Influence of local sequence context on damaged base conformation in human DNA polymerase ι: Molecular dynamics studies of nucleotide incorporation opposite a benzo[a]pyrene-derived adenine lesion

Nucleic Acids Research

Volumn 37, Issue 21, 2009, Pages 7095-7109

  Donny clark, Kerry ^a   Broyde, Suse ^a  

^a NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; BASE; BENZO[A]PYRENE; CYTOSINE; DEOXYGUANOSINE TRIPHOSPHATE; DNA POLYMERASE; DNA POLYMERASE IOTA; THREONINE; UNCLASSIFIED DRUG; 2'-DEOXYADENOSINE TRIPHOSPHATE; 2'-DEOXYCYTIDINE 5'-TRIPHOSPHATE; ANTI BENZO(A)PYRENE DA ADDUCT; ANTI-BENZO(A)PYRENE-DA ADDUCT; BENZO[A]PYRENE DERIVATIVE; CARCINOGEN; DEOXYADENOSINE PHOSPHATE; DEOXYADENOSINE TRIPHOSPHATE; DEOXYCYTIDINE PHOSPHATE; DEOXYCYTIDINE TRIPHOSPHATE; DEOXYGUANOSINE PHOSPHATE; DNA DIRECTED DNA POLYMERASE; MAGNESIUM; PYRIMIDINE NUCLEOTIDE; THYMIDINE 5'-TRIPHOSPHATE; THYMIDINE TRIPHOSPHATE;

ARTICLE; BASE PAIRING; CONTROLLED STUDY; DNA CONFORMATION; DNA DAMAGE; DNA SEQUENCE; HYDROGEN BOND; MOLECULAR DYNAMICS; MOLECULAR MODEL; PRIORITY JOURNAL; PROTEIN FUNCTION; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS; BASE MISPAIRING; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; CONFORMATION; DNA ADDUCT; HUMAN; METABOLISM; NUCLEOTIDE SEQUENCE;

BASE PAIR MISMATCH; BASE PAIRING; BASE SEQUENCE; BENZOPYRENES; CARCINOGENS, ENVIRONMENTAL; COMPUTER SIMULATION; DEOXYADENINE NUCLEOTIDES; DEOXYCYTOSINE NUCLEOTIDES; DEOXYGUANINE NUCLEOTIDES; DNA ADDUCTS; DNA DAMAGE; DNA-DIRECTED DNA POLYMERASE; HUMANS; HYDROGEN BONDING; MAGNESIUM; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; THYMINE NUCLEOTIDES;

EID: 75349085033     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp745     Document Type: Article

References (88)

1. Luch, A. (2005) Nature and nurture-lessons from chemical carcinogenesis. Nat. Rev. Cancer, 5, 113-125.
2. Clapp, R.W., Jacobs, M.M. and Loechler, E.L. (2008) Environmental and occupational causes of cancer: new evidence 2005-2007. Rev. Environ. Health, 23, 1-37.
3. 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.
4. Lehmann, A.R., Niimi, A., Ogi, T., Brown, S., Sabbioneda, S., Wing, J.F., Kannouche, P.L. and Green, C.M. (2007) Translesion synthesis: Y-family polymerases and the polymerase switch. DNA Repair (Amst), 6, 891-899.
5. Waters, L.S., Minesinger, B.K., Wiltrout, M.E., D'Souza, S., Woodruff, R.V. and Walker, G.C. (2009) Eukaryotic translesion polymerases and their roles and regulation in DNA damage tolerance. Microbiol. Mol. Biol. Rev., 73, 134-154.
6. Yang, W. and Woodgate, R. (2007) What a difference a decade makes: insights into translesion DNA synthesis. Proc. Natl Acad. Sci. USA, 104, 15591-15598.
7. McDonald, J.P., Rapic-Otrin, V., Epstein, J.A., Broughton, B.C., Wang, X., Lehmann, A.R., Wolgemuth, D.J. and Woodgate, R. (1999) Novel human and mouse homologs of Saccharomyces cerevisiae DNA polymerase η. Genomics, 60, 20-30.
8. Tissier, A., McDonald, J.P., Frank, E.G. and Woodgate, R. (2000) poli, a remarkably error-prone human DNA polymerase. Genes Dev., 14, 1642-1650.
9. Ohmori, H., Friedberg, E.C., Fuchs, R.P., Goodman, M.F., Hanaoka, F., Hinkle, D., Kunkel, T.A., Lawrence, C.W., Livneh, Z., Nohmi, T. et al. (2001) The Y-family of DNA polymerases. Mol. Cell, 8, 7-8.
10. Zhang, Y., Yuan, F., Wu, X. and Wang, Z. (2000) Preferential incorporation of G opposite template T by the low-fidelity human DNA polymerase i. Mol. Cell Biol., 20, 7099-7108.
11. McCulloch, S.D. and Kunkel, T.A. (2008) The fidelity of DNA synthesis by eukaryotic replicative and translesion synthesis polymerases. Cell Res., 18, 148-161.
12. Johnson, R.E., Washington, M.T., Haracska, L., Prakash, S. and Prakash, L. (2000) Eukaryotic polymerases i and ζ act sequentially to bypass DNA lesions. Nature, 406, 1015-1019.
13. Vidal, A.E. and Woodgate, R. (2009) Insights into the cellular role of enigmatic DNA polymerase i. DNA Repair (Amst), 8, 420-423.
14. Nair, D.T., Johnson, R.E., Prakash, S., Prakash, L. and Aggarwal, A.K. (2004) Replication by human DNA polymerase-i occurs by Hoogsteen base-pairing. Nature, 430, 377-380.
15. Nair, D.T., Johnson, R.E., Prakash, L., Prakash, S. and Aggarwal, A.K. (2006) An incoming nucleotide imposes an anti to syn conformational change on the templating purine in the human DNA polymerase-i active site. Structure, 14, 749-755.
16. + Hoogsteen base pair. Structure, 13, 1569-1577.
17. Kirouac, K.N. and Ling, H. (2009) Structural basis of error-prone replication and stalling at a thymine base by human DNA polymerase i. EMBO J., 28, 1644-1654.
18. Saenger, W. (1984) Principles of Nucleic Acid Structure. Springer, New York.
19. Nair, D.T., Johnson, R.E., Prakash, L., Prakash, S. and Aggarwal, A.K. (2009) DNA synthesis across an abasic lesion by human DNA polymerase i. Structure, 17, 530-537.
20. 2-dG and N6-dA lesions catalyzed by DNA bypass polymerases. J. Biol. Chem., 277, 30488-30494.
21. Washington, M.T., Minko, I.G., Johnson, R.E., Wolfle, W.T., Harris, T.M., Lloyd, R.S., Prakash, S. and Prakash, L. (2004) Efficient and error-free replication past a minor-groove DNA adduct by the sequential action of human DNA polymerases i and k. Mol. Cell Biol., 24, 5687-5693.
22. Wolfle, W.T., Johnson, R.E., Minko, I.G., Lloyd, R.S., Prakash, S. and Prakash, L. (2005) Human DNA polymerase i promotes replication through a ring-closed minor-groove adduct that adopts a syn conformation in DNA. Mol. Cell Biol., 25, 8748-8754.
23. 2-guanine DNA adducts by human DNA polymerase i. J. Biol. Chem., 281, 12315-12324.
24. 2-ethylguanine by human DNA polymerase i. J. Biol. Chem., 284, 1732-1740.
25. Johnson, R.E., Haracska, L., Prakash, L. and Prakash, S. (2006) Role of Hoogsteen edge hydrogen bonding at template purines in nucleotide incorporation by human DNA polymerase i. Mol. Cell Biol., 26, 6435-6441.
26. Johnson, R.E., Prakash, L. and Prakash, S. (2005) Biochemical evidence for the requirement of Hoogsteen base pairing for replication by human DNA polymerase i. Proc. Natl Acad. Sci. USA, 102, 10466-10471.
27. Donny-Clark, K., Shapiro, R. and Broyde, S. (2009) Accommodation of an N-(deoxyguanosin-8-yl)-2-acetylaminofluorene adduct in the active site of human DNA polymerase i: Hoogsteen or Watson-Crick base pairing? Biochemistry, 48, 7-18.
28. 6-ethenodeoxyadenosine lesion by human DNA polymerase i. Nat. Struct. Mol. Biol., 13, 619-625.
29. Johnson, R.E., Yu, S.L., Prakash, S. and Prakash, L. (2007) A role for yeast and human translesion synthesis DNA polymerases in promoting replication through 3-methyl adenine. Mol. Cell. Biol., 27, 7198-7205.
30. Plosky, B.S., Frank, E.G., Berry, D.A., Vennall, G.P., McDonald, J.P. and Woodgate, R. (2008) Eukaryotic Y-family polymerases bypass a 3-methyl-2'-deoxyadenosine analog in vitro and methyl methanesulfonate-induced DNA damage in vivo. Nucleic Acids Res., 36, 2152-2162.
31. Choi, J.Y., Lim, S., Eoff, R.L. and Guengerich, F.P. (2009) Kinetic analysis of base pairing preference for nucleotide incorporation opposite template pyrimidines by human DNA polymerase i. J. Mol. Biol, 389, 264-274.
32. 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.
33. 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.
34. Cavalieri, E.L. and Rogan, E.G. (1995) Central role of radical cations in metabolic activation of polycyclic aromatic hydrocarbons. Xenobiotica, 25, 677-688.
35. Meehan, T. and Straub, K. (1979) Double-stranded DNA steroselectively binds benzo[a]pyrene diol epoxides. Nature, 277, 410-412.
36. 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.
37. Szeliga, J. and Dipple, A. (1998) DNA adduct formation by polycyclic aromatic hydrocarbon dihydrodiol epoxides. Chem. Res. Toxicol., 11, 1-11.
38. 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, 8a-dihydroxy-9α, 10α-epoxy-7, 8, 9, 10-tetrahydrobenzo[a]pyrene. Proc. Natl Acad. Sci. USA, 75, 5358-5361.
39. Page, J.E., Zajc, B., Oh-hara, T., Lakshman, M.K., Sayer, J.M., Jerina, D.M. and Dipple, A. (1998) Sequence context profoundly influences the mutagenic potency of trans-opened benzo[a]pyrene 7, 8-diol 9, 10-epoxide-purine nucleoside adducts in site-specific mutation studies. Biochemistry, 37, 9127-9137.
40. 6 at the second position of N-ras codon 61. J. Biol. Chem., 270, 4990-5000.
41. Frank, E.G., Sayer, J.M., Kroth, H., Ohashi, E., Ohmori, H., Jerina, D.M. and Woodgate, R. (2002) Translesion replication of benzo[a]pyrene and benzo[c]phenanthrene diol epoxide adducts of deoxyadenosine and deoxyguanosine by human DNA polymerase i. Nucleic Acids Res., 30, 5284-5292.
42. Bigger, C.A., St. John, J., Yagi, H., Jerina, D.M. and Dipple, A. (1992) Mutagenic specificities of four stereoisomeric benzo[c]phenanthrene dihydrodiol epoxides. Proc. Natl Acad. Sci. USA, 89, 368-372.
43. Wolfle, W.T., Johnson, R.E., Minko, I.G., Lloyd, R.S., Prakash, S. and Prakash, L. (2006) Replication past a trans-4-hydroxynonenal minor-groove adduct by the sequential action of human DNA polymerases i and k. Mol. Cell Biol., 26, 381-386.
44. 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.
45. Fiser, A., Do, R.K. and Sali, A. (2000) Modeling of loops in protein structures. Protein Sci., 9, 1753-1773.
46. Fiser, A. and Sali, A. (2003) Modeller: generation and refinement of homology-based protein structure models. Methods Enzymol., 374, 461-491.
47. Fiser, A. and Sali, A. (2003) ModLoop: automated modeling of loops in protein structures. Bioinformatics, 19, 2500-2501.
48. Berman, H.M., Olson, W.K., Beveridge, D.L., Westbrook, J., Gelbin, A., Demeny, T., Hsieh, S.H., Srinivasan, A.R. and Schneider, B. (1992) The nucleic acid database. A comprehensive relational database of three-dimensional structures of nucleic acids. Biophys. J., 63, 751-759.
49. Potapova, O., Chan, C., DeLucia, A.M., Helquist, S.A., Kool, E.T., Grindley, N.D. and Joyce, C.M. (2006) DNA polymerase catalysis in the absence of Watson-Crick hydrogen bonds: analysis by singleturnover kinetics. Biochemistry, 45, 890-898.
50. Mizukami, S., Kim, T.W., Helquist, S.A. and Kool, E.T. (2006) Varying DNA base-pair size in subangstrom increments: evidence for a loose, not large, active site in low-fidelity Dpo4 polymerase. Biochemistry, 45, 2772-2778.
51. Cornell, W.D., Cieplak, P., Bayly, C.I., Gould, I.R., Merz, K.M., Ferguson, D.M., Spellmeyer, D.C., Fox, T., Caldwell, J.W. and Kollman, P.A. (1995) A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J. Am. Chem. Soc., 117, 5179-5197.
52. Cheatham, T.E. III, 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.
53. Duan, Y., Wu, C., Chowdhury, S., Lee, M.C., Xiong, G., Zhang, W., Yang, R., Cieplak, P., Luo, R., Lee, T. et al. (2003) A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. J. Comput. Chem., 24, 1999-2012.
54. Wang, J.M., Cieplak, P. and Kollman, P.A. (2000) How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules? J. Comput. Chem., 21, 1049-1074.
55. Hornak, V., Abel, R., Okur, A., Strockbine, B., Roitberg, A. and Simmerling, C. (2006) Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins, 65, 712-725.
56. Perez, A., Marchan, I., Svozil, D., Sponer, J., Cheatham, T.E. 3rd, Laughton, C.A. and Orozco, M. (2007) Refinement of the AMBER force field for nucleic acids: improving the description of α/γ conformers. Biophys. J, 92, 3817-3829.
57. Williams, D.E. (1991) Net atomic charge and multipole models for the ab initio molecular electric potential. Rev. Comp. Chem., 2, 219-271.
58. Reynolds, C.A., Essex, J.W. and Richards, W.G. (1992) Atomic charges for variable molecular conformations. J. Am. Chem. Soc., 114, 9075-9079.
59. Hehre, W.J., Ditchfie, R. and Pople, J.A. (1972) Self-consistent molecular orbital methods. 12. Further extensions of gaussian-type basis sets for use in molecular orbital studies of organic molecules. J. Chem. Phys., 56, 2257-2261.
60. Frisch, M.J., Trucks, G.W., Schlegel, H.B., Scuseria, G.E., Robb, M.A., Cheeseman, J.R., Montgomery, J.A. Jr, Vreven, T., Kudin, K.N., Burant, J.C. et al. (2004) Gaussian, Inc., Wallingford, CT.
61. Bayly, C.I., Cieplak, P., Cornell, W.D. and Kollman, P.A. (1993) A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges-the RESP model. J. Phys. Chem., 97, 10269-10280.
62. Cieplak, P., Cornell, W.D., Bayly, C. and Kollman, P.A. (1995) Application of the multimolecule and multiconformational RESP methodology to biopolymers-charge derivation for DNA, RNA, and proteins. J. Chem. Phys., 16, 1357-1377.
63. 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.
64. Wang, J., Wolf, R.M., Caldwell, J.W., Kollman, P.A. and Case, D.A. (2004) Development and testing of a general amber force field. J. Comput. Chem., 25, 1157-1174.
65. Case, D.A., Darden, T.A., Cheatham, T.E. 3rd, Simmerling, C.L., Wang, J., Duke, R.E., Luo, R., Merz, K.M., Pearlman, D.A., Crowley, M. et al.(2006) University of California, San Francisco.
66. Mezei, M. (1997) Optimal position of the solute for simulations. J. Comp. Chem., 18, 812-815.
67. Jorgensen, W.L., Chandrasekhar, J., Madura, J.D., Impey, R.W. and Klein, M.L. (1983) Comparison of simple potential functions for simulating liquid water. J. Chem. Phys., 79, 926-935.
68. Darden, T., York, D. and Pedersen, L. (1993) Particle mesh Ewald-an nlog(n) method for Ewald sums in large systems. J. Chem. Phys., 98, 10089-10092.
69. Essmann, U., Perera, L., Berkowitz, M.L., Darden, T., Lee, H. and Pedersen, L.G. (1995) A smooth particle mesh Ewald method. J. Chem. Phys., 103, 8577-8593.
70. Ryckaert, J.P., Ciccotti, G. and Berendsen, H.J.C. (1977) Numerical-integration of Cartesian equations of motion of a system with constraints-molecular dynamics of N-alkanes. J. Comput. Phys., 23, 327-341.
71. Izaguirre, J.A., Catarello, D.P., Wozniak, J.M. and Skeel, R.D. (2001) Langevin stabilization of molecular dynamics. J. Chem. Phys., 114, 2090-2098.
72. Berendsen, H.J.C., Postma, J.P.M., van Gunsteren, W.F., DiNola, A. and Haak, J.R. (1984) Molecular dynamics with coupling to an external bath. J. Chem. Phys., 81, 3684-3690.
73. Harvey, S.C., Tan, R.K.Z. and Cheatham, T.E. 3rd. (1998) The flying ice cube: velocity rescaling in molecular dynamics leads to violation of energy equipartition. J. Comput. Chem., 19, 726-740.
74. Case, D.A., Pearlman, D.A., Caldwell, J.W., Cheatham, T.E. III, Ross, W.S., Simmerling, C.L., Darden, T.A., Merz, K.M., Stanton, A.L., Cheng, J.J. et al. (1999) AMBER 6. University of California, San Francisco, CA.
75. Heyer, L.J., Kruglyak, S. and Yooseph, S. (1999) Exploring expression data: identification and analysis of coexpressed genes. Genome Res., 9, 1106-1115.
76. Bonneau, J.T.R., Ruczinski, I., Chivian, D., Rohl, C., Strauss, E.M.C. and Baker, D. (2001) Rosetta in CASP4: progress in ab initio protein structure prediction. Proteins Struct. Funct. Genet., 45, 119-126.
77. Shao, J., Tanner, S.W., Thompson, N. and Cheatham, T.E. 3rd (2007) Clustering molecular dynamics trajectories: 1. Characterizing the performance of different clustering algorithms. J. Chem. Theory Comput., 3, 2312-2334.
78. Simmerling, C., Elber, R. and Zhang, J. (1995) 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. (eds), Modeling of Biomolecular Structure and Mechanisms. Kluwer Academic Publishers, Dordrecht, Netherlands, pp. 241-265.
79. Wang, L., Yu, X., Hu, P., Broyde, S. and Zhang, Y. (2007) A water-mediated and substrate-assisted catalytic mechanism for Sulfolobus solfataricus DNA polymerase IV. J. Am. Chem. Soc., 129, 4731-4737.
80. 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.
81. Frank, E.G. and Woodgate, R. (2007) Increased catalytic activity and altered fidelity of human DNA polymerase i in the presence of manganese. J. Biol. Chem., 282, 24689-24696.
82. Boulard, Y., Cognet, J.A.H., Gabarro-Arpa, J., Le Bret, M., Carbonnaux, C. and Fazakerley, G.V. (1995) Solution structure of an oncogenic DNA duplex, the K-ras gene and the sequence containing a central C·A or A·G mismatch as a function of pH: nuclear magnetic resonance and molecular dynamics studies. J. Mol. Biol., 246, 194-208.
83. Lee, G.H. and Matsushita, H. (2005) Genetic linkage between Pol i deficiency and increased susceptibility to lung tumors in mice. Cancer Sci., 96, 256-259.
84. Ohkumo, T., Kondo, Y., Yokoi, M., Tsukamoto, T., Yamada, A., Sugimoto, T., Kanao, R., Higashi, Y., Kondoh, H., Tatematsu, M. et al. (2006) UV-B radiation induces epithelial tumors in mice lacking DNA polymerase g and mesenchymal tumors in mice deficient for DNA polymerase i. Mol. Cell Biol., 26, 7696-7706.
85. Dumstorf, C.A., Clark, A.B., Lin, Q., Kissling, G.E., Yuan, T., Kucherlapati, R., McGregor, W.G. and Kunkel, T.A. (2006) Participation of mouse DNA polymerase i in strand-biased mutagenic bypass of UV photoproducts and suppression of skin cancer. Proc. Natl Acad. Sci. USA, 103, 18083-18088.
86. Wang, Y., Woodgate, R., McManus, T.P., Mead, S., McCormick, J.J. and Maher, V.M. (2007) Evidence that in xeroderma pigmentosum variant cells, which lack DNA polymerase η, DNA polymerase i causes the very high frequency and unique spectrum of UV-induced mutations. Cancer Res., 67, 3018-3026.
87. Ziv, O., Geacintov, N.E., Nakajima, S., Yasui, A. and Livneh, Z. (2009) DNA polymerase z cooperates with polymerases k and i in translesion DNA synthesis across pyrimidine photodimers in cells from XPV patients. Proc. Natl Acad. Sci. USA, 106, 11552-11557.
88. 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 potentials. Biochemistry, 38, 2956-2968.