Origin of the heterogeneous distribution of the yield of guanyl radical in UV laser photolyzed DNA

Biophysical Journal

Volumn 88, Issue 4, 2005, Pages 2766-2778

  Angelov, Dimitar ^a,b   Beylot, Benedicte ^a   Spassky, Annick ^a  

^a Ecole Normale Superieure de Cachan   (France)

^b INSTITUTE OF SOLID STATE PHYSICS   (Bulgaria)

Author keywords

[No Author keywords available]

Indexed keywords

BUFFER; DNA; DNA FORMAMIDOPYRIMIDINE GLYCOSYLASE; DOUBLE STRANDED DNA; EDETIC ACID; GUANYL RADICAL; HYDROCHLORIC ACID; NUCLEIC ACID BASE; OLIGOMER; OXAZOLONE; PIPERIDINE DERIVATIVE; RADICAL; SINGLE STRANDED DNA; SODIUM CHLORIDE; UNCLASSIFIED DRUG;

ARTICLE; DNA STRUCTURE; IONIZATION; LASER; MODEL; OXIDATION; PARAMETER; PHOTOLYSIS; QUANTUM MECHANICS; RADIATION ENERGY; ROOM TEMPERATURE; SPECTROPHOTOMETRY; STRUCTURE ANALYSIS; TEMPERATURE DEPENDENCE; ULTRAVIOLET RADIATION;

EID: 22144434798     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.104.049015     Document Type: Article

References (75)

1. Abdurashidova, G., M. B. Danailov, A. Ochem, G. Triolo, V. Djeliova, S. Radulescu, A. Vindigly, S. Riva, and A. Filaschi. 2003. Localization of protein bound to replication origin of human DNA along the cell cycle. EMBO J. 22:4294-4303.
2. Angelov, D., M. Charra, C. W. Müller, J. Cadet, and S. Dimitrov. 2003. Solution study of the NF-κB p50-DNA complex by UV laser protein-DNA cross-linking. Photochem. Photobiol. 77:592-596.
3. Angelov, D., M. Charra, M. Seve, J. Côté, S. Khochbin, and S. Dimitrov. 2000. Differential remodeling of the HIV-1 nucleosome upon transcription activators and SWI/SNF complex binding. J. Mol. Biol. 302:315-326.
4. Angelov, D., F. Lenouvel, F. Hans, C. V. Müller, P. Bouvet, E. Moudrianakis, J. Cadet, and S. Dimitrov. 2004. The histone octamer is "invisible" when NF-κB binds to the nucleosome. J. Biol. Chem. 279:42374-42382.
5. Angelov, D., E. Novakov, S. Khochbin, and S. Dimitrov. 1999. Ultraviolet laser footprinting of histone H1(0)-four-way junction DNA complexes. Biochemistry. 38:11333-11339.
6. Angelov, D., A. Spassky, M. Berger, and J. Cadet. 1997. High-intensity UV laser photolysis of DNA and purine 2′-deoxyribonucleosides: formation of 8-oxopurine damage and oligonucleotide strand cleavage as revealed by HPLC and gel electrophoresis studies. J. Am. Chem. Soc. 119:11373-11380.
7. Angelov, D., J. M. Vitolo, V. Mutskov, S. Dimitrov, and J. Hayes. 2001. Preferential interaction of the core histone tail domains with linker DNA. Proc. Natl. Acad. Sci. USA. 98:6599-6604.
8. Becker, M. M., D. Lesser, M. Kurpiewsky, A. Baranger, and L. Jen-Jacobsen. 1988. Ultraviolet footprinting accurately maps sequence-specific contacts and DNA kinking in Eco RI endonuclease-DNA complex. Proc. Natl. Acad. Sci. USA. 85:6247-6251.
9. Becker, D., and M. D. Sevilla. 1993. The chemical consequences of radiation damage to DNA. Adv. Radiat. Biol. 17:121-180.
10. Becker, M. M., and J. C. Wang. 1984. Use of light for footprinting DNA in vivo. Nature. 309:682-687.
11. Beylot, B. 1998. PhD thesis. University Paris VI, Paris, France.
12. Beylot, B., and A. Spassky. 2001. Chemical probing shows that the intron-encoded endonuclease 1-SceI distorts DNA through binding in monomeric form to its homing site. J. Biol. Chem. 276:25243-25253.
13. Bixon, M., B. Giese, S. Wessely, T. Langenbacher, M. E. Michel-Beyerle, and J. Iortner. 1999. Long-range charge hopping in DNA. Proc. Natl. Acad. Sci. USA. 96:11713-11716.
14. Breslin, D. T., and G. B. Schuster. 1996. Anthraquinone photonucleases: mechanisms for GG-selective and nonselective cleavage of double-stranded DNA. J. Am. Chem. Soc. 118:2311-2319.
15. Bruisnma, R., G. Grüner, M. R. D'Orsogna, and J. Rudnick. 2000. Fluctuation-facilitated charge migration along DNA. Phys. Rev. Lett. 85:4393-4396.
16. Burrows, C. J., and J. Muller. 1998. Oxidative nucleobase modifications leading to strand scission. Chem. Rev. 98:1109-1151.
17. Cadet, J., and P. Vigny. 1990. The photochemistry of nucleic acids. In Bioorganic Photochemistry. H. Morrison, editor. John Wiley & Sons, Hoboken, NJ. 1-272.
18. Candeias, L. P., P. O'Neill, G. D. D. Jones, and S. Steenken. 1992. lonization of polynucleotides and DNA in aqueous solution by 193 nm pulsed laser light: identification of base-derived radicals. Int. J. Radiat. Biol. 61:15-20.
19. Candeias, L. P., and S. Steenken. 1993. Electron transfer in di(deoxy) nucleoside phosphates in aqueous solution: rapid migration of oxidative damage (via adenine) to guanine. J. Am. Chem. Soc. 115:2437-2440.
20. Colleaux, L., L. D'Auriol, F. Galibert, and B. Dujon. 1988. Recognition and cleavage site of the intron-encooled omega transposase. Proc. Natl. Acad. Sci. USA. 85:6022-6026.
21. Conwell, E. M., and S. V. Rakhmanova. 2000. Polarons in DNA. Proc. Natl. Acad. Sci. USA. 97:4556-4560.
22. Croke, D. T., W. Blau, C. OhUigin, J. M. Kelly, and D. J. McConnell. 1988. Photolysis of phosphodiester bond in plasmid DNA by high-intensity UV laser irradiation. Photochem. Photobiol. 47:527-536.
23. Cullis, P. M., M. E. Malone, and L. A. Merson-Davies. 1996. Guanine radical cations are precursors of 7,8-dihydro-8oxo-2′-deoxyguanosine but are not precursors of immediate strand breaks in DNA. J. Am. Chem. Soc. 118:2775-2781.
24. Dandliker, P. J., R. E. Holmlin, and J. K. Barton. 1997. Oxidative thymine dimer repair in the DNA helix. Science. 275:1465-1468.
25. Douki, T., D. Angelov, and J. Cadet. 2001. UV laser photolysis of DNA: effect of duplex stability on charge-transfer efficiency. J. Am. Chem. Soc. 123:11360-11366.
26. Douki, T., and J. Cadet. 1999. Modification of DNA bases by photosensitized one-electron oxidation. Int. J. Radiat. Biol. 75:571-581.
27. Douki, T., J.-L. Ravanat, D. Angelov, J. R. Wagner, and J. Cadet. 2004. Effects of duplex stability on charge transfer efficiency within DNA. Top. Curr. Chem. 236:1-25.
28. Eisinger, J., and A. A. Lamola. 1971. The excited state of nucleic acids. In Excited States of Proteins and Nucleic Acids. R. F. Steiner and I. Weinryb, editors. Plenum Press, New York. 107-198.
29. Fukui, K., and K. Tanaka. 1998. Distance dependence of photoinduced electron transfer in DNA. Angew. Chem. Int. Ed. Engl. 37:158-161.
30. Georghiou, S., S. Zhu, R. Weidner, C.-R. Huang, and G. Ge. 1990. Singlet-singlet energy transfer along the helix of a double-stranded nucleic acid at room temperature. J. Biomol. Struct. Dyn. 8:657-674.
31. Giese, B. 2002. Electron transfer in DNA. Curr. Opin. Chem. Biol. 6:612-618.
32. Giese, B., S. Wessely, M. Spormann, U. Lindemann, E. Meggers, and M. E. Michel-Beyerle. 1999. On the mechanism of long-range electron transfer through DNA. Angew. Chem. Int. Ed. Engl. 38:996-998.
33. Görner. H. 1994. Photochemistry of DNA and related biomolecules: quantum yield and consequences of photoionization. Photochem. Photobiol. 26:117-139.
34. Gregoli, S., M. Olast, and A. Bertinchamps. 1979. Charge migration phenomena in γ-irradiated costacking complexes of DNA nucleotides. II. An ESR study of various complexes in frozen solution. Radiat. Res. 77:417-431.
35. Guéron, M., J. Eisinger, and R. G. Shulman. 1967. Excited states of nucleotides and singlet energy transfer in polynucleotides. J. Chem. Phys. 47:4077-4091.
36. Guéron, M., and R. G. Shulman. 1968. Energy transfer in polynucleotides. Annu. Rev. Biochem. 37:571-596.
37. Guillo, L. A., B. Beylot, P. Vigny, and A. Spassky. 1996. Formation of cyclobutane thymine dimers from UVA photosensitization of pyridopsoralen monoadducted DNA. Photochem. Photobiol. 64:349-355.
38. Hall, D. B., R. E. Holmlin, and J. K. Barton. 1996. Oxidative DNA damage through long-range electron transfer. Nature. 382:731-735.
39. Hall, D. B., S. O. Kelly, and J. K. Barton. 1998. Long-range and short-range oxidative damage to DNA: photoinduced damage to guanines in ethidium-DNA assemblies. Biochemistry. 37:15933-15940.
40. Henderson, P. T., D. Jones, G. Hampikian, Y. Kan, and G. Schuster. 1999. Long-distance charge transport in duplex DNA: the phonon-assisted polaron-like hopping mechanism. Proc. Natl. Acad. Sci. USA. 96:8353-8358.
41. Hush, N. S., and A. S. Cheung. 1975. Ionization potentials and donor properties of nucleic acid bases and related compounds. Chem. Phys. Lett. 34:11-13.
42. Isenberg, I., R. Rosenbluth, and S. L. Baird, Jr. 1967. Comparative phosphorescence quenching of DNAs of different composition. Biophys. J. 7:365-373.
43. Jortner, J., M. Bixon, T. Langenbacher, and M. E. Michel-Beyerle. 1998. Charge transfer and transport in DNA. Proc. Natl. Acad. Sci. USA. 95:12759-12765.
44. Kang, H., K. T. Lee, B. Jung, Y. J. Ko, and S. K. Kim. 2002. Intrinsic lifetimes of the excited states of DNA and RNA bases. J. Am. Chem. Soc. 124:12958-12959.
45. Kasai, H., Z. Yamaizumi, M. Berger, and J. Cadet. 1992. Photosensitized formation of 7,8-dihydro-8-oxo-2′-deoxyguanosine (8-hydroxy-2′- deoxyguanosine) in DNA by riboflavin: a non singlet oxygen mediated reaction. J. Am. Chem. Soc. 114:9692-9694.
46. Kelley, S., and J. K. Barton. 1999. Electron transfer between bases in double helical DNA. Science. 283:375-381.
47. Kelley, S. O., R. E. Holmlin, E. D. A. Stemp, and J. K. Barton. 1997. Photoinduced electron transfer in ethidium-modified DNA duplexes: dependence on distance and base stacking. J. Am. Chem. Soc. 119:9861-9870.
48. Kovalsky, O. I., I. G. Panyutin, and E. I. Budowsky. 1990. Sequence-specificity of the alkali-sensitive lesions induced in DNA by high-intensity ultraviolet laser radiation. Photochem. Photobiol. 52:509-517.
49. Ly, D., L. Sanii, and G. B. Schuster. 1999. Mechanism of charge transport in DNA: internally-linked anthraquinone conjugates support phonon-assisted polaron hopping. J. Am. Chem. Soc. 121:9400-9410.
50. Malone, M. E., M. C. R. Symons, and A. W. Parker. 1994. DNA in glasses at 77 K: high energy ionizing radiation versus UV electron ejection. Int. J. Radiat. Biol. 66:511-515.
51. Meggers, E., M. E. Michel-Beyerle, and B. Giese. 1998. Sequence dependent long range hole transport in DNA. J. Am. Chem. Soc. 120:12950-12955.
52. Melvin, T., S. Botchway, A. W. Parker, and P. O'Neill. 1996. Migration of photo-induced oxidative damage in models for DNA. J. Am. Chem. Soc. 118:10031-10036.
53. Melvin, T., S. M. T. Cunnifre, P. O'Neill, A. W. Parker, and T. Roldan-Arjona. 1998. Guanine is the target for direct ionization damage in DNA, as detected using excision enzymes. Nucleic Acids Res. 26:4935-4942.
54. Melvin, T., M. A. Plumb, S. W. Botchway, P. O'Neill, and A. W. Parker. 1995. 193 nm light induced single strand breakage of DNA predominantly at guanine. Photochem. Photobiol. 61:584-591.
55. Mutskov, V., D. Gerber, D. Angelov, J. Ausio, J. Workman, and S. Dimitrov. 1998. Persistent interactions of core histone tails with nucleosomal DNA following acetylation and transcription factor binding. Mol. Cell. Biol. 18:6293-6304.
56. Nagaich, A. K., D. A. Walker, R. Wolford, and G. L. Hager. 2004. Rapid periodic binding and displacement of the glucocorticoid receptor during chromatin remodeling. Mol. Cell. 14:163-174.
57. Nakatani, K., J. Shirai, S. Sando, and I. Saito. 1997. Guanine specific DNA cleavage by photoirradiation of dibenzoyldiazomethane-oligonucleotide conjugates. J. Am. Chem. Soc. 119:7626-7635.
58. Nikogosyan, D. N. 1990. Two-quantum photochemistry of nucleic acids: comparison with conventional low-intensity UV photochemistry and radiation chemistry. Int. J. Radiat. Biol. 37:233-299.
59. Nikogosyan, D. N., D. A. Angelov, and A. A. Oraevsky. 1982. Determination of parameters of excited states of DNA and RNA bases by laser UV photolysis. Photochem. Photobiol. 35:627-635.
60. Nikogosyan, D. N., and V. S. Letokhov. 1983. Nonlinear laser photophysics, photochemistry and photobiology of nucleic acids. Riv. Nuovo Cimento. Soc. Ital. 6:1-74.
61. Nikogosyan, D. N., A. A. Oraevsky, and V. S. Letokhov. 1985. Two-step picosecond UV excitation of polynucleotides and energy transfer. Chem. Phys. 97:31-34.
62. O'Neill, P., and M. Fielden. 1994. Primary free radical processes in DNA. Adv. Radiat. Biol. 17:53-121.
63. Orlov, V. M., A. N. Smirnov, and Y. M. Varshavski. 1976. Ionization potentials and electron-donor ability of nucleic acid bases and their analogs. Tetrahedron Lett. 48:4377-4378.
64. Pashev, I. G., S. I. Dimitrov, and D. Angelov. 1991. Cross-linking proteins to nucleic acids by ultraviolet laser irradiation. Trends Biochem. Sci. 16:323-326.
65. Ravanat, J.-L., M. Berger, S. Boiteux, J. Lavai, and J. Cadet. 1993. Excision of 7,8-dihydro 8-oxoguanine from DNA by the Fpg protein. J. Chem. Phys. 90:871-879.
66. Russmann, C., M. Truss, A. Fix, C. Naumer, T. Hermann, J. Schmitt, J. Stollhoff, R. Beigang, and M. Beato. 1997. Crosslinking of progesterone receptor to DNA using tunable nanosecond, picosecond and femtosecond UV laser pulses. Nucleic Acids Res. 25:2478-2484.
67. Saito, I., M. Takayama, H. Sugiyama, and K. Nakatani. 1995. Photoinduced DNA cleavage via electron-transfer: demonstration that guanine residues located 5′ to guanine are the most electron-donating sites. J. Am. Chem. Soc. 117:6406-6407.
68. Schlag, E. W., D.-Y. Yang, S.-Y. Sheu, H. L. Selzle, S. H. Lin, and P. M. Rentzepis. 2000. Dynamical principles in biological processes: a model of charge migration in proteins and DNA. Proc. Natl. Acad. Sci. USA. 97:9849-9854.
69. Spassky, A., and D. Angelov. 1997. Influence of the local helical conformation on the guanine modifications generated from one-electron DNA oxidation. Biochemistry. 36:6571-6576.
70. Spassky, A., and D. Angelov. 2002. Temperature-dependence of UV laser one electron oxidative guanine modifications as a probe of local stacking fluctuations and conformational transitions. J. Mol. Biol. 323:9-15.
71. Vigny, P., and J.-P. Ballini. 1977. Excited states of nucleic acids at 300 K and electronic energy transfer. In Excited States in Organic Chemistry and Biochemistry. B. Pullman and N. Goldblum, editors. D. Riedel, Boston, MA. 1-13.
72. Voityuk, A., J. Jortner, M. Bixon, and M. Rösch. 2000. Energetics of hole transfer in DNA. Chem. Phys. Lett. 324:430-434.
73. Wan, C. Z., T. Fiebig, S. O. Kelley, C. R. Treadway, J. K. Barton, and A. H. Zewail. 1999. Femtosecond dynamics of DNA-mediated electron transfer. Proc. Natl. Acad. Sci. USA. 96:6014-6019.
74. Wan, C. Z., T. Fiebig, O. Schiemann, J. K. Barton, and A. H. Zewail. 2000. Femtosecond direct observation of charge transfer between bases in DNA. Proc. Natl. Acad. Sci. USA. 97:14052-14055.
75. Yoshioka, Y., Y. Kitagawa, Y. Takano, K. Yamaguchi, T. Nakamura, and I. Saito. 1999. Experimental and theoretical studies on the selectivity of GGG triplets toward one-electron oxidation in B-form DNA. J. Am. Chem. Soc. 121:8712-8719.