High-resolution crystal structure of the intramolecular d(TpA) thymine-adenine photoadduct and its mechanistic implications

Nucleic Acids Research

Volumn 35, Issue 4, 2007, Pages 1048-1053

  Davies, R Jeremy H ^a   Malone, John F ^a   Gan, Yu ^b   Cardin, Christine J ^b   Lee, Michael P H ^c   Neidle, Stephen ^c  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b UNIVERSITY OF READING   (United Kingdom)

^c UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; AMIDINE; AMPHOLYTE; ANION; CYCLOBUTANE; DINUCLEOSIDE PHOSPHATE; DNA; PYRIMIDINE; THYMINE;

ARTICLE; CHEMICAL BOND; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIMERIZATION; DNA ADDUCT; ISOMERIZATION; MOLECULAR MECHANICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHOTOREACTIVITY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN STRUCTURE; PROTON TRANSPORT; QUANTUM YIELD; STEREOCHEMISTRY; STRUCTURE ANALYSIS; ULTRAVIOLET RADIATION;

CRYSTALLOGRAPHY, X-RAY; DNA ADDUCTS; HETEROCYCLIC COMPOUNDS WITH 4 OR MORE RINGS; MODELS, MOLECULAR; OLIGODEOXYRIBONUCLEOTIDES; STEREOISOMERISM;

EID: 34047150795     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkl1101     Document Type: Article

References (38)

1. Crespo-Hernández,C.E., Cohen,B., Hare,P.M. and Kohler,B. (2004) Ultrafast excited-state dynamics in nucleic acids. Chem. Rev., 104, 1977-2019.
2. Cadet,J. and Vigny,P. (1990). The photochemistry of nucleic acids. In: Morrison,H (ed), Bioorganic Photochemistry, Vol. 1. John Wiley and Sons, New York, pp. 1-272.
3. Davies,R.J.H. (1995) Ultraviolet radiation damage in DNA. Biochem. Soc. Trans., 23, 407-418.
4. Ravanat,J-L., Douki,T. and Cadet,J. (2001) Direct and indirect effects of UV radiation on DNA and its components. J. Photochem. Photobiol. B: Biol., 63, 88-102.
5. Sage,E., Drouin,R. and Rouabhia,R. (eds) (2005) From DNA photolesions to mutations, skin cancer and cell death. Comprehensive Series in Photochemical and Photobiological Sciences, Vol. 5. RSC Publishing, Cambridge, UK.
6. Douki,T. and Cadet,J. (2001) Individual determination of the yield of the main UV-induced dimeric pyrimidine photoproducts in DNA suggests a high mutagenicity of CC photolesions. Biochemistry, 40, 2495-2501.
7. Huggins,W., Ghosh,S.K., Nanda,K. and Wollenzien,P. (2005) Internucleotide movements during formation of 16 S rRNA-rRNA photocrosslinks and their connection to the 30 S subunit conformational dynamics. J. Mol. Biol., 354, 358-374.
8. Pörschke,D. (1973) Analysis of a specific photoreaction in oligoand polydeoxyadenylic acids. J. Am. Chem. Soc., 95, 8440-8446.
9. Kumar,S., Sharma,N.D., Davies,R.J.H., Phillipson,D.W. and McCloskey,J.A. (1987) The isolation and characterisation of a new type of dimeric adenine photoproduct in UV-irradiated deoxyadenylates. Nucleic Acids Res., 15, 1199-1216.
10. Kumar,S., Joshi,P.C., Sharma,N.D., Bose,S.N., Davies,R.J.H., Takeda,N. and McCloskey,J.A. (1991) Adenine photodimerization in deoxyadenylate sequences: Elucidation of the mechanism through structural studies of a major d(ApA) photoproduct. Nucleic Acids Res., 19, 2841-2847.
11. Bose,S.N., Davies,R.J.H., Sethi,S.K. and McCloskey,J.A. (1983) Formation of an adenine-thymine photoadduct in the deoxydinucleoside monophosphate d(TpA) and in DNA. Science, 220, 723-725.
12. Bose,S.N. and Davies,R.J.H. (1984) The photoreactivity of T-A sequences in oligodeoxyribonucleotides and DNA. Nucleic Acids Res., 12, 7903-7914.
13. Clingen,P.H. and Davies,R.J.H. (1997) Quantum yields of adenine photodimerization in poly(deoxyadenylic acid) and DNA. J. Photochem. Photobiol. B: Biol., 38, 81-87.
14. Koning,T.M.G., Davies,R.J.H. and Kaptein,R. (1990) The solution structure of the intramolecular photoproduct of d(TpA) derived with the use of NMR and a combination of distance geometry and molecular dynamics. Nucleic Acids Res., 18, 277-284.
15. Bose,S.N., Kumar,S., Davies,R.J.H., Sethi,S.K. and McCloskey,J.A. (1984) The photochemistry of d(T-A) in aqueous solution and in ice. Nucleic Acids Res., 12, 7929-7947.
16. Zhao,X., Nadji,S., Kao,J.L-F. and Taylor,J-S. (1996) The structure of d(TpA)*, the major photoproduct of thymidylyl-(3′-5′)-deoxyadenosine. Nucleic Acids Res., 24, 1554-1560.
17. Sheldrick,G.M. (1998) SHELX 97-2. University of Göttingen, Germany.
18. Macrae,C.F., Edgington,P.R., McCabe,P., Pidcock,E., Shields,G.P., Taylor,R., Towler,M. and van de Streek,J. (2006) Mercury: Visualization and analysis of crystal structures. J. Appl. Cryst., 39, 453-457.
19. Neidle,S. (2002) Nucleic Acid Structure and Recognition. Oxford University Press, Oxford.
20. Park,H., Zhang,K., Ren,Y., Nadji,S., Sinha,N., Taylor,J-S. and Kang,C. (2002) Crystal structure of a DNA decamer containing a cis-syn thymine dimer. Proc. Natl. Acad. Sci. U.S.A., 99, 15965-15970.
21. Vassylyev,D.G., Kashiwagi,T., Mikami,Y., Ariyoshi,M., Iwai,S., Ohtsuka,E. and Morikawa,K. (1995) Atomic model of a pyrimidine dimer excision-repair enzyme complexed with a DNA substrate - structural basis for damaged DNA recognition. Cell, 83, 773-782.
22. Mees,A., Klar,T., Gnau,P., Hennecke,U., Eker,A.P.M., Carell,T. and Essen,L-O. (2004) Crystal structure of a photolyase bound to a CPD-like lesion after in situ repair. Science, 306, 1789-1793.
23. Ling,H., Boudsocq,F., Plosky,B.S., Woodgate,R. and Yang,W. (2003) Replication of a cis-syn thymine dimer at atomic resolution. Nature, 424, 1083-1087.
24. Yokoyama,H., Mizutani,R., Satow,Y., Komatsu,Y., Ohtsuka,E. and Nikaido,O. (2000) Crystal structure of the 64M-2 antibody Fab fragment in complex with a DNA dT(6-4)T photoproduct formed by ultraviolet radiation. J. Mol. Biol., 299, 711-723.
25. Saintomé, C., Clivio,P., Favre,A., Fourrey,J-L. and Riche,C. (1996) RNA photolabeling mechanistic studies: X-ray crystal structure of the photoproduct formed between 4-thiothymidine and adenosine upon near UV irradiation. J. Am. Chem. Soc., 118, 8142-8143.
26. Crespo-Hernández,C.E., Cohen,B. and Kohler,B. (2005) Base stacking controls excited-state dynamics in A.T DNA. Nature, 436, 1141-1144.
27. Markovitsi,D., Onidas,D., Gustavsson,T., Talbot,F. and Lazzarotto,E. (2005) Collective behavior of Franck-Condon excited states and energy transfer in DNA double helices. J. Am. Chem. Soc., 127, 17130-17131.
28. Zhao,X., Kao,J.L-F. and Taylor,J-S. (1995) Preparation and characterization of a deoxyoligonucleotide 49-mer containing a site-specific thymidylyl-(3′-5′)-deoxyadenosine photoproduct. Biochemistry, 34, 1386-1392.
29. Wang,Y., Taylor,J-S. and Gross,M.L. (2001) Isolation and mass spectrometric characterization of dimeric adenine photoproducts in oligodeoxynucleotides. Chem. Res. Toxicol., 14, 738-745.
30. Wang,Y., Taylor,J-S. and Gross,M.L. (2001) Fragmentation of photomodified oligodeoxynucleotides adducted with metal ions in an electrospray-ionization ion-trap mass spectrometer. J. Am. Mass Spectrom., 12, 1174-1179.
31. Kundu,L.M., Linne,U., Marahiel,M. and Carell,T. (2004) RNA is more UV resistant than DNA: The formation of UV-induced DNA lesions is strongly sequence and conformation dependent. Chem. Eur. J., 10, 5697-5705.
32. Wang,Y., Gross,M.L. and Taylor,J-S. (2001) Use of a combined enzymatic digestion/ESI mass spectrometry assay to study the effect of TATA-binding protein on photoproduct formation in a TATA box. Biochemistry, 40, 11785-11793.
33. Zhao,X. and Taylor,J-S. (1996) Mutation spectra of TA*, the major photoproduct of thymidylyl-(3′-5′)-deoxyadenosine, in Escherichia coli under SOS conditions. Nucleic Acids Res., 24, 1561-1566.
34. Youderian,P., Bouvier,S. and Susskind,M.M. (1982) Sequence determinants of promoter activity. Cell, 30, 843-853.
35. LeClerc,J., Istock,N.L., Saran,B.R. and Allen,R.Jr (1984) Sequence analysis of ultraviolet-induced mutations in M13lacZ hybrid phage DNA. J. Mol. Biol., 180, 217-237.
36. Basic-Zaninovic,T., Meschini,R., Calcagnile,A.S., Palombo,F., D'Errico,M., Proietti-De Sanctis,L. and Dogliotti,E. (1995) Strand bias of ultraviolet light-induced mutations in a transcriptionally active gene in human cells. Mol. Carcinogenesis, 14, 214-225.
37. Otoshi,E., Yagi,T., Mori,T., Matsunaga,T., Nikaido,O., Kim,S-T., Hitomi,K., Ikenaga,M. and Todo,T. (2000) Respective roles of cyclobutane pyrimidine dimers, (6-4) photoproducts, and minor photoproducts in ultraviolet mutagenesis of repair-deficient xeroderma pigmentosum A cells. Cancer Res., 60, 1729-1735.
38. You,Y-H., Lee,D-H., Yoon,J-H., Nakajima,S., Yasui,A. and Pfeifer,G.P. (2001) Cyclobutane pyrimidine dimers are responsible for the vast majority of mutations induced by UVB irradiation in mammalian cells. J. Biol. Chem., 276, 44688-44694.