Following an environmental carcinogen N2-dG adduct through replication: Elucidating blockage and bypass in a high-fidelity DNA polymerase

Nucleic Acids Research

Volumn 35, Issue 13, 2007, Pages 4275-4288

  Xu, Pingna ^a   Oum, Lida ^a   Beese, Lorena S ^b   Geacintov, Nicholas E ^a   Broyde, Suse ^a  

^a NEW YORK UNIVERSITY   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BENZO[A]PYRENE DERIVATIVE; CARCINOGEN; DNA POLYMERASE; NUCLEOTIDE; OLIGONUCLEOTIDE; PURINE; BENZO(A)PYRENE N2 DG ADDUCT; BENZO(A)PYRENE N2-DG ADDUCT; DEOXYGUANOSINE; DNA; DNA DIRECTED DNA POLYMERASE BETA; DRUG DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS; BACTERIAL GENETICS; CHEMICAL STRUCTURE; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; ENZYME STRUCTURE; GENE INSERTION; GENE REPLICATION; IN VIVO STUDY; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; BINDING SITE; BIOLOGY; BIOSYNTHESIS; CHEMISTRY; CONFORMATION; DNA ADDUCT; DNA REPLICATION; HYDROGEN BOND; METABOLISM;

BENZOPYRENES; BINDING SITES; CARCINOGENS; COMPUTATIONAL BIOLOGY; DEOXYGUANOSINE; DNA; DNA ADDUCTS; DNA POLYMERASE I; DNA REPLICATION; HYDROGEN BONDING; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; NUCLEOTIDES;

EID: 34547829269     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkm416     Document Type: Article

References (72)

1. Luch,A. (2005) Nature and nurture - lessons from chemical carcinogenesis. Nat. Rev. Cancer, 5, 113-125.
2. Fontcuberta,M., Arques,J.F., Martinez,M., Suarez,A., Villalbi,J.R., Centrich,F., Serrahima,E., Duran,J. and Casas,C. (2006) Polycyclic aromatic hydrocarbons in food samples collected in Barcelona, Spain. J. of Food Prot., 69, 2024-2028.
3. Tuntawiroon,J., Mahidol,C., Navasumrit,P., Autrup,H. and Ruchirawat,M. (2006) Increased health risk in Bangkok children exposed to polycyclic aromatic hydrocarbons from traffic-related sources. Carcinogenesis 28, 816-822.
4. Burczynski,M.E., Harvey,R.G. and Penning,T.M. (1998) Expression and characterization of four recombinant human dihydrodiol dehydrogenase isoforms: Oxidation of trans-7, 8-dihydroxy-7, 8-dihydrobenzo[a]pyrene to the activated o-quinone metabolite benzo[a]pyrene-7,8-dione. Biochemistry, 37, 6781-6790.
5. Cavalieri,E.L. and Rogan,E.G. (1995) Central role of radical cations in metabolic activation of polycyclic aromatic hydrocarbons. Xenobiotica 25, 677-688.
6. Conney,A.H. (1982) Induction of microsomal enzymes by foreign chemicals and carcinogenesis by polycyclic aromatic hydrocarbons: G. H. A. Clowes Memorial Lecture. Cancer Res., 42, 4875-4917.
7. Buening,M.K., Wislocki,P.G., Levin,W., Yagi,H., Thakker,D.R., Akagi,H., Koreeda,M., Jerina,D.M. and Conney,A.H. (1978) Tumorigenicity of the optical enantiomers of the diastereomeric benzo[a]pyrene 7,8-diol-9,10-epoxides in newborn mice: Exceptional activity of (+)-7β,8α-dihydroxy-9α,10α-epoxy-7,8,9, 10-tetrahydrobenzo[a]pyrene. Proc. Natl Acad. Sci. USA, 75, 5358-5361.
8. Szeliga,J. and Dipple,A. (1998) DNA adduct formation by polycyclic aromatic hydrocarbon dihydrodiol epoxides. Chem. Res. Toxicol., 11, 1-11.
9. Cheng,S.C., Hilton,B.D., Roman,J.M. and Dipple,A. (1989) DNA adducts from carcinogenic and noncarcinogenic enantiomers of benzo[a]pyrene dihydrodiol epoxide. Chem. Res. Toxicol., 2, 334-340.
10. Geacintov,N.E., Cosman,M., Hingerty,B.E. Amin,S., Broyde,S. and Pate,J.D.J. (1997) NMR solution structures of stereoisometric covalent polycyclic aromatic carcinogen-DNA adduct: Principles, patterns, and diversity. Chem. Res. Toxicol., 10, 111-146.
11. Meehan,T. and Straub,K. (1979) Doublb-stranded DNA steroselectively binds benzo[a]pyrene diol epoxides. Nature, 277, 410-412.
12. Alekseyev,Y.O. and Romano,L.J. (2000) In vitro replication of primer-templates containing benzo[a]pyrene adducts by exonuclease-deficient Escherichia coli DNA polymerase I (Klenow fragment): Effect of sequence context on lesion bypass. Biochemistry 39, 10431-10438.
13. Hanrahan,C.J., Bacolod,M.D., Vyas,R.R., Liu,T., Geacintov,N.E., Loechler,E.L. and Basu,A.K. (1997) Sequence specific mutagenesis of the major (+)-anti-benzo[a]pyrene diol epoxide-DNA adduct at a mu tational hot spot in vitro and in Escherichia coli cells. Chem. Res. Toxicol., 10 369-377.
14. Zhuang,P., Kolbanovskiy,A., Amin,S. and Geacintov,N.E. (2001) Base sequence dependence of in vitro translesional DNA replication past a bulky lesion catalyzed by the exo- Klenow fragment of Pol I. Biochemistry, 40, 6660-6669.
15. 2-dG benzo[a] pyrene adduct s in the identical 5′-CGC sequence used in NMR studies: G←T mutations dominate in each case. Mutagenesis, 20 441-448.
16. 2-dG adduct are b ypassed by different lesion-bypass DNA polymerases in E. coli. DNA Repair (Amst), 5, 515-522.
17. 2-deoxyguanosine adducts of 7,8-dihydroxy-9,10-epoxy-7,8,9,10-tetrahydrobenzo[a]pyre ne: Configuration of the adduct bond is more important than those of the hydroxyl groups. Biochemistry, 36, 13263-13269.
18. 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.
19. Moriya,M., Spiegel,S., Fernandes,A., Amin,S., Liu,T., Geacintov,N. and Grollman,A.P. (1996) Fidelity of translesional synthesis past benzo[a]pyrene diol epoxide-2′-deoxyguanosine DNA adducts: Marked effects of host cell, sequence context, and chirality. Biochemistry 35, 16646-16651.
20. 2-Gua adduct of the (+)-anti-benzo i apyrene dio l epoxide is capable of inducing G←A and G←C, in addition to G←T,mutations. Biochemistry, 34, 13545-13553.
21. Shen,X., Sayer,J.M., Kroth,H., Ponten,I., O'Donnell,M., Woodgate,R., Jerina,D.M. and Goodman,M.F. (2002) Efficiency and accuracy of SOS-induced DNA polymerases replicating benzo[a]pyrene-7,8-diol 9,1 0-epoxide A and G adducts. J. Biol. Chem. 277, 5265-5274.
22. 2-2′-d eoxyguanosine adducts in Escherichia coli and simian kidney cells. Biochemistry, 37 10164-10172.
23. 2-dG DNA adducts in yeast cells. Nucleic Acids Res., 34, 417-425.
24. Avkin,S., Goldsmith,M., Velasco-Miguel,S., Geacintov,N., Friedberg,E.C. and Livneh,Z. (2004) Quantitative analysis of translesion DNA synthesis across a benzo[a]pyrene-guanine adduct in mammalian cells: The role of DNA polymerase κ. J. Biol. Chem., 279, 53298-53305.
25. Pages,V. and Fuchs,R.P. (2002) How DNA lesions are turned into mutations within cells? Oncogene, 21, 8957-8966.
26. Friedberg,E.C., Lehmann,A.R. and Fuchs,R.P. (2005) Trading places: How do DNA polymerases switch during translesion DNA synthesis? Mol. Cell 18, 499-505.
27. Plosky,B.S. and Woodgate,R. (2004) Switching from high-fidelity replicases to low-fidelity lesion-bypass polymerases. Curr. Opin. Genet. Dev., 14, 113-119.
28. McCulloch,S.D., Kokoska,R.J., Chilkova,O., Welch,C.M., Johansson,E., Burgers,P.M. and Kunkel,T.A. (2004) Enzymatic switching for efficient and accurate translesion DNA replication. Nucleic Acids Res., 32, 4665-4675.
29. Lehmann,A.R. (2006) Translesion synthesis in mammalian cells. Exp. Cell Res., 312, 2673-2676.
30. Prakash,S., Johnson,R.E. and Prakash,L. (2005) Eukaryotic translesion synthesis DNA polymerases: Specificity of structure and function. Annu. Rev. Biochem., 74, 317-353.
31. Guengerich,F.P. (2006) Interactions of carcinogen-bound DNA with individual DNA polymerases. Chem. Rev., 106, 420-452.
32. Lenne-Samuel,N., Janel-Bintz,R., Kolbanovskiy,A., Geacintov,N.E. and Fuchs,R.P. (2000) The processing of a Benzo[a]pyrene adduct into a frameshift or a base substitution mutation requires a different set of genes in Escherichia coli. Mol. Microbiol., 38, 299-307.
33. 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.
34. Kiefer,J.R., Mao,C., Hansen,C.J., Basehore,S.L., Hogrefe,H.H., Braman,J.C. and Beese,L.S. (1997) Crystal structure of a thermostable Bacillus DNA polymerase I large fragment at 2.1 A resolution. Structure, 5, 95-108.
35. Johnson,S.J., Taylor,J.S. and Beese,L.S. (2003) Processive DNA synthesis observed in a polymerase crystal suggests a mechanism for the prevention of frameshift mutations. Proc. Natl Acad. Sci. USA, 100, 3895-3900.
36. Beard,W.A. and Wilson,S.H. (1998) Structural insights into DNA polymerase β fidelity: Hold tight if you want it right. Chem. Biol. 5, 13.
37. Frieden,M., Pedroso,E. and Kool,E.T. (1999) Tightening the belt on polymerases: Evaluating the physical constraints on enzyme substrate size. Angew. Chem. Int. Ed. Engl., 38, 3654-3657.
38. Sawaya,M.R., Prasad,R., Wilson,S.H., Kraut J. and Pelletier,H. (1997) Crystal structures of human DNA polymerase β complexed with gapped and nicked DNA: Evidence for an induced fit mechanism. Biochemistry, 36, 11205-11215.
39. Wong,I., Patel,S.S. and Johnson,K.A. (1991) An induced-fit kinetic mechanism for DNA replication fidelity: Direct measurement by single-turnover kinetics. Biochemistry, 30, 526-537.
40. Doublie,S. and Ellenberger,T. (1998) The mechanism of action of T7 DNA polymerase. Curr. Opin. Struct. Biol., 8, 704-712.
41. Li,Y., Korolev,S. and Waksman,G. (1998) Crystal structures of open and closed forms of binary and ternary complexes of the large fragment of Thermus aquaticus DNA polymerase I: Structural basis for nucleotide incorporation. Embo J., 17, 7514-7525.
42. Pelletier,H., Sawaya,M.R., Kumar,A., Wilson,S.H. and Kraut,J. (1994) Structures of ternary complexes of rat DNA polymerase β, a DNA template-primer, and ddCTP. Science, 264, 1891-1903.
43. Steitz,T.A. (1999) DNA polymerases: Structural diversity and common mechanisms. J. Biol. Chem., 274, 17395-17398.
44. 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]pyre ne adduct that blocks replication. J. Biol. Chem., 280, 3764-3770.
45. Beard,W.A., Bebenek,K., Darden,T.A., Li,L., Prasad,R., Kunkel,T.A. and Wilson,S.H. (1998) Vertical-scanning mutagenesis of a critical tryptophan in the minor groove binding track of HIV-1 reverse transcriptase. Molecular nature of polymerase-nucleic acid interactions. J. Biol. Chem., 273, 30435-30442.
46. Bebenek,K., Beard,W.A., Darden,T.A., Li,L., Prasad,R., Luton,B.A., Gorenstein,D.G., Wilson,S.H. and Kunkel,T.A. (1997) A minor groove binding track in reverse transcriptase. Nat. Struct. Biol., 4 194-197.
47. Latham,G.J., Forgacs,E., Beard,W.A., Prasad,R., Bebenek,K., Kunkel,T.A., Wilson,S.H. and Lloyd,R.S. (2000) Vertical-scanning mutagenesis of a critical tryptophan in the 'minor groove binding track' of HIV-1 reverse transcriptase. Major groove DNA adducts identify specific protein interactions in the minor groove. J. Biol. Chem., 275, 15025-15033.
48. Morales,J. and Kool,E.T. (1999) Minor groove interactions between polymerase and DNA: More essential to replication than Watson-Crick hydrogen bonds. J. Am. Chem. Soc., 121, 2323-2324.
49. Polesky,A.H., Dahlberg,M.E., Benkovic,S.J., Grindley,N.D. and Joyce,C.M. (1992) Side chains involved in catalysis of the polymerase reaction of DNA polymerase I from Escherichia coli. J. Biol. Chem., 267, 8417-8428.
50. Perlow,R.A. and Broyde,S. (2001) Evading the proofreading machinery of a replicative DNA polymerase: Induction of a mutation by an environmental carcinogen. J. Mol. Biol., 309, 519-536.
51. Perlow,R.A. and Broyde,S. (2002) Toward understanding the mutagenicity of an environmental carcinogen: Structural insights into nucleotide incorporation preferences. J. Mol. Biol., 322, 291-309.
52. Perlow,R.A. and Broyde,S. (2003) Extending the understanding of mutagenicity: Structural insights into primer-extension past a [benzoa]pyrene diol epoxide-DNA adduct. J. Mol. Biol., 327, 797-818.
53. Berman,H.M., Westbrook,J., Feng,Z., Gilliland,G., Bhat,T.N., Weissig,H., Shindyalov,I.N. and Bourne,P.E. (2000) The Protein Data Bank. Nucleic Acids Res., 28, 235-242.
54. Xie,X.M., Geacintov,N.E. and Broyde,S. (1999) Stereochemical origin of opposite orientations in DNA adducts derived from enantiomeric anti benzo[a]pyrene diol epoxides with different tumorigenic potentia ls. Biochemistry, 38, 2956-2968.
55. Case,D.A., Pearlman,D.A., Caldwell,J.W., Cheatham,T.E.I., Wang,J., Ross,W.S., Simmerling,C.L., Darden,T.A., Merz,K.M. et al. (2002) AMBER 7 University of California, San Francisco, CA.
56. Cornell,W., Cieplak,P., Bayly,C., Gould,I., Merz,K., Ferguson,D., Spellmeyer,D., Fox,T., Caldwell,J. et al. (1995) A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J. Am. Chem. Soc., 117, 5179-5197.
57. Cheatham,T.E. 3rd, Cieplak,P. and Kollman,P.A. (1999) A modified version of the Cornell et al. force field with improved sugar pucker phases and helical repeat. J. Biomol. Struct. Dyn., 16, 845-862.
58. Delano,W.L. (2002) The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA.
59. Batra,V.K., Beard,W.A., Shock,D.D., Krahn,J.M., Pedersen,L.C. and Wilson,S.H. (2006) Magnesium-induced assembly of a complete DNA polymerase catalytic complex. Structure, 14, 757-766.
60. Rothwell,P.J. and Waksman,G. (2005) Structure and mechanism of DNA polymerases. Adv. Protein Chem., 71, 401-440.
61. Jordan,F. (1973) Lennard-Jones potential calculations of the barrier to rotation around the glycosidic C-N linkage in selected purine nucleosides and nucleotides. A direct comparison of the results of 6-12 potential calculations with results of semiempirical molecular orbital studies. J. Theor. Biol., 41, 375-395.
62. Brautigam,C.A. and Steitz,T.A. (1998) Structural and functional insights provided by crystal structures of DNA polymerases and their substrate complexes. Curr. Opin. Struct. Biol., 8, 54-63.
63. Yang,W., Lee,J.Y. and Nowotny,M. (2006) Making and breaking nucleic acids: Two-Mg2 + -ion catalysis and substrate specificity. Mol. Cell 22, 5-13.
64. Cosman,M., Hingerty,B.E., Geacintov,N.E., Broyde,S. and Patel,D.J. (1995) Structural alignments of (+)- and (-)-trans-anti- benzo[a]pyrene-dG adducts positioned at a DNA template-primer junction. Biochemistry, 34, 15334-15350.
65. Hsu,G.W., Kiefer,J.R., Burnouf,D., Becherel,O.J., Fuchs,R.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.
66. Johnson,S.J. and Beese,L.S. (2004) Structures of mismatch replication errors observed in a DNA polymerase. Cell, 116, 803-816.
67. Hruszkewycz,A.M., Canella,K.A., Peltonen,K., Kotrappa,L. and Dipple,A. (1992) DNA polymerase action on benzo[a]pyrene-DNA adducts. Carc inogenesis, 13, 2347-2352.
68. Lipinski,L.J., Ross,H.L., Zajc,B., Sayer,J.M., Jerina,D.M. and Dipple,A. (1998) Effect of single benzo[a]pyrene diol epoxide-deoxyguanosine adducts on the action of DNA polymerases in vitro. Int. J. Oncol., 13, 269-273.
69. Shibutani,S., Margulis,L.A., Geacintov,N.E. and Grollman,A.P. (1993) Translesional synthesis on a DNA template containing a single stereoisomer of dG-(+)- or dG-(-)-anti-BPDE (7,8-dihydroxy-anti-9,10-epoxy-7,8,9,10-tetrahydrobenzo[a]pyrene). Biochemistry, 32, 7531-7541.
70. Hansson,T., Oostenbrink,C. and van Gunsteren,W. (2002) Molecular dynamics simulations. Curr. Opin. Struct. Biol., 12, 190-196.
71. Karplus,M. and Kuriyan,J. (2005) Molecular dynamics and protein function. Proc. Natl Acad. Sci. USA, 102, 6679-6685.
72. Karplus,M. and McCammon,J.A. (2002) Molecular dynamics simulations of biomolecules. Nat. Struct. Biol., 9, 646-652.