Crosslinking of DNA repair and replication proteins to DNA in cells treated with 6-thioguanine and UVA
Open accessAbstract
The DNA of patients taking immunosuppressive and anti-inflammatory thiopurines contains 6-thioguanine (6-TG) and their skin is hypersensitive to ultraviolet A (UVA) radiation. DNA 6-TG absorbs UVA and generates reactive oxygen species that damage DNA and proteins. Here, we show that the DNA damage includes covalent DNA-protein crosslinks. An oligonucleotide containing a single 6-TG is photochemically crosslinked to cysteine-containing oligopeptides by low doses of UVA. Crosslinking is significantly more efficient if guanine sulphonate (G(SO3))--an oxidized 6-TG and a previously identified UVA photoproduct--replaces 6-TG, suggesting that G(SO3) is an important reaction intermediate. Crosslinking occurs via oligopeptide sulphydryl and free amino groups. The oligonucleotide-oligopeptide adducts are heat stable but are partially reversed by reducing treatments. UVA irradiation of human cells containing DNA 6-TG induces extensive heat- and reducing agent-resistant covalent DNA-protein crosslinks and diminishes the recovery of some DNA repair and replication proteins from nuclear extracts. DNA-protein crosslinked material has an altered buoyant density and can be purified by banding in cesium chloride (CsCl) gradients. PCNA, the MSH2 mismatch repair protein and the XPA nucleotide excision repair (NER) factor are among the proteins detectable in the DNA-crosslinked material. These findings suggest that the 6-TG/UVA combination might compromise DNA repair by sequestering essential proteins.
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Proposed structures of DPCs formed between oligonucleotides and short peptides involve covalent binding of 6-TG with cysteine residues through disulfide generation.
“Some of the proposed structures of DPCs formed between oligonucleotides and short peptides involve covalent binding of highly reactive 6-TG with cysteine residues through the generation of a disulfide (214).”
From Photoinduced Damage to Cellular DNA: Direct and Photosensitized Reactions<sup>†</sup> (2012) · cites this paper as [214]
Free peptide amino groups were suggested to participate in 6-TG-mediated formation of DPCs.
“Free peptide amino groups were also suggested to participate in the 6-TG-mediated formation of DPCs.”
From Photoinduced Damage to Cellular DNA: Direct and Photosensitized Reactions<sup>†</sup> (2012) · cites this paper as [214]
6-TG-photosensitized formation of DPCs and DNA ICLs was observed in model compounds and CCRF-CEM leukemia cells.
“The formation of two other main classes of 6-TG-photosensitized photoproducts, including DPCs and DNA ICLs, was also observed in model compounds and CCRF-CEM leukemia cells (214,215).”
From Photoinduced Damage to Cellular DNA: Direct and Photosensitized Reactions<sup>†</sup> (2012) · cites this paper as [214]
DPCs generated in cellular DNA are resistant to reduction treatment, unlike those formed in model studies, ruling out disulfide structures.
“However, the DPCs that were generated in cellular DNA were resistant to reduction treatment in contrast to those formed in model studies (214), ruling out the possible structures that were discussed above.”
From Photoinduced Damage to Cellular DNA: Direct and Photosensitized Reactions<sup>†</sup> (2012) · cites this paper as [214]
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- Authors
- Gueranger, Q., Kia, A., Frith, D., & Karran, P.
- Affiliations
- Cancer Research UK (GB)
- Corresponding author
- Karran, Peter
- Venue
- Nucleic Acids Research
- Publisher
- Oxford University Press (OUP)
- Published
- 2011-03-11
- Volume
- 39
- Issue
- 12
- Pages
- 5057-5066
- ISSN
- 0305-1048 (ISSN-L)
- 1362-4962
- PMC
- PMC3130278
- OpenAlex
- W2135942209
- Cited by
- 47
- References
- 27
- Citations by year
- 2026: 1 · 2025: 3 · 2023: 2 · 2022: 3 · 2021: 5 · 2020: 1 · 2019: 2 · 2018: 1 · 2017: 2 · 2016: 5 · 2015: 1 · 2014: 4 · 2013: 4 · 2012: 9
- FWCI
- 2.73
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Nucleic Acids Research (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Funders
- Cancer Research UK (11584)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Carcinogens and Genotoxicity Assessment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA and Nucleic Acid Chemistry
- Keywords
- 6-thioguanine, UVA, photoproducts, reactive oxygen species, DNA repair proteins, DNA replication proteins, PCNA, MSH2, XPA, nucleotide excision repair, DNA mismatch repair, protein sequestration
- MeSH terms
- DNA, DNA Damage, DNA Repair, DNA Replication, DNA-Binding Proteins, Humans, Nuclear Proteins, Oligopeptides, Thioguanine, Tumor Cells, Cultured, Ultraviolet Rays, Electrophoresis, Gel, Two-Dimensional, Proliferating Cell Nuclear Antigen, MutS Homolog 2 Protein, Xeroderma Pigmentosum Group A Protein, Photochemical Processes
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