The role of specific amino acid residues in the active site of Escherichia coli DNA polymerase I on translesion DNA synthesis across from and past an N-2-aminofluorene adduct

Biochemistry

Volumn 46, Issue 10, 2007, Pages 2599-2607

  Lone, Samer ^a,b   Romano, Louis J ^a  

^a WAYNE STATE UNIVERSITY   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CARCINOGENS; DNA; ENZYME KINETICS; MUTAGENESIS; NUCLEOTIDES; TUMORS;

DNA LESIONS; DNA SYNTHESIS; MUTANTS; POLYMERASE GEOMETRY;

ESCHERICHIA COLI;

2 FLUORENYLAMINE; ALANINE; AMINO ACID; CARCINOGEN; DNA; DNA DIRECTED DNA POLYMERASE BETA; FLUORENE DERIVATIVE; GLUTAMIC ACID; NUCLEOTIDE; PHENYLALANINE; SERINE; TYROSINE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; DNA ADDUCT; DNA REPLICATION; DNA SYNTHESIS; DNA TEMPLATE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME INHIBITION; ESCHERICHIA COLI; GEOMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SEQUENCE ANALYSIS; STEADY STATE;

2-ACETYLAMINOFLUORENE; BINDING SITES; DNA; DNA ADDUCTS; DNA POLYMERASE I; ESCHERICHIA COLI;

ESCHERICHIA COLI;

EID: 33947272480     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi061324o     Document Type: Article

References (52)

1. 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.
2. Goodman, M. F. (1997) Hydrogen bonding revisited: geometric selection as a principal determinant of DNA replication fidelity, Proc. Natl. Acad. Sci. U.S.A. 94, 10493-10495.
3. Johnson, K. A. (1993) Conformational coupling in DNA polymerase fidelity. Annu. Rev. Biochem. 62, 685-713.
4. Doublie, S., Sawaya, M. R., and Ellenberger, T. (1999) An open and closed case for all polymerases. Structure Fold Des. 7, R31-35.
5. 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.
6. Kunkel, T. A., and Bebenek, K. (2000) DNA replication fidelity, Annu. Rev. Biochem. 69, 497-529.
7. Bell, J. B., Eckert, K. A., Joyce, C. M., and Kunkel, T. A. (1997) Base miscoding and strand misalignment errors by mutator Klenow polymerases with amino acid substitutions at tyrosine 766 in the O helix of the fingers subdomain. J. Biol. Chem. 272, 7345-7351.
8. Carooll, S. S., Cowart, M., and Benkovic, S. J. (1991) A mutant of DNA polymerase 1 (Klenow fragment) with reduced fidelity. Biochemistry 30, 804-813.
9. Minnick, D. T., Bebenek, K., Osheroff, W. P., Turner, R. M., Jr., Astatke, M., Liu, L., Kunkel, T. A., and Joyce, C. M. (1999) Side chains that influence fidelity at the polymerase active site of Escherichia coli DNA polymerase 1 (Klenow fragment), J. Biol. Chem. 274, 3067-3075.
10. Astalke, M., Grindley, N. D., and Joyce, C. M. (1998) How E. coli DNA polymerase 1 (Klenow fragment) distinguishes between deoxy- and dideoxynucleotides, J. Mol. Biol. 278, 147-165.
11. Astatke, M., Ng, K., Grindley, N. D., and Joyce, C. M. (1998) A single side chain prevents Escherichia coli DNA polymerase 1 (Klenow fragment) from incorporating ribonucleotides. Proc: Natl. Acad. Sci. U.S.A. 95, 3402-3407.
12. Minnick, D. T., Liu, L., Grindley, N. D., Kunkel, T. A., and Joyce, C. M. (2002) Discrimination against purine-pyrimidine mispairs in the polymerase active site of DNA polymerase 1: a structural explanation, Proc. Natl. Acad. Sci. U.S.A. 99, 1194-1199.
13. 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.
14. 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.
15. Beland, F. A., and Kadlubar, F. F. (1985) Formation and persistence of arylamine DNA adducts in vivo. Environ. Health Perfect. 62, 19-30.
16. Belguise-Valladier, P., and Fuchs, R. P. P. (1991) Strong sequence-dependent polymorphism in adduct-induced DNA structure: analysis of single N-2-acetylaminofluorene residues bound within the Nar I mutation hot spot. Biochemistry 30, 10091-10100.
17. Hingerty, B. E., and Broyde, S. (1986), J. Biomol. Struct. Dyn. 4, 365-372.
18. Mao, B., Hingerty, B. E., Broyde, S., and Patel, D. J. (1998) Solution structure of the aminofluorene [AF]-external conformer of the anti-[AF]-C8-dG adduct opposite dC in a DNA duplex, Biochemistry 37, 95-106.
19. 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.
20. 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. Rex. Toxicol. 11, 391-407.
21. van Houte, L. P. A., Bokma, J. T., Lutgerink, J. T., Westra, J. G., Retel, J., and van Grondelle, R. (1987) An optical study of the configuration of the aminofluorene-DNA complex, Carcinogenesis 8, 759-766.
22. Bichara, M., and Fuchs, R. P. P. (1985) DNA binding and mutation spectra of the carcinogen N-2-aminofluorene in Escherichia coli. A correlation between the conformation of the premutagenic lesion and the mutation specificity, J. Mol. Biol. 183, 341-351.
23. Hoffmann, G. R., and Fuchs, R. P. (1997) Mechanisms of frameshift mutations: insight from aromatic amines, Chem. Res. Toxicol. 10, 347-359.
24. Koffel-Schwartz, N., Verdier, J. M., Bichara, M., Freund, A. M., Daune, M. P., and Fuchs, R. P. (1984) Carcinogen-induced mutation spectrum in wild-type, uvrA and umuC strains of Escherichia coli. Strain specificity and mutation-prone sequences, J. Mol. Biol. 177, 33-51.
25. Lone, S., and Romano, L. J. (2003) Mechanistic insights into replication across from bulky DNA adducts: a mutant polymerase 1 allows an N-acetyl-2-aminofluorene adduct to be accommodated during DNA synthesis. Biochemistry 42, 3826-3834.
26. Joyce, C. M., and Derbyshire, V. (1995) Purification of Escherichia coli DNA polymerase I and Klenow fragment. Methods Enzymol. 262, 3-13.
27. Setlow, P. (1974) DNA polymerase I from Escherichia coli, Methods Enzymol. 29, 3-12.
28. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
29. Dzantiev, L., and Romano, L. J. (1999) Interaction of Escherichia coli DNA polymerase I (Klenow fragment) with primer-templates containing N-acetyl-2-aminofluorene or N-2- aminofluorene adducts in the active site, J. Biol. Chem. 274, 3279-3284.
30. Shibutani, S., and Grollman, A. P. (1993) Nucleotide misincorporation on DNA templates containing N- (deoxyguanosin-N2-yl)-2-(acetylamino)fluorene, Chem. Res. Toxicol. 6, 819-824.
31. 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.
32. Mendelman, L. V., Boosalis, M. S., Petruska, J., and Goodman, M. F. (1989) Nearest neighbor influences on DNA polymerase insertion fidelity, J. Biol. Chem. 264, 14415-14423.
33. Mendelman, L. V., Petruska, J., and Goodman, M. F. (1990) Base mispair extension kinetics. Comparison of DNA polymerase alpha and reverse transcriptase, J. Biol. Chem. 265, 2338-2346.
34. 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, 73-114.
35. Doisy, R., and Tang, M. S. (1995) Effect of aminofluorene and (acetylamino)fluorene adducts on the DNA replication mediated by Escherichia coli polymerases I (Klenow fragment) and III, Biochemistry 34, 4358-4368.
36. Shibutani, S., Naomi, S., and Grollman, A. P. (1998) Mutagenic Specificity of (Acetylamino)fluorene-Derived DNA Adducts in Mammalian Cells, Biochemistry 37, 12034-12041.
37. Gill, J. P., and Romano, L. J. (2005) Mechanism for N-acetyl-2- aminofluorene-induced frameshift mutagenesis by Escherichia coli DNA polymerase 1 (Klenow fragment). Biochemistry 44, 15387-15395.
38. Shibutani, S., and Grollman, A. P. (1997) Molecular mechanisms of mutagenesis by aromatic amines and amides, Mutat. Res. 376, 71-78.
39. Minnick, D. T., Astatke, M., Joyce, C. M., and Kunkel, T. A. (1996) A thumb subdomain mutant of the large fragment of Escherichia coli DNA polymerase I with reduced DNA binding affinity, processivity, and frameshift fidelity, J. Biol. Chem. 271, 24954-24961.
40. Joyce, C. M., and Steitz, T. A. (1994) Function and structure relationships in DNA polymerases, Annu. Rev. Biochem. 63, 777-822.
41. Li, Y., Kong, Y., Korolev, S., and Waksman, G. (1998) Crystal structures of the Klenow fragment of Thermus aquaticus DNA polymerase I complexée with deoxyribonucleoside triphosphates, Protein Sci. 7, 1116-1123.
42. Ling, H., Boudsocq, F., Plosky, B. S., Woodgate, R., and Yang, W. (2003) Replication of a cis-syn thymine dimer at atomic resolution, Nature 424, 1083-1087.
43. Ling, H., Boudsocq, F., Woodgate, R., and Yang, W. (2001) Crystal structure of a Y-family DNA polymerase in action: a mechanism for error-prone and lesion-bypass replication, Cell 107, 91-102.
44. Ling, H., Boudsocq, F., Woodgate, R., and Yang, W. (2004) Snapshots of replication through an abasic lesion; structural basis for base substitutions and frameshifts, Mol. Cell 13, 751-762.
45. Ling, H., Sayer, J. M., Plosky, B. S., Yagi, H., Boudsocq, F., Woodgate, R., Jerina, D. M., and Yang, W. (2004) Crystal structure of a benzo[a]pyrene diol epoxide adduct in a ternary complex with a DNA polymerase, Proc. Natl. Acacl. Sci. U.S.A. 101, 2265-2269.
46. Bresson, A., and Fuchs, R. P. (2002) Lesion bypass in yeast cells: Pol eta participates in a multi-DNA polymerase process, EMBO J. 21, 3881-3887.
47. Nelson, J. R., Gibbs, P. E., Nowicka, A. M., Hinkle, D. C., and Lawrence, C. W. (2000) Evidence for a second function for Saccharomyces cerevisiae Rev 1p, Mol. Microbiol. 37, 549-554.
48. Prakash, S., and Prakash, L. (2002) Translesion DNA synthesis in eukaryotes: a one- or two-polymerase affair, Genes Dev. 16, 1872-1883.
49. Woodgate, R. (2001) Evolution of the two-step model for UV-mutagenesis, Mutat. Res. 485, 83-92.
50. Yang, W. (2003) Damage repair DNA polymerases Y, Curr. Opin. Struct. Biol. 13, 23-30.
51. Haracska, L., Washington, M. T., Prakash, S., and Prakash, L. (2001) Inefficient bypass of an abasic site by DNA polymerase eta, J. Biol. Chem. 276, 6861-6866.
52. Johnson, R. E., Washington, M. T., Haracska, L., Prakash, S., and Prakash, L. (2000) Eukaryotic polymerases iota and zeta act sequentially to bypass DNA lesions, Nature 406, 1015-1019.