Identifying the features of purine dNTPs that allow accurate and efficient DNA replication by herpes simplex virus I DNA polymerase

Biochemistry

Volumn 48, Issue 15, 2009, Pages 3554-3564

  Cavanaugh, Nisha A ^a   Urban, Milan ^a   Beckman, Jeffrey ^a   Spratt, Thomas E ^b   Kuchta, Robert D ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASE PAIRS; CHEMICAL FEATURES; DNA POLYMERASE; DNA REPLICATIONS; HERPES SIMPLEX VIRUS; HERPES SIMPLEX VIRUS 1; PURINE NUCLEOTIDES; TRIPHOSPHATE; VIRAL GENOMES;

DNA; GENES; HYDROGEN; HYDROGEN BONDS; MONOMERS; NUCLEIC ACIDS; NUCLEOTIDES; POLYMERIZATION; VIRUSES;

POLYMERS;

ADENINE; DNA POLYMERASE; PHOSPHATE; PURINE; PYRIMIDINE; VIRUS DNA;

ARTICLE; CHEMICAL STRUCTURE; DNA REPLICATION; DNA STRUCTURE; ELECTRON; HERPES SIMPLEX VIRUS 1; HYDROGEN BOND; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL;

BASE PAIRING; DNA REPLICATION; DNA, VIRAL; DNA-DIRECTED DNA POLYMERASE; EXODEOXYRIBONUCLEASES; HERPESVIRUS 1, HUMAN; HUMANS; PROTEIN SUBUNITS; PURINE NUCLEOTIDES; VIRAL PROTEINS; VIRUS REPLICATION;

HERPES; HUMAN HERPESVIRUS 1;

EID: 65249142734     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi8022202     Document Type: Article

References (37)

1. Lehman, I. R., and Boehmer, P. E. (1999) Replication of herpes simplex virus DNA. J. Biol. Chem. 274, 28059-28062.
2. Boehmer, P. E., and Lehman, I. R. (1997) Herpes simplex virus DNA replication. Annu. Rev. Biochem. 66, 347-384.
3. Johnson, P. A., Best, M. G., Friedmann, T., and Parris, D. S. (1991) Isolation of a herpes simplex virus type 1 mutant deleted for the essential UL42 gene and characterization of its null phenotype. J. Virol. 65, 700-710.
4. Stow, N. D. (1992) Herpes simplex virus type 1 origin-dependent DNA replication in insect cells using recombinant baculoviruses. J. Gen. Virol. 73, 313-321.
5. Wu, C. A., Nelson, N. J., McGeoch, D. J., and Challberg, M. D. (1988) Identification of herpes simplex virus type 1 genes required for origin-dependent DNA synthesis. J. Virol. 62, 435-443.
6. Roberts, J. D., and Kunkel, T. A. (1996) in DNA Replication in Eukaryotic Cells: Concepts, Enzymes and Systems (Depamphilis, M. L., Ed.) pp 217-247, CSHL Press, Plainview, NY.
7. Kunkel, T. A., and Bebenek, K. (1988) Recent studies of the fidelity of DNA synthesis. Biochim. Biophys. Acta 951, 1-15.
8. Bebenek, K., Abbotts, J., Wilson, S. H., and Kunkel, T. A. (1993) Error-prone polymerization by HIV-1 reverse transcriptase. Contribution of template-primer misalignment, miscoding, and termination probability to mutational hot spots. J. Biol. Chem. 268, 10324-10334.
9. Chaudhuri, M., Song, L., and Parris, D. S. (2003) The herpes simplex virus type 1 DNA polymerase processivity factor increases fidelity without altering pre-steady-state rate constants for polymerization or excision. J. Biol. Chem. 278, 8996-9004.
10. Song, L., Chaudhuri, M., Knopf, C. W., and Parris, D. S. (2004) Contribution of the 3′- to 5′-exonuclease activity of herpes simplex virus type 1 DNA polymerase to the fidelity of DNA synthesis. J. Biol. Chem. 279, 18535-18543.
11. Chiaramonte, M., Moore, C. L., Kincaid, K., and Kuchta, R. D. (2003) Facile polymerization of dNTPs bearing unnatural base analogues by DNA polymerase alpha and Klenow fragment (DNA polymerase I). Biochemistry 42, 10472-10481.
12. Kincaid, K., Beckman, J., Zivkovic, A., Halcomb, R. L., Engels, J. W., and Kuchta, R. D. (2005) Exploration of factors driving incorporation of unnatural dNTPS into DNA by Klenow fragment (DNA polymerase I) and DNA polymerase alpha. Nucleic Acids Res. 33, 2620-2628.
13. Beard, W. A., and Wilson, S. H. (2000) Structural design of a eukaryotic DNA repair polymerase: DNA polymerase beta. Mutat. Res. 460, 231-244.
14. 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 I: a structural explanation. Proc. Natl. Acad. Sci. U.S.A. 99, 1194-1199.
15. Joyce, C. M., and Benkovic, S. J. (2004) DNA polymerase fidelity: kinetics, structure, and checkpoints. Biochemistry 43, 14317-14324.
16. Echols, H., and Goodman, M. F. (1991) Fidelity mechanisms in DNA replication. Annu. Rev. Biochem. 60, 477-511.
17. Knopf, C. W. (1998) Evolution of viral DNA-dependent DNA polymerases. Virus Genes 16, 47-58.
18. Wong, S. W., Wahl, A. F., Yuan, P. M., Arai, N., Pearson, B. E., Arai, K., Korn, D., Hunkapiller, M. W., and Wang, T. S. (1988) Human DNA polymerase alpha gene expression is cell proliferation dependent and its primary structure is similar to both prokaryotic and eukaryotic replicative DNA polymerases. EMBO J. 7, 37-47.
19. Hopfner, K P., Eichinger, A., Engh, R. A., Laue, F., Ankenbauer, W., Huber, R., and Angerer, B. (1999) Crystal structure of a thermostable type B DNA polymerase from Thermococcus gor-gonarius. Proc. Natl. Acad. Sci. U.S.A. 96, 3600-3605.
20. Beckman, J., Kincaid, K., Hocek, M., Spratt, T., Engels, J., Cosstick, R., and Kuchta, R. D. (2007) Human DNA polymerase alpha uses a combination of positive and negative selectivity to polymerize purine dNTPs with high fidelity. Biochemistry 46, 448-460.
21. Patro, J. N., Milan, U., and Kuchta, R. D. (2009) Role of the 2-amino group of purines during dNTP polymerization by human DNA polymerase α. Biochemistry 48, 180-918.
22. Cavanaugh, N. A., and Kuchta, R. D. (2009) Initiation of new DNA strands by the herpes simplex virus-1 primase-helicase complex and either herpes DNA polymerase or human DNA polymerase alpha. J. Biol. Chem. 284, 1523-1532.
23. Maniatis, T., Fritsch, E. F., and Sambrook, J. (1982) Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Woodbury, NY.
24. 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.
25. Goodman, M. F., Creighton, S., Bloom, L. B., and Petruska, J. (1993) Biochemical basis of DNA replication fidelity. Crit. Rev. Biochem. Mol. Biol. 28, 83-126.
26. Reineks, E. Z., and Berdis, A. J. (2004) Evaluating the contribution of base stacking during translesion DNA replication. Biochemistry 43, 393-404.
27. 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.
28. Morales, J. C., and Kool, E. T. (2000) Varied molecular interactions at the active sites of several DNA polymerases: nonpolar nucleoside isosteres as probes. J. Am. Chem. Soc. 122, 1001-1007.
29. Moore, C. L., Zivkovic, A., Engels, J. W., and Kuchta, R. D. (2004) Human DNA primase uses Watson-Crick hydrogen bonds to distinguish between correct and incorrect nucleoside triphosphates. Biochemistry 43, 12367-12374.
30. 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.
31. Sowers, L. C., Boulard, Y., and Fazakerley, G. V. (2000) Multiple structures for the 2-aminopurine-cytosine mispair. Biochemistry 39, 7613-7620.
32. Sowers, L. C., Fazakerley, G. V., Eritja, R., Kaplan, B. E., and Goodman, M. F. (1986) Base pairing and mutagenesis: observation of a protonated base pair between 2-aminopurine and cytosine in an oligonucleotide by proton NMR. Proc. Natl. Acad. Sci. U.S.A. 83, 5434-5438.
33. Franklin, M. C., Wang, J., and Steitz, T. A. (2001) Structure of the replicating complex of a pol alpha family DNA polymerase. Cell (Cambridge, MA) 105, 657-667.
34. Yang, G., Wang, J., and Konigsberg, W. (2005) Base selectivity is impaired by mutants that perturb hydrogen bonding networks in the RB69 DNA polymerase active site. Biochemistry 44, 3338-3346.
35. Wang, T. S., Wong, S. W., and Korn, D. (1989) Human DNA polymerase alpha: predicted functional domains and relationships with viral DNA polymerases. FASEB J. 3, 14-21.
36. Kelley, S. O., and Barton, J. K. (1999) Electron transfer between bases in double helical DNA. Science 283, 375-381.
37. Liu, S., Knafels, J. D., Chang, J. S., Waszak, G. A., Baldwin, E. T, Deibel, M. R., Jr., Thomsen, D. R., Homa, F. L., Wells, P. A., Tory, M. C., Poorman, R. A., Gao, H, Qiu, X., and Seddon, A. P. (2006) Crystal structure of the herpes simplex virus 1 DNA polymerase. J. Biol. Chem. 281, 18193-18200.