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Abstract

Most of the energy deposited in cells by ionizing radiation is channeled into the production of abundant free secondary electrons with ballistic energies between 1 and 20 electron volts. Here it is shown that reactions of such electrons, even at energies well below ionization thresholds, induce substantial yields of single- and double-strand breaks in DNA, which are caused by rapid decays of transient molecular resonances localized on the DNA's basic components. This finding presents a fundamental challenge to the traditional notion that genotoxic damage by secondary electrons can only occur at energies above the onset of ionization, or upon solvation when they become a slowly reacting chemical species.

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REFERENCES AND NOTES

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J. F. Ward, in Advances in Radiation Biology 5, J. T. Lett and H. Adler, Eds. (Academic Press, New York, 1977), pp. 181–239.
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O. Yamamoto, in Aging, Carcinogenesis and Radiation Biology, K. Smith, Ed. (Plenum, New York, 1976), pp. 165–192.
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A. F. Fuciarelli and J. D. Zimbrick, Eds., Radiation Damage in DNA: Structure/Function Relationships at Early Times (Battelle, Columbus, OH, 1995).
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C. von Sonntag, The Chemical Basis for Radiation Biology (Taylor and Francis, London, 1987).
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International Commission on Radiation Units and Measurements, ICRU Report 31 (ICRU, Washington, DC, 1979).
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S. M. Pimblott and J. A. LaVerne, in (3), pp. 3–12.
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D. Srdoc et al., in IAEA CRP Atomic and Molecular Data for Radiotherapy and Radiation Research, M. Inokuti, Ed. (IAEA Press, Vienna, 1995), chapter 8.
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The only previous low-energy work concerned DNA damage by 25- to 4000-eV electrons [see
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]. In that study, the samples were exposed to high background gas pressures (10−5 to 10−6 torr) and contained salt (EDTA, ratio of DNA to EDTA = 1:1 by weight) during electron irradiation; the latter was reported to shield the DNA toward low-energy electrons.
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Huels M. A., Parenteau L., Sanche L., J. Chem. Phys. 100, 3940 (1994).
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For a review, see
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16
Each sample consisted of 500 ng of purified DNA in 10 μl of nanopure water, which was deposited on a tantalum substrate over a measured area of ∼6 mm average diameter. After lyophilization, this results in a pure solid calculated to have an average thickness of 10 nm at a known density of 1.7 g cm−3, assuming minimal clustering of the plasmids in the solid.
17
Desiccation leaves plasmid DNA with its structural water of about 2.5 water molecules per base pair [
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], with the plasmid solids containing a mixture of A and C conformations. Removal of this intrinsic hydration water is believed to lead to substantial conformational changes and DSBs, which are not observed in our unirradiated control samples held under UHV.
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B. D. Michael et al., in (3), pp. 251–258.
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For a review, see
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For vertical electron attachment energies in gas-phase nucleobases below 5 eV, see
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Sieger M. T., Simpson W. C., Orlando T. M., Nature 394, 554 (1998).
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L. G. Christophorou, E. Illenberger, W. Schmidt, Eds., Linking the Gaseous and Condensed Phases of Matter: The Behavior of Slow Electrons (Plenum, New York, 1994).
29
Sample exposure-response curves can be seen at Science Online (www.sciencemag.org/feature/data/1044957.shl).
30
We thank A. J. Waker for helpful comments and suggestions. Supported by the Medical Research Council of Canada.

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Published In

Science
Volume 287 | Issue 5458
3 March 2000

Submission history

Received: 30 August 1999
Accepted: 7 January 2000
Published in print: 3 March 2000

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Authors

Affiliations

Badia Boudaı̈ffa
Canadian Medical Research Council Group in Radiation Sciences, Department of Nuclear Medicine and Radiobiology, Faculty of Medicine, University of Sherbrooke, Québec J1H 5N4, Canada.
Pierre Cloutier
Canadian Medical Research Council Group in Radiation Sciences, Department of Nuclear Medicine and Radiobiology, Faculty of Medicine, University of Sherbrooke, Québec J1H 5N4, Canada.
Darel Hunting
Canadian Medical Research Council Group in Radiation Sciences, Department of Nuclear Medicine and Radiobiology, Faculty of Medicine, University of Sherbrooke, Québec J1H 5N4, Canada.
Michael A. Huels*
Canadian Medical Research Council Group in Radiation Sciences, Department of Nuclear Medicine and Radiobiology, Faculty of Medicine, University of Sherbrooke, Québec J1H 5N4, Canada.
Léon Sanche
Canadian Medical Research Council Group in Radiation Sciences, Department of Nuclear Medicine and Radiobiology, Faculty of Medicine, University of Sherbrooke, Québec J1H 5N4, Canada.

Notes

*
To whom correspondence should be addressed. E-mail: [email protected]

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