Different divalent cations alter the kinetics and fidelity of DNA polymerases

Journal of Biological Chemistry

Volumn 291, Issue 40, 2016, Pages 20869-20875

  Vashishtha, Ashwani Kumar ^a   Wang, Jimin ^a   Konigsberg, William H ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYLATION; CATALYSIS; COORDINATION REACTIONS; DNA; METAL IONS; MOLECULES; POLYMERS; POSITIVE IONS;

CATALYTIC FUNCTIONS; DIVALENT METAL ION; INTRINSIC PROPERTY; NON-BRIDGING OXYGEN ATOMS; OCTAHEDRAL COMPLEX; OCTAHEDRAL COORDINATION GEOMETRY; PHOSPHORYL TRANSFER REACTIONS; TRANSFER REACTION;

METALS;

BASE; BERYLLIUM; CADMIUM; CALCIUM; CARBOXYLIC ACID; COBALT; DIVALENT CATION; DNA; DNA DIRECTED DNA POLYMERASE BETA; DNA POLYMERASE; EXONUCLEASE; LEAD; MAGNESIUM; MANGANESE; METAL ION; NICKEL; OXYGEN; PHOSPHORUS; SILVER; STRONTIUM; ZINC; DNA DIRECTED DNA POLYMERASE; METAL;

BINDING AFFINITY; DNA DAMAGE CHECKPOINT; DNA REPLICATION; DNA SYNTHESIS; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME FIDELITY; ENZYME KINETICS; ENZYME MECHANISM; ENZYME STRUCTURE; EXCISION REPAIR; HUMAN; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; SHORT SURVEY; TAUTOMER; BIOSYNTHESIS; CHEMISTRY; KINETICS; METABOLISM;

CATIONS, DIVALENT; DNA; DNA-DIRECTED DNA POLYMERASE; KINETICS; METALS;

EID: 84988977190     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.R116.742494     Document Type: Short Survey

References (58)

1. Drake, J. W. (1969) Comparative rates of spontaneous mutation. Nature 221, 1132
2. Goodman, M. F., and Tippin, B. (2000) The expanding polymerase universe. Nat. Rev. Mol. Cell Biol. 1, 101-109
3. Filée, J., Forterre, P., Sen-Lin, T., and Laurent, J. (2002) Evolution of DNA polymerase families: evidences for multiple gene exchange between cellular and viral proteins. J. Mol. Evol. 54, 763-773
4. Vashishtha, A. K., and Kuchta, R. D. (2016) Effects of acyclovir, Foscarnet, and ribonucleotides on herpes simplex virus-1 DNA polymerase: mechanistic insights and a novel mechanism for preventing stable incorporation of ribonucleotides into DNA. Biochemistry 55, 1168-1177
5. Vashishtha, A. K., and Kuchta, R. D. (2015) Polymerase and exonuclease activities in herpes simplex virus type 1 DNA polymerase are not highly coordinated. Biochemistry 54, 240-249
6. Xia, S., Wang, M., Blaha, G., Konigsberg, W. H., and Wang, J. (2011) Structural insights into complete metal ion coordination from ternary complexes of B family RB69 DNA polymerase. Biochemistry 50, 9114-9124
7. Snow, E. T., Xu, L. S., and Kinney, P. L. (1993) Effects of nickel ions on polymerase activity and fidelity during DNA replication in vitro. Chem. Biol. Interact 88, 155-173
8. Vaisman, A., Ling, H., Woodgate, R., and Yang, W. (2005) Fidelity of Dpo4: effect of metal ions, nucleotide selection and pyrophosphorolysis. EMBO J. 24, 2957-2967
9. Pelletier, H., Sawaya, M. R., Wolfle, W., Wilson, S. H., and Kraut, J. (1996) A structural basis for metal ion mutagenicity and nucleotide selectivity in human DNA polymerase β. Biochemistry 35, 12762-12777
10. Irimia, A., Loukachevitch, L. V., Eoff, R. L., Guengerich, F. P., and Egli, M. (2010) Metal-ion dependence of the active-site conformation of the translesion DNA polymerase Dpo4 from Sulfolobus solfataricus. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 66, 1013-1018
11. Sirover, M. A., Dube, D. K., and Loeb, L. A. (1979) On the fidelity of DNA replication: metal activation of Escherichia coli DNA polymerase I. J. Biol. Chem. 254, 107-111
12. Sirover, M. A., and Loeb, L. A. (1977) On the fidelity of DNA replication. Effect of metal activators during synthesis with avian myeloblastosis virus DNA polymerase. J. Biol. Chem. 252, 3605-3610
13. Miyaki, M., Murata, I., Osabe, M., and Ono, T. (1977) Effect of metal cations on misincorporation by E. coli DNA polymerases. Biochem. Biophys. Res. Commun. 77, 854-860
14. Goodman, M. F., Keener, S., Guidotti, S., and Branscomb, E. W. (1983) On the enzymatic basis for mutagenesis by manganese. J. Biol. Chem. 258, 3469-3475
15. Sirover, M. A., and Loeb, L. A. (1976) Infidelity of DNA synthesis in vitro: screening for potential metal mutagens or carcinogens. Science 194, 1434-1436
16. Lee, H. R., Wang, M., and Konigsberg, W. (2009) The reopening rate of the fingers domain is a determinant of base selectivity for RB69 DNA polymerase. Biochemistry 48, 2087-2098
17. Villani, G., Tanguy Le Gac, N., Wasungu, L., Burnouf, D., Fuchs, R. P., and Boehmer, P. E. (2002) Effect of manganese on in vitro replication of damaged DNA catalyzed by the herpes simplex virus type-1 DNA polymerase. Nucleic Acids Res. 30, 3323-3332
18. Xia, S., and Konigsberg, W. H. (2014) RB69 DNA polymerase structure, kinetics, and fidelity. Biochemistry 53, 2752-2767
19. Beard, W. A., and Wilson, S. H. (2014) Structure and mechanism of DNA polymerase β. Biochemistry 53, 2768-2780
20. Sobol, R. W., and Wilson, S. H. (2001) Mammalian DNA β-polymerase in base excision repair of alkylation damage. Prog. Nucleic Acid Res. Mol. Biol. 68, 57-74
21. Beard, W. A., and Wilson, S. H. (2000) Structural design of a eukaryotic DNA repair polymerase: DNA polymerase β. Mutat Res. 460, 231-244
22. Yang, L., Arora, K., Beard, W. A., Wilson, S. H., and Schlick, T. (2004) Critical role of magnesium ions in DNA polymerase β's closing and active site assembly. J. Am. Chem. Soc. 126, 8441-8453
23. Bakhtina, M., Lee, S., Wang, Y., Dunlap, C., Lamarche, B., and Tsai, M. D. (2005) Use of viscogens, dNTPαS, and rhodium(III) as probes in stopped-flow experiments to obtain new evidence for the mechanism of catalysis by DNA polymerase β. Biochemistry 44, 5177-5187
24. Nakamura, T., Zhao, Y., Yamagata, Y., Hua, Y. J., and Yang, W. (2012) Watching DNA polymerase η make a phosphodiester bond. Nature 487, 196-201
25. 2+ is essential for catalyzing DNA synthesis. Science 352, 1334-1337
26. Xia, S., Wang, J., and Konigsberg, W. H. (2013) DNA mismatch synthesis complexes provide insights into base selectivity of a B family DNA polymerase. J. Am. Chem. Soc. 135, 193-202
27. Doublié, S., Tabor, S., Long, A. M., Richardson, C. C., and Ellenberger, T. (1998) Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 Å resolution. Nature 391, 251-258
28. 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. U.S.A. 100, 3895-3900
29. Jain, R., Rajashankar, K. R., Buku, A., Johnson, R. E., Prakash, L., Prakash, S., and Aggarwal, A. K. (2014) Crystal structure of yeast DNA polymerase ε catalytic domain. PLoS ONE 9, e94835
30. Vashishtha, A. K., and Konigsberg, W. H. (2016) Effect of different divalent cations on the kinetics and fidelity of RB69 DNA polymerase. Biochemistry 55, 2661-2670
31. Tabor, S., and Richardson, C. C. (1989) Effect of manganese ions on the incorporation of dideoxynucleotides by bacteriophage T7 DNA polymerase and Escherichia coli DNA polymerase I. Proc. Natl. Acad. Sci. U.S.A. 86, 4076-4080
32. Hori, K., Mark, D. F., and Richardson, C. C. (1979) Deoxyribonucleic acid polymerase of bacteriophage T7: characterization of the exonuclease activities of the gene 5 protein and the reconstituted polymerase. J. Biol. Chem. 254, 11598-11604
33. Kuchta, R. D., Mizrahi, V., Benkovic, P. A., Johnson, K. A., and Benkovic, S. J. (1987) Kinetic mechanism of DNA polymerase I (Klenow). Biochemistry 26, 8410-8417
34. Venkitaraman, A. R. (1989) Use of modified T7 DNA polymerase (sequenase version 2.0) for oligonucleotide site-directed mutagenesis. Nucleic Acids Res. 17, 3314
35. Joyce, C. M. (1989) How DNA travels between the separate polymerase and 3′-5′-exonuclease sites of DNA polymerase I (Klenow fragment). J. Biol. Chem. 264, 10858-10866
36. Irimia, A., Zang, H., Loukachevitch, L. V., Eoff, R. L., Guengerich, F. P., and Egli, M. (2006) Calcium is a cofactor of polymerization but inhibits pyrophosphorolysis by the Sulfolobus solfataricus DNA polymerase Dpo4. Biochemistry 45, 5949-5956
37. Sirover, M. A., and Loeb, L. A. (1976) Metal-induced infidelity during DNA synthesis. Proc. Natl. Acad. Sci. U.S.A. 73, 2331-2335
38. Sirover, M. A., and Loeb, L. A. (1976) Metal activation of DNA synthesis. Biochem. Biophys. Res. Commun. 70, 812-817
39. Seal, G., Shearman, C. W., and Loeb, L. A. (1979) On the fidelity of DNA replication: studies with human placenta DNA polymerases. J. Biol. Chem. 254, 5229-5237
40. Zhang, H., Cao, W., Zakharova, E., Konigsberg, W., and De La Cruz, E. M. (2007) Fluorescence of 2-aminopurine reveals rapid conformational changes in the RB69 DNA polymerase-primer/template complexes upon binding and incorporation of matched deoxynucleoside triphosphates. Nucleic Acids Res. 35, 6052-6062
41. Hariharan, C., Bloom, L. B., Helquist, S. A., Kool, E. T., and Reha-Krantz, L. J. (2006) Dynamics of nucleotide incorporation: snapshots revealed by 2-aminopurine fluorescence studies. Biochemistry 45, 2836-2844
42. Frey, M. W., Sowers, L. C., Millar, D. P., and Benkovic, S. J. (1995) The nucleotide analog 2-aminopurine as a spectroscopic probe of nucleotide incorporation by the Klenow fragment of Escherichia coli polymerase I and bacteriophage T4 DNA polymerase. Biochemistry 34, 9185-9192
43. 2+) on in vitro DNA replication by DNA polymerase α. Cancer Res. 54, 2337-2341
44. Bock, C. W., Katz, A. K., Markham, G. D., and Glusker, J. P. (1999) Manganese as a replacement for magnesium and zinc: functional comparison of the divalent ions. J. Am. Chem. Soc. 121, 7360-7372
45. Dube, D. K., and Loeb, L. A. (1975) Manganese as a mutagenic agent during in vitro DNA synthesis. Biochem. Biophys. Res. Commun. 67, 1041-1046
46. Jin, Y. H., Clark, A. B., Slebos, R. J., Al-Refai, H., Taylor, J. A., Kunkel, T. A., Resnick, M. A., and Gordenin, D. A. (2003) Cadmium is a mutagen that acts by inhibiting mismatch repair. Nat. Genet. 34, 326-329
47. Hays, H., and Berdis, A. J. (2002) Manganese substantially alters the dynamics of translesion DNA synthesis. Biochemistry 41, 4771-4778
48. Beckman, R. A., Mildvan, A. S., and Loeb, L. A. (1985) On the fidelity of DNA replication: manganese mutagenesis in vitro. Biochemistry 24, 5810-5817
49. Kunkel, T. A., and Bebenek, K. (2000) DNA replication fidelity. Annu. Rev. Biochem. 69, 497-529
50. Harris, V. H., Smith, C. L., Cummins, W. J., Hamilton, A. L., Adams, H., Dickman, M., Hornby, D. P., and Williams, D. M. (2003) The effect of tautomeric constant on the specificity of nucleotide incorporation during DNA replication: support for the rare tautomer hypothesis of substitution mutagenesis. J. Mol. Biol. 326, 1389-1401
51. Topal, M. D., and Fresco, J. R. (1976) Complementary base pairing and the origin of substitution mutations. Nature 263, 285-289
52. Bebenek, K., Pedersen, L. C., and Kunkel, T. A. (2011) Replication infidelity via a mismatch with Watson-Crick geometry. Proc. Natl. Acad. Sci. U.S.A. 108, 1862-1867
53. Wang, W., Hellinga, H. W., and Beese, L. S. (2011) Structural evidence for the rare tautomer hypothesis of spontaneous mutagenesis. Proc. Natl. Acad. Sci. U.S.A. 108, 17644-17648
54. Doetsch, P. W., Chan, G. L., and Haseltine, W. A. (1985) T4 DNA polymerase (3′-5′) exonuclease, an enzyme for the detection and quantitation of stable DNA lesions: the ultraviolet light example. Nucleic Acids Res. 13, 3285-3304
55. Kunkel, T. A., and Soni, A. (1988) Exonucleolytic proofreading enhances the fidelity of DNA synthesis by chick embryo DNA polymerase-γ. J. Biol. Chem. 263, 4450-4459
56. Cotton, F. A., Wilkinson, G., Murillo, C. A., and Bochmann, M. (1999) Advanced Inorganic Chemistry, 6th Ed., pp. 692-854, John Wiley & Sons, New York
57. Harding, M. M. (2006) Small revisions to predicted distances around metal sites in proteins. Acta Crystallogr. D Biol. Crystallogr. 62, 678-682
58. Mildvan, A. S., and Loeb, L. A. (1979) The role of metal ions in the mechanisms of DNA and RNA polymerases. CRC Crit. Rev. Biochem. 6, 219-244