by electrons with energies above 6 eV [11]. We note that only for electrons with energies below 15 eV the microscopic mechanisms for strand breakage have been investigated [10,11,[37][38][39] (for brief discussion on higher energy electrons, see Supplementary Materials).…”

“…For example, SSBs in DNA are produced favorably by electrons with energies between 0 and 4 eV [36], while DSBs are mostly induced by electrons with energies above 6 eV [11]. We note that only for electrons with energies below 15 eV the microscopic mechanisms for strand breakage have been investigated [10,11,[37][38][39] (for brief discussion on higher energy electrons, see Supplementary Materials). In all the ICD processes during the cascade two or more neighboring ions are produced directly leading to damaging Coulomb explosion [3,40].…”

“…Low-energy electrons (LEEs) [10,11], as well as radical cations [12], the direct products of the ICD, are known to be effective in causing single-and double-strand breaks in DNA. Recent experiments even suggest that ICD electrons contribute up to about 50% of the single-strand breaks (SSB) in DNA [13].…”