A Major Role of DNA Polymerase δ in Replication of Both the Leading and Lagging DNA Strands

Molecular Cell

Volumn 59, Issue 2, 2015, Pages 163-175

  Johnson, Robert E ^a   Klassen, Roland ^a,b   Prakash, Louise ^a   Prakash, Satya ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF KASSEL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYCYTIDINE TRIPHOSPHATE; DEOXYGUANOSINE TRIPHOSPHATE; DNA DIRECTED DNA POLYMERASE DELTA; DNA POLYMERASE; EXONUCLEASE; HOLOENZYME; MUTAGENIC AGENT; DNA DIRECTED DNA POLYMERASE ALPHA; DNA DIRECTED DNA POLYMERASE GAMMA; EXODEOXYRIBONUCLEASE; EXODEOXYRIBONUCLEASE I; FUNGAL DNA; POL3 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; URA3 PROTEIN, S CEREVISIAE;

ALLELE; ARTICLE; DNA REPLICATION; DNA SEQUENCE; DNA STRAND; DNA SYNTHESIS; ENZYME ACTIVE SITE; FRAMESHIFT MUTATION; FUNGAL GENOME; FUNGAL STRAIN; GENETICS; IN VITRO STUDY; MISMATCH REPAIR; NONHUMAN; SACCHAROMYCES CEREVISIAE; YEAST; AMINO ACID SUBSTITUTION; BASE MISPAIRING; METABOLISM; MUTATION; SITE DIRECTED MUTAGENESIS;

AMINO ACID SUBSTITUTION; BASE PAIR MISMATCH; DNA POLYMERASE II; DNA POLYMERASE III; DNA REPLICATION; DNA, FUNGAL; EXODEOXYRIBONUCLEASES; GENOME, FUNGAL; MUTAGENESIS, SITE-DIRECTED; MUTATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84937413584     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.05.038     Document Type: Article

References (47)

1. Acharya N., Klassen R., Johnson R.E., Prakash L., Prakash S. PCNA binding domains in all three subunits of yeast DNA polymerase δ modulate its function in DNA replication. Proc. Natl. Acad. Sci. USA 2011, 108:17927-17932.
2. Boulet A., Simon M., Faye G., Bauer G.A., Burgers P.M.J. Structure and function of the Saccharomyces cerevisiae CDC2 gene encoding the large subunit of DNA polymerase III. EMBO J. 1989, 8:1849-1854.
3. Clausen A.R., Zhang S., Burgers P.M., Lee M.Y., Kunkel T.A. Ribonucleotide incorporation, proofreading and bypass by human DNA polymerase δ. DNA Repair (Amst.) 2013, 12:121-127.
4. Clausen A.R., Lujan S.A., Burkholder A.B., Orebaugh C.D., Williams J.S., Clausen M.F., Malc E.P., Mieczkowski P.A., Fargo D.C., Smith D.J., Kunkel T.A. Tracking replication enzymology invivo by genome-wide mapping of ribonucleotide incorporation. Nat. Struct. Mol. Biol. 2015, 22:185-191.
5. Daigaku Y., Keszthelyi A., Müller C.A., Miyabe I., Brooks T., Retkute R., Hubank M., Nieduszynski C.A., Carr A.M. A global profile of replicative polymerase usage. Nat. Struct. Mol. Biol. 2015, 22:192-198.
6. Feng W., D'Urso G. Schizosaccharomyces pombe cells lacking the amino-terminal catalytic domains of DNA polymerase epsilon are viable but require the DNA damage checkpoint control. Mol. Cell. Biol. 2001, 21:4495-4504.
7. Fu Y.V., Yardimci H., Long D.T., Ho T.V., Guainazzi A., Bermudez V.P., Hurwitz J., van Oijen A., Schärer O.D., Walter J.C. Selective bypass of a lagging strand roadblock by the eukaryotic replicative DNA helicase. Cell 2011, 146:931-941.
8. Ganai R.A., Bylund G.O., Johansson E. Switching between polymerase and exonuclease sites in DNA polymerase ε. Nucleic Acids Res. 2015, 43:932-942.
9. Genschel J., Bazemore L.R., Modrich P. Human exonuclease I is required for 5' and 3' mismatch repair. J.Biol. Chem. 2002, 277:13302-13311.
10. Georgescu R.E., Langston L., Yao N.Y., Yurieva O., Zhang D., Finkelstein J., Agarwal T., O'Donnell M.E. Mechanism of asymmetric polymerase assembly at the eukaryotic replication fork. Nat. Struct. Mol. Biol. 2014, 21:664-670.
11. Handa T., Kanke M., Takahashi T.S., Nakagawa T., Masukata H. DNA polymerization-independent functions of DNA polymerase epsilon in assembly and progression of the replisome in fission yeast. Mol. Biol. Cell 2012, 23:3240-3253.
12. Hartwell L.H. Sequential function of gene products relative to DNA synthesis in the yeast cell cycle. J.Mol. Biol. 1976, 104:803-817.
13. Ilves I., Petojevic T., Pesavento J.J., Botchan M.R. Activation of the MCM2-7 helicase by association with Cdc45 and GINS proteins. Mol. Cell 2010, 37:247-258.
14. Johnson R.E., Kovvali G.K., Prakash L., Prakash S. Requirement of the yeast MSH3 and MSH6 genes for MSH2-dependent genomic stability. J.Biol. Chem. 1996, 271:7285-7288.
15. Kesti T., Flick K., Keränen S., Syväoja J.E., Wittenberg C. DNA polymerase ε catalytic domains are dispensable for DNA replication, DNA repair, and cell viability. Mol. Cell 1999, 3:679-685.
16. Koh K.D., Balachander S., Hesselberth J.R., Storici F. Ribose-seq: global mapping of ribonucleotides embedded in genomic DNA. Nat. Methods 2015, 12:251-257. 3, 257.
17. Langston L.D., Zhang D., Yurieva O., Georgescu R.E., Finkelstein J., Yao N.Y., Indiani C., O'Donnell M.E. CMG helicase and DNA polymerase ε form a functional 15-subunit holoenzyme for eukaryotic leading-strand DNA replication. Proc. Natl. Acad. Sci. USA 2014, 111:15390-15395.
18. Larrea A.A., Lujan S.A., Nick McElhinny S.A., Mieczkowski P.A., Resnick M.A., Gordenin D.A., Kunkel T.A. Genome-wide model for the normal eukaryotic DNA replication fork. Proc. Natl. Acad. Sci. USA 2010, 107:17674-17679.
19. Lea D.E., Coulson C.A. The distribution of the numbers of mutants in bacterial populations. J.Genet. 1949, 49:264-285.
20. Lujan S.A., Williams J.S., Pursell Z.F., Abdulovic-Cui A.A., Clark A.B., Nick McElhinny S.A., Kunkel T.A. Mismatch repair balances leading and lagging strand DNA replication fidelity. PLoS Genet. 2012, 8:e1003016.
21. Lujan S.A., Williams J.S., Clausen A.R., Clark A.B., Kunkel T.A. Ribonucleotides are signals for mismatch repair of leading-strand replication errors. Mol. Cell 2013, 50:437-443.
22. 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. 2011, 7:e1002407.
23. Morrison A., Bell J.B., Kunkel T.A., Sugino A. Eukaryotic DNA polymerase amino acid sequence required for 3'----5' exonuclease activity. Proc. Natl. Acad. Sci. USA 1991, 88:9473-9477.
24. Mortimer R.K., Johnston J.R. Genealogy of principal strains of the yeast genetic stock center. Genetics 1986, 113:35-43.
25. Moyer S.E., Lewis P.W., Botchan M.R. Isolation of the Cdc45/Mcm2-7/GINS (CMG) complex, a candidate for the eukaryotic DNA replication fork helicase. Proc. Natl. Acad. Sci. USA 2006, 103:10236-10241.
26. Navas T.A., Zhou Z., Elledge S.J. DNA polymerase epsilon links the DNA replication machinery to the S phase checkpoint. Cell 1995, 80:29-39.
27. Nick McElhinny S.A., Stith C.M., Burgers P.M., Kunkel T.A. Inefficient proofreading and biased error rates during inaccurate DNA synthesis by a mutant derivative of Saccharomyces cerevisiae DNA polymerase delta. J.Biol. Chem. 2007, 282:2324-2332.
28. Nick McElhinny S.A., Gordenin D.A., Stith C.M., Burgers P.M.J., Kunkel T.A. Division of labor at the eukaryotic replication fork. Mol. Cell 2008, 30:137-144.
29. Nick McElhinny S.A., Kumar D., Clark A.B., Watt D.L., Watts B.E., Lundström E.B., Johansson E., Chabes A., Kunkel T.A. Genome instability due to ribonucleotide incorporation into DNA. Nat. Chem. Biol. 2010, 6:774-781.
30. Nieduszynski C.A., Hiraga S., Ak P., Benham C.J., Donaldson A.D. OriDB: a DNA replication origin database. Nucleic Acids Res. 2007, 35:D40-D46.
31. Pavlov Y.I., Shcherbakova P.V., Kunkel T.A. Invivo consequences of putative active site mutations in yeast DNA polymerases alpha, epsilon, delta, and zeta. Genetics 2001, 159:47-64.
32. Pursell Z.F., Isoz I., Lundström E.-B., Johansson E., Kunkel T.A. Yeast DNA polymerase ε participates in leading-strand DNA replication. Science 2007, 317:127-130.
33. Reijns M.A., Kemp H., Ding J., de Procé S.M., Jackson A.P., Taylor M.S. Lagging-strand replication shapes the mutational landscape of the genome. Nature 2015, 518:502-506.
34. Simon M., Giot L., Faye G. The 3' to 5' exonuclease activity located in the DNA polymerase δ subunit of Saccharomyces cerevisiae is required for accurate replication. EMBO J. 1991, 10:2165-2170.
35. Sitney K.C., Budd M.E., Campbell J.L. DNA polymerase III, a second essential DNA polymerase, is encoded by the S.cerevisiae CDC2 gene. Cell 1989, 56:599-605.
36. Sokolsky T., Alani E. EXO1 and MSH6 are high-copy suppressors of conditional mutations in the MSH2 mismatch repair gene of Saccharomyces cerevisiae. Genetics 2000, 155:589-599.
37. Sukhanova M.V., D'Herin C., van der Kemp P.A., Koval V.V., Boiteux S., Lavrik O.I. Ddc1 checkpoint protein and DNA polymerase e interact with nick-containing DNA repair intermediate in cell free extracts of Saccharomyces cerevisiae. DNA Repair (Amst.) 2011, 10:815-825.
38. Suyari O., Kawai M., Ida H., Yoshida H., Sakaguchi K., Yamaguchi M. Differential requirement for the N-terminal catalytic domain of the DNApolymerase ε p255 subunit in the mitotic cell cycle and the endocycle. Gene 2012, 495:104-114.
39. Swan M.K., Johnson R.E., Prakash L., Prakash S., Aggarwal A.K. Structural basis of high-fidelity DNA synthesis by yeast DNA polymerase δ. Nat. Struct. Mol. Biol. 2009, 16:979-986.
40. Tishkoff D.X., Boerger A.L., Bertrand P., Filosi N., Gaida G.M., Kane M.F., Kolodner R.D. Identification and characterization of Saccharomyces cerevisiae EXO1, a gene encoding an exonuclease that interacts with MSH2. Proc. Natl. Acad. Sci. USA 1997, 94:7487-7492.
41. Tran H.T., Gordenin D.A., Resnick M.A. The 3'->5' exonucleases of DNA polymerases δ and ε and the 5'->3' exonuclease Exo1 have major roles in postreplication mutation avoidance in Saccharomyces cerevisiae. Mol. Cell. Biol. 1999, 19:2000-2007.
42. Tsurimoto T., Stillman B. Replication factors required for SV40 DNA replication invitro. II. Switching of DNA polymerase alpha and delta during initiation of leading and lagging strand synthesis. J.Biol. Chem. 1991, 266:1961-1968.
43. Tsurimoto T., Stillman B. Replication factors required for SV40 DNA replication invitro. I. DNA structure-specific recognition of a primer-template junction by eukaryotic DNA polymerases and their accessory proteins. J.Biol. Chem. 1991, 266:1950-1960.
44. Tsurimoto T., Melendy T., Stillman B. Sequential initiation of lagging and leading strand synthesis by two different polymerase complexes at the SV40 DNA replication origin. Nature 1990, 346:534-539.
45. Waga S., Stillman B. Anatomy of a DNA replication fork revealed by reconstitution of SV40 DNA replication invitro. Nature 1994, 369:207-212.
46. Williams J.S., Clausen A.R., Nick McElhinny S.A., Watts B.E., Johansson E., Kunkel T.A. Proofreading of ribonucleotides inserted into DNA by yeast DNA polymerase e. DNA Repair (Amst.) 2012, 11:649-656.
47. Yu C., Gan H., Han J., Zhou Z.X., Jia S., Chabes A., Farrugia G., Ordog T., Zhang Z. Strand-specific analysis shows protein binding at replication forks and PCNA unloading from lagging strands when forks stall. Mol. Cell 2014, 56:551-563.