Radical Reaction Pathways Initiated by Direct Energy Deposition in DNA by Ionizing Radiation

Radical and Radical Ion Reactivity in Nucleic Acid Chemistry

Volumn , Issue , 2009, Pages 41-68

  Bernhard, William A ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Radical anions; Radical mobility, combination reactions and trapping; Radical reaction pathways and direct energy deposition in DNA by ionizing radiation

Indexed keywords

EID: 84862296202     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9780470526279.ch2     Document Type: Chapter

References (86)

1. Krisch, R. E.; Flick, M. B.; Trumbore, C. N. Radiation chemical mechanisms of singleand double-strand break formation in irradiated SV40 DNA. Radiat. Res. 1991, 126, 251-259.
2. Bernhard, W. A.; Purkayastha, S.; Milligan, J. R. Which DNA damage is likely to be relevant in hormetic responses? Dose-Response 2008, 6, 184-195.
3. Becker, D.; Sevilla, M. D. In Specialist Periodical Reports: Electron Paramagnetic Resonance; Gilbert, B. C., Ed.; The Royal Society of Chemistry: Cambridge, UK, 1998; Vol. 16; pp 79-115.
4. Bernhard, W. A.; Close, D. M. In Charged Particle and Photon Interactions with Matter; Mozumder, A.; Hatano, Y., Eds.; Marcel Dekker, New York, 2003, pp. 471-489.
5. Sevilla, M. D.; Bernhard, W. A. In Radiation Chemistry: From Basics to Applications in Material and Life Sciences; Spotheim-Maurizot, M., Mostafavi, M., Douki, T., Belloni, J., Eds.; EDP Sciences: Les Ulis, France, 2008; pp 191-202.
6. Sevilla, M. D.; Becker, D. In Specialist Periodical Reports: Electron Paramagnetic Resonance; Gilbert, B. C., Ed.; The Royal Society of Chemistry: Cambridge, UK, 2004; Vol. 19; pp 243-278.
7. Sevilla, M. D.; Engelhardt, M. L. Mechanisms for radiation damage in DNA constituents and DNA. Reactions of the N1-substituted thymine p-cation radicals. Faraday Discuss. Chem. Soc. 1977, 63, 255-263.
8. Spalletta, R. A.; Bernhard, W. A. Influence of primary structure on initial free radical products trapped in A:T polydeoxynucleotides x-irradiated at 4 K. Radiat. Res. 1993, 133, 143-150.
9. Bernhard, W. A. In Advances in Radiation Biology, Vol. 9; Lett, J. T.; Adler, H., Eds.; Academic Press, New York, 1981, pp. 199-280.
10. Steenken, S. Purine bases, nucleosides, and nucleotides: Aqueous solution redox chemistry and transformation reactions of their radical cations and e- and OH adducts. Chem. Rev. 1989, 89, 503-520.
11. Steenken, S. Structure, acid/base properties and transformation reaction of purine radicals. Free Radical Commun. 1989, 6, 117-120.
12. Steenken, S. Electron-transfer-induced acidity/basicity and reactivity changes of purine and pyrimidine bases. Consequences of redox processes for DNA base pairs. Free Radical Res. Commun. 1992, 16, 349-379.
13. Steenken, S. Electron transfer in DNA? Competition by ultra-fast proton transfer? Biol. Chem. 1997, 378, 1293-1297.
14. Colson, A. O.; Besler, B.; Sevilla, M. D. Ab initio molecular orbital calculations on DNA base pair radical ions: effect of base pairing on proton-transfer energies, electron affinities, and ionization potentials. J. Phys. Chem. 1992, 96, 9787-9794.
15. Wang, W.; Becker, D.; Sevilla, M. D. The influence of hydration on the absolute yields of primary ionic free radicals in g-irradiated DNA at 77 K. I. Total radical yields, Radiat. Res. 1993, 135, 146-154.
16. Becker, D.; Sevilla, M. D. In Advances in Radiation Biology; Lett, J. T., Sinclair, W. K., Eds.; Academic Press: San Diego, 1993; Vol. 17; pp 121-180.
17. Hildenbrand, K.; Schulte-Frohlinde, D. ESR spectra of radicals of single-stranded and double-stranded DNA in aqueous solution. Implications for . OH-induced strand breakage, Free Radical Res. Commun 1990, 11, 195-206.
18. Nelson, W. H.; Sagstuen, E.; Hole, E. O.; Close, D. M. On the proton transfer behavior of the primary oxidation product in irradiated DNA. Radiat. Res. 1992, 131, 10-17.
19. Swarts, S. G.; Becker, D.; Sevilla, M.; Wheeler, K. T. Radiation-induced DNAdamage as a function of hydration. II. Base damage from electron-loss centers, Radiat. Res. 1996, 145, 304-314.
20. Swarts, S. G.; Gilbert, D. C.; Sharma, K. K.; Razskazovskiy, Y.; Purkayastha, S.; Naumenko, K. A.; Bernhard, W. A. Mechanisms of direct radiation damage in DNA, based on a study of the yields of base damage, deoxyribose damage, and trapped radicals in d(GCACGCGTGC.2. Radiat. Res. 2007, 168, 367-381.
21. Close, D. M.; Nelson, W. H. ESR and ENDOR study of adenosine single crystals x-irradiated at 10 K. Radiat. Res. 1989, 117, 367-378.
22. Nelson, W. H.; Sagstuen, E.; Hole, E. O.; Close, D. M. Electron spin resonance and electron nuclear double resonance study of X-irradiated deoxyadenosine: Proton transfer behavior of primary ionic radicals. Radiat. Res. 1998, 149, 75-86.
23. Flossmann, W.; Mueller, A.; Westhof, E. Radicals in irradiated monocrystals of the basepair complex 9-ethyl adenine:1-methyl uracil, Int. J. Radiat. Biol. Relat. Stud. Phys., Chem. Med. 1974, 26, 481-492.
24. Hole, E. O.; Sagstuen, E.; Nelson, W. H.; Close, D. M. Free radical formation in single crystals of 9-methyladenine x-irradiated at 10 K. An electron paramagnetic resonance and electron nuclear double resonance study. Radiat. Res. 1995, 144, 258-265.
25. Hole, E. O.; Sagstuen, E.; Nelson, W. H.; Close, D. M. Free radical formation in X-irradiated crystals of 20-deoxycytidine hydrochloride. Electron magnetic resonance studies at 10 K. Radiat. Res. 2000, 153, 823-834.
26. Herak, J. N.; Krilov, D.; McDowell, C. A. ENDOR study of the stable radicals in g-or x-ray-irradiated single crystal of deoxycytidine-50-phosphate. J. Magn. Reson. 1976,23,1-7.
27. Weiland, B.;Hüttermann, J. Free radicals from x-irradiated "dry" and hydrated lyophilized DNA as studied by electron spin resonance spectroscopy: Analysis of spectral components between 77 K and room temperature, Int. J. Radiat. Biol. 1998, 74, 341-358.
28. Sharma, K. K.; Purkayastha, S.; Bernhard, W. A. Unaltered free base release from d(CGCGCG)2 produced by the direct effect of ionizing radiation at 4 K and room temperature. Radiat. Res. 2007, 167, 501-507.
29. Flossmann, W.; Westhof, E.; Mueller, A. Radical formation in salts of pyrimidines. III. Cytosine. H2Ocrystals, Int. J. Radiat. Biol. Relat. Stud. Phys., Chem. Med.1976,30,301-315.
30. Anderson, R. F.; Shinde, S. S.; Maroz, A. Cytosine-gated hole creation and transfer inDNA in aqueous solution, J. Am. Chem. Soc. 2006, 128, 15966-15967.
31. Sevilla, M. D. Electron spin resonance study of N1-substituted thymine p-cation radicals, J. Phys. Chem. 1976, 80, 1898-1901.
32. Schmidt, J. An ESR analysis of a heat-stable radical in gamma-irradiated single crystals of 1-methylthymine. J. Chem. Phys 1975, 62, 370-375.
33. Purkayastha, S.; Milligan, J. R.; Bernhard, W. A. The role of hydration in the distribution of free radical trapping in directly ionized DNA. Radiat. Res. 2006, 166, 1-8.
34. Ezra, F. S.; Bernhard, W. A. Electron spin resonance of g-irradiated salts of diethyl phosphoric acid. Radiat. Res. 1974, 60, 350-354.
35. Roginskaya, M.; Bernhard, W. A.; Marion, R. T.; Razskazovskiy, Y. The release of 5-methylene-2-furanone from irradiated DNA catalyzed by cationic polyamines and divalent metal cations. Radiat. Res. 2005, 163, 85-89.
36. Roginskaya, M.; Razskazovskiy, Y.; Bernhard, W. A. 2-deoxyribonolactone lesions in X-ray-irradiated DNA: Quantitative determination by catalytic 5-methylene-2-furanone release. Angew. Chem. Int. Ed. 2005, 44, 6210-6213.
37. Xue, L.; Greenberg, M. M. Use of fluorescence sensors to determine that 2-deoxyribonolactone is the major alkali-labile deoxyribose lesion produced in oxidatively damaged DNA. Angew. Chem. 2007, 119, 567-570.
38. Pogozelski, W. K.; Tullius, T. D. Oxidative strand scission of nucleic acids: Routes initiated by hydrogen abstraction from the sugar moiety. Chem. Rev. 1998, 98, 1089-1107.
39. Sharma, K. K. K.; Milligan, J. R.; Bernhard, W. A. Multiplicity of DNA single-strand breaks produced in pUC18 exposed to the direct effects of ionizing radiation. Radiat. Res. 2008, 170, 156-162.
40. Boudaiffa, B.; Hunting, D.; Cloutier, P.; Huels, M. A.; Sanche, L. Induction of single-and double-strand breaks in plasmidDNAby 100-1500 eVelectrons. Int. J. Radiat. Biol. 2000, 76, 1209-1221.
41. Huels, M. A.; Boudaiffa, B.; Cloutier, P.; Hunting, D.; Sanche, L. Single, double, and multiple double strand breaks induced in DNA by 3-100 eVelectrons. J. Am. Chem. Soc. 2003, 125, 4467-4477.
42. Purkayastha, S.; Milligan, J. R.; Bernhard, W. A. Correlation of free radical yields with strand break yields produced in plasmid DNA by the direct effect of ionizing radiation. J. Phys. Chem. B 2005, 109, 16967-16973.
43. Bernhard, W. A. Sites of electron trapping in DNA as determined by ESR of one-electron reduced oligonucleotides. J. Phys. Chem. 1989, 93, 2187-2189.
44. Wang, W.; Sevilla, M. D. Protonation of nucleobase anions in gamma-irradiated DNA and model systems. Which DNA base is the ultimate sink for the electron? Radiat. Res. 1994, 138, 9-17.
45. Yan, M.; Becker, D.; Summerfield, S.; Renke, P.; Sevilla, M. D. Relative abundance and reactivity of primary ion radicals in g-irradiated DNA at low temperatures. 2. Single-vs double-stranded DNA. J. Phys. Chem. 1992, 96, 1983-1989.
46. Hole, E. O.; Sagstuen, E.; Nelson, W. H.; Close, D. M. Primary reduction and oxidation of thymine derivatives: ESR/ENDOR of thymidine and 1-methylthymine x-irradiated at 10 K. J. Phys. Chem. 1991, 95, 1494-1503.
47. Sagstuen, E.; Hole, E. O.; Nelson, W. H.; Close, D. M. Radiation-induced free-radical formation in thymine derivatives: EPR/ENDOR of anhydrous thymine single crystals x-irradiated at 10 K. J. Phys. Chem. 1992, 96, 1121-1126.
48. Sagstuen, E.; Hole, E. O.; Nelson, W. H.; Close, D. M. Radiation damage to DNA base pairs. I. Electron paramagnetic resonance and electron nuclear double resonance study of single crystals of the complex 1-methylthymine.cntdot.9-methyladenine x-irradiated at 10 K. Radiat. Res. 1996, 146, 425-435.
49. Ormerod, M. G. Free radical formation in irradiated deoxyribonucleic acid, Int. J. Radiat. Biol. 1965, 9, 291-300.
50. Salovey, R.; Shulman, R. G.;Walsh, W. M., Jr. Electron spin resonance of irradiated DNA. J. Chem. Phys. 1963, 39, 839-840.
51. Sagstuen, E.; Hole, E. O.; Nelson, W. H.; Close, D. M. Protonation state of radiationproduced cytosine anions and cations in the solid state: EPR/ENDOR of cytosine monohydrate single crystals x-irradiated at 10 K. J. Phys. Chem. 1992, 96, 8269-8276.
52. Debije, M. G.; Bernhard, W. A. Thermally stable sites for electron capture in directly ionized DNA: Free radicals produced by the net gain of hydrogen at C5/C6 of cytosine and thymine in crystalline oligodeoxynucleotides. J. Phys. Chem. A 2002, 106, 4608-4615.
53. Debije, M. G.; Close, D. M.; Bernhard, W. A. Reductive damage in directly ionized DNA: saturation of the C51/4C6 bond of cytosine in dCGCG)2 crystals. Radiat. Res. 2002, 157, 235-242.
54. Goodhead, D. T. Initial events in the cellular effects of ionizing radiations: Clustered damage in DNA. Int. J. Radiat. Biol. 1994, 65, 7-17.
55. Ward, J. F. DNA damage produced by ionizing radiation in mammalian cells: Identities, mechanisms of formation, and reparability. Prog. Nucleic Acid Res. Mol. Biol. 1988, 35, 95-125.
56. Mozumder, A.; Magee, J. L. Theory of radiation chemistry. VII. Structure and reactions in low LET tracks. J. Chem. Phys 1966, 45, 3332-3341.
57. von Sonntag, C. The Chemical Basis of Radiation Biology; Taylor and Francis, New York, 1987.
58. Bernhard, W. A.; Mroczka, N.; Barnes, J. Combination is the dominant free radical process initiated in DNA by ionizing radiation: An overview based on solid-state EPR studies, Int. J. Radiat. Biol. 1994, 66, 491-497.
59. Wallace, S. S. Enzymic processing of radiation-induced free radical damage in DNA. Radiat. Res. 1998, 150, S60-S79.
60. Weinfeld, M.; Rasouli-Nia, A.; Chaudhry, M. A.; Britten, R. A. Response of base excision repair enzymes to complex DNA lesions. Radiat. Res. 2001, 156, 584-589.
61. Sevilla, M. D.; Becker, D. Radiation damage in DNA. Electron Spin Reson. 1994, 14, 130-165.
62. Spalletta, R. A.; Bernhard, W. A. Free radical yields in A:T polydeoxynucleotides, oligodeoxynucleotides, and monodeoxynucleotides at 4 K. Radiat. Res. 1992, 130, 7-14.
63. Barton, J. K. Photoinduced electron transfer through the double helix: IsDNAa wire? Proc. Robert A. Welch Found. Conf. Chem. Res. 1993, 37TH, 171-179.
64. Dandiliker, P. J.; Holmlin, R. E.; Barton, J. K. Oxidative thymine dimer repair in the DNA helix. Science 1997, 275, 1465-1468.
65. Kelley, S.; Barton, J. DNA-mediated electron transfer from a modified base to ethidium: p-stacking as a modulator of reactivity, Chem. Biol. 1998, 5, 413-425.
66. Debije, M. G.; Milano, M. T.; Bernhard, W. A. DNA responds to ionizing radiation as an insulator, not as a "molecular wire." Angew. Chem., Int. Ed. 1999, 38, 2752-2756.
67. Debije, M. G.; Bernhard, W. A. Free radical yields in crystalline DNA X-irradiated at 4 K, Radiat. Res. 1999, 152, 583-589.
68. Debije, M. G.; Bernhard, W. A. Electron and hole transfer induced by thermal annealing of crystalline DNA X-irradiated at 4 K, J. Phys. Chem. B 2000, 104, 7845-7851.
69. Debije, M. G.; Strickler, M. D.; Bernhard, W. A. On the efficiency of hole and electron transfer from the hydration layer toDNA: An EPR study of crystallineDNAX-irradiated at 4 K. Radiat. Res. 2000, 154, 163-170.
70. Giese, B. Electron transfer in DNA. Curr. Opin. Chem. Biol. 2002, 6, 612-618.
71. Schuster, G. B. Long-range charge transfer inDNA: Transient structural distortions control the distance dependence. Acc. Chem. Res. 2000, 33, 253-260.
72. Cai, Z.; Gu, Z.; Sevilla, M. D. Electron spin resonance study of the temperature dependence of electron transfer inDNA: Competitive processes of tunneling, protonation at carbon, and hopping. J. Phys. Chem. B 2000, 104, 10406-10411.
73. Cai, Z.; Sevilla, M. D. Electron Spin Resonance Study of Electron Transfer in DNA: Inter-Double-Strand Tunneling Processes, J. Phys. Chem. B 2000, 104, 6942-6949.
74. Cai, Z.; Gu, Z.; Sevilla, M. D. Electron spin resonance study of electron and hole transfer in DNA: Effects of hydration, aliphatic amine cations, and histone proteins. J. Phys. Chem. B 2001, 105, 6031-6041.
75. Cai, Z.; Li, X.; Sevilla, M. D. Excess electron transfer inDNA: Effect of base sequence and proton transfer. J. Phys. Chem. B 2002, 106, 2755-2762.
76. Cai, Z.; Sevilla, M. D. Electron and hole transfer from DNA base radicals to oxidized products of guanine in DNA. Radiat. Res. 2003, 159, 411-419.
77. Cai, Z.; Sevilla, M. D. In Long Range Transfer in DNA, Vol. II; Shuster, G., Ed.; Springer-Verlag, New York, 2004, Vol. 237 of Topics in Current Chemistry, pp. 103-128.
78. Messer, A.; Carpenter, K.; Frozley, K.; Buchanan, J.; Yang, S.; Razskazovskii, Y.; Cai, Z.; Sevilla, M. Electron spin resonance study of electron transfer rates in DNA: Determination of the tunneling constant b for single-step excess electron transfer. J. Phys. Chem. B 2000, 104, 1128-1136.
79. Shafirovich, V.; Dourandin, A.; Geacintov, N. E. Proton-coupled electron-transfer reactions at a distance in DNA duplexes: Kinetic deuterium isotope effect. J. Phys. Chem. B 2001, 105, 8431-8435.
80. Barton, J. K. DNA-mediated electron transfer: Chemistry at a distance. Pure Appl. Chem. 1998, 70, 873-879.
81. Odom, D. T.; Barton, J. K. Long-range oxidative damage inDNA/RNAduplexes. Biochem. 2001, 40, 8727-8737.
82. Ly, A.; Bullick, S.;Won, J.-H.; Milligan, J. R. Cationic peptides containing tyrosine protect against radiation-induced oxidative DNA damage. Int. J. Radiat. Biol. 2006, 82, 421-433.
83. Giese, B.; Spichty, M.; Wessely, S. Long-distance charge transport through DNA. An extended hopping model. Pure Appl. Chem. 2001, 73, 449-453.
84. Purkayastha, S.; Bernhard, W. A. What is the initial chemical precursor of DNA strand breaks generated by direct-type effects? J. Phys. Chem. B 2004, 108, 18377-18382.
85. Purkayastha, S.; Milligan, J. R.; Bernhard, W. A. An investigation into the mechanisms of DNA strand breakage by direct ionization of variably hydrated plasmid DNA. J. Phys. Chem. B 2006, 110, 26286-26291.
86. Purkayastha, S.; Milligan, J. R.; Bernhard, W. A. On the chemical yield of base lesions, strand breaks, and clustered damage generated in plasmid DNA by the direct effect of X rays. Radiat. Res. 2007, 168, 357-366.