Sequence effects on translesion synthesis of an aminofluorene-DNA adduct: Conformational, thermodynamic, and primer extension kinetic studies

Biochemistry

Volumn 51, Issue 9, 2012, Pages 1983-1995

  Vaidyanathan, V G ^a   Cho, Bongsup P ^a  

^a UNIVERSITY OF RHODE ISLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; BASE PAIRS; CONFORMATIONAL HETEROGENEITY; DNA POLYMERASE; INSERTION RATES; KINETIC STUDY; KLENOW FRAGMENT; LESION SITE; PRIMER EXTENSION; STRUCTURAL FACTOR; STRUCTURE-FUNCTION RELATIONSHIP; TRANSLESION DNA SYNTHESIS; TRANSLESION SYNTHESIS;

NUCLEOTIDES;

DNA;

AMINOFLUORENE; DNA DIRECTED DNA POLYMERASE BETA; EXONUCLEASE; FLUORENE DERIVATIVE; NUCLEOTIDE; UNCLASSIFIED DRUG;

ARTICLE; BASE PAIRING; CATALYSIS; CIRCULAR DICHROISM; CONFORMATION; CONTROLLED STUDY; DIFFERENTIAL SCANNING CALORIMETRY; DNA ADDUCT; DNA SEQUENCE; DNA TEMPLATE; FLUORINE NUCLEAR MAGNETIC RESONANCE; GENE INSERTION; KINETICS; PRIORITY JOURNAL; SYNTHESIS; THERMODYNAMICS; TRANSLESION SYNTHESIS;

BASE PAIRING; BASE SEQUENCE; DEOXYGUANOSINE; DNA; DNA ADDUCTS; DNA POLYMERASE I; DNA REPLICATION; FLUORENES; KINETICS; MOLECULAR CONFORMATION; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; STEREOISOMERISM; THERMODYNAMICS;

EID: 84857809367     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi2017443     Document Type: Article

References (51)

1. Luch, A. (2005) Nature and nurture: Lessons from chemical carcinogenesis Nat. Rev. Cancer 5, 113-125
2. Hubscher, U. and Maga, G. (2011) DNA replication and repair bypass machines Curr. Opin. Chem. Biol. 5, 627-635
3. Kelly, M. R. (2011) DNA Repair in Cancer Therapy, Academic Press, Amsterdam.
4. Seo, K.-Y., Jelinsky, S. A., and Loechler, E. L. (2000) Factors that influence the mutagenic patterns of DNA adducts from chemical carcinogens Mutat. Res. 463, 215-246
5. Shibutani, S., Suzuki, N., Tan, X., Johnson, F., and Grollman, A. P. (2001) Influence of Flanking Sequence Context on the Mutagenicity of Acetylaminofluorene-Derived DNA Adducts in Mammalian Cells Biochemistry 40, 3717-3722
6. Skipper, P. L., Kim, M. Y., Sun, H. L., Wogan, G. N., and Tannenbaum, S. R. (2010) Monocyclic aromatic amines as potential human carcinogens: Old is new again Carcinogenesis 31, 50-58
7. Neumann, H. G. (2007) Aromatic amines in experimental cancer research: Tissue-specific effects, an old problem and new solutions Crit. Rev. Toxicol. 37, 211-236
8. Turesky, R. J. and Le Marchand, L. (2011) Metabolism and biomarkers of heterocyclic aromatic amines in molecular epidemiology studies: Lessons learned from aromatic amines Chem. Res. Toxicol. 24, 1169-1214
9. Heflich, R. H. and Neft, R. E. (1994) Genetic toxicity of 2-acetylaminofluorene, 2-aminofluorene and some of their metabolites and model metabolites Mutat. Res. 318, 73-174
10. Beland, F. A. and Kadlubar, F. F. (1990) Handbook of Experimental Pharmacology, pp 267-325, Spring-Verlag, Heidelberg, Germany.
11. 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
12. Cho, B. (2010) Structure-function characteristics of aromatic amine-DNA adducts. In The Chemical Biology of DNA Damage, pp 217-238, Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, Germany.
13. Lukin, M. and de Los Santos, C. (2006) NMR structures of damaged DNA Chem. Rev. 106, 607-686
14. Cho, B. P. (2004) Dynamic conformational heterogeneities of carcinogen-DNA adducts and their mutagenic relevance J. Environ. Sci. Health, Part C: Environ. Carcinog. Ecotoxicol. Rev. 22, 57-90
15. Patnaik, S. and Cho, B. P. (2010) Structures of 2-acetylaminofluorene modified DNA revisited: Insight into conformational heterogeneity Chem. Res. Toxicol. 23, 1650-1652
16. 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
17. Dutta, S., Li, Y., Johnson, D., Dzantiev, L., Richardson, C. C., Romano, L. J., and Ellenberger, T. (2004) Crystal structures of 2-acetylaminofluorene and 2-aminofluorene in complex with T7 DNA polymerase reveal mechanisms of mutagenesis Proc. Natl. Acad. Sci. U.S.A. 101, 16186-16191
18. 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
19. Meneni, S., Liang, F., and Cho, B. P. (2007) Examination of the Long-range Effects of Aminofluorene-induced Conformational Heterogeneity and Its Relevance to the Mechanism of Translesional DNA Synthesis J. Mol. Biol. 366, 1387-1400, Erratum, volume 1398, p 1786
20. Nagalingam, A., Seo, K. Y., and Loechler, E. L. (2005) Mutagenesis studies of the major benzo[a]pyrene N2-dG adduct in a 5′-TG versus a 5′-UG sequence: Removal of the methyl group causes a modest decrease in the [G->T/G->A] mutational ratio Mutagenesis 20, 105-110
21. Meneni, S., Shell, S. M., Zou, Y., and Cho, B. P. (2007) Conformation-specific recognition of carcinogen-DNA adduct in Escherichia coli nucleotide excision repair Chem. Res. Toxicol. 20, 6-10
22. 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
23. Ruan, Q., Liu, T., Kolbanovskiy, A., Liu, Y., Ren, J., Skorvaga, M., Zou, Y., Lader, J., Malkani, B., Amin, S., Van Houten, B., and Geacintov, N. E. (2007) 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, 7006-7015
24. Cai, Y., Patel, D. J., Geacintov, N. E., and Broyde, S. (2007) 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, 292-305
25. -) activity on damaged DNA templates: Effect of proximal and distal template damage on DNA synthesis Biochemistry 36, 15336-15342
26. Rechkoblit, O., Kolbanovskiy, A., Malinina, L., Geacintov, N. E., Broyde, S., and Patel, D. J. (2010) Mechanism of error-free and semitargeted mutagenic bypass of an aromatic amine lesion by Y-family polymerase Dpo4 Nat. Struct. Mol. Biol. 17, 379-388
27. Suzuki, N., Ohashi, E., Hayashi, K., Ohmori, H., Grollman, A. P., and Shibutani, S. (2001) Translesional synthesis past acetylaminofluorene-derived DNA adducts catalyzed by human DNA polymerase κ and Escherichia coli DNA polymerase IV Biochemistry 40, 15176-15183
28. Liang, F. and Cho, B. P. (2007) Probing the thermodynamics of aminofluorene-induced translesion DNA synthesis by differential scanning calorimetry J. Am. Chem. Soc. 129, 12108-12109
29. Liang, F. and Cho, B. P. (2011) Conformational and thermodynamic impact of bulky aminofluorene adduction on simulated translesion DNA synthesis Chem. Res. Toxicol. 24, 597-605
30. Liang, F., Meneni, S., and Cho, B. P. (2006) Induced circular dichroism characteristics as conformational probes for carcinogenic aminofluorene-DNA adducts Chem. Res. Toxicol. 19, 1040-1043
31. 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
32. Elmquist, C. E., Wang, F., Stover, J. S., Stone, M. P., and Rizzo, C. J. (2007) Conformational differences of the C8-deoxyguanosine adduct of 2-amino-3-methylimidazo[4,5-f]quinoline (IQ) within the NarI recognition sequence Chem. Res. Toxicol. 20, 445-454
33. Wang, F., DeMuro, N. E., Elmquist, C. E., Stover, J. S., Rizzo, C. J., and Stone, M. P. (2006) Base-displaced intercalated structure of the food mutagen 2-amino-3-methylimidazo[4,5-f]quinoline in the recognition sequence of the NarI restriction enzyme, a hotspot for -2 bp deletions J. Am. Chem. Soc. 128, 10085-10095
34. Wang, F., Elmquist, C. E., Stover, J. S., Rizzo, C. J., and Stone, M. P. (2007) DNA sequence modulates the conformation of the food mutagen 2-amino-3-methylimidazo[4,5-f]quinoline in the recognition sequence of the NarI restriction enzyme Biochemistry 46, 8498-8516
35. 19F NMR, UV, and CD spectroscopy Biochemistry 46, 13310-13321
36. Brown, K., Hingerty, B. E., Guenther, E. A., Krishnan, V. V., Broyde, S., Turteltaub, K. W., and Cosman, M. (2001) Solution structure of the 2-amino-1- methyl-6-phenylimidazo[4,5-b]pyridine C8-deoxyguanosine adduct in duplex DNA Proc. Natl. Acad. Sci. U.S.A. 98, 8507-8512
37. 19F NMR Evidence J. Am. Chem. Soc. 119, 5384-5389
38. Gu, Z., Gorin, A., Hingerty, B. E., Broyde, S., and Patel, D. J. (1999) Solution structures of aminofluorene [AF]-stacked conformers of the syn [AF]-C8-dG adduct positioned opposite dC or dA at a template-primer junction Biochemistry 38, 10855-10870
39. Mao, B., Gu, Z., Gorin, A., Hingerty, B. E., Broyde, S., and Patel, D. J. (1997) Solution structure of the aminofluorene-stacked conformer of the syn [AF]-C8-dG adduct positioned at a template-primer junction Biochemistry 36, 14491-14501
40. Broyde, S., Wang, L., Zhang, L., Rechkoblit, O., Geacintov, N. E., and Patel, D. J. (2008) DNA adduct structure-function relationships: Comparing solution with polymerase structures Chem. Res. Toxicol. 21, 45-52
41. Hsu, G. W., Kiefer, J. R., Burnouf, D., Becherel, O. J., Fuchs, R. P. P., and Beese, L. S. (2004) Observing Translesion Synthesis of an Aromatic Amine DNA Adduct by a High-fidelity DNA Polymerase J. Biol. Chem. 279, 50280-50285
42. Norman, D., Abuaf, P., Hingerty, B. E., Live, D., Grunberger, D., Broyde, S., and Patel, D. J. (1989) NMR and computational characterization of the N-(deoxyguanosin-8-yl)aminofluorene adduct [(AF)G] opposite adenosine in DNA: (AF)G[syn]·A[anti] pair formation and its pH dependence Biochemistry 28, 7462-7476
43. Jaloszynski, P., Ohashi, E., Ohmori, H., and Nishimura, S. (2005) Error-prone and inefficient replication across 8-hydroxyguanine (8-oxoguanine) in human and mouse ras gene fragments by DNA polymerase κ Genes Cells 10, 543-550
44. Maddukuri, L., Eoff, R. L., Choi, J. Y., Rizzo, C. J., Guengerich, F. P., and Marnett, L. J. (2010) In vitro bypass of the major malondialdehyde- and base propenal-derived DNA adduct by human Y-family DNA polymerases κ, l, and Rev1 Biochemistry 49, 8415-8424
45. Berthet, N., Roupioz, Y., Constant, J. F., Kotera, M., and Lhomme, J. (2001) Translesional synthesis on DNA templates containing the 2′-deoxyribonolactone lesion Nucleic Acids Res. 29, 2725-2732
46. Asagoshi, K., Terato, H., Ohyama, Y., and Ide, H. (2002) Effects of a guanine-derived formamidopyrimidine lesion on DNA replication: translesion DNA synthesis, nucleotide insertion, and extension kinetics J. Biol. Chem. 277, 14589-14597
47. Liang, F. and Cho, B. P. (2010) Enthalpy-entropy contribution to carcinogen-induced DNA conformational heterogeneity Biochemistry 49, 259-266
48. Johnson, S. J. and Beese, L. S. (2004) Structures of mismatch replication errors observed in a DNA polymerase Cell 116, 803-816
49. Hsu, G. W., Huang, X., Luneva, N. P., Geacintov, N. E., and Beese, L. S. (2005) Structure of a high fidelity DNA polymerase bound to a benzo[a]pyrene adduct that blocks replication J. Biol. Chem. 280, 3764-3770
50. Alekseyev, Y. O. and Romano, L. J. (2002) Effects of benzo[a]pyrene adduct stereochemistry on downstream DNA replication in vitro: Evidence for different adduct conformations within the active site of DNA polymerase I (Klenow fragment) Biochemistry 41, 4467-4479
51. Forgacs, E., Latham, G., Beard, W. A., Prasad, R., Bebenek, K., Kunkel, T. A., Wilson, S. H., and Lloyd, R. S. (1997) Probing structure/function relationships of HIV-1 reverse transcriptase with styrene oxide N2-guanine adducts J. Biol. Chem. 272, 8525-8530