Clustered DNA Damages Induced by 2-20 eV Electrons and Transient

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Clustered DNA Damages Induced by 2-20 eV Electrons and Transient Anions: General Mechanism and Correlation to Cell Death Yanfang Dong, Yingxia Gao, Wenhui Liu, Ting Gao, Yi Zheng, and Leon Sanche J. Phys. Chem. Lett., Just Accepted Manuscript • DOI: 10.1021/acs.jpclett.9b01063 • Publication Date (Web): 17 May 2019 Downloaded from http://pubs.acs.org on May 17, 2019

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The Journal of Physical Chemistry Letters

Clustered DNA Damages Induced By 2-20 Ev Electrons and Transient Anions: General Mechanism and Correlation to Cell Death Yanfang Dong,a Yingxia Gao,a Wenhui Liu,a Ting gao,a Yi Zheng,a* and Léon Sancheb aState

Key Laboratory of Photocatalysis on Energy and Environment, Faculty of chemistry, Fuzhou

University, Fuzhou 350116, P.R. China; bDepartment of Nuclear Medicine and Radiobiology and Clinical Research Center, Faculty of Medicine, Université de Sherbrooke, Sherbrooke, QC Canada J1H 5N4

RECEIVED DATE: TITLE RUNNING HEAD: clustered DNA damages by LEEs

*CORRESPONDING AUTHOR: Yi Zheng Faculty of Chemistry, Fuzhou University, Fuzhou 350116, P.R. China. Email address: [email protected]

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Abstract The mechanisms of action of low energy electrons (LEEs) generated in large quantities by ionizing radiation constitutes an essential element of our understanding of early events in radiolysis and radiobiology. We present the 2- 20 eV electron-energy dependence of the yields of base damages (BDs), BD-related crosslinks (CLs) and non-double strand break (NDSB) clustered damages induced in DNA. These new yield functions are generated by LEE impact on plasmid DNA films. The damage is analyzed by gel electrophoresis with and without enzyme treatment. Maxima at 5 and 10 eV in BDs and BD-related CLs yields functions and two others, at 6 and 10 eV, in those of NDSB clustered damages are ascribed to core-excited transient anions that decay into bond-breaking channels. The mechanism causing all types of DNA damages can be attributed to the capture of a single electron by a base followed by multiple different electron transfer pathways.

Keywords:

clustered DNA damages, low-energy electrons, base modifications, transient anions

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Defining the initial events in Radiation Chemistry and Biology constitutes an essential element of our understanding of the action of high-energy radiation (HER) in condensed matter, including living organisms and humans. When ionization occurs, these events comprise the immediate reactions of the ion and resulting radicals, and the interactions of the secondary electrons, whose distribution lies essentially below 30 eV.1 Once thermalized secondary electrons become

chemically

reactive species, i.e., solvated electrons.2,3 The relevance of the chemistry induced by radiation is now well-established in many fields,4,5 but in the last decade, it has been shown that secondary low-energy electrons (LEEs) also play a significant, and often distinctive, role in inducing chemical and biomolecular radiation damage.3,6,7,8 Understanding the mechanisms of action of precursors of solvated electrons (i.e., LEEs) is pertinent to many areas of physical chemistry.3,9 Such a comprehension is more specifically needed in recent experiments that generate exclusively LEEs in solution with visible or UV light incident on plasmonic nanostructures. These new techniques can follow, in real time, the subsequent generation of pre-solvated and solvated electrons and their reactions.10,11,12,13,14 In applied radiobiology, the action and number of generated LEEs has implications in radiotherapy alone, or combined with chemotherapy15,16, and possibly in estimating the risks of health effects from HER exposure on earth or in space17. As a general strategy, emerging new cancer treatments try to increase the biological effectiveness of HER at the tumor site.15,16,18 Preferential reduction of cancer cells is usually achieved by producing large localized densities of LEEs, which decreases radiation damage to healthy tissues for the same total dose.15,18 Among the most effective of these modalities, we find targeted radionuclide therapy (TRT),18,19 as well as nanoparticle-aided20 and heavy-ion radiotherapy15,21. Since many radiosensitizers and chemotherapeutic drugs amplify LEE4


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induced damage,9,16 fundamental knowledge on LEE-interactions is expected to improve, not only radiotherapy, but also treatments, which combine in concomitance chemo- and radio-therapy22,23. Recent pre-clinical studies have shown that basic information on the reaction of LEEs with Ptchemotherapeutic agents bound to DNA could help predict the most efficient drug23 and the best time delay between its intravenous administration and tumor irradiation in chemoradiation treatments.24,25 LEEs are also strongly implicated in the processing of biological materials by femtosecond lasers.26,27,28 Beside reactive radicals, laser-induced plasmas can produce high-density avalanches of 0-15 eV electrons in solution.29 These species are expected to be involved in the destruction of cells, via DNA bond breaking, in ultrafast-laser nano-surgery28,30 and cancer therapy26. Ever since the observation that electrons with energies between 0-20 eV can damage biological DNA,31,32 via transient anion (TA) formation and their decay into bond-breaking channels, a multitude of different experiments have been performed to probe the ensuing damage.2,7,33,34,35 Simple DNA components (the bases, sugar and phosphate groups and nucleotides) were investigated in the gas33,36 or micro-solvation phases37,38 and more recently in solution by pulse radiolysis.39,40 Multi- or sub-monolayer (ML) film experiments in ultra-high vacuum (UHV) permitted investigating simple to extremely complex targets, such as plasmid DNA, and revealed biologically-significant damages by post-irradiation sample analysis.34,41,42 These experiments have the advantage of a monochromatic electron source, whose energy can be varied from close to zero to hundreds of eVs. With this characteristic, structures in the energy-dependence of product yields (i.e., the yield functions) from complex biomolecules can be identified and related to mechanisms of damage and their energy requirements.41,43 From such measurements, double and single strand breaks (DSBs and SSBs) induced by LEE bombardment of thin films of plasmid DNA were found to be created essentially via 5



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the formation of TAs of basic units that decay into dissociative electron attachment (DEA) and autoionization. Such yield functions have not been reported for base-damage (BD) related single and clustered lesions, which are expected to constitute a significant portion of the total damage inflicted to DNA by LEEs.44,45 Clustered DNA lesions, defined as two or more lesions within 20 base pairs (bp) in the helix, are characteristic of HER,46,47,48 and the most toxic. They consist of a DSB and, in the same or opposite strand, BDs (i.e., pyrimidine or purine lesions or abasic sites), a SSB with a BD, as well as a multitude of combinations of these lesions.49,50,51 DSB accounts for less than 30% of total complex DNA damages.50 Generally, BDs are important component of clustered damages and crosslinks (CLs) that affect mutagenic outcomes;49,50,51,52 Hence, the electron-energy dependence of these other types of clustered lesions, particularly non-DSB clustered damages, is essential to identify the mechanisms of action of LEEs leading to cellular damage and their role in the detrimental biological effects of HER.47,48 We present in this letter, the yield functions for BDs, BD-related CLs and non-DSB clustered lesions produced by 2-20 eV LEEs. Each of these functions exhibits two strong maxima that are interpreted to arise from the transitory formation of core-excited anions and a variety of electron transfer pathways. Furthermore, all clustered lesions can be correlated to the death of cells, whose DNA was irradiated with such electrons. Five-ML-thick films of plasmid DNA (pGEM-3Zf(−), 3197 bp) were exposed in UHV, to a monoenergetic LEE beam, having an energy spread of ± 0.3 eV and calibrated within ± 0.5 eV absolute energy.43 Irradiation procedures and damage analysis44 are described in the online Supplement. Two fractions of the irradiated sample were treated with base excision repair endonuclease III (Nth) and 6


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formamidopyrimidine N-glycosylase (Fpg), which cleave the base lesions of the pyrimidines and purines, respectively, to yield a correlated strand break.53 In this manner, BDs could be revealed as SSBs by electrophoresis and differentiated from SSBs, DSBs and CLs, directly formed by LEE impact that were present in the DNA gels analysed without enzyme treatment. The yields for various DNA lesions induced by a single electron were derived from the initial slope (S) of respective dose-exposure curves, corresponding to the percentage of damaged molecules per incident electron.44 Exposureresponse curves obtained with 10 eV electrons are shown in Fig. 1s of the Supplement as an example. The yields (Y) of CLs, SSBs, DSBs and loss of supercoiled DNA per incident electron per DNA molecule were obtained from Y=S/f, where f is the percentage of supercoiled DNA in the control.43 Each of these curves required the accumulation of 252 data points for a total of 4,536 measurements. Previous results of the yields of SSBs, DSBs and some inter-duplex CLs were repeated to check for consistency and to compare all damage yields under exactly the same experimental conditions. The yield functions for BDs and non-DSB clustered damages could therefore be directly compared to those of SSBs and DSBs. Yield functions for the loss of the initial supercoiled DNA conformation, SSBs, DSBs and CLs, with and without enzyme treatments, are shown in the Supplement. After enzyme treatment, the rise in SSBs is attributed to isolated BDs and possible formation of intrastrand CLs, via the reaction of a base radical with a nearby base or the 5’-deoxyribose moiety of the nucleotide54 in the same chain. All BD-related yield functions are presented in Fig. 1; they include those of isolated BDs and intrastrand CLs, inter-duplex CLs, BD-related inter-duplex CLs and non-DSB clustered damages. Inter-duplex CLs arise from a radical formed on a strand, which react with a nearly DNA molecule. BD-related inter-duplex CLs refer to those that are revealed by enzyme treatment. The non-DSB 7



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clustered damages arise from additional DSBs after enzymatic treatment, revealing two BDs or a BD adjacent to a strand break located in opposite strands within 20 bp. These lesions could also involve interstrand CLs, cleaved at two opposite linking positions by the enzyme as in nucleotide excision repair.54,55 Yields for formation of DSBs, non-DSB clustered lesions, SSBs and BDs induced by 2–20 eV electron impact on DNA films of 5 ML thickness, are shown in Fig. 2 B-E. Fig. 2A represents the electron energy dependence of the inverse of the transformation (i.e., survival) efficiency of E. coli bacteria, after LEE-bombardment of the DNA necessary for their viability.56,57 In these experiments, E. coli bacteria were incubated in an ampicillin-rich environment, which would normally kill them. However, they could survive owing to the injection of undamaged plasmids that encode an enzyme, capable of inactivating the antibiotic. When, prior to their injection, these plasmids were irradiated with electrons of different energies, with identical fluence, cell survival was found to be energy dependent as shown in Fig 2A. The SSB and DSB yield functions in Fig. 2 agree well with previous results.43 BDs and SSBs are the most numerous lesions in the total DNA damage, while yields of CLs, DSBs and non-DSB clustered damages are one order of magnitude smaller. At 10 eV, maxima are seen in the yield functions of all types of lesions and BDs are the highest. These observations strongly suggest that the initial process (i.e., TAs formed around 10 eV), causing all measurable types of damages is the same, including that responsible for the decrease in cell viability. Similarly, maxima at 5 eV for CLs, SSBs and BDs, and at 6 eV, for DSBs and non-DSB cluster lesions can be interpreted as due to the formation of TAs.41,43

In the 5-6 eV range, the TAs causing cluster lesions are located one eV higher than those

creating a single damage site. Although some TAs may contribute to both the 5 and 6 eV peaks, the 8


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higher-energy one is likely to arise from the decay of a different mixture of TAs, because of the energy requirement to break two bonds. In fact, this condition may explain the shift to higher peak energy in going from SSBs to DSBs. As expected, the low-energy maxima in Fig. 2A also lie at a higher energy than that of single damages, since cell function is usually not perturbed by repairable single lesions. Below 13 eV in Fig. 2, the similarity in shape and peak energies between curves A, B and C indicates that TAs causing clustered lesions are implicated in cell death. The rise at 2 eV in the SSB and BD yield functions (Fig. 2 D and E) is probably due to the formation of a shape resonance, previously identified at 2.2 eV, as temporary electron attachment to a base by Martin et al.32 These authors found that no DSB formation below 4 eV,32 as in the present experiments for all clustered damages. Thus, more than 3 eV is necessary to produce interstrand cluster damage. The energies of all previously identified core-excited TAs below 13 eV can be assembled into the two bands drawn in Fig. 1 and 2.43 The resonances in these two groups result from incident electron capture by the positive electron affinity of specific electronically excited states of the bases.41,43 The correlation between these bands and the maxima in all curves of Fig. 1 and 2 indicates that all lesions are most likely caused by the decay into bond-breaking channels of these TAs. In Table 1s of the supplement, we present previous energy assignments of the decay channels of these TAs, by electron-energy-loss spectroscopy (EELS) of condensed DNA bases and electron stimulated desorption of anions and neutral radicals from films of oligonucleotides.41,58,59,60,61,62 From these, we find that, not only could many DEA channels account for these damages,41,58,62 but also autoionization of TAs identified EELS59. When autoionization occurs, the autodetaching electron can transfer in the same, or to the other strand, and break a bond via DEA. If the detaching electron leaves the base in a dissociative electronic state, resulting from an n→π∗, π→σ∗ or π→π∗ transition,59 then BD can also 9



occurs, creating a double (i.e., clustered) lesion.

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Shao et al. proposed a unifying mechanism to

explain how the capture of a single LEE by a DNA base could produce isolated or clustered lesions, without a double collision within the same DNA, which is a much less probable process. However, their hypothesis assumed that the initial TAs are the same for all types of damages.44 The present results confirm this assumption and the postulated mechanism of damage, by the observation and identification of the TAs and their decay in all measurable destructive channels below 20 eV. The mechanism is briefly illustrated in Scheme 1. A LEE is first captured by a base, as shown theoretically63 below 3 eV, and experimentally up to 10 eV for long DNA strands64,65. The resulting TA can produce a single lesion (i.e., a BD or an abasic site) via DEA. Alternatively, if autoionization of the TA occurs, the base can be left intact or in a dissociative state. In either case, the autoionizing electron can transfer to another nearby site,63,64 where it could break another bond via DEA. Considering that a base lesion can transform into a SSB within the same strand,54 this simple initial process explains all observed damages. Only initial base dissociation or release from a neutral excited state can lead to a cluster damage, whose type depends on the autoionizing-electron receptor site (i.e., a base or a phosphate group). Owing to the possibility of electron transfer along the chains,66 that site can be located within 20 bp. Following autoionization at the initial TA site, the additional damage could be SSB or BD on the same or opposite strand. Among the simplest interstrand cluster damages, we find double BDs, a SSB with an adjacent BD and DSBs. We presented the most complete energy-dependence of the major DNA lesions induced by 220 eV electrons. Maxima in yield functions of single damages indicate the formation of core-excited TAs at 5 and 10 eV. Resonances are located at 6 and 10 eV in the case of cluster damages. The later could be correlated to cell death induced by LEE-damaged DNA. BDs were found to be major 10


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contributors to DNA lesions. All damages arise from the same initial core-excited TAs followed or not by electron transfer within DNA. The present results suggest that LEEs could efficiently induce different types of DNA clustered damages in cells, which are much more difficult to repair than individual isolated lesions. Supporting Information. Experimental procedures, yields of DNA damages with and without enzymes as a function of electron energies, table comparing energies of main decay channels of transient anions.

Acknowledgements. Financial support for this work was provided by the Canadian Institutes of Health Research (PJT162325), the State Key Laboratory of Photocatalysis on Energy and Environment (Fuzhou University, SKLPEE-2017B03) and the National Natural Science Foundation of China (21673044). The authors would like to thank Dr. Andrew Bass and Hakim Belmouaddine for constructive comments and corrections.

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Scheme 1. Diagram of the reaction pathways of a single LEE leading to all measured DNA damages. The electron (e-) is initially captured by a base, forming a core-excited transient anion (TA) (A). Dissociative electron attachment (DEA) to the base can produce a base damage (BD) (B). Alternatively, the additional electron can autodetach from the base anion and transfer to the phosphate group, where it can produce a SSB. When the autodetaching electron leaves the base in a dissociative state, the base is damaged, and multiple damages, whose type depend on the electron transfer pathway, become possible (B). Transfer to the opposite base can result in two adjacent BDs (C), whereas transfer to the phosphate unit in the same or opposite strand, can cause a strand break via C−O bond breakage (SSB via DEA + BD) (D) or a DSB, if the BD is converted to a strand break (E). Electron hopping between bases can create BDs or SSB farther away from the initial electron capture site.

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Fig. 1 Yields of inter-duplex crosslinks (■), BD-related inter-duplex crosslinks (●), isolated BD (▲) and non-DSB clustered damages (♦), as a function of electron energy. The dash lines indicate resonance peaks at 5 and 10 eV for all damages, apart from non-DSB cluster lesions, where the peak is located at 6 eV. The bands delineate the energies of core-excited TAs observed by electron stimulated desorption (ESD) and electron spectroscopy. The error bars represent the standard deviation in the measurement of the initial slope of fluence-response curves. Each of the 7 points of these response curves is the result of 8 independent measurements.

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Fig. 2. The inverted percentage curve (A) represents the transformation efficiency of JM109 E.coli cells. It was produced by irradiating with 0.5 to 22 eV electrons, PGEM3Zf(-) plasmids necessary for survival of these cells (reference 56). Yields of DNA damages induced by 2–20 eV electron impact on DNA films of 5-ML thickness, for formation of DSBs (B), non-DSB clustered damages (C), SSBs (D) and BDs (E). The bands delineate the energies of core-excited TAs observed by ESD and electron spectroscopy. The dash lines indicate the energies of prominent peaks at 5, 6 and 10 eV. The error bars in B to E represent the standard deviation in the measurement of the initial slope of fluence-response curves. Each of the 7 points of these response curves is the result of 8 independent measurements. Below 4 eV in B and C, no yield was detected above the error margin.

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Clustered DNA Damages Induced by 2-20 eV Electrons and Transient

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