An archaeal family-B DNA polymerase variant able to replicate past DNA damage: Occurrence of replicative and translesion synthesis polymerases within the B family

Nucleic Acids Research

Volumn 42, Issue 15, 2014, Pages 9949-9963

  Jozwiakowski, Stanislaw K ^a,b   Keith, Brian J ^b   Gilroy, Louise ^b   Doherty, Aidan J ^a   Connolly, Bernard A ^b  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED DNA POLYMERASE BETA; ENZYME VARIANT; ARCHAEAL PROTEIN; DNA DIRECTED DNA POLYMERASE; DNA DIRECTED DNA POLYMERASE ALPHA; PRIMER DNA; PYRIMIDINE DIMER;

ARTICLE; BASE MISPAIRING; CONTROLLED STUDY; DNA BASE COMPOSITION; DNA DAMAGE; DNA TEMPLATE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME STRUCTURE; ENZYME SYNTHESIS; PRIORITY JOURNAL; CHEMISTRY; DNA REPLICATION; ENZYMOLOGY; ESCHERICHIA COLI; GENETICS; METABOLISM; MUTATION; THERMOCOCCUS;

ARCHAEAL PROTEINS; BASE PAIR MISMATCH; DNA DAMAGE; DNA POLYMERASE II; DNA PRIMERS; DNA REPLICATION; DNA-DIRECTED DNA POLYMERASE; ESCHERICHIA COLI; MUTATION; PYRIMIDINE DIMERS; TEMPLATES, GENETIC; THERMOCOCCUS;

EID: 84922557556     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku683     Document Type: Article

References (64)

1. Braithwaite, D.K. and Ito, J. (1993) Compilation, alignment, and phylogenetic relationships of DNA polymerases. Nucleic Acids Res., 21, 787-802.
2. Joyce, C.M. and Steitz, T.A. (1994) Function and structure relationships in DNA polymerases. Annu. Rev. Biochem., 63, 777-822.
3. Bebenek, K. and Kunkel, T.A. (2004) Functions of DNA polymerases. DNA Repair Replication, 69, 137-165.
4. Brautigam, C.A. and Steitz, T.A. (1998). Structural and functional insights provided by crystal structures of DNA polymerases and their substrate complexes. Curr. Opin. Struct. Biol., 8, 54-63.
5. Stillman, B. (2008) DNA polymerases at the replication fork in eukaryotes. Mol. Cell, 30, 259-260.
6. Burgers, P.M.J. (2009) Polymerase dynamics at the eukaryotic DNA replication fork. J. Biol. Chem., 284, 4041-4045.
7. Ishino, Y. and Ishino, S. (2012) Rapid progress in DNA replication studies is the archaea, the third domain of life. Sci. China Life Sci., 55, 386-403.
8. Waters, L.S., Minesinger, B.K., Wiltrout, M.E, D'Souza, S., Woodruff, R.V. and Walker, R.V (2009) Eukaryotic translesion polymerases and their roles and regulation in DNA damage tolerance. Microbiol. Mol. Biol. Rev., 73, 134-154.
9. Schneider, S., Schorr, S. and Carell, T. (2009) Crystal structure analysis of DNA lesion repair and tolerancemechanisms. Curr. Opin. Struct. Biol, 19, 87-95.
10. Yang, W. and Woodgate, R. (2007) What a difference a decade makes: insights into translesion DNA synthesis. Proc. Natl. Acad. Sci. U.S.A., 104, 15591-15598.
11. McCulloch, S.D. and Kunkel, T.A. (2008) The fidelity of DNA synthesis by eukaryotic replicative and translesion synthesis polymerases. Cell Res., 18, 148-161.
12. Nick McElhinny, S.A., Gordenin, D.A., Stith, C.M., Burgers, P.M. and Kunkel, T.A. (2008) Division of labor at the eukaryotic replication fork. Mol. Cell, 30, 137-144.
13. Pursell, Z.F., Isoz, I., Lundstrom, E.B., Johansson, E. and Kunkel, T.A. (2007) Yeast DNA polymerase ϵ participates in leading-strand DNA replication. Science, 317, 127-130.
14. Perera, R.L., Torella, R., Klingel, S., Kilkenny, M.L., Maman, J.D and Pellegrini, L. (2013) Mechanism for priming DNA synthesis by yeast DNA Polymerase α. eLife, 2, e00482.
15. Swan, M.K., Johnson, R.E., Prakash, L., Prakash, S. and Aggarwal, A.K. (2009) Structural basis of high-fidelity DNA synthesis by yeast DNA polymerase 8. Nat. Struct. Mol. Biol, 16, 979-986.
16. Hogg, M., Ostermal, P, Byundl, G.O., Ganail, R.A., Lundström, E.-B., Sauer-Eriksson, A.E. and Johansson, E. (2014) Structural basis for processive DNA synthesis by yeast DNA polymerase ϵ. Nat. Struct. Mol. Biol, 21, 49-55.
17. Barry, E.R. and Bell, S.D. (2006) DNA replication in the archaea. Microbiol. Mol. Biol. Rev., 70, 876-887.
18. Kelman, Z. and White, M.F. (2005) Archaeal DNA replication and repair. Curr. Opin. Microbiol., 8, 669-676.
19. Cann, I.K., Komori, K., Toh, H., Kanai, S. and Ishino Y. (1998) A heterodimeric DNA polymerase: evidence that members of Euryarchaeota possess a distinct DNA polymerase. Proc. Natl. Acad Sci. U.S.A., 95, 14250-14255.
20. Cann, I.K. and Ishino, Y (1999) Archaeal DNA replication: identifying the pieces to solve a puzzle. Genetics, 152, 1249-1267.
21. Cubonova, L., Richardson, T., Burkhart, B.W., Kelman, Z., Connolly, B.A., Reeve, JN. and Santangelo, T.J. (2013) Archaeal DNA polymerase D but not DNA polymerase B is required for genome replication in Thermococcus kodakarensis. J. Bacteriol., 195, 2322-2328.
22. Sarmiento, F., Mrazek, J. and Whitman, W.B. (2013) Genome-scale analysis of gene function in the hydrogenotrophic methanogenic archaeon Methanococcusmaripaludis. Proc. Natl. Acad. Sci. U.S.A., 110, 4726-4731.
23. Lundberg, K.S., Shoemaker, D.D, Adams, M.W., Short, J.M., Sorge, J.A. and Mathur, E.J. (1991) High-fidelity amplification using a thermostable DNA polymerase isolated from Pyrococcus furiosus. Gene, 108, 1-6.
24. Cline, J., Braman, J.C. and Hogrefe, H.H. (1996) PCR fidelity of Pfu DNA polymerase and other thermostable DNA polymerases. Nucleic Acids Res, 24, 3546-3551.
25. Terpe, K. (2013) Overview of thermostable DNA polymerases for classical PCR applications: from molecular and biochemical fundamentals to commercial systems. Appl. Microbiol. Biotechnol., 97, 10243-10254.
26. Rangarajan, S., Woodgate, R. and Goodman, M.F. (1999) A phenotype for enigmatic DNA polymerase II: A pivotal role for pol II in replication restart in UV-irradiated Escherichia coli. Proc. Natl Acad. Sci. U.S.A., 96, 9224-9229.
27. Wang, F. and Yang, W. (2009) Structural insight into translesion synthesis by DNA Pol II. Cell, 139, 1279-1289.
28. Lawrence, CW. (2002) Cellular roles of DNA polymerase ζ and Rev1 protein. DNA Repair, 1, 425-435.
29. Lawrence, CW. (2004) Cellular functions of DNA polymerase ζ and Rev1 protein. Adv. Protein Chem., 69, 167-203.
30. Gan, GN, Wittschieben, J.P, Wittschieben, B.O. and Wood, R.D. (2008) DNA polymerase zeta (pol zeta) in higher eukaryotes. Cell Res., 18, 174-183.
31. Prakash, S. and Prakash, L. (2002) Translesion DNA synthesis in eukaryotes: a one-or two-polymerase affair. Genes Dev, 16, 1872-1833.
32. Leigh, J.A., Albers, S.J., Atomi, H. and Allers, T (2011) Model organisms for genetics in the domain Archaea: methanogens, halophiles, Thermococcales and Sulfolobales. FEMS Microbiol. Rev., 35, 577-608.
33. Biles, B.D. and Connolly, B.A. (2004) Low fidelity Pyrococcus furiosus DNA polymerase mutants useful in error-prone PCR. Nucleic Acids Res., 32, e176.
34. Jozwiakowski, S.K. and Connolly, B.A. (2011) A modified family-B archaeal DNA polymerase with reverse transcriptase activity. ChemBioChem, 12, 35-37.
35. Shaw, ND and Arya, D.P (2008) Recognition of the unique structure of DNA: RNA hybrids. Biochemie, 90, 1026-1039.
36. Keith, B.J., Jozwiakowski, S.K. and Connolly, B.A. (2013) A plasmid-based lacZα gene assay for DNA polymerase fidelity measurement. Anal. Biochem., 433, 153-161.
37. Jozwiakowski, S.K. and Connolly, B.A. (2009) Plasmid-based lacZa assay for DNA polymerase fidelity: application to archaeal family-B DNA polymerase. Nucleic Acids Res., 37, e102.
38. Kelley, L.A. and Sternberg, M.J.E. (2009) Protein structure prediction on the web: a case study using the Phyre server. Nat. Protoc, 4, 363-371.
39. Kim, S.W., Kim, D.-U., Kim, J.K., Kang, L.-W. and Cho, H.-S. (2008) Crystal structure of Pfu, the high fidelity DNA polymerase from Pyrococcus furiosus. Int. J. Biol. Macromol., 42, 356-361.
40. Firbank, S.J., Wardle, J., Heslop, P, Lewis, R.J. and Connolly, B.A. (2008) Uracil recognition in archaeal DNA polymerases captured by X-ray crystallography. J. Mol. Biol, 381, 529-539.
41. Pettersen, E.F., Goddard, TD, Huang, CC, Couch, GS., Greenblatt, D.M., Meng, E.C and Ferrin, TE. (2004) UCSF Chimera visualisation system for exploratory research and analysis. J. Comput. Chem., 25, 1605-1612.
42. Reha-Krantz, L.J. (2010) DNA polymerase proofreading: multiple roles maintain genome stability. Biochim. Biophys. Acta, 1804, 1049-1063.
43. Boiteux, S. and Guillet, M. (2004) Abasic sites in DNA: repair and biological consequences in Saccharomyces cerevisiae. DNA Repair, 3, 1-12.
44. Teoule, R., Bert, C and Bonicel, A. (1977) Thymine fragment damage retained in the DNA polynucleotide chain after gamma irradiation in aerated solutions. Radiat. Res., 72, 190-200.
45. Leadon, S.A. (1987) Production of thymine glycols in DNA by radiation and chemical carcinogens as detected by a monoclonal antibody. Br. J. Cancer, 55(Suppl. VIII), 113-117.
46. Cadet, J., Sageb, E. and Doukia, T (2005) Ultraviolet radiation-mediated damage to cellular DNA. Mutat. Res., 571, 3-17.
47. Pfeifer, GP, You, Y-H. and Besaratinia, A. (2005) Mutations induced by ultraviolet light. Mutat. Res., 571, 19-31.
48. Wang, Z., Lazarov, E., O'Donnell, M. and Goodman, M.F., (2002) Why Escherichia coli polymerase II makes more base substitution errors in AT-compared with GC-rich DNA. J. Biol. Chem., 277, 4446-4454.
49. Goodman, M.F. (2002) Coping with replication 'train wrecks' in Escherichia coli using Pol V, Pol II and RecA proteins. Trends Biochem. Sci, 25, 189-195.
50. Johnson, R.E., Washington, M.T., Haracska, L., Prakash, S. and Prakash, L. (2000) Eukaryotic polymerases ι and ζ act sequentially to bypass DNA lesions. Nature, 406, 1015-1019.
51. Johnson, R.E., Haracska, L., Prakash, S. and Prakash, L. (2001) Role of DNA polymerase η in the bypass of a (6-4) TT photoproduct. Mol. Cell. Biol, 21, 3558-3563.
52. Haracska, L., Unk, I., Johnson, R.E., Johansson, E., Burgers, PM.J, Prakash, S. and Prakash, L. (2001) Roles of yeast DNA polymerases 8 and ζ and of Rev1 in the bypass of abasic sites. Genes Dev, 15, 945-954.
53. Johnson, R.E., Yu, S.-L., Prakash, S. and Prakash, L. (2003) Yeast DNA polymerase zeta (ζ) is essential for error-free replication past thymine glycol. Genes Dev, 17, 77-87.
54. 6-methylguanine. Mol Cell. Biol, 23, 1453-1459.
55. Lawrence, C.W. and Maher, V.M. (2001) Mutagenesis in eukaryotes dependent on DNA polymerase zeta and Rev1p. Philos. Trans. R Soc. Lond. B. Biol. Sci, 356, 41-46.
56. Northam, M.R., Moore, E.A., Mertz, T.M., Binz, S.K., Stith, C.M., Stepchenkova, E.I, Wendt, K.L., Burgers, P.M.J. and Shcherbakova, P.V. (2014) DNA polymerases ζ and Rev1 mediate error-prone bypass of non-B DNA structures. Nucleic Acids Res., 42, 290-306.
57. Franklin, M.C., Wang, J. and Steitz, T.A. (2001) Structure of the replicating complex of a pol α family DNA polymerase. Cell, 105, 657-667.
58. Kunkel, T.A. and Bebenek, K. (2000) DNA replication fidelity. Annu. Rev. Biochem., 69, 497-529.
59. Kunkel, T.A. (2004) DNA replication fidelity. J. Biol. Chem., 279, 16895-16898.
60. Sabouri, N, Viberg, J., Goyal, DK., Johansson, E. and Chabes, A. (2008) Evidence for lesion bypass by yeast replicative DNA polymerases during DNA damage. Nucleic Acids Res., 36, 5660-5667.
61. Sabouri, N and Johansson, E. (2009) Translesion synthesis of abasic sites by yeast DNA polymerase ϵ. J. Biol. Chem., 284, 31555-31563.
62. Heller, R.C. and Marians, K.J. (2006) Replisome assembly and the direct restart of stalled replication forks. Nat. Rev. Mol Cell Biol, 7, 932-943.
63. Fenton, A.K. and Gerdes, K. (2013) Direct interaction of FtsZ and MreB is required for septum synthesis and cell division in Escherichia coli. EMBO J., 32, 1953-1965.
64. Cozens, C, Pinheiro, VB., Vaisman, A., Woodgate, R. and Holliger, P, (2012) A short adaptive path from DNA to RNA polyerases. Proc Nat. Acad. Sci. U.S.A., 109, 8067-8072.