DNA−Protein Cross-Linking via Guanine Oxidation: Dependence upon Protein and Photosensitizer
Abstract
DNA-protein cross-links form when guanine undergoes a 1-electron oxidation in a flash-quench experiment, and the importance of reactive oxygen species, protein, and photosensitizer is examined here. In these experiments, a strong oxidant produced by oxidative quenching of a DNA-bound photosensitizer generates an oxidized guanine base that reacts with protein to form the covalent adduct. These cross-links are cleaved by hot piperidine and are not the result of reactive oxygen species, since neither a hydroxyl radical scavenger (mannitol) nor oxygen affects the yield of DNA-histone cross-linking, as determined via a chloroform extraction assay. The cross-linking yield depends on protein, decreasing as histone > cytochrome c > bovine serum albumin. The yield does not depend on the cytochrome oxidation state, suggesting that reduction of the guanine radical by ferrocytochrome c does not compete effectively with cross-linking. The photosensitizer strongly influences the cross-linking yield, which decreases in the order Ru(phen)(2)dppz(2+) [phen = 1,10-phenanthroline; dppz = dipyridophenazine] > Ru(bpy)(3)(2+) [bpy = 2,2'-bipyridine] > acridine orange > ethidium, in accordance with measured oxidation potentials. A long-lived transient absorption signal for ethidium dication in poly(dG-dC) confirms that guanine oxidation is inefficient for this photosensitizer. From a polyacrylamide sequencing gel of a (32)P-labeled 40-mer, all of these photosensitizers are shown to damage guanines preferentially at the 5' G of 5'-GG-3' steps, consistent with a 1-electron oxidation. Additional examination of ethidium shows that it can generate cross-links between histone and plasmid DNA (pUC19) and that the yield depends on the quencher. Altogether, these results illustrate the versatility of the flash-quench technique as a way to generate physiologically relevant DNA-protein adducts via the oxidation of guanine and expand the scope of such cross-linking reactions to include proteins that may associate only transiently with DNA.
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Independent proofs support covalent attachment of nucleophilic amino acids to guanine radical cation upon one-electron oxidation of oligonucleotides mediated by Type I photosensitizer, flash quench, or biphotonic ionization.
“Other independent proofs that support the covalent attachment of nucleophilic amino acids to Gua •+ upon one-electron oxidation of oligonucleotides mediated by a Type I photosensitizer, the flash quench technique or biphotonic ionization, are available (219-222).”
From Photoinduced Damage to Cellular DNA: Direct and Photosensitized Reactions<sup>†</sup> (2012) · cites this paper as [219]
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- Authors
- Kurbanyan, K., Nguyen, K. L., To, P., Rivas, E. V., Lueras, A. M. K., Kosinski, C., Steryo, M., González, A., Mah, D. A., & Stemp, E. D. A.
- Affiliations
- Mount St. Mary's University (US)
- ORCID
- Stemp, Eric D. A.
- Venue
- Biochemistry
- Publisher
- American Chemical Society (ACS)
- Published
- 2003-08-05
- Volume
- 42
- Issue
- 34
- Pages
- 10269-10281
- ISSN
- 0006-2960 (ISSN-L)
- 1520-4995
- OpenAlex
- W2001111321
- Cited by
- 53
- References
- 107
- Citations by year
- 2026: 1 · 2025: 2 · 2023: 1 · 2022: 1 · 2021: 1 · 2020: 2 · 2019: 3 · 2018: 2 · 2017: 2 · 2016: 3 · 2015: 1 · 2014: 3 · 2013: 4 · 2012: 4
- FWCI
- 1.15
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Biochemistry (publishedVersion)
- PubMed (publishedVersion)
- Funders
- California Institute of Technology
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA and Nucleic Acid Chemistry
- Physical Sciences › Chemistry › Physical and Theoretical Chemistry › Photochemistry and Electron Transfer Studies
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Photodynamic Therapy Research Studies
- Keywords
- DNA-protein crosslinks, guanine oxidation, photosensitizers, reactive oxygen species, histones, cytochrome c, ferrocytochrome c, ethidium, acridine orange, ruthenium complexes, dipyridophenazine, oxidative quenching, transient absorption spectroscopy
- MeSH terms
- Animals, Base Sequence, Cattle, Cross-Linking Reagents, Cytochrome c Group, DNA, DNA Damage, Electrochemistry, Electrophoresis, Polyacrylamide Gel, Guanine, Heme, Histones, Horses, Molecular Sequence Data, Oxidation-Reduction, Photochemistry, Piperidines, Serum Albumin, Bovine, Photosensitizing Agents, Hydroxyl Radical
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