Steric and electrostatic effects in DNA synthesis by the SOS-induced DNA polymerases II and IV of Escherichia coli

Biochemistry

Volumn 46, Issue 48, 2007, Pages 13874-13881

  Silverman, Adam P ^a   Jiang, Qingfei ^b   Goodman, Myron F ^b   Kool, Eric T ^a  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA SYNTHESIS; GENOMIC DNA; POLAR THYMINE BASE;

ELECTROSTATICS; ENZYME KINETICS; ESCHERICHIA COLI; HYDROGEN BONDS; SYNTHESIS (CHEMICAL);

DNA;

DNA DIRECTED DNA POLYMERASE ALPHA; DNA POLYMERASE; DNA POLYMERASE IV; THYMIDINE; UNCLASSIFIED DRUG;

ARTICLE; DNA SYNTHESIS; ELECTRICITY; ESCHERICHIA COLI; HYDROGEN BOND; NUCLEOTIDE INSERTION; PRIORITY JOURNAL; STEADY STATE; STEREOSPECIFICITY;

BASE SEQUENCE; DNA POLYMERASE BETA; DNA POLYMERASE II; DNA PRIMERS; DNA REPLICATION; ELECTROSTATICS; SOS RESPONSE (GENETICS);

ARCHAEA; ESCHERICHIA COLI;

EID: 36849052403     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi700851z     Document Type: Article

References (44)

1. Latham, G. J., McNees, A. G., De Corte, B., Harris, C. M., Harris, T. M., O'Donnell, M., and Lloyd, R. S. (1996) Comparison of the efficiency of synthesis past single bulky DNA adducts in vivo and in vitro by the polymerase III holoenzyme, Chem. Res. Toxicol. 9, 1167-1175.
2. Rangarajan, S., Woodgate, R., and Goodman, M. F. (2002) Replication restart in UV-irradiated Escherichia coli involving pols II, III, V, PriA, RecA and RecFOR proteins, Mol. Microbiol. 43, 618-628.
3. Kobayashi, S., Valentine, M. R., Pham, P., O'Donnell, M., and Goodman, M. F. (2002) Fidelity of Escherichia coli DNA polymerase IV, J. Biol. Chem. 277, 34198-34207.
4. Wang, Z., Lazarov, E., O'Donnell, M., and Goodman, M. F. (2002) Resolving a fidelity paradox, J. Biol. Chem. 277, 4446-4454.
5. Goodman, M. F. (2002) Error-prone repair DNA polymerases in prokaryotes and eukaryotes, Annu. Rev. Biochem. 71, 17-50.
6. Napolitano, R., Janel-Bintz, R., Wagner, J., and Fuchs, R. P. P. (2000) All three SOS-inducible DNA polymerases (Pol II, Pol IV and Pol V) are involved in induced mutagenesis, EMBO J. 19, 6259-6265.
7. Kim, S. R., Matsui, K., Yamada, M., Gruz, P., and Nohmi, T. (2001) Roles of chromosomal and episomal dinB genes encoding DNA pol IV in targeted and untargeted mutagenesis in Escherichia coli, Mol. Genet. Genomics 266, 207-215.
8. Delmas, S., and Matic, I. (2006) Interplay between replication and recomination in Escherichia coli: Impact of the alternative DNA polymerases, Proc. Natl. Acad. Sci. U.S.A. 103, 4564-4569.
9. McKenzie, G. J., Lee, P. L., Lombardo, M.-J., Hastings, P. J., and Rosenberg, S. M. (2001) SOS mutator DNA polymerase IV functions in adaptive mutation and not adaptive amplification, Mol. Cell 7, 571-579.
10. Kool, E. T. (2002) Active site tightness and substrate fit in DNA replication, Annu. Rev. Biochem. 69, 497-529.
11. Moran, S., Ren, R. X.-F., Rummey, S., IV, and Kool, E. T. (1997) Difluorotoluene, a nonpolar isostere for thymidine, codes specifically and efficiently for adenine in DNA replication, J. Am. Chem. Soc. 119, 2056-2057.
12. Kool, E. T., and Sintim, H. O. (2006) The difluorotoluene debate: A decade later, Chem. Commun. 35, 3665-3675.
13. Matray, T. J., and Kool, E. T. (1999) A specific partner for abasic damage in DNA, Nature 399, 704-708.
14. Kool, E. T. (1998) Replication of non-hydrogen bonded bases by DNA polymerases: A mechanism for steric matching, Biopolymers 48, 3-17.
15. Echols, H., and Goodman, M. F. (1991) Fidelity mechanisms in DNA-replication, Annu. Rev. Biochem. 60, 477-511.
16. Schweitzer, B. A., and Kool, E. T. (1994) Aromatic nonpolar nucleosides as hydrophobic isosteres of pyrimidines and purine nucleosides, J. Org. Chem. 59, 7238-7242.
17. Morales, J. C., and Kool, E. T. (1998) Efficient replication between non-hydrogen-bonded nucleoside shape analogs, Nat. Struct. Biol. 5, 950-954.
18. Ogawa, A. K., Wu, Y. Q., Berger, M., Schultz, P. G., and Romesberg, F. E. (2000) Rational design of an unnatural base pair with increased kinetic selectivity, J. Am. Chem. Soc. 122, 8803-8804.
19. Sintim, H. O., and Kool, E. T. (2006) Remarkable sensitivity to DNA base shape in the DNA polymerase active site, Angew. Chem., Int. Ed. 45, 1974-1979.
20. Hirao, I., Kimoto, M., Mitsui, T., Fujiwara, T., Kawai, R., Sato, A., Harada, Y., and Yokoyama, S. (2006) An unnatural hydrophobic base pair system: Site-specific incorporation of nucleotide analogs into DNA and RNA, Nat. Methods 3, 729-735.
21. Kim, T. W., and Kool, E. T. (2004) A set of nonpolar thymidine nucleoside analogues with gradually increasing size, Org. Lett. 6, 3949-3952.
22. Kim, T. W., and Kool, E. T. (2005) A series of nonpolar thymidine analogs of increasing size: DNA base pairing and stacking properties, J Org. Chem. 70, 2048-2053.
23. Kim, T. W., Delaney, J. C., Essigmann, J. M., and Kool, E. T. (2005) Probing the active site tightness of DNA polymerase in subangstrom increments, Proc. Natl. Acad. Sci. U.S.A. 102, 15803-15808.
24. Kim, T. W., Brieba, L. G., Ellenberger, T., and Kool, E. T. (2006) Functional evidence for a small and rigid active site in a high fidelity DNA polymerase, J. Biol. Chem. 281, 2289-2295.
25. 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.
26. Deleted in press.
27. Cai, H., Yu, H., McEntee, K., Kunkel, T. A., and Goodman, M. F. (1995) Purification and properties of wild-type and exonuclease-deficient DNA polymerase II from Escherichia coli, J. Biol. Chem. 270, 15327-15335.
28. Washington, M. T., Helquist, S. A., Kool, E. T., Prakash, L., and Prakash, S. (2003) Requirement of Watson-Crick hydrogen bonding for DNA synthesis by yeast DNA polymerase η, Mol. Cell. Biol. 23, 5107-5112.
29. Summerer, D., and Marx, A. (2001) DNA polymerase, selectivity: Sugar interactions monitored with high-fidelity nucleotides, Angew. Chem., Int. Ed. 40, 3693-3695.
30. Wolfle, W. T., Washington, M. T., Kool, E. T., Spratt, T. E., Helquist, S. A., Prakash, L., and Prakash, S. (2005) Evidence for a Watson-Crick hydrogen bonding requirement in DNA synthesis by human DNA polymerase κ, Mol. Cell. Biol. 25, 7137-7143.
31. Lee, C. H., Chandani, S., and Loechler, E. L. (2006) Humology modeling of four Y-family, lesion-bypass DNA polymerases: The case that E. coli Pol IV and human Pol κ are orthologs, and E. coli Pol V and human Pol η are orthologs, J. Mol. Graphics Modell. 25, 87-102.
32. Franklin, M. C., Wang, J., and Steitz, T. A. (2001) Structure of the replicating complexof a Pol α family DNA polymerase, Cell 105, 657-667.
33. Hogg, M., Wallace, S. S., and Doublie, S. (2004) Crystallographic snapshots of a replicative DNA polymerase encountering an abasic site, EMBO J. 23, 1483-1493.
34. Freisinger, E., Grollman, A. P., Miller, H., and Kisker, C. (2004) Lesion (in)tolerance reveals insights into DNA replication fidelity, EMBO J. 23, 1494-1505.
35. Anderson, W. F., Prince, D. B., Yu, H., McEntee, K., and Goodman, M. F. (1994) Crystallization of DNA polymerase II from Escherichia coli, J. Mol. Biol. 238, 120-122.
36. Hashimoto, H., Nishioka, M., Fujiwara, S., Takagi, M., Imanaka, T., Inoue, T., and Kai, Y. (2001) Crystal structure of DNA polymerase from hyperthermophilic archaeon Pyrococcus kodakaraensis KOD1, J. Mol. Biol. 306, 469-477.
37. Wang, J., Sattar, A. K., Wang, C. C., Karam, J. D., Konigsberg, W. H., and Steitz, T. A. (1997) Crystal structure of a pol α family replication DNA polymerase from bacteriophage RB69, Cell 89, 1087-1099.
38. Zhao, Y., Jeruzalmi, D., Moarefi, I., Leighton, L., Lasken, R., and Kuriyan, J. (1999) Crystal structure of an archaebacterial DNA polymerase, Structure 7, 1189-1199.
39. Kim, S.-R., Maenhaur-Michel, G., Yamada, M., Yamamoto, Y., Matsui, K., Sofuni, T., Nohmi, T., and Ohmori, H. (1997) Multiple pathways for SOS-induced matagenesis in Escherichia coli: An overexpression of dinB/dinP results in strongly enhancing mutagenesis in the absence of any exogenous treatment to damage DNA, Proc. Natl. Acad. Sci. U.S.A. 94, 13792-13797.
40. 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. Acad. Sci. U.S.A. 101, 2265-2269.
41. Perlow-Poehnelt, R. A., Likhterov, I., Wang, L. H., Scicchitano, D. A., Geacintov, N. E., and Broyde, S. (2007) Increased flexibility enhances misincorporation: Temperature effects on nucleotide incorporation opposite a bulky carcinogen-DNA adduct by a Y-family DNA polymerase, J. Biol. Chem. 282, 1397-1408.
42. Paz-Elizur, T., Takeshita, M., Goodman, M. F., O'Donnell, M., and Livneh, Z. (1996) Mechanism of translesion DNA synthesis by DNA polymerase II. Comparison to DNA polymerases I and III core, J. Biol. Chem. 271, 24662-24669.
43. Fuchs, R. P., Koffel-Schwartz, N., Pelet, S., Janel-Bintz, R., Napolitano, R., Becherel, O. J., Broschard, T. H., Burnouf, D. Y., and Wagner, J. (2001) DNA polymerases II and V mediate respectively mutagenic (-2 frameshift) and error-free bypass of a single N-2-acetylaminofluorene adduct, Biochem. Soc. Trans. 29, 191-195.
44. Kanuri, M., Nechev, L. V., Kiehna, S. E., Tamura, P. J., Harris, C. M., Harris, T. M., and Lloyd, R. S. (2005) Evidence for Escherichia coli polymerase II mutagenic bypass of intrastrand DNA crosslinks, DNA Repair 4, 1374-1380.