Structural basis for processive DNA synthesis by yeast DNA polymerase É

Nature Structural and Molecular Biology

Volumn 21, Issue 1, 2014, Pages 49-55

  Hogg, Matthew ^a   Osterman, Pia ^a   Bylund, Göran O ^a   Ganai, Rais A ^a   Lundström, Else Britt ^a   Sauer Eriksson, A Elisabeth ^a   Johansson, Erik ^a  

^a UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84893772675     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2712     Document Type: Article

References (54)

1. Burgers, P.M. Polymerase dynamics at the eukaryotic DNA replication fork. J. Biol. Chem. 284, 4041-4045 (2009).
2. Miyabe, I., Kunkel, T.A. & Carr, A.M. The major roles of DNA polymerases epsilon and delta at the eukaryotic replication fork are evolutionarily conserved. PLoS Genet. 7, e1002407 (2011).
3. Nick McElhinny, S.A., Gordenin, D.A., Stith, C.M., Burgers, P.M. & Kunkel, T.A. Division of labor at the eukaryotic replication fork. Mol. Cell 30, 137-144 (2008).
4. Larrea, A.A. et al. Genome-wide model for the normal eukaryotic DNA replication fork. Proc. Natl. Acad. Sci. USA 107, 17674-17679 (2010).
5. Pursell, Z.F., Isoz, I., Lundstrom, E.B., Johansson, E. & Kunkel, T.A. Yeast DNA polymerase ε participates in leading-strand DNA replication. Science 317, 127-130 (2007).
6. Hamatake, R.K. et al. Purifcation and characterization of DNA polymerase II from the yeast Saccharomyces cerevisiae: identifcation of the catalytic core and a possible holoenzyme form of the enzyme. J. Biol. Chem. 265, 4072-4083 (1990).
7. Araki, H., Hamatake, R.K., Johnston, L.H. & Sugino, A. DPB2, the gene encoding DNA polymerase II subunit B, is required for chromosome replication in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 88, 4601-4605 (1991).
8. Isoz, I., Persson, U., Volkov, K. & Johansson, E. The C-terminus of Dpb2 is required for interaction with Pol2 and for cell viability. Nucleic Acids Res. 40, 11545-11553 (2012).
9. Ohya, T., Maki, S., Kawasaki, Y. & Sugino, A. Structure and function of the fourth subunit (Dpb4p) of DNA polymerase ε in Saccharomyces cerevisiae. Nucleic Acids Res. 28, 3846-3852 (2000).
10. Araki, H. et al. Cloning DPB3, the gene encoding the third subunit of DNA polymerase II of Saccharomyces cerevisiae. Nucleic Acids Res. 19, 4867-4872 (1991).
11. Tsubota, T., Maki, S., Kubota, H., Sugino, A. & Maki, H. Double-stranded DNA binding properties of Saccharomyces cerevisiae DNA polymerase ε and of the Dpb3p-Dpb4p subassembly. Genes Cells 8, 873-888 (2003).
12. Aksenova, A. et al. Mismatch repair-independent increase in spontaneous mutagenesis in yeast lacking non-essential subunits of DNA polymerase ε. PLoS Genet. 6, e1001209 (2010).
13. Shcherbakova, P.V. et al. Unique error signature of the four-subunit yeast DNA polymerase ε. J. Biol. Chem. 278, 43770-43780 (2003).
14. Chilkova, O. et al. The eukaryotic leading and lagging strand DNA polymerases are loaded onto primer-ends via separate mechanisms but have comparable processivity in the presence of PCNA. Nucleic Acids Res. 35, 6588-6597 (2007).
15. Núñez-Ramírez, R. et al. Flexible tethering of primase and DNA Pol a in the eukaryotic primosome. Nucleic Acids Res. 39, 8187-8199 (2011).
16. Palles, C. et al. Germline mutations affecting the proofreading domains of POLE and POLD1 predispose to colorectal adenomas and carcinomas. Nat. Genet. 45, 136-144 (2013).
17. Kandoth, C. et al. Integrated genomic characterization of endometrial carcinoma. Nature 497, 67-73 (2013).
18. Church, D.N. et al. DNA polymerase e and ô exonuclease domain mutations in endometrial cancer. Hum. Mol. Genet. 22, 2820-2828 (2013).
19. Johansson, E. & Macneill, S.A. The eukaryotic replicative DNA polymerases take shape. Trends Biochem. Sci. 35, 339-347 (2010).
20. Swan, M.K., Johnson, R.E., Prakash, L., Prakash, S. & Aggarwal, A.K. Structural basis of high-fdelity DNA synthesis by yeast DNA polymerase Ô. Nat. Struct. Mol. Biol. 16, 979-986 (2009).
21. Perera, R.L. et al. Mechanism for priming DNA synthesis by yeast DNA Polymerase a. eLife 2, e00482 (2013).
22. Franklin, M.C., Wang, J. & Steitz, T.A. Structure of the replicating complex of a pol a family DNA polymerase. Cell 105, 657-667 (2001).
23. Nuutinen, T. et al. The solution structure of the amino-terminal domain of human DNA polymerase e subunit B is homologous to C-domains of AAA+ proteins. Nucleic Acids Res. 36, 5102-5110 (2008).
24. Asturias, F.J. et al. Structure of Saccharomyces cerevisiae DNA polymerase e by cryo-electron microscopy. Nat. Struct. Mol. Biol. 13, 35-43 (2006).
25. Hartlepp, K.F. et al. The histone fold subunits of Drosophila CHRAC facilitate nucleosome sliding through dynamic DNA interactions. Mol. Cell. Biol. 25, 9886-9896 (2005).
26. Liu, S. et al. Crystal structure of the herpes simplex virus 1 DNA polymerase. J. Biol. Chem. 281, 18193-18200 (2006).
27. Yang, W. Nucleases: diversity of structure, function and mechanism. Q. Rev. Biophys. 44, 1-93 (2011).
28. Morrison, A. & Sugino, A. The 3'→5' exonucleases of both DNA polymerases O and e participate in correcting errors of DNA replication in Saccharomyces cerevisiae. Mol. Gen. Genet. 242, 289-296 (1994).
29. Savino, C. et al. Insights into DNA replication: the crystal structure of DNA polymerase B1 from the archaeon Sulfolobus solfataricus. Structure 12, 2001-2008 (2004).
30. Holm, L. & Rosenstrom, P. Dali server: conservation mapping in 3D. Nucleic Acids Res. 38, W545-W549 (2010).
31. Garcia-Diaz, M., Bebenek, K., Krahn, J.M., Kunkel, T.A. & Pedersen, L.C. A closed conformation for the Pol A. catalytic cycle. Nat. Struct. Mol. Biol. 12, 97-98 (2005).
32. Garcia-Diaz, M., Bebenek, K., Krahn, J.M., Pedersen, L.C. & Kunkel, T.A. Role of the catalytic metal during polymerization by DNA polymerase X. DNA Repair (Amst.) 6, 1333-1340 (2007).
33. Fortune, J.M. et al. Saccharomyces cerevisiae DNA polymerase Ô: high fdelity for base substitutions but lower fdelity for single-and multi-base deletions. J. Biol. Chem. 280, 29980-29987 (2005).
34. Xia, S., Christian, T.D., Wang, J. & Konigsberg, W.H. Probing minor groove hydrogen bonding interactions between RB69 DNA polymerase and DNA. Biochemistry 51, 4343-4353 (2012).
35. Wang, M. et al. Insights into base selectivity from the 1.8 A resolution structure of an RB69 DNA polymerase ternary complex. Biochemistry 50, 581-590 (2011).
36. Pata, J.D. Structural diversity of the Y-family DNA polymerases. Biochim. Biophys. Acta 1804, 1124-1135 (2010).
37. Stocki, S.A., Nonay, R.L. & Reha-Krantz, L.J. Dynamics of bacteriophage T4 DNA polymerase function: identifcation of amino acid residues that affect switching between polymerase and 3'-^ 5' exonuclease activities. J. Mol. Biol. 254, 15-28 (1995).
38. Hogg, M., Aller, P., Konigsberg, W., Wallace, S.S. & Doublie, S. Structural and biochemical investigation of the role in proofreading of a β hairpin loop found in the exonuclease domain of a replicative DNA polymerase of the B family. J. Biol. Chem. 282, 1432-1444 (2007).
39. Williams, L.N., Herr, A.J. & Preston, B.D. Emergence of DNA Polymerase £ antimutators that escape error-induced extinction in yeast. Genetics 193, 751-770 (2013).
40. Doublié, S., Tabor, S., Long, A.M., Richardson, C.C. & Ellenberger, T. Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 A resolution. Nature 391, 251-258 (1998).
41. Ling, H., Boudsocq, F., Woodgate, R. & Yang, W. Crystal structure of a Y-family DNA polymerase in action: a mechanism for error-prone and lesion-bypass replication. Cell 107, 91-102 (2001).
42. Nakamura, T., Zhao, Y, Yamagata, Y, Hua, Y.J. & Yang, W. Watching DNA polymerase r\make a phosphodiester bond. Nature 487, 196-201 (2012).
43. Sabouri, N. & Johansson, E. Translesion synthesis of abasic sites by yeast DNA polymerase ε. J. Biol. Chem. 284, 31555-31563 (2009).
44. Kabsch, W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 26, 795-800 (1993).
45. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763 (1994).
46. McCoy, A.J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
47. Adams, P.D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).
48. Terwilliger, T. SOLVE and RESOLVE: automated structure solution, density modifcation and model building. J. Synchrotron Radiat. 11, 49-52 (2004).
49. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004).
50. Emsley, P., Lohkamp, B., Scott, W.G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).
51. Murshudov, G.N., Vagin, A.A. & Dodson, E.J. Refnement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (1997).
52. Chilkova, O., Jonsson, B.H. & Johansson, E. The quaternary structure of DNA polymerase ε from Saccharomyces cerevisiae. J. Biol. Chem. 278, 14082-14086 (2003).
53. Hogg, M., Sauer-Eriksson, A.E. & Johansson, E. Promiscuous DNA synthesis by human DNA polymerase θ. Nucleic Acids Res. 40, 2611-2622 (2012).
54. Potterton, L. et al. Developments in the CCP4 molecular-graphics project. Acta Crystallogr. D Biol. Crystallogr. 60, 2288-2294 (2004).