Nuclear magnetic resonance solution structures of covalent aromatic amine-DNA adducts and their mutagenic relevance

Chemical Research in Toxicology

Volumn 11, Issue 5, 1998, Pages 391-407

  Patel, Dinshaw J ^a   Mao, Bing ^a   Gu, Zhengtian ^a   Hingerty, Brian E ^b   Gorin, Andrey ^a   Basu, Ashis K ^c   Broyde, Suse ^d  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b OAK RIDGE NATIONAL LABORATORY   (United States)

^c UNIVERSITY OF CONNECTICUT   (United States)

^d NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC AMINE; CARCINOGEN; DOUBLE STRANDED DNA; INSECTICIDE; SINGLE STRANDED DNA;

DEACETYLATION; DNA ADDUCT; DNA REPLICATION; MUTAGENESIS; MUTAGENICITY; NUCLEAR MAGNETIC RESONANCE; NUCLEIC ACID BASE SUBSTITUTION; ONCOGENE; PROTEIN CONFORMATION; REVIEW;

AMINES; ANIMALS; DNA ADDUCTS; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MUTAGENS; SOLUTIONS;

EID: 0031800438     PISSN: 0893228X     EISSN: None     Source Type: Journal    
DOI: 10.1021/tx9702143     Document Type: Review

References (81)

1. Beland, F. A., and Kadlubar, F. F. (1990) Chemical carcinogenesis and mutagenesis. In Handbook of Experimental Pharmacology (Cooper, C. S., and Grover, P. L., Eds.) Vol. 94/I, pp 267-325, Springer-Verlag, Heidelberg.
2. Kriek, E. (1992) Fifty years of research on N-acetyl-2-aminofluorene, one of the most versatile compounds in experimental cancer research. J. Cancer Res. Clin. Oncol. 118, 481-489.
3. 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.
4. Hoffman, G. R., and Fuchs, R. P. P. (1997) Mechanisms of frameshift mutations: insight from aromatic amines. Chem. Res. Toxicol. 10, 347-359.
5. Weissberger, J. H. (1988) Past, present and future role of carcinogenic and mutagenic N-substituted aryl compounds in human cancer causation. In Carcinogenic and Mutagenic Responses to Aromatic Amines and Nitroarenes (King, C. M., Romano, L. J., and Schueltze, D., Eds.) pp 3-19, Elsevier, New York.
6. Sugimura, T. (1992) Multistep Carcinogenesis: a 1992 perspective. Science 258, 603-607.
7. Vineis, P. (1994) Epidemiology of cancer from exposure to arylamines. Environ. Health Perspect. 102 (6), 7-10.
8. Layton, D. W., Bogen, K. T., Knize, M. G., Hatch, F. T., Johnson, V. M., and Felton, J. S. (1995) Cancer risk of heterocyclic amines in cooked foods: an analysis and implications for research. Carcinogenesis 16, 39-52.
9. 8-AF. Carcinogenesis 12, 813-818.
10. 2-yl)- 2-(acetylamino)fluorene. Chem. Res. Toxicol. 6, 819-824.
11. Gulp, S. J., Poirier, M. C., and Beland, F. A. (1993) Biphasic removal of DNA adducts in a repetitive DNA sequence after dietary administration of 2-acetylaminofluorene. Environ. Health Perspect. 99, 273-275.
12. Belguise-Valladier, P., and Fuchs, R. P. 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.
13. Doisy, R., and Tang, M.-S. (1995) Effect of aminofluorene and (acetylamino)fluorene adducts on the DNA replication mediated by Escherichia coli Polymerascs I (Klenow fragment) and III. Biochemistry 34, 4358-4368.
14. Fuchs, R. P. P., Schwartz, N., and Daune, M. P. (1981) Hotspots of frameshift mutations induced by the ultimate carcinogen N-acetoxy-N-2-acetylaminofluorene. Nature 294, 657-659.
15. Koffel-Schwartz, N., Verdier, J.-M., Bichara, M., Freund, A.-M., Daune, M. P., and Fuchs, R. P. P. (1984) Carcinogen induced mutation spectrum in wild-type, uvr A and umu C strains of Bscherichia coli. J. Mol. Biol. 177, 33-51.
16. Burnouf, D., Koehl, P., and Fuchs, R. P. P. (1989) Single adduct mutagenesis: Strong effect of the position of a single acetylaminofluorene adduct within a mutation hot spot. Proc. Natl. Acad. Sci. U.S.A. 86, 4147-4689.
17. Fuchs, R. P. P. (1984) DNA binding spectrum of the carcinogen N-acetoxy-N-2-acetylamino fluorene significantly differs from the mutation spectrum. J. Mol. Biol. 177, 173-180.
18. Bichara, M., and Fuchs, R. P. P. (1985) DNA binding and mutation spectra of the carcinogen N-2-aminofluorene in E. coli: a correlation between the conformation of the premutagenic lesion and the mutation specificity. J. Mol. Biol. 183, 341-351.
19. Melchior, W. B., Jr., Marques, M. M., and Beland, F. A. (1994) Mutations induced by aromatic amine adducts in pBR322. Carcinogenesis 15, 889-899.
20. Tebbs, R. S., and Romano, L. J. (1994) Mutagenesis at a site- specifically modified NarI sequence by acetylated and deacetylated aminofluorene adducts. Biochemistry 33, 8998-9006.
21. Koffel-Schwartz, N., and Fuchs, R. P. P. (1995) Sequence determinants for -2 frameshift mutagenesis at NarI-derived hot spots. J. Mol. Biol. 252, 507-513.
22. Shibutani, S. and Grollman, A. P. (1997) Molecular mechanisms of mutagenesis by aromatic amines and amides. Mutat. Res. 376, 71-78.
23. Weinberg, R. A. (1996) How cancer arises. Sci. Am. 275, 62-70.
24. Bos J. L. (1989) Acts oncogenes in human cancer: a review. Cancer Res. 49, 4682-4689.
25. Conti, C. J. (1992) Mutations of genes of the ras family in human and experimental tumors. Comp. Mol. Carcinogen. 370, 357-378.
26. Harris, C. C. (1993) p53: At the crossroads of molecular carcinogenesis and risk assessment. Science 262, 1080-1981.
27. Husgafvel-Pursiainen, K., and Kannio, A. (1906) Cigarette smoking and p53 mutations in lung cancer and bladder cancer. Environ. Health Perspect. 104 (3), 553-556.
28. Geacintov, N. E., Cosman, M., Hingerty, B. E., Amin, S., Broyde, S., and Patel, D. J. (1997) NMR solution structures of stereoisomeric polycyclic aromatic carcinogen-DNA adducts: principles, patterns and diversity. Chem. Res. Toxicol. 10, 111-146.
29. O'Handley, S. F., Sanford, D. G., Xu, R., Lester, C. C., Hingerty, B. E., Broyde, S., and Krugh, T. R. (1993) Structural characterization of an N-acetyl-2-aminofluorene (AAF) modified DNA oligomer by NMR, energy minimization and molecular dynamics. Biochemistry 32, 2481-2497.
30. Grunberger, D., Nelson, J. H., Cantor, C., and Weinstein, I. B. (1970) Coding and conformational properties of oligonucleotides modified with the carcinogen N-2-acetylaminofluorene. Proc. Natl. Acad. Sci. U.S.A. 66, 488-404.
31. Fuchs, R. P. P., and Duane, M. (1971) Changes of stability and conformation of DNA following the covalent binding of a carcinogen. FEBS Lett. 14, 206-208.
32. Hingerty, B., and Broyde, S. (1982) Conformation of the deoxydinucleoside monophosphate dCpdG modified at carbon 8 of guanine with 2-(acetylamino)fluorene. Biochemistry 21, 3243- 3252.
33. Broyde, S., and Hingerty, B. E. (1983) Conformation of 2-aminofluorene modified DNA. Biopolymers 22, 2423-2441.
34. Shapiro, R., Sidawi, D., Miao, Y.-S., Hingerty, B. E., Schmidt, K. E., Moskowitz, J., and Broyde, S. (1994) Conformation of amine- modified DNA: 2-aminofluorene and 2-(acetylamino) fluorene- modified deoxydinucleoside monophosphates with all possible nearest neighbors - a comparison of search and optimization methods. Chem. Res. Toxicol. 7, 239-252.
35. Eckel, L. M., and Krugh, T. R. (1994) 2-Aminofluorene modified DNA duplex exists in two interchangeable conformations. Nature Struct. Biol. 1, 89-94.
36. Eckel, L. M., and Krugh, T. R. (1994) Structural characterization of two interchangeable conformations of a 2-aminofluorene- modified DNA oligomer by NMR and energy minimizations. Biochemistry 33, 13611-13624.
37. Cho, B. P., Beland, F. A., and Marques, M. M. (1994) NMR structural studies of a 15-mer duplex from a ras protooncogene modified with the carcinogen 2-aminofluorene: conformational heterogeneity. Biochemistry 33, 1373-1384.
38. 19F NMR evidence. J. Am. Chem. Soc. 119, 5384-5389.
39. Vousden, K. H., Bos, J. L., Marshall, C. J., and Phillips, D. H. (1986) Mutations activating human c-Ha-ras1 protooncogene (HRAS1) induced by chemical carcinogens and depurination. Proc. Natl Acad. Sci. U.S.A. 83, 1222-1226.
40. Wiseman, R. W., Stowers, S. J., Miller, E. C., Anderson, M. W., and Miller, J. A. (1986) Activating mutations of the C-Ha-ras protooncogene in chemically induced hepatomas of the male B6C3 F1 mouse. Proc. Natl. Acad. Sci. U.S.A. 83, 5825-5829.
41. 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-ideoxyguanosin-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.
42. 8-dG adduct opposite dC in a DNA duplex. Biochemistry 37, 81-94.
43. 8-dG adduct opposite dC in a DNA. duplex. Biochemistry 37, 95-106.
44. Hingerty B. E., and Broyde, S. (1986) Energy-minimized structures of carcinogen-DNA adducts: 2-acetylaminofluorene and 2-aminofluorene: J. Biomol. Struct. Dyn. 4, 365-371.
45. Cho, B. P., Beland, F. A., and Marques, M. M. (1992) NMR studies of a 15-mer DNA sequence from a ras protooncogene modified a the first base of codon 61 with the carcinogen 4-aminobiphenyl. Biochemistry 31, 9587-9602.
46. Broyde, S., Hingerty, B. E., and Srinivasan, A. R. (1985) Influence of the carcinogen 4-aminobiphenyl on DNA conformation. Car cinogenesis 6, 719-725.
47. Shapiro, R., Underwood, G. R., Zawadzka, H., Broyde, S., and Hingerty, B. E. (1986) Conformation of d(CpG) modified by the Carcinogen 4-aminobiphenyl: a Combined experimental and theo retical analysis. Biochemistry 25, 2198-2205.
48. Akayama, M., Watanabe, T., and Kakihana, M. (1986) Internal rotation of biphenyl in solution studied by IR and NMR spectra. J. Phys. Chem. 90, 1751-1755.
49. Mao, B., Vyas, R. R., Hingerty, B. E., Broyde, S., Basu, A. K., and Patel, D. J. (1996) Solution conformation of the N-(deoxyguanosin-8-yl)-1-aminopyrene ([AP]dG) adduct opposite dC in aDNA duplex. Biochemistry 35, 12659-12670.
50. 8-dG adduct positioned at a DNA template-primer junction. Biochemistry 36, 14491-14501.
51. 8-dG adduct positioned opposite dC at a template-primer junction. Biochemistry, submitted.
52. 8-dG adduct positioned opposite dA at a template-primer junction. Biochemistry, submitted.
53. Basu, A. K., and Essigmann, J. M. (1988) Site specifically modified oligodeoxynucleotides as probes for the structural and biological effects of DNA damaging agents. Chem. Res. Toxicol. 1, 1-18.
54. Carothers, A. M., Urlaub, G., Mucha, J., Yuan, W., Chasin, L. A., and Grunberger, D. (1993) A mutational hot spot induced by N-hydroxy-aminofluorene in dihydrofolate reductase mutants of Chinese hamster ovary cells. Carcinogenesis 14, 2181-2184.
55. Patel, D. J. (1982) Antibiotic-DNA interactions: intermodular nuclear Overhauser effects in the netropsin-d(C-G-C-G-A-A-T-T- C-G-CG) complex in solution. Proc. Natl. Acad. Sci. U.S.A. 79, 6425-6428.
56. Kopka, M. L., Yoon, C., Goodsell, D., Pjura, P., and Dickerson, R. E. (1985) The molecular origin of DNA-drug specificity in netropsin and distamycin. Proc. Natl. Acad. Sci. U.S.A. 82, 1376-1380.
57. Abuaf, P., Hingerty, B. E., Broyde, S., and Grunberger, D. (1995) Solution conformation of the N-(deoxyguanosin-8-yl)-aminofluorene adduct opposite deoxyinosine and deoxyguanosine in DNA by NMR and computational characterization. Chem. Res. Toxicol. 8, 369-378.
58. Gu, Z., Gorin, A., Krishnaswami, R., Hingerty, H. E., Basu, A. K., Broyde, S., and Patel, D. J. (1998) Solution structure of the N-(deoxyguanosin-8-yl)-1-aminopyrene ([AP]dG) adduct opposite dA in a DNA duplex. Biochemistry, submitted.
59. 8-modified syn guanine into the major groove. Biochemistry 34, 6226-6238.
60. Mao, B., Hingerty, B. E., Broyde, S., and Patel, D. J. (1995) Solution conformation of [AF]dG opposite a - 2 deletion site in a DNA duplex: intercalation of the covalently attached aminofluorene ring into the helix with base displacement of the C8-modified syn guanine and adjacent unpaired 3′-adenine into the major groove. Biochemistry 34, 16641-16653.
61. 8-dG adduct opposite a -2 deletion site in the NarI hotspot sequence context. Biochemistry 36, 14479-14490.
62. Milhé, C., Dhalluin, C., Fuchs, R. P. P., and Lefevre, J. F. (1994) NMR evidence of the stabilization by the carcinogen N-2-acetylaminofluorene of a frameshift intermediate. Nucleic Acids Res. 32, 4646-4652.
63. Milhé, C., Fuchs, R. P. P., and Lefevre, J. F. (1996) NMR data show that the carcinogen N-2-acetylaminofluorene stabilizes an intermediate of - 2 frameshift mutagenesis in a region of high mutation frequency. Eur. J. Biochem. 235, 120-127.
64. Ya, N.-Q., Smirnov, S., Cosman, M., Bhanot, S., Ibanez, V., and Geacintov, N. E. (1994) Thermal stabilities of benzo[a]pyrenediol epoxide-modified oligonucleotide duplexes. Effects of mismatched complementary strands and bulges. In Structural Biology; The State of the Art. Proceedings of the 8th Conversation (Sarma, R. H., and Sarma, M. H., Eds.) Vol. 2, pp 349-366, Adenine Press: New York.
65. Mekhovich, O., Tang, M.-S., and Romano, L. (1998) The rate of incision of N-acetyl-2-aminofluorene and N-2-aminofluorene adducts by UvrABC nuclease is adduct and sequence specific. A comparison of the rates of UvrABC incision and protein-DNA complex formation. Biochemistry 37, 571-579.
66. O'Handley, S. F. (1991) Structural analysis of a carcinogen- modified DNA oligomer by NMR spectroscopy. Ph.D. Thesis, University of Rochester, Rochester, NY.
67. Kunkel, T. A. (1990) Misalignment-mediated DNA synthesis errors. Biochemistry 29, 8003-8011.
68. Kunkel, T. A. (1992) DNA replication fidelity. J. Biol. Chem. 267, 18251-18254.
69. Schaaper, R. M., Koffei-Schwartz, N., and Fuchs, R. P. P. (1990) N-acetoxy-N-acetyl-2-aminofluorene induced mutagenesis in the lacI gene of Escherichia coli. Carcinogenesis 11, 1087-1095.
70. Lambert, I. B., Napolitano, R. L., and Fuchs, R. P. P. (1992) Carcinogen-induced frameshift mutagenesis in repetitive sequences. Proc. Natl. Acad. Sci. U.S.A. 89, 1310-1314.
71. Shibutani, S., and Grollman, A. P. (1993) On the mechanism of frameshift (deletion) mutagenesis in vitro. J. Biol. Chem. 268, 11703-11710.
72. Friedberg, E. C., Walter, G. C., and Siede, W. (1995) DNA Repair and Mutagenesis, p 386, ASM Press, Washington, DC.
73. Peltomaki, P. (1997). DNA mismatch repair gene mutations in human cancer. Environ. Health Perspect. 105 (Suppl. 4), 775- 780.
74. Shapiro, R., Ellis, S., Hingerty, B. E., and Broyde, S. (1998) Effect of ring size on conformations of aromatic amine - DNA adducts: The aniline-C8 guanine adduct resides in the B-DNA major groove. Chem. Res. Toxicol. 11, 335-341.
75. 3 sequence: effects of SOS proofreading and mismatch repair. Biochemistry 35, 4568-4577.
76. Rodriguez, H., and Loechler, E. L. (1995) Are base substitution and frameshift mutagenesis pathways interrelated? An analysis based upon studies of the frequencies and specificities of mutations induced by the (+)-anti diol epoxide of benzo[a]pyrene. Mutat. Res. 326, 29-37.
77. Fountain, M. A., and Krugh, T. R. (1995) Structural characterization of a (+)-trans-anti-benzo[a]pyrene-DNA. adduct using NMR, restrained energy minimization, and molecular dynamics. Biochemistry 34, 3152-3161.
78. Broyde, S., and Hingerty, B. E. (1984) Mutagenicity of polycyclic aromatic hydrocarbons and amines: a conformational hypothesis, Ann. N. Y. Acad. Sci. 435, 119-122.
79. Moore, P. D., Rabkin, S. D., Osborn, A. L., King, C. M., and Strauss, B. S. (1982) The effect of acetylated and deacetylated aminofluorene adducts on in vitro DNA synthesis. Proc. Natl. Acad. Sci. U.S.A. 79, 7166-7170.
80. Shibutani, S., Takeshita, M., and Grollman, A. P. (1991) Insertion of specific bases during DNA synthesis past the oxidation damaged base 8-oxodG. Nature 349, 431-434.
81. Moriya, M., Zhang, W., Johnson, F., and Grollman, A. P. (1994) Mutagenic potency of exocyclic DNA adducts: marked differences between Escherichia coli and simian kidney cells. Proc. Natl. Acad. Sci. U.S.A. 91, 11899-11903.