Probing the effects of DNA-protein interactions on DNA hole transport: The N-terminal histone tails modulate the distribution of oxidative damage and chemical lesions in the nucleosome core particle

Biochemistry

Volumn 51, Issue 14, 2012, Pages 3129-3142

  Davis, William B ^a   Bjorklund, Chad C ^a   Deline, Marshall ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

8-OXOGUANINE; DNA-PROTEIN COMPLEXES; DNA-PROTEIN INTERACTION; GENOMIC DNA; GENOMIC REGIONS; GUANINE RADICALS; HISTONE OCTAMERS; HISTONE PROTEINS; HOLE TRANSPORTS; LOCAL ENVIRONMENTS; LOW SALT CONCENTRATION; N-TERMINALS; NAKED DNA; NUCLEOBASES; NUCLEOSOME CORE PARTICLES; NUCLEOSOMES; OXIDATIVE DAMAGE; POSITIVE CHARGES; SALT CONCENTRATION; SHARP INCREASE; STRUCTURAL CHANGE;

ASSOCIATION REACTIONS; GENES; HOLE MOBILITY; IONIC STRENGTH; OXYGEN; POSITIVE IONS; PROTEINS; SALT REMOVAL;

DNA;

8 HYDROXYGUANINE; DNA; GENOMIC DNA; HISTONE; NAKED DNA; PROTEIN DERIVATIVE;

AMINO TERMINAL SEQUENCE; ARTICLE; DNA DAMAGE; EUCHROMATIN; HETEROCHROMATIN; IONIC STRENGTH; MOLECULAR DYNAMICS; NUCLEOSOME; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DNA INTERACTION;

ANTHRAQUINONES; BINDING SITES; BIOLOGICAL TRANSPORT; CHROMATIN; COMPUTER SIMULATION; DNA; DNA-FORMAMIDOPYRIMIDINE GLYCOSYLASE; HISTONES; NUCLEOSOMES; OXIDATION-REDUCTION;

EUKARYOTA;

EID: 84859561107     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201734c     Document Type: Article

References (85)

1. Genereux, J. C., Boal, A. K., and Barton, J. K. (2010) DNA-mediated charge transport in redox sensing and signaling J. Am. Chem. Soc. 132, 891-905
2. Giese, B. (2002) Long-distance electron transfer through DNA Annu. Rev. Biochem. 71, 51-70
3. Schuster, G. B., Ed. (2004) Long-Range Charge Transfer in DNA, Vols. 236-237, Springer, Heidelberg, Germany.
4. Wagenknecht, H.-A., Ed. (2005) Charge Transfer in DNA, Wiley-VCH, Weinheim, Germany.
5. Berlin, Y. A., Burin, A. L., and Ratner, M. A. (2002) Elementary steps for charge transport in DNA: Thermal activation vs. tunneling Chem. Phys. 275, 61-74
6. Bixon, M. and Jortner, J. (2006) Shallow traps for thermally induced hole hopping in DNA Chem. Phys. 326, 252-258
7. O'Neill, M. A. and Barton, J. K. (2004) DNA Charge Transport: Conformationally Gated Hopping through Stacked Domains J. Am. Chem. Soc. 126, 11471-11483
8. Voityuk, A. A. (2009) Can Charge Transfer in DNA Significantly Be Modulated by Varying the π Stack Conformation? J. Phys. Chem. B 113, 14365-14368
9. Kubar, T. and Elstner, M. (2008) What governs the charge transfer in DNA? The role of DNA conformation and environment J. Phys. Chem. B 112, 8788-8798
10. Barnett, R. N., Cleveland, C. L., Joy, A., Landman, U., and Schuster, G. B. (2001) Charge Migration in DNA: Ion-Gated Transport Science 294, 567-571
11. Seidel, C. A. M., Schulz, A., and Sauer, M. H. M. (1996) Nucleobase-specific quenching of fluorescent dyes. 1. Nucleobase one-electron redox potentials and their correlation with static and dynamic quenching efficiencies J. Phys. Chem. 100, 5541-5553
12. Sistare, M. F., Codden, S. J., Heimlich, G., and Thorp, H. H. (2000) Effects of Base Stacking on Guanine Electron Transfer: Rate Constants for G and GG Sequences of Oligonucleotides from Catalytic Electrochemistry J. Am. Chem. Soc. 122, 4742-4749
13. Lewis, F. D., Liu, J. Q., Zuo, X. B., Hayes, R. T., and Wasielewski, M. R. (2003) Dynamics and Energetics of Single-Step Hole Transport in DNA Hairpins J. Am. Chem. Soc. 125, 4850-4861
14. Voityuk, A., Jortner, J., Bixon, M., and Rösch, N. (2000) Energetics of hole transfer in DNA Chem. Phys. Lett. 324, 430-434
15. Liu, C. S., Hernandez, R., and Schuster, G. B. (2004) Mechanism for radical cation transport in duplex DNA oligonucleotides J. Am. Chem. Soc. 126, 2877-2884
16. Osakada, Y., Kawai, K., Fujitsuka, M., and Majima, T. (2006) Charge transfer through DNA nanoscaled assembly programmable with DNA building blocks Proc. Natl. Acad. Sci. U.S.A. 103, 18072-18076
17. Misiaszek, R., Crean, C., Joffe, A., Geacintov, N. E., and Shafirovich, V. (2004) Oxidative DNA damage associated with combination of guanine and superoxide radicals and repair mechanisms via radical trapping J. Biol. Chem. 279, 32106-32115
18. Giese, B. and Spichty, M. (2000) Long Distance Charge Transport through DNA: Quantification and Extension of the Hopping Model ChemPhysChem 1, 195-198
19. Nunez, M. E., Holmquist, G. P., and Barton, J. K. (2001) Evidence for DNA charge transport in the nucleus Biochemistry 40, 12465-12471
20. Merino, E. J. and Barton, J. K. (2008) DNA oxidation by charge transport in mitochondria Biochemistry 47, 1511-1517
21. Merino, E. J., Davis, M. L., and Barton, J. K. (2009) Common mitochondrial DNA mutations generated through DNA-mediated charge transport Biochemistry 48, 660-666
22. Rajski, S. R. and Barton, J. K. (2001) How different DNA-binding protiens affect long-range oxidative damage to DNA Biochemistry 40, 5556-5564
23. Lee, P. E., Demple, B., and Barton, J. K. (2009) DNA-mediated redox signaling for transcriptional activation of SoxR Proc. Natl. Acad. Sci. U.S.A. 106, 13164-13168
24. Rajski, S. R., Kumar, S., Roberts, R. J., and Barton, J. K. (1999) Protein-mediated DNA electron transfer J. Am. Chem. Soc. 121, 5615-5616
25. Nakatani, K., Dohno, C., Ogawa, A., and Saito, I. (2002) Suppression of DNA-mediated charge transport by BamHI binding Chem. Biol. 9, 361-366
26. Boon, E. M., Pope, M. A., Williams, S. D., David, S. S., and Barton, J. K. (2002) DNA-mediated charge transport as a probe of MutY/DNA interaction Biochemistry 41, 8464-8470
27. Nunez, M. E., Noyes, K. T., and Barton, J. K. (2002) Oxidative charge transport through DNA in nucleosome core particles Chem. Biol. 9, 403-415
28. Bjorklund, C. C. and Davis, W. B. (2006) Attenuation of DNA charge transport by compaction into a nucleosome core particle Nucleic Acids Res. 34, 1836-1846
29. Bjorklund, C. C. and Davis, W. B. (2007) Stable DNA-protein cross-links are products of DNA charge transport in a nucleosome core particle Biochemistry 46, 10745-10755
30. Voityuk, A. A. and Davis, W. B. (2007) Hole Transfer Energetics in Structurally Distorted DNA: The Nucleosome Core Particle J. Phys. Chem. B 111, 2976-2985
31. Andrews, A. J. and Luger, K. (2011) Nucleosome structure(s) and stability: Variations on a theme Annu. Rev. Biophys. 40, 99-117
32. Grewal, S. I. and Moazed, D. (2003) Heterochromatin and epigenetic control of gene expression Science 301, 798-802
33. Zheng, C. and Hayes, J. J. (2003) Structures and interactions of the core histone tail domains Biopolymers 68, 539-546
34. Davis, W. B., Bjorklund, C. C., and Cho, P. S. (2010) Hole Transport Dynamics in Mixed Sequence DNA Can Vary with Salt Concentration: An Experimental and Theoretical Analysis J. Phys. Chem. C 114, 20821-20833
35. Margolin, Y. and Dedon, P. C. (2010) A general method for quantifying sequence effects on nucleobase oxidation in DNA Methods Mol. Biol. 610, 325-340
36. Gasper, S. M. and Schuster, G. B. (1997) Intramolecular photoinduced electron transfer to anthraquinones linked to duplex DNA: The effect of gaps and traps on long-range radical cation migration J. Am. Chem. Soc. 119, 12762-12771
37. Lowary, P. T. and Widom, J. (1998) New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning J. Mol. Biol. 276, 19-42
38. Hoch, D. A., Stratton, J. J., and Gloss, L. M. (2007) Protein-protein Forster resonance energy transfer analysis of nucleosome core particles containing H2A and H2A.Z J. Mol. Biol. 371, 971-988
39. Mangenot, S., Leforestier, A., Vachette, P., Durand, D., and Livolant, F. (2002) Salt-induced conformation and interaction changes of nucleosome core particles Biophys. J. 82, 345-356
40. Makde, R. D., England, J. R., Yennawar, H. P., and Tan, S. (2010) Structure of RCC1 chromatin factor bound to the nucleosome core particle Nature 467, 562-566
41. Vasudevan, D., Chua, E. Y., and Davey, C. A. (2010) Crystal structures of nucleosome core particles containing the '601' strong positioning sequence J. Mol. Biol. 403, 1-10
42. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD: Visual Molecular Dynamics J. Mol. Graphics 14, 33-38
43. Lu, X.-J. and Olson, W. K. (2003) 3DNA: A software package for the analysis, rebuilding and visualization of three-dimensional nucleic acid structures Nucleic Acids Res. 31, 5108-5121
44. Bohm, L., Briand, G., Sautiere, P., and Crane-Robinson, C. (1982) Proteolytic digestion studies of chromatin core-histone structure. Identification of limit peptides from histone H2B Eur. J. Biochem. 123, 299-303
45. Bohm, L., Briand, G., Sautiere, P., and Crane-Robinson, C. (1981) Proteolytic digestion studies of chromatin core-histone structure. Identification of a limit peptide of histone H3 and H4 Eur. J. Biochem. 119, 67-74
46. Bohm, L., Crane-Robinson, C., and Sautiere, P. (1980) Proteolytic digestion studies of chromatin core-histone structure. Identification of a limit peptide of histone H2A Eur. J. Biochem. 106, 525-530
47. Bertin, A., Leforestier, A., Durand, D., and Livolant, F. (2004) Role of histone tails in the conformation and interactions of nucleosome core particles Biochemistry 43, 4773-4780
48. Polach, K. J., Lowary, P. T., and Widom, J. (2000) Effects of core histone tail domains on the equilibrium constants for dynamic DNA site accessibility in nucleosomes J. Mol. Biol. 298, 211-223
49. Cadet, J., Douki, T., and Ravanat, J.-L. (2008) Oxidatively Generated Damage to the Guanine Moiety of DNA: Mechanistic Aspects and Formation in Cells Acc. Chem. Res. 41, 1075-1083
50. Reynisson, J. and Steenken, S. (2002) DFT calcultaions on the electrophillic reaction with water of the guanine and adenine radical cations. A model for the situation in DNA Phys. Chem. Chem. Phys. 4, 527-532
51. Yun, B. H., Lee, Y. A., Kim, S. K., Kuzmin, V., Kolbanovskiy, A., Dedon, P. C., Geacintov, N. E., and Shafirovich, V. (2007) Photosensitized oxidative DNA damage: From hole injection to chemical product formation and strand cleavage J. Am. Chem. Soc. 129, 9321-9332
52. Burrows, C. J. and Muller, J. G. (1998) Oxidative Nucleobase Modifications Leading to Strand Scission Chem. Rev. 98, 1109-1152
53. Cullis, P. M., Malone, M. E., and Merson-Davies, L. A. (1996) Guanine Radical Cations Are Precursors of 7,8-Dihydro-8-oxo-2′-deoxyguanosine but Are Not Precursors of Immediate Strand Breaks in DNA J. Am. Chem. Soc. 118, 2775-2781
54. Duarte, V., Gasparutto, D., Jaquinod, M., and Cadet, J. (2000) In vitro DNA synthesis opposite oxazolone and repair of this DNA damage using modified oligonucleotides Nucleic Acids Res. 28, 1555-1563
55. Spassky, A. and Angelov, D. (1997) Influence of the local helical conformation on the guanine modifications generated from one-electron DNA oxidation Biochemistry 36, 6571-6576
56. Spassky, A. and Angelov, D. (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
57. Kan, Y. and Schuster, G. B. (1999) Long-Range Guanine Damage in Single-Stranded DNA: Charge Transport through a Duplex Bridge and in a Single-Stranded Overhang J. Am. Chem. Soc. 121, 10857-10864
58. Henderson, P. T., Jones, D., Hampikian, G., Kan, Y., and Schuster, G. B. (1999) Long-distance charge transport in duplex DNA: The phonon-assisted polaron-like hopping mechanism Proc. Natl. Acad. Sci. U.S.A. 96, 8353-8358
59. Voityuk, A. A., Siriwong, K., and Rosch, N. (2004) Environmental fluctuations facilitate electron-hole transfer from guanine to adenine in DNA π stacks Angew. Chem., Int. Ed. 43, 624-627
60. Hatcher, E., Balaeff, A., Keinan, S., Venkatramani, R., and Beratan, D. N. (2008) PNA versus DNA: effects of structural fluctuations on electronic structure and hole transport mechanisms J. Am. Chem. Soc. 130, 11752-11761
61. Voityuk, A. A. (2008) Electronic couplings and on-site energies for hole transfer in DNA: Systematic quantum mechanical/molecular dynamic study J. Chem. Phys. 128, 115101
62. Troisi, A. and Orlandi, G. (2001) The hole transfer in DNA: Calculation of electron coupling between close bases Chem. Phys. Lett. 344, 509-518
63. Grozema, F. C., Tonzani, S., Berlin, Y. A., Schatz, G. C., Siebbeles, L. D., and Ratner, M. A. (2008) Effect of structural dynamics on charge transfer in DNA hairpins J. Am. Chem. Soc. 130, 5157-5166
64. van Stroe, A. J. and Janssen, L. J. J. (1993) Determination of the diffusion coefficient of oxygen in sodium chloride solutions with a transient pulse technique Anal. Chim. Acta 279, 213-219
65. Ju, L.-K. and Ho, C. S. (1985) Measuring oxygen diffusion coefficients with polarographic oxygen electrodes: I. Electrolyte solutions Biotechnol. Bioeng. 27, 1495-1499
66. Li, G., Levitus, M., Bustamante, C., and Widom, J. (2005) Rapid spontaneous accessibility of nucleosomal DNA Nat. Struct. Mol. Biol. 12, 46-53
67. Li, G. and Widom, J. (2004) Nucleosomes facilitate their own invasion Nat. Struct. Mol. Biol. 11, 763-769
68. Koopmans, W. J., Buning, R., Schmidt, T., and van Noort, J. (2009) spFRET using alternating excitation and FCS reveals progressive DNA unwrapping in nucleosomes Biophys. J. 97, 195-204
69. Wang, X. and Hayes, J. J. (2006) Physical methods used to study core histone tail structures and interactions in solution Biochem. Cell Biol. 84, 578-588
70. Smith, R. M. and Rill, R. L. (1989) Mobile histone tails in nucleosomes. Assignments of mobile segments and investigations of their role in chromatin folding J. Biol. Chem. 264, 10574-10581
71. Hill, C. S. and Thomas, J. O. (1990) Core histone-DNA interactions in sea urchin sperm chromatin. The N-terminal tail of H2B interacts with linker DNA Eur. J. Biochem. 187, 145-153
72. Ballestar, E., Boix-Chornet, M., and Franco, L. (2001) Conformational changes in the nucleosome followed by the selective accessibility of histone glutamines in the transglutaminase reaction: Effects of ionic strength Biochemistry 40, 1922-1929
73. Mutskov, V., Gerber, D., Angelov, D., Ausio, J., Workman, J., and Dimitrov, S. (1998) Persistent interactions of core histone tails with nucleosomal DNA following acetylation and transcription factor binding Mol. Cell. Biol. 18, 6293-6304
74. Cary, P. D., Moss, T., and Bradbury, E. M. (1978) High-resolution proton-magnetic-resonance studies of chromatin core particles Eur. J. Biochem. 89, 475-482
75. Ballestar, E. and Franco, L. (1997) Use of the transglutaminase reaction to study the dissociation of histone N-terminal tails from DNA in nucleosome core particles Biochemistry 36, 5963-5969
76. Baneres, J. L., Martin, A., and Parello, J. (1997) The N tails of histones H3 and H4 adopt a highly structured conformation in the nucleosome J. Mol. Biol. 273, 503-508
77. Lee, K. M. and Hayes, J. J. (1997) The N-terminal tail of histone H2A binds to two distinct sites within the nucleosome core Proc. Natl. Acad. Sci. U.S.A. 94, 8959-8964
78. Yang, Z., Zheng, C., and Hayes, J. J. (2007) The core histone tail domains contribute to sequence-dependent nucleosome positioning J. Biol. Chem. 282, 7930-7938
79. Hayes, J. J., Tullius, T. D., and Wolffe, A. P. (1990) The structure of DNA in a nucleosome Proc. Natl. Acad. Sci. U.S.A. 87, 7405-7409
80. Svoboda, P. and Harms-Ringdahl, M. (2005) Influence of chromatin structure and radical scavengers on yields of radiation-induced 8-oxo-dG and DNA strand breaks in cellular model systems Radiat. Res. 164, 303-311
81. Cloutier, J. F., Castonguay, A., O'Connor, T. R., and Drouin, R. (2001) Alkylating agent and chromatin structure determine sequence context-dependent formation of alkylpurines J. Mol. Biol. 306, 169-188
82. Uberbacher, E. C., Ramakrishnan, V., Olins, D. E., and Bunick, G. J. (1983) Neutron scattering studies of nucleosome structure at low ionic strength Biochemistry 22, 4916-4923
83. Eberharter, A. and Becker, P. B. (2002) Histone acetylation: A switch between repressive and permissive chromatin. Second in review series on chromatin dynamics EMBO Rep. 3, 224-229
84. Zheng, C. and Hayes, J. J. (2003) Intra- and inter-nucleosomal protein-DNA interactions of the core histone tail domains in a model system J. Biol. Chem. 278, 24217-24224
85. Menoni, H., Gasparutto, D., Hamiche, A., Cadet, J., Dimitrov, S., Bouvet, P., and Angelov, D. (2007) ATP-dependent chromatin remodeling is required for base excision repair in conventional but not in variant H2A.Bbd nucleosomes Mol. Cell. Biol. 27, 5949-5956