Skip to main content
SpringerLink
Log in

Sensitized photochemistry of di(4-tetrazolouracil) dinucleoside monophosphate as a route to dicytosine cyclobutane photoproduct precursors

  • Paper
  • Published:
Photochemical & Photobiological Sciences Aims and scope Submit manuscript

Abstract

The DNA cis-syn cyclobutane photoproduct formed between two adjacent cytosine residues is highly mutagenic and responsible for the tandem CC to TT transition. However, its instability has prevented its in vitro study, so far. With a view to prepare oligodeoxynucleotides containing the CC cyclobutane lesion, we have synthesized in good yield a ditetrazolouracil cyclobutane dinucleotide photoproduct as a stable precursor of this photoproduct. Our approach also overcomes the low photochemical reactivity of the cytosine-cytosine deoxydinucleoside monophosphate.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Notes and references

  1. D. L. Mitchell, J. Jen, J. E. Cleaver, Sequence specificity of cyclobutane pyrimidine dimers in DNA treated with solar (ultraviolet B) radiation, Nucleic Acids Res., 1992, 20, 225–229.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. T. Douki, J. Cadet, Individual determination of the yield of the main UV-induced dimeric pyrimidine photoproducts in DNA suggests a high mutagenicity of CC photolesions, Biochemistry, 2001, 40, 2495–2501.

    Article  CAS  PubMed  Google Scholar 

  3. T. Douki, A. Reynaud-Angelin, J. Cadet, E. Sage, Bipyrimidine photoproducts rather than oxidative lesions are the main type of DNA damage involved in the genotoxic effect of solar UVA radiation, Biochemistry, 2003, 42, 9221–9226.

    Article  CAS  PubMed  Google Scholar 

  4. S. Mouret, C. Baudouin, M. Charveron, A. Favier, J. Cadet, T. Douki, Cyclobutane pyrimidine dimers are predominant DNA lesions in whole human skin exposed to UVA radiation, Proc. Natl. Acad. Sci. U. S. A., 2006, 103, 13765–13770.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. E. Otoshi, T. Yagi, T. Mori, T. Matsunaga, O. Nikaido, S.-T. Kim, K. Hitomi, M. Ikenaga, T. Todo, Respective roles of cyclobutane pyrimidine dimers, (6-4) photoproducts, and minor photoproducts in ultraviolet mutagenesis of repair-deficient Xeroderma pigmentosum A cells, Cancer Res., 2000, 60, 1729–1735.

    CAS  PubMed  Google Scholar 

  6. L. Daya-Grosjean, A. Sarasin, The role of UV induced lesions in skin carcinogenesis: an overview of oncogene and tumor suppressor gene modifications in Xeroderma pigmentosum skin tumors, Mutat. Res., Fundam. Mol. Mech. Mutagen., 2005, 571, 43–56.

    Article  CAS  Google Scholar 

  7. W. Peng, B. R. Shaw, Accelerated deamination of cytosine residues in UV-induced cyclobutane pyrimidine dimers leads to CC?TT transitions, Biochemistry, 1996, 35, 10172–10181.

    Article  CAS  PubMed  Google Scholar 

  8. A. Burger, D. Fix, H. Liu, J. Hays, R. Bockrath, In vivo deamination of cytosine-containing cyclobutane pyrimidine dimers in E. coli: a feasible part of UV-mutagenesis, Mutat. Res., Fundam. Mol. Mech. Mutagen., 2003, 522, 145–156.

    Article  CAS  Google Scholar 

  9. J.-S. Taylor, C. L. O’Day, cis-syn Thymine dimers are not absolute blocks to replication by DNA polymerase I of Escherichia coli in vitro, Biochemistry, 1990, 29, 1624–1632.

    Article  CAS  PubMed  Google Scholar 

  10. I. Tessman, S.-K. Liu, M. A. Kennedy, Mechanism of SOS mutagenesis of UV-irradiated DNA: mostly error-free processing of deaminated cytosine, Proc. Natl. Acad. Sci. U. S. A., 1992, 89, 1159–1163.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. N. Jiang, J.-S. Taylor, In vitro evidence that UV-induced C?T mutations at dipyrimidine sites could result from replicative bypass of cis-syn cyclobutane dimers or their deamination products, Biochemistry, 1993, 32, 472–481.

    Article  CAS  PubMed  Google Scholar 

  12. D.-H. Lee, G. P. Pfeifer, Deamination of 5-methylcytosines within cyclobutane pyrimidine dimers is an important component of UVB mutagenesis, J. Biol. Chem., 2003, 278, 10314–10321.

    Article  CAS  PubMed  Google Scholar 

  13. K. Takasawa, C. Masutani, F. Hanaoka, S. Iwai, Chemical synthesis and translesion replication of a cis-syn cyclobutane thymine-uracil dimer, Nucleic Acids Res., 2004, 32, 1738–1745.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. B. Vu, V. J. Cannistraro, L. Sun, J.-S. Taylor, DNA synthesis past a 5-methylC-containing cis-syn-cyclobutane pyrimidine dimer by yeast Pol ? is highly nonmutagenic, Biochemistry, 2006, 45, 9327–9335.

    Article  CAS  PubMed  Google Scholar 

  15. M. J. Horsfall, A. Borden, C. W. Lawrence, Mutagenic properties of the T-C cyclobutane dimer, J. Bacteriol., 1997, 179, 2835–2839.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Q. Song, S. M. Sherrer, Z. Suo, J.-S. Taylor, Preparation of site-specific T = mCG cis-syn cyclobutane dimer-containing template and its error-free bypass by yeast and human polymerase ?, J. Biol. Chem., 2012, 287, 8021–8028.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. C. Y. Shin-Darlak, A. M. Skinner, M. S. Turker, A role for Pms2 in the prevention of tandem CC?TT substitutions induced by ultraviolet radiation and oxidative stress, DNA Repair, 2005, 4, 51–57.

    Article  CAS  PubMed  Google Scholar 

  18. S.-L. Yu, R. E. Johnson, S. Prakash, L. Prakash, Requirement of DNA polymerase ? for error-free bypass of UV-induced CC and TC photoproducts, Mol. Cell. Biol., 2001, 21, 185–188.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. J.-H. Yoon, L. Prakash, S. Prakash, Highly error-free role of DNA polymerase ? in the replicative bypass of UV-induced pyrimidine dimers in mouse and human cells, Proc. Natl. Acad. Sci. U. S. A., 2009, 106, 18219–18224.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. J.-H. Choi, G. P. Pfeifer, The role of polymerase ? in UV mutational spectra, DNA Repair, 2005, 4, 211–220.

    Article  CAS  PubMed  Google Scholar 

  21. A. Vaisman, R. Woodgate, Unique misinsertion specificity of pol? may decrease the mutagenic potential of deaminated cytosines, EMBO J., 2001, 20, 6520–6529.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. A. M. Skinner, M. S. Turker, High frequency induction of CC to TT tandem mutations in DNA repair-proficient mammalian cells, Photochem. Photobiol., 2008, 84, 222–227.

    CAS  PubMed  Google Scholar 

  23. S. Queille, L. Luron, A. Spatz, M. F. Avril, V. Ribrag, P. Duvillard, C. Hiesse, A. Sarasin, J. P. Armand, L. Daya-Grosjean, Analysis of skin cancer risk factors in immunosuppressed renal transplant patients shows high levels of UV-specific tandem CC to TT mutations of the p53 gene, Carcinogenesis, 2006, 28, 724–731.

    Article  PubMed  Google Scholar 

  24. A. M. Skinner, C. Dan, M. S. Turker, The frequency of CC to TT tandem mutations in mismatch repair-deficient cells is increased in a cytosine run, Mutagenesis, 2008, 23, 87–91.

    Article  CAS  PubMed  Google Scholar 

  25. S. Mouret, M. Charveron, A. Favier, J. Cadet, T. Douki, Differential repair of UVB-induced cyclobutane pyrimidine dimers in cultured human skin cells and whole human skin, DNA Repair, 2008, 7, 704–712.

    Article  CAS  PubMed  Google Scholar 

  26. V. J. Cannistraro, J.-S. Taylor, Acceleration of 5-methylcytosine deamination in cyclobutane dimers by G and its implications for UV-induced C-to-T mutation hotspots, J. Mol. Biol., 2009, 392, 1145–1157.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. K. B. Freeman, P. V. Hariharan, H. E. Johns, The ultraviolet photochemistry of cytidylyl-(3’-5’)-cytidine, J. Mol. Biol., 1965, 13, 833–848.

    Article  CAS  Google Scholar 

  28. P. V. Hariharan, H. E. Johns, Photochemical cross sections in cytidylyl-(3’-5’)-cytidine, Can. J. Biochem., 1968, 46, 911–918.

    Article  CAS  PubMed  Google Scholar 

  29. G. G. Gurzadyan, H. Görner, Depopulation of highly excited singlet states of DNA model compounds: quantum yields of 193 and 254 nm photoproducts of pyrimidine monomers and dinucleoside monophosphates, Photochem. Photobiol., 1996, 63, 143–153.

    Article  CAS  PubMed  Google Scholar 

  30. T. Douki, J. Cadet, Formation of cyclobutane dimers and (6-4) photoproducts upon far-UV photolysis of 5-methylcytosine-containing dinucleoside monophosphates, Biochemistry, 1994, 33, 11942–11950.

    Article  CAS  PubMed  Google Scholar 

  31. T. Douki, T. Zalizniak, J. Cadet, Far-UV-induced dimeric photoproducts in short oligonucleotides: sequence effects, Photochem. Photobiol., 1997, 66, 171–179.

    Article  CAS  PubMed  Google Scholar 

  32. S.-T. Kim, A. Sancar, Effect of base, pentose, and phosphodiester backbone structures on binding and repair of pyrimidine dimers by Escherichia coli DNA photolyase, Biochemistry, 1991, 30, 8623–8630.

    Article  CAS  PubMed  Google Scholar 

  33. J. Cadet and P. Vigny, The Photochemistry of Nucleic Acids in Bioorganic Photochemistry, ed. H. Morrison, John Wiley & Sons, New York, 1990, vol. 1, pp. 1–272.

    CAS  Google Scholar 

  34. J. Yamamoto, K. Nishiguchi, K. Manabe, C. Masutani, F. Hanaoka, S. Iwai, Photosensitized [2 + 2] cycloaddition of N-acetylated cytosine affords stereoselectively formation of cyclobutane pyrimidine dimer, Nucleic Acids Res., 2011, 39, 1165–1175.

    Article  CAS  PubMed  Google Scholar 

  35. H. C. Shah, V. H. Shah, N. D. Desai, A novel strategy for the synthesis of 2-amino-4,6-diarylnicotinonitrile, ARKIVOC, 2009, ii, 76–87. and references cited

    Article  Google Scholar 

  36. K. Ciszewski, L. Celewicz, K. Golankiewicz, Novel synthetic route to 1-substituted cytosines, Synthesis, 1995, 777–779.

    Google Scholar 

  37. L. P. Kotra, P. Wang, M. Bartlett, K. Shanmuganathan, Z. Xu, S. Cavalcanti, M. G. Newton, C. K. Chu, 4-Azido-2-pyrimidinone nucleosides and related chemistry, J. Org. Chem., 1997, 62, 7267–7271.

    Article  CAS  PubMed  Google Scholar 

  38. R. E. Rycyna, J. L. Alderfer, Ultraviolet irradiation of nucleic acids: formation, purification, and solution conformational analyses of the cis-syn and trans-syn photodimers of UpU, Biochemistry, 1988, 27, 3142–3151.

    Article  CAS  PubMed  Google Scholar 

  39. The proper chemical name is tetrazolo[4,5-c]pyrimidin-2-one

  40. L. De Napoli, L. Mayol, G. Piccialli, M. Rossi, C. J. Santacroce, Synthesis of novel pyrimidine nucleoside analogues, J. Heterocycl. Chem., 1986, 23, 1401–1403.

    Article  Google Scholar 

  41. L. De Napoli, A. Messere, D. Montesarchio, C. Santacroce, Synthesis of 4-substituted pyrimidine 2’,3’-dideoxynucleosides, Nucleosides Nucleotides, 1991, 10, 1719–1728.

    Article  Google Scholar 

  42. K. Ciszewski, L. Celewicz, K. Golankiewicz, Synthesis of 6-substituted tetrazolo[1,5-c]pyrimidin-5(6)ones: new modification of 3’-azido-3’-deoxythymidine, Biochem. Biophys. Res. Commun., 1992, 187, 1545–1550.

    Article  CAS  PubMed  Google Scholar 

  43. T. S. Mansour, C. A. Evans, M. A. Siddiqui, M. Charron, B. Zacharie, N. Nguyen-Ba, N. Lee, B. Korba, Structure-activity relationship of pyrimidine heterosubstituted nucleoside analogues, Nucleosides Nucleotides, 1997, 16, 993–1001.

    Article  CAS  Google Scholar 

  44. L. P. Kotra, P. Wang, M. Bartlett, K. Shanmuganathan, Z. Xu, S. Cavalcanti, M. G. Newton, C. K. Chu, 4-Azido-2-pyrimidinone nucleosides and related chemistry, J. Org. Chem., 1997, 62, 7267–7271.

    Article  CAS  PubMed  Google Scholar 

  45. F. Peyrane, M. Cesario, P. Clivio, Photochemical ring expansion of 4-azidouracil: a route to 5 H-1,3,5-triazepin-2,4-dione in the nucleoside series, J. Org. Chem., 2006, 71, 1742–1745.

    Article  CAS  PubMed  Google Scholar 

  46. Y. Hayakawa, M. Kataoka, Facile synthesis of oligodeoxynucleotides via the phosphoramidite method without nucleoside base protection, J. Am. Chem. Soc., 1998, 120, 12395–12401.

    Article  CAS  Google Scholar 

  47. F. Peyrane, P. Clivio, The chemistry of 4-azido-2-pyrimidinone nucleosides revisited, J. Org. Chem., 2005, 70, 1961–1962.

    Article  CAS  PubMed  Google Scholar 

  48. F.-T. Liu, N. C. Yang, Photochemistry of cytosine derivatives. 1. Photochemistry of thymidylyl-(3’?5’)-deoxycytidine, Biochemistry, 1978, 17, 4865–4876.

    Article  CAS  PubMed  Google Scholar 

  49. J. Kemmink, R. Boelens, R. Kaptein, Two-dimensional 1H NMR study of two cyclobutane type photodimers of thymidylyl-(3’-5’)-thymidine, Eur. Biophys. J., 1987, 14, 293–299.

    Article  CAS  PubMed  Google Scholar 

  50. T. M. G. Koning, J. J. G. van Soest, R. Kaptein, NMR studies of bipyrimidine cyclobutane photodimers, Eur. J. Biochem., 1991, 195, 29–40.

    Article  CAS  PubMed  Google Scholar 

  51. W. A. Tabaczynski, D. G. E. Lemaire, B. P. Ruzsicska, J. L. Alderfer, An NMR and conformational investigation of the trans-syn cyclobutane photodimers of dTpdU, Biopolymers, 1993, 33, 1365–1375.

    Article  CAS  PubMed  Google Scholar 

  52. W. A. Tabaczynski, D. G. E. Lemaire, B. P. Ruzsicska, J. L. Alderfer, An NMR and conformational investigation of the trans-syn cyclobutane photodimers of dUpdT, Biopolymers, 1999, 50, 185–191.

    Article  CAS  PubMed  Google Scholar 

  53. J. L. F. Kao, S. Nadji, J.-S. Taylor, Identification and structure determination of a third cyclobutane photodimer of thymidylyl-(3’?5’)-thymidine: the trans-syn-II product, Chem. Res. Toxicol., 1993, 6, 561–567.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut de Chimie des Substances Naturelles, CNRS, 1 Avenue de la Terrasse, 91190, Gif-sur-Yvette, France

    Frédéric Peyrane

  2. Institut de Chimie Moléculaire de Reims, UMR 7312 CNRS Université de Reims Champagne Ardenne, UFR Pharmacie, 51 rue Cognacq-Jay, 51096, Reims Cedex, France

    Pascale Clivio

Authors
  1. Frédéric Peyrane
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pascale Clivio
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pascale Clivio.

Additional information

† Electronic supplementary information (ESI) available. See DOI: 10.1039/c3pp25402j

Rights and permissions

Reprints and permissions

About this article

Cite this article

Peyrane, F., Clivio, P. Sensitized photochemistry of di(4-tetrazolouracil) dinucleoside monophosphate as a route to dicytosine cyclobutane photoproduct precursors. Photochem Photobiol Sci 12, 1366–1374 (2013). https://doi.org/10.1039/c3pp25402j

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1039/c3pp25402j

Search

Navigation