The efficiencies of damage recognition and excision correlate with duplex destabilization induced by acetylaminofluorene adducts in human nucleotide excision repair

Chemical Research in Toxicology

Volumn 25, Issue 11, 2012, Pages 2462-2468

  Yeo, Jung Eun ^a   Khoo, Andy ^a   Fagbemi, Adebanke F ^a   Schärer, Orlando D ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE; N (2 FLUORENYL)ACETAMIDE;

ARTICLE; BINDING AFFINITY; CHEMICAL BINDING; CONTROLLED STUDY; DNA ADDUCT; DNA DAMAGE; ELECTROPHORETIC MOBILITY; ESCHERICHIA COLI; EXCISION REPAIR; HELA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; MOLECULAR RECOGNITION; NONHUMAN; THERMODYNAMICS;

2-ACETYLAMINOFLUORENE; DNA ADDUCTS; DNA REPAIR; HUMANS; MODELS, MOLECULAR; MOLECULAR STRUCTURE; OLIGODEOXYRIBONUCLEOTIDES; THERMODYNAMICS;

EID: 84869407113     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx3003033     Document Type: Article

References (45)

1. Friedberg, E. C., Walker, G. C., Siede, W., Wood, R. D., Schultz, R. A., and Ellenberger, T. (2005) DNA Repair and Mutagenesis, 2 nd ed., ASM Press, Washington, DC.
2. Gillet, L. C. and Schärer, O. D. (2006) Molecular mechanisms of mammalian global genome nucleotide excision repair Chem. Rev. 106, 253-276
3. Liu, Y., Reeves, D., Kropachev, K., Cai, Y., Ding, S., Kolbanovskiy, M., Kolbanovskiy, A., Bolton, J. L., Broyde, S., Van Houten, B., and Geacintov, N. E. (2011) Probing for DNA damage with beta-hairpins: Similarities in incision efficiencies of bulky DNA adducts by prokaryotic and human nucleotide excision repair systems in vitro DNA Repair (Amsterdam) 10, 684-696
4. Gunz, D., Hess, M. T., and Naegeli, H. (1996) Recognition of DNA adducts by human nucleotide excision repair. Evidence for a thermodynamic probing mechanism J. Biol. Chem. 271, 25089-25098
5. Hess, M. T., Schwitter, U., Petretta, M., Giese, B., and Naegeli, H. (1997) Bipartite substrate discrimination by human nucleotide excision repair Proc. Natl. Acad. Sci. U.S.A. 94, 6664-6669
6. Cai, Y., Patel, D. J., Broyde, S., and Geacintov, N. E. (2010) Base sequence context effects on nucleotide excision repair J. Nucleic Acids 2010, 174252
7. Geacintov, N. E., Broyde, S., Buterin, T., Naegeli, H., Wu, M., Yan, S., and Patel, D. J. (2002) Thermodynamic and structural factors in the removal of bulky DNA adducts by the nucleotide excision repair machinery Biopolymers 65, 202-210
8. Isaacs, R. J. and Spielmann, H. P. (2004) A model for initial DNA lesion recognition by NER and MMR based on local conformational flexibility DNA Repair (Amsterdam) 3, 455-464
9. Naegeli, H. and Sugasawa, K. (2011) The xeroderma pigmentosum pathway: decision tree analysis of DNA quality DNA Repair (Amsterdam) 10, 673-683
10. Schärer, O. D. (2007) Achieving broad substrate specificity in damage recognition by binding accessible nondamaged DNA Mol. Cell 28, 184-186
11. Buterin, T., Meyer, C., Giese, B., and Naegeli, H. (2005) DNA quality control by conformational readout on the undamaged strand of the double helix Chem. Biol. 12, 913-922
12. Maillard, O., Solyom, S., and Naegeli, H. (2007) An aromatic sensor with aversion to damaged strands confers versatility to DNA repair PLoS Biol. 5, e79
13. Min, J. H. and Pavletich, N. P. (2007) Recognition of DNA damage by the Rad4 nucleotide excision repair protein Nature 449, 570-575
14. Sugasawa, K., Okamoto, T., Shimizu, Y., Masutani, C., Iwai, S., and Hanaoka, F. (2001) A multistep damage recognition mechanism for global genomic nucleotide excision repair Genes Dev. 15, 507-521
15. Mathieu, N., Kaczmarek, N., and Naegeli, H. (2010) Strand- and site-specific DNA lesion demarcation by the xeroderma pigmentosum group D helicase Proc. Natl. Acad. Sci. U.S.A. 107, 17545-17550
16. Sugasawa, K., Akagi, J., Nishi, R., Iwai, S., and Hanaoka, F. (2009) Two-step recognition of DNA damage for mammalian nucleotide excision repair: Directional binding of the XPC complex and DNA strand scanning Mol. Cell 36, 642-653
17. Kuper, J., Wolski, S. C., Michels, G., and Kisker, C. (2012) Functional and structural studies of the nucleotide excision repair helicase XPD suggest a polarity for DNA translocation EMBO J. 31, 494-502
18. Pugh, R. A., Wu, C. G., and Spies, M. (2012) Regulation of translocation polarity by helicase domain 1 in SF2B helicases EMBO J. 31, 503-514
19. Lukin, M., Zaliznyak, T., Johnson, F., and de los Santos, C. (2012) Structure and stability of DNA containing an aristolactam II-dA lesion: implications for the NER recognition of bulky adducts Nucleic Acids Res. 40, 2759-2770
20. Sidorenko, V. S., Yeo, J. E., Bonala, R. R., Johnson, F., Schärer, O. D., and Grollman, A. P. (2012) Lack of recognition by global-genome nucleotide excision repair accounts for the high mutagenicity and persistence of aristolactam-DNA adducts Nucleic Acids Res. 40, 2494-2505
21. Fuchs, R. P. and Fujii, S. (2007) Translesion synthesis in Escherichia coli: lessons from the NarI mutation hot spot DNA Repair (Amsterdam) 6, 1032-1041
22. Patel, D. J., Mao, B., Gu, Z., Hingerty, B. E., Gorin, A., Basu, A. K., and Broyde, S. (1998) Nuclear magnetic resonance solution structures of covalent aromatic amine-DNA adducts and their mutagenic relevance Chem. Res. Toxicol. 11, 391-407
23. Belguise-Valladier, P. and Fuchs, R. P. (1995) N-2-aminofluorene and N-2 acetylaminofluorene adducts: the local sequence context of an adduct and its chemical structure determine its replication properties J. Mol. Biol. 249, 903-913
24. Jain, V., Hilton, B., Patnaik, S., Zou, Y., Chiarelli, M. P., and Cho, B. P. (2012) Conformational and thermodynamic properties modulate the nucleotide excision repair of 2-aminofluorene and 2-acetylaminofluorene dG adducts in the NarI sequence Nucleic Acids Res. 40, 3939-3951
25. Jain, N., Meneni, S., Jain, V., and Cho, B. P. (2009) Influence of flanking sequence context on the conformational flexibility of aminofluorene-modified dG adduct in dA mismatch DNA duplexes Nucleic Acids Res. 37, 1628-1637
26. Wang, L. and Broyde, S. (2006) A new anti conformation for N-(deoxyguanosin-8-yl)-2-acetylaminofluorene (AAF-dG) allows Watson-Crick pairing in the Sulfolobus solfataricus P2 DNA polymerase IV (Dpo4) Nucleic Acids Res. 34, 785-795
27. Gillet, L. C., Alzeer, J., and Schärer, O. D. (2005) Site-specific incorporation of N-(deoxyguanosin-8-yl)-2-acetylaminofluorene (dG-AAF) into oligonucleotides using modified "ultra-mild" DNA synthesis Nucleic Acids Res. 33, 1961-1969
28. Mekhovich, O., Tang, M., and Romano, L. J. (1998) Rate of incision of N-acetyl-2-aminofluorene and N-2-aminofluorene adducts by UvrABC nuclease is adduct- and sequence-specific: Comparison of the rates of UvrABC nuclease incision and protein-DNA complex formation Biochemistry 37, 571-579
29. Meneni, S. R., Shell, S. M., Gao, L., Jurecka, P., Lee, W., Sponer, J., Zou, Y., Chiarelli, M. P., and Cho, B. P. (2007) Spectroscopic and theoretical insights into sequence effects of aminofluorene-induced conformational heterogeneity and nucleotide excision repair Biochemistry 46, 11263-11278
30. Mu, D., Bertrand-Burggraf, E., Huang, J. C., Fuchs, R. P., Sancar, A., and Fuchs, B. P. (1994) Human and E.coli excinucleases are affected differently by the sequence context of acetylaminofluorene-guanine adduct Nucleic Acids Res. 22, 4869-4871
31. Seeberg, E. and Fuchs, R. P. (1990) Acetylaminofluorene bound to different guanines of the sequence -GGCGCC- is excised with different efficiencies by the UvrABC excision nuclease in a pattern not correlated to the potency of mutation induction Proc. Natl. Acad. Sci. U.S.A. 87, 191-194
32. Zou, Y., Shell, S. M., Utzat, C. D., Luo, C., Yang, Z., Geacintov, N. E., and Basu, A. K. (2003) Effects of DNA adduct structure and sequence context on strand opening of repair intermediates and incision by UvrABC nuclease Biochemistry 42, 12654-12661
33. Shibutani, S., Gentles, R., Johnson, F., and Grollman, A. P. (1991) Isolation and characterization of oligodeoxynucleotides containing dG-N2-AAF and oxidation products of dG-C8-AF Carcinogenesis 12, 813-818
34. Sugasawa, K., Masutani, C., Uchida, A., Maekawa, T., van der Spek, P. J., Bootsma, D., Hoeijmakers, J. H., and Hanaoka, F. (1996) HHR23B, a human Rad23 homolog, stimulates XPC protein in nucleotide excision repair in vitro Mol. Cell. Biol. 16, 4852-4861
35. Biggerstaff, M. and Wood, R. D. (1999) Assay for nucleotide excision repair protein activity using fractionated cell extracts and UV-damaged plasmid DNA Methods Mol. Biol. 113, 357-372
36. Shivji, M. K., Moggs, J. G., Kuraoka, I., and Wood, R. D. (1999) Dual-incision assays for nucleotide excision repair using DNA with a lesion at a specific site Methods Mol. Biol. 113, 373-392
37. Bohon, J. and de los Santos, C. R. (2005) Effect of 6-thioguanine on the stability of duplex DNA Nucleic Acids Res. 33, 2880-2886
38. Allawi, H. T. and SantaLucia, J., Jr. (1997) Thermodynamics and NMR of internal G.T mismatches in DNA Biochemistry 36, 10581-10594
39. Zaliznyak, T., Bonala, R., Johnson, F., and de Los Santos, C. (2006) Structure and stability of duplex DNA containing the 3-(deoxyguanosin-N2-yl)-2- acetylaminofluorene (dG(N2)-AAF) lesion: a bulky adduct that persists in cellular DNA Chem. Res. Toxicol. 19, 745-752
40. Gillet, L. C. and Schärer, O. D. (2002) Preparation of C8-amine and acetylamine adducts of 2′-deoxyguanosine suitably protected for DNA synthesis Org. Lett. 4, 4205-4208
41. Cai, Y., Kropachev, K., Xu, R., Tang, Y., Kolbanovskii, M., Kolbanovskii, A., Amin, S., Patel, D. J., Broyde, S., and Geacintov, N. E. (2010) Distant neighbor base sequence context effects in human nucleotide excision repair of a benzo[a]pyrene-derived DNA lesion J. Mol. Biol. 399, 397-409
42. Mocquet, V., Kropachev, K., Kolbanovskiy, M., Kolbanovskiy, A., Tapias, A., Cai, Y., Broyde, S., Geacintov, N. E., and Egly, J. M. (2007) The human DNA repair factor XPC-HR23B distinguishes stereoisomeric benzo[a]pyrenyl-DNA lesions EMBO J. 26, 2923-2932
43. Mu, H., Kropachev, K., Wang, L., Zhang, L., Kolbanovskiy, A., Kolbanovskiy, M., Geacintov, N. E., and Broyde, S. (2012) Nucleotide excision repair of 2-acetylaminofluoreneand 2-aminofluorene-(C8)-guanine adducts: Molecular dynamics simulations elucidate how lesion structure and base sequence context impact repair efficiencies Nucleic Acids Res. 10.1093/nar/gks788
44. Batty, D., Rapic'-Otrin, V., Levine, A. S., and Wood, R. D. (2000) Stable binding of human XPC complex to irradiated DNA confers strong discrimination for damaged sites J. Mol. Biol. 300, 275-290
45. Hey, T., Lipps, G., Sugasawa, K., Iwai, S., Hanaoka, F., and Krauss, G. (2002) The XPC-HR23B complex displays high affinity and specificity for damaged DNA in a true-equilibrium fluorescence assay Biochemistry 41, 6583-6587