Mechanism of efficient and accurate nucleotide incorporation opposite 7,8-Dihydro-8-oxoguanine by Saccharomyces cerevisiae DNA polymerase η

Molecular and Cellular Biology

Volumn 25, Issue 6, 2005, Pages 2169-2176

  Carlson, Karissa D ^a   Washington, M Todd ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

8 HYDROXYGUANINE; DEOXYADENOSINE TRIPHOSPHATE; DEOXYCYTIDINE TRIPHOSPHATE; DIMER; DNA POLYMERASE; NUCLEOTIDE; THYMINE;

ARTICLE; BINDING AFFINITY; CATALYSIS; DNA TEMPLATE; ENZYME BINDING; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; STEADY STATE;

BASE PAIRING; DNA DAMAGE; DNA REPLICATION; DNA-DIRECTED DNA POLYMERASE; GUANINE; NUCLEOTIDES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TEMPLATES, GENETIC;

SACCHAROMYCES CEREVISIAE;

EID: 14844364365     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.6.2169-2176.2005     Document Type: Article

References (49)

1. Beckman, K. B., and B. N. Ames. 1997. Oxidative decay of DNA. J. Biol. Chem. 272:19633-19636.
2. Brieba, L. G., B. F. Eichman, R. J. Kokoska, S. Doublie, T. A. Kunkel, and T. Ellenberger. 2004. Structural basis for the dual coding potential of 8-oxoguanosine by a high-fidelity DNA polymerase. EMBO J. 23:3452-3461.
3. Capson, T. L., J. A. Peliska, B. F. Kaboord, M. W. Frey, C. Lively, M. Dahlberg, and S. J. Benkovic. 1992. Kinetic characterization of the polymerase and exonuclease activities of the gene 43 protein of bacteriophage T4. Biochemistry 31:10984-10994.
4. Creighton, S., L. B. Bloom, and M. F. Goodman. 1995. Gel fidelity assay measuring nucleotide misinsertion, exonucleolytic proofreading, and lesion bypass efficiencies. Methods Enzymol. 262:232-256.
5. Dahlberg, M. E., and S. J. Benkovic. 1991. Kinetic mechanism of DNA polymerase I (Klenow fragment): identification of a second conformational change and evaluation of the internal equilibrium constant. Biochemistry 30:4835-4843.
6. Einolf, H. J., and F. P. Guengerich. 2001. Fidelity of nucleotide insertion at 8-oxo-7,8-dihydroguanine by mammalian DNA polymerase δ. Steady-state and pre-steady state kinetic analysis. J. Biol. Chem. 276:3764-3771.
7. Fiala, K. A., and Z. Suo. 2004. Mechanism of DNA polymerization catalyzed by Sulfolobus solfataricus P2 DNA polymerase IV. Biochemistry 43:2116-2125.
8. Fiala, K. A., and Z. Suo. 2004. Pre-steady state kinetic studies of the fidelity of Sulfolobus solfataricus P2 DNA polymerase IV. Biochemistry 43:2106-2115.
9. Freisinger, E., A. P. Grollman, H. Miller, and C. Kisker. 2004. Lesion (in)tolerance reveals insights into DNA replication fidelity. EMBO J. 23: 1494-1505.
10. - and human immunodeficiency virus-1 reverse transcriptase using steady state and pre-steady state kinetics. Biochemistry 36:6475-6487.
11. Furge, L. L., and F. P. Guengerich. 1999. Explanation of pre-steady state kinetics and decreased burst amplitude of HIV-1 reverse transcriptase at sites of modified DNA bases with an additional, nonproductive enzyme-DNA-nucleotide complex. Biochemistry 38:4818-4825.
12. Graves, S. W., A. A. Johnson, and K. A. Johnson. 1998. Expression, purification, and initial kinetic characterization of the large subunit of the human mitochondrial DNA polymerase. Biochemistry 37:6050-6058.
13. Haracska, L., S. L. Yu, R. E. Johnson, L. Prakash, and S. Prakash. 2000. Efficient and accurate replication in the presence of 7,8-dihydro-8-oxoguanine by DNA polymerase η. Nat. Genet. 25:458-461.
14. Helbock, H. J., K. B. Beckman, M. K. Shigenaga, P. B. Walter, A. A. Woodall, H. C. Yeo, and B. N. Ames. 1998. DNA oxidation matters: the HPLC-electrochemical detection assay of 8-oxodeoxyguanosine and 8-oxoguanine. Proc. Natl. Acad. Sci. USA 95:288-293.
15. Hsu, G. W., M. Ober, T. Carell, and L. S. Beese. 2004. Error-prone replication of oxidatively damaged DNA by a high-fidelity DNA polymerase. Nature 431:217-221.
16. Johnson, K. A. 1992. Transient-state kinetic analysis of enzyme reaction pathway. Enzymes XX:1-61.
17. Johnson, K. A. 1995. Rapid quench kinetic analysis of polymerases, adenosine triphosphatases, and enzyme intermediates. Methods Enzymol. 249:38-61.
18. Johnson, R. E., C. M. Kondratick, S. Prakash, and L. Prakash. 1999. hRAD30 mutations in the variant form of xeroderma pigmentosum. Science 285:263-265.
19. Johnson, R. E., M. T. Washington, S. Prakash, and L. Prakash. 2000. Fidelity of human DNA polymerase η. J. Biol. Chem. 275:7447-7450.
20. Johnson, R. E., S. Prakash, and L. Prakash. 1999. Efficient bypass of a thymine-thymine dimer by yeast DNA polymerase, Polη. Science 283:1001-1004.
21. Johnson, R. E., S. Prakash, and L. Prakash. 1999. Requirement of DNA polymerase activity of yeast Rad30 protein for its biological function. J. Biol. Chem. 274:15975-15977.
22. Kouchakdjian, M., B. Verraiah, S. Shibutani, M. Eisenberg, F. Johnson, A. P. Grollman, and D. J. Patel. 1991. NMR structural studies of the ionizing radiation adduct 7-hydroxy-8-oxodeoxyguanosine (8-oxo-tH-dG) opposite deoxyadenosine in a DNA duplex. 8-oxo-7H-dG(syn)·dA(anti) alignment at lesion site. Biochemistry 30:1403-1412.
23. Krahn, J. M., W. A. Beard, H. Miller, A. P. Grollman, and S. H. Wilson. 2003. Structure of DNA polymerase β with the mutagenic DNA lesion 8-oxodeoxyguanine reveals structural insights into its coding potential. Structure 11:121-127.
24. Kuchta, R. D., V. Mizrahi, P. A. Benkovic, K. A. Johnson, and S. J. Benkovic. 1987. Kinetic mechanism of DNA polymerase I (Klenow). Biochemistry 26:8410-8417.
25. Lipscomb, L. A., M. E. Peek, M. L. Morningstar, S. M. Verghis, E. M. Miller, A. Rich, J. M. Essigmann, and L. D. Williams. 1995. X-ray structure of a DNA decamer containing 7,8-dihydro-8-oxoguanine. Proc. Natl. Acad. Sci. USA 92:719-723.
26. -. Biochemistry 35:9840-9849.
27. Masutani, C., R. Kusumoto, A. Yamada, N. Dohmae, M. Yokoi, M. Yuasa, M. Araki, S. Iwai, K. Takio, and F. Hanaoka. 1999. The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase eta. Nature 399:700-704.
28. Matsuda, T., K. Bebenek, C. Matsutani, F. Hanaoka, and T. A. Kunkel. 2000. Low fidelity of DNA synthesis by human DNA polymerase η. Nature 404:1011-1013.
29. McAuley-Hecht, K. E., G. A. Leonard, N. J. Gibson, J. B. Thomson, W. P. Watson, W. N. Hunter, and T. Brown. 1994. Crystal structure of a DNA duplex containing 8-hydrodeoxyguanine-adenine base pairs. Biochemistry 33:10266-10270.
30. McDonald, J. P., A. S. Levine, and R. Woodgate. 1997. The Saccharomyces cerevisiae RAD30 gene, a homologue of Escherichia coli dinB and umuC, is DNA damage inducible and functions in a novel error-free postreplication repair mechanism. Genetics 147:1557-1568.
31. Miller, H., R. Prasad, S. H. Wilson, F. Johnson, and A. P. Grollman. 2000. 8-Oxo-dGTP incorporation by DNA polymerase β is modified by active-site residue Asn279. Biochemistry 39:1029-1033.
32. Mizrahi, V., R. N. Henrie, J. F. Marlier, K. A. Johnson, and S. J. Benkovic. 1985. Rate-limiting steps in the DNA polymerase I reaction pathway. Biochemistry 24:4010-4018.
33. Moriya, M. 1993. Single-stranded shuttle phagemid for mutagenesis studies in mammalian cells: 8-oxoguanine in DNA induced targeted G·C→ T·A transversions in simian kidney cells. Proc. Natl. Acad. Sci. USA 90:1122-1126.
34. Oda, Y., S. Uesugi, M. Ikehara, S. Nishimura, Y. Kawase, H. Ishikawa, H. Inoue, and E. Ohtsuda. 1991. NMR studies of a DNA containing 8-hydroxydeoxyguanosine. Nucleic Acid Res. 19:1407-1412.
35. Patel, S. S., I. Wong, and K. A. Johnson. 1991. Pre-steady-state kinetic analysis of processive DNA replication including complete characterization of an exonuclease-defident mutant. Biochemistry 30:511-525.
36. Roettger, M. P., K. A. Fiala, S. Sompalli, Y. Dong, and Z. Suo. 2004. Pre-steady state kinetic studies of the fidelity of human DNA polymerase μ. Biochemistry 43:13827-13838.
37. Roush, A. A., M. Suarez, E. C. Friedberg, M. Radman, and W. Siede. 1998. Deletion of the Saccharomyces cerevisiae gene RAD30 encoding an Escherichia coli DinB homolog confers UV radiation sensitivity and altered mutability. Mol. Gen. Genet. 257:686-692.
38. Shibutani, S., M. Takeshita, and A. P. Grollman. 1991. Insertions of specific bases during DNA synthesis past the oxidation-damaged base 8-oxo-dG. Nature 349:431-434.
39. Sun, L., K. Zhou, P. Hohler, E. T. Kool, F. Yuan, Z. Wang, and J. S. Taylor. 2003. Yeast Pol η holds a cis-syn thymine dimer loosely in the active site during elongation opposite the 3′-T of the dimer, but tightly opposite the 5′-T. Biochemistry 42:9431-9437.
40. Trincao, J., R. E. Johnson, C. R. Escalante, S. Prakash, L. Prakash, and A. K. Aggarwal. 2001. Structure of the catalytic core of S. cerevisiae DNA polymerase η: implications for translesion DNA synthesis. Mol. Cell 8:417-426.
41. Vaisman, A., and R. Woodgate. 2001. Unique misinsertion specificity of polι may decrease the mutagenic potential of deaminated cytosines. EMBO J. 20:6520-6529.
42. Washington, M. T., L. Prakash, and S. Prakash. 2001. Yeast DNA polymerase η utilizes an induced-fit mechanism of nucleotide incorporation. Cell 107:917-927.
43. Washington, M. T., L. Prakash, and S. Prakash. 2003. Mechanism of nucleotide incorporation opposite a thymine-thymine dimer by yeast DNA polymerase η. Proc. Natl. Acad. Sci. USA 100:12093-12098.
44. Washington, M. T., R. E. Johnson, S. Prakash, and L. Prakash. 1999. Fidelity and processivity of Saccharomyces cerevisiae DNA polymerase η. J. Biol. Chem. 274:36835-36838.
45. Washington, M. T., R. E. Johnson, L. Prakash, and S. Prakash. 2003. The mechanism of nucleotide incorporation by human DNA polymerase η differs from that of the yeast enzyme. Mol. Cell. Biol. 23:8316-8322.
46. Washington, M. T., R. E. Johnson, L. Prakash, and S. Prakash. 2004. Human DNA polymerase ι utilizes different nucleotide incorporation mech-anisms dependent upon the template base. Mol. Cell. Biol. 24:936-943.
47. Washington, M. T., R. E. Johnson, S. Prakash, and L. Prakash. 2000. Accuracy of thymine-thymine dimer bypass by Saccharomyces cerevisiae DNA polymerase η. Proc. Natl. Acad. Sci. USA 97:3094-3099.
48. Werneburg, B. G., J. Ahn, X. Zhong, R. J. Hondal, V. S. Kraynov, and M. D. Tsai. 1996. DNA polymerase β: pre-steady-state kinetic analysis and roles of arginine-283 in catalysis and fidelity. Biochemistry 35:7041-7050.
49. Zhong, X., S. S. Patel, B. G. Werneburg, and M. D. Tsai. 1997. DNA polymerase β: multiple conformational changes in the mechanism of catalysis. Biochemistry 36:11891-11900.