Differential Nucleotide Excision Repair Susceptibility of Bulky DNA Adducts in Different Sequence Contexts: Hierarchies of Recognition Signals

Journal of Molecular Biology

Volumn 385, Issue 1, 2009, Pages 30-44

  Cai, Yuqin ^a   Patel, Dinshaw J ^b   Geacintov, Nicholas E ^a   Broyde, Suse ^a  

^a NEW YORK UNIVERSITY   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

benzo a pyrenyl guanine lesion; GG mutation hotspot; guanine amino group; nucleotide excision repair susceptibility; sequence dependent conformational variability

Indexed keywords

7,8,9,10 TETRAHYDRO 7,8 DIHYDROXYBENZO[A]PYRENE 9,10 OXIDE; AMINO ACID; BENZO[A]PYRENE; DEOXYGUANOSINE; DEOXYINOSINE; DOUBLE STRANDED DNA; UNCLASSIFIED DRUG;

ARTICLE; BASE PAIRING; CRYSTAL STRUCTURE; DNA ADDUCT; DNA DAMAGE; DNA FLANKING REGION; DNA SEQUENCE; DNA STRUCTURE; EXCISION REPAIR; GENETIC SUSCEPTIBILITY; HYDROGEN BOND; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL;

EID: 57749188239     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.09.087     Document Type: Article

References (57)

1. Wood R.D. DNA damage recognition during nucleotide excision repair in mammalian cells. Biochimie 81 (1999) 39-44
2. Sugasawa K., Shimizu Y., Iwai S., and Hanaoka F. A molecular mechanism for DNA damage recognition by the xeroderma pigmentosum group C protein complex. DNA Repair (Amst.) 1 (2002) 95-107
3. Sugasawa K., Okamoto T., Shimizu Y., Masutani C., Iwai S., and Hanaoka F. A multistep damage recognition mechanism for global genomic nucleotide excision repair. Genes Dev. 15 (2001) 507-521
4. Hess M.T., Schwitter U., Petretta M., Giese B., and Naegeli H. Bipartite substrate discrimination by human nucleotide excision repair. Proc. Natl Acad. Sci. USA 94 (1997) 6664-6669
5. Gunz D., Hess M.T., and Naegeli H. Recognition of DNA adducts by human nucleotide excision repair: evidence for a thermodynamic probing mechanism. J. Biol. Chem. 271 (1996) 25089-25098
6. Gillet L.C., and Scharer O.D. Molecular mechanisms of mammalian global genome nucleotide excision repair. Chem. Rev. 106 (2006) 253-276
7. Evans E., Moggs J.G., Hwang J.R., Egly J.M., and Wood R.D. Mechanism of open complex and dual incision formation by human nucleotide excision repair factors. EMBO J. 16 (1997) 6559-6573
8. Dip R., Camenisch U., and Naegeli H. Mechanisms of DNA damage recognition and strand discrimination in human nucleotide excision repair. DNA Repair (Amst.) 3 (2004) 1409-1423
9. Buterin T., Meyer C., Giese B., and Naegeli H. DNA quality control by conformational readout on the undamaged strand of the double helix. Chem. Biol. 12 (2005) 913-922
10. Missura M., Buterin T., Hindges R., Hubscher U., Kasparkova J., Brabec V., and Naegeli H. Double-check probing of DNA bending and unwinding by XPA-RPA: an architectural function in DNA repair. EMBO J. 20 (2001) 3554-3564
11. Blagoev K.B., Alexandrov B.S., Goodwin E.H., and Bishop A.R. Ultra-violet light induced changes in DNA dynamics may enhance TT-dimer recognition. DNA Repair (Amst.) 5 (2006) 863-867
12. Isaacs R.J., and Spielmann H.P. A model for initial DNA lesion recognition by NER and MMR based on local conformational flexibility. DNA Repair (Amst.) 3 (2004) 455-464
13. Maillard O., Camenisch U., Clement F.C., Blagoev K.B., and Naegeli H. DNA repair triggered by sensors of helical dynamics. Trends Biochem. Sci. 32 (2007) 494-499
14. Cai Y., Patel D.J., Geacintov N.E., and Broyde S. Dynamics of a benzo[a]pyrene-derived guanine DNA lesion in TGT and CGC sequence contexts: enhanced mobility in TGT explains conformational heterogeneity, flexible bending, and greater susceptibility to nucleotide excision repair. J. Mol. Biol. 374 (2007) 292-305
15. Geacintov N.E., Naegeli H., Patel D.J., and Broyde S. Structural aspects of polycyclic aromatic carcinogen-damaged DNA and its recognition by NER proteins. In: Siede W., Kow Y., and Doetsch P. (Eds). DNA Damage Recognition (2005), Taylor and Francis, New York, NY 263-296
16. Geacintov N.E., Broyde S., Buterin T., Naegeli H., Wu M., Yan S., and Patel D.J. Thermodynamic and structural factors in the removal of bulky DNA adducts by the nucleotide excision repair machinery. Biopolymers 65 (2002) 202-210
17. 6-adenine adducts: unusual thermal stabilization of modified DNA duplexes. Chem. Res. Toxicol. 15 (2002) 249-261
18. Buterin T., Hess M.T., Luneva N., Geacintov N.E., Amin S., Kroth H., et al. Unrepaired fjord region polycyclic aromatic hydrocarbon-DNA adducts in ras codon 61 mutational hot spots. Cancer Res. 60 (2000) 1849-1856
19. Conney A.H. Induction of microsomal enzymes by foreign chemicals and carcinogenesis by polycyclic aromatic hydrocarbons: G. H. A. Clowes Memorial Lecture. Cancer Res. 42 (1982) 4875-4917
20. Koreeda M., Moore P.D., Wislocki P.G., Levin W., Yagi H., and Jerina D.M. Binding of benzo[a]pyrene 7,8-diol-9,10-epoxides to DNA, RNA, and protein of mouse skin occurs with high stereoselectivity. Science 199 (1978) 778-781
21. Straub K.M., Meehan T., Burlingame A.L., and Calvin M. Identification of the major adducts formed by reaction of benzo[a]pyrene diol epoxide with DNA in vitro. Proc. Natl Acad. Sci. USA 74 (1977) 5285-5289
22. Weinstein I.B., Jeffrey A.M., Jennette K.W., Blobstein S.H., Harvey R.G., Harris C., et al. Benzo[a]pyrene diol epoxides as intermediates in nucleic acid binding in vitro and in vivo. Science 193 (1976) 592-595
23. Kropachev, K., Kolbanovskii, M., Cai, Y., Rodríguez, F., Kolbanovskii, A., Liu, Y. et al. (2008). The sequence dependence of human nucleotide excision repair efficiencies of benzo[a]pyrene-derived lesions: insights into the structural factors that favor dual incisions. J. Mol. Biol. Submitted.
24. Vousden K.H., Bos J.L., Marshall C.J., and Phillips D.H. Mutations activating human c-Ha-ras1 protooncogene (HRAS1) induced by chemical carcinogens and depurination. Proc. Natl Acad. Sci. USA 83 (1986) 1222-1226
25. Wei S.J.C., Chang R.L., Hennig E., Cui X.X., Merkler K.A., Wong C.Q., et al. Mutagenic selectivity at the Hprt locus in V-79 cells-comparison of mutations caused by bay-region benzo[a]pyrene 7,8-diol-9,10-epoxide enantiomers with high and low carcinogenic activity. Carcinogenesis 15 (1994) 1729-1735
26. Hanrahan C.J., Bacolod M.D., Vyas R.R., Liu T., Geacintov N.E., Loechler E.L., and Basu A.K. Sequence specific mutagenesis of the major (+)-anti-benzo[a]pyrene diol epoxide-DNA adduct at a mutational hot spot in vitro and in Escherichia coli cells. Chem. Res. Toxicol. 10 (1997) 369-377
27. Rodriguez H., and Loechler E.L. Mutational specificity of the (+)-anti-diol epoxide of benzo[a]pyrene in a supF gene of an Escherichia coli plasmid: DNA sequence context influences hotspots, mutagenic specificity and the extent of SOS enhancement of mutagenesis. Carcinogenesis 14 (1993) 373-383
28. Rodriguez F.A., Cai Y., Lin C., Tang Y., Kolbanovskiy A., Amin S., et al. Exocyclic amino groups of flanking guanines govern sequence-dependent adduct conformations and local structural distortions for minor groove-aligned benzo[a]pyrenyl-guanine lesions in a GG mutation hotspot context. Nucleic Acids Res. 35 (2007) 1555-1568
29. Cosman M., de los Santos C., Fiala R., Hingerty B.E., Singh S.B., Ibanez V., et al. Solution conformation of the major adduct between the carcinogen (+)-anti-benzo[a]pyrene diol epoxide and DNA. Proc. Natl Acad. Sci. USA 89 (1992) 1914-1918
30. Xu R., Mao B., Amin S., and Geacintov N.E. Bending and circularization of site-specific and stereoisomeric carcinogen-DNA adducts. Biochemistry 37 (1998) 769-778
31. Min J.H., and Pavletich N.P. Recognition of DNA damage by the Rad4 nucleotide excision repair protein. Nature 449 (2007) 570-575
32. Case D.A., Darden T.A., Cheatham III T.E., Simmerling C.L., Wang J., Duke R.E., et al. AMBER 8.0 (2004), University of California, San Francisco, CA
33. Simmerling C., Elber R., and Zhang J. MOIL-View-a program for visualization of structure and dynamics of biomolecules and STO-a program for computing stochastic paths. In: Pullman A., et al. (Ed). Modeling of Biomolecular Structure and Mechanisms (1995), Kluwer, Dordrecht, The Netherlands
34. Calladine C.R. Mechanics of sequence-dependent stacking of bases in B-DNA. J. Mol. Biol. 161 (1982) 343-352
35. Gueron M., and Leroy J.L. Studies of base pair kinetics by NMR measurement of proton exchange. Methods Enzymol. 261 (1995) 383-413
36. Patel D.J., Pardi A., and Itakura K. DNA conformation, dynamics, and interactions in solution. Science 216 (1982) 581-590
37. Dickerson R.E. DNA bending: the prevalence of kinkiness and the virtues of normality. Nucleic Acids Res. 26 (1998) 1906-1926
38. Gorin A.A., Zhurkin V.B., and Olson W.K. B-DNA twisting correlates with base-pair morphology. J. Mol. Biol. 247 (1995) 34-48
39. Olson W.K., Gorin A.A., Lu X.J., Hock L.M., and Zhurkin V.B. DNA sequence-dependent deformability deduced from protein-DNA crystal complexes. Proc. Natl Acad. Sci. USA 95 (1998) 11163-11168
40. Fratini A.V., Kopka M.L., Drew H.R., and Dickerson R.E. Reversible bending and helix geometry in a B-DNA dodecamer: CGCGAATTBrCGCG. J. Biol. Chem. 257 (1982) 14686-14707
41. Kollman P.A., Massova I., Reyes C., Kuhn B., Huo S., Chong L., et al. Calculating structures and free energies of complex molecules: combining molecular mechanics and continuum models. Acc. Chem. Res. 33 (2000) 889-897
42. Liu T., Xu J., Tsao H., Li B., Xu R., Yang C., et al. Base sequence-dependent bends in site-specific benzo[a]pyrene diol epoxide-modified oligonucleotide duplexes. Chem. Res. Toxicol. 9 (1996) 255-261
43. Xu, J. (1999). Sequence dependence of carcinogen-induced DNA bending. PhD thesis, New York University.
44. Thoma B.S., and Vasquez K.M. Critical DNA damage recognition functions of XPC-hHR23B and XPA-RPA in nucleotide excision repair. Mol. Carcinog. 38 (2003) 1-13
45. Mocquet V., Kropachev K., Kolbanovskiy M., Kolbanovskiy A., Tapias A., Cai Y., et al. The human DNA repair factor XPC-HR23B distinguishes stereoisomeric benzo[a]pyrenyl-DNA lesions. EMBO J. 26 (2007) 2923-2932
46. Ruan Q., Liu T., Kolbanovskiy A., Liu Y., Ren J., Skorvaga M., et al. Sequence context- and temperature-dependent nucleotide excision repair of a benzo[a]pyrene diol epoxide-guanine DNA adduct catalyzed by thermophilic UvrABC proteins. Biochemistry 46 (2007) 7006-7015
47. Yang W. Structure and mechanism for DNA lesion recognition. Cell Res. 18 (2008) 184-197
48. Lu X.J., and Olson W.K. 3DNA: a software package for the analysis, rebuilding and visualization of three-dimensional nucleic acid structures. Nucleic Acids Res. 31 (2003) 5108-5121
49. Xu R., Mao B., Xu J., Li B., Birke S., Swenberg C.E., and Geacintov N.E. Stereochemistry-dependent bending in oligonucleotide duplexes induced by site-specific covalent benzo[a]pyrene diol epoxide-guanine lesions. Nucleic Acids Res. 23 (1995) 2314-2319
50. Cornell W.D., Cieplak P., Bayly C.I., Gould I.R., Merz K.M., Ferguson D.M., et al. A 2nd generation force field for the simulation of proteins, nucleic acids, and organic molecules. J. Am. Chem. Soc. 117 (1995) 5179-5197
51. Cheatham T.E., Cieplak P., and Kollman P.A. A modified version of the Cornell et al. force field with improved sugar pucker phases and helical repeat. J. Biomol. Struct. Dyn. 16 (1999) 845-862
52. Yan S., Wu M., Patel D.J., Geacintov N.E., and Broyde S. Simulating structural and thermodynamic properties of carcinogen-damaged DNA. Biophys. J. 84 (2003) 2137-2148 Erratum in: Biophys J. 92, 697
53. Case D.A., Pearlman D.A., Caldwell J.W., Cheatham III T.E., Wang J., Ross W.S., et al. AMBER 7.0 (2002), University of California, San Francisco, CA
54. Ravishanker G., Swaminathan S., Beveridge D.L., Lavery R., and Sklenar H. Conformational and helicoidal analysis of 30 PS of molecular dynamics on the d(CGCGAATTCGCG) double helix: "curves," dials and windows. J. Biomol. Struct. Dyn. 6 (1989) 669-699
55. Ravishanker G., and Beveridge D.L. MD Toolchest 2.0 (1993), Wesleyan University, Middletown, CT
56. DeLano W.L. The PyMOL Molecular Graphics System (2002), DeLano Scientific, Palo Alto, CA
57. Hingerty B.E., Figueroa S., Hayden T.L., and Broyde S. Prediction of DNA structure from sequence: a build-up technique. Biopolymers 28 (1989) 1195-1222