Proper functioning of the GINS complex is important for the fidelity of DNA replication in yeast

Molecular Microbiology

Volumn 92, Issue 4, 2014, Pages 659-680

  Grabowska, Ewa ^a   Wronska, Urszula ^a   Denkiewicz, Milena ^a   Jaszczur, Malgorzata ^a   Respondek, Aleksandra ^a   Alabrudzinska, Malgorzata ^a   Suski, Catherine ^a   Makiela Dzbenska, Karolina ^a   Jonczyk, Piotr ^a   Fijalkowska, Iwona J ^a  

^a INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; DNA DIRECTED DNA POLYMERASE EPSILON; DNA DIRECTED DNA POLYMERASE ZETA; GINS COMPLEX; NUCLEOTIDYLTRANSFERASE; PROTEIN PSF1P; UNCLASSIFIED DRUG; CLEAVAGE AND POLYADENYLATION SPECIFICITY FACTOR; DNA BINDING PROTEIN; MULTIENZYME COMPLEX; MUTANT PROTEIN; NONHISTONE PROTEIN; NUCLEAR PROTEIN; PFS1 PROTEIN, S CEREVISIAE; PFS2 PROTEIN, S CEREVISIAE; PSF3 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; SLD5 PROTEIN, S CEREVISIAE;

ARTICLE; CONTROLLED STUDY; DNA REPLICATION; FUNGAL GENE; GENE MUTATION; MUTAGENESIS; MUTATOR GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PSF1 1 GENE; PSF1 100 GENE; REPLISOME; SACCHAROMYCES CEREVISIAE; ENZYMOLOGY; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE;

SACCHAROMYCES CEREVISIAE;

CHROMOSOMAL PROTEINS, NON-HISTONE; DNA MUTATIONAL ANALYSIS; DNA REPLICATION; DNA-BINDING PROTEINS; MRNA CLEAVAGE AND POLYADENYLATION FACTORS; MULTIENZYME COMPLEXES; MUTANT PROTEINS; NUCLEAR PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84899957836     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12580     Document Type: Article

References (110)

1. Abdulovic, A.L., Minesinger, B.K., and Jinks-Robertson, S. (2008) The effect of sequence context on spontaneous Pol zeta-dependent mutagenesis in Saccharomyces cerevisiae. Nucleic Acids Res 36: 2082-2093.
2. Aksenova, A., Volkov, K., Maceluch, J., Pursell, Z.F., Rogozin, I.B., Kunkel, T.A., etal. (2010) Mismatch repair-independent increase in spontaneous mutagenesis in yeast lacking non-essential subunits of DNA polymerase epsilon. PLoS Genet 6: e1001209.
3. Amberg, D.C., Burke, D.J., and Strathern, J.N. (2005) Methods in Yeast Genetics. A Cold Spring Harbor Laboratory Course Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
4. Araki, H., Leem, S.-H., Phongdara, A., and Sugino, A. (1995) Dpb11 which interacts with DNA polymerase II (ε) in Saccharomyces cerevisiae, has a dual role in S-phase progression and the cell cycle checkpoint. Proc Natl Acad Sci USA 92: 11791-11795.
5. Barkley, L.R., Song, I.Y., Zou, Y., and Vaziri, C. (2009) Reduced expression of GINS complex members induces hallmarks of pre-malignancy in primary untransformed human cells. Cell Cycle 8: 1577-1588.
6. Beard, W.A., and Wilson, S.H. (2003) Structural insights into the origins of DNA polymerase fidelity. Structure 11: 489-496.
7. Bebenek, K., and Kunkel, T.A. (1990) Frameshift errors initiated by nucleotide misincorporation. Proc Natl Acad Sci USA 87: 4946-4950.
8. Bermudez, V.P., Farina, A., Raghavan, V., Tappin, I., and Hurwitz, J. (2011) Studies on human DNA polymerase ε and GINS complex and their role in DNA replication. J Biol Chem 286: 28963-28977.
9. Boeke, J.D., Lacroute, F., and Fink, G.R. (1984) A positive selection for mutants lacking orotidine-5-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol Gen Genet 197: 345-346.
10. Boiteux, S., and Jinks-Robertson, S. (2013) DNA repair mechanisms and the bypass of DNA damage in Saccharomyces cerevisiae. Genetics 193: 1025-1064.
11. Boronat, S., and Campbell, J.L. (2007) Mitotic Cdc6 stabilizes APC substrates by a partially Cdc28-independent mechanism and this stabilization is suppressed by deletion of Cdc55. Mol Cell Biol 27: 1158-1171.
12. Budd, M., and Campbell, J.L. (1987) Temperature-sensitive mutations in the yeast DNA polymerase I gene. Proc Natl Acad Sci USA 84: 2838-2842.
13. Burch, B.D., Godfrey, A.C., Gasdaska, P.Y., Salzler, H.R., Duronio, R.J., Marzluff, W.F., and Dominski, Z. (2011) Interaction between FLASH and Lsm11 is essential for histone pre-mRNA processing in vivo in Drosophila. RNA 17: 1132-1147.
14. Burgers, P.M. (2009) Polymerase dynamics at the eukaryotic DNA replication fork. J Biol Chem 284: 4041-4045.
15. Cassier, C., Chanet, R., Henriques, J.A., and Moustacchi, E. (1980) The effects of three PSO genes on induced mutagenesis: a novel class of mutationally defective yeast. Genetics 96: 841-857.
16. Chang, Y.P., Wang, G., Bermudez, V., Hurwitz, J., and Chen, X.S. (2007) Crystal structure of the GINS complex and functional insights into its role in DNA replication. Proc Natl Acad Sci USA 10: 12685-12690.
17. Chen, C., and Kolodner, R.D. (1999) Gross chromosomal rearrangement in Saccharomyces cerevisiae replication and recombination deficient mutants. Nat Genet 23: 81-85.
18. Choi, J., Lim, H.S., Kim, J.J., Song, O.K., and Cho, Y. (2007) Crystal structure of the human GINS complex. Genes Dev 21: 1316-1321.
19. De Falco, M., Ferrari, E., De Felice, M., Rossi, M., Hubscher, U., and Pisani, F.M. (2007) The human GINS complex binds to and specifically stimulates human DNA polymerase α-primase. EMBO Rep 8: 99-103.
20. D'Errico, M., Parlanti, E., and Dogliotti, E. (2008) Mechanism of oxidative damage repair and relevance to human pathology. Mutat Res 289: 4-14.
21. Drake, J.W. (1991) A constant rate of spontaneous mutation in DNA-based microbes. Proc Natl Acad Sci USA 88: 7160-7164.
22. Endo, K., Tago, Y., Daigaku, Y., and Yamamoto, K. (2007) Error-free RAD52 pathway and error-prone REV3 pathway determines spontaneous mutagenesis in Saccharomyces cerevisiae. Genes Genet Syst 82: 35-42.
23. Fields, S., and Song, O. (1989) A novel genetic system to detect protein-protein interactions. Nature 340: 245-246.
24. Fijalkowska, I.J., Schaaper, R.M., and Jonczyk, P. (2012) DNA replication fidelity in Escherichia coli: a multi-DNA polymerase affair. FEMS Microbiol Rev 36: 1105-1121.
25. Flores-Rozas, H., and Kolodner, R.D. (1998) The Saccharomyces cerevisiae MLH3 gene functions in MSH3-dependent suppression of frameshift mutations. Proc Natl Acad Sci USA 95: 12404-12409.
26. Gambus, A., Jones, R.C., Sanchez-Diaz, A., Kanemaki, M., van Deursen, F., Edmondson, R.D., and Labib, K. (2006) GINS maintains association of Cdc45 with MCM in replisome progression complexes at eukaryotic DNA replication forks. Nat Cell Biol 8: 358-366.
27. Gan, G.N., Wittschieben, J.P., Wittschieben, B.Ø., and Wood, R.D. (2008) DNA polymerase zeta (pol zeta) in higher eukaryotes. Cell Res 18: 174-183.
28. Gawel, D., Pham, P.T., Fijalkowska, I.J., Jonczyk, P., and Schaaper, R.M. (2008) Role of accessory DNA polymerases in DNA replication in Escherichia coli: analysis of the dnaX36 mutator mutant. J Bacteriol 190: 1730-1742.
29. Gawel, D., Jonczyk, P., Fijalkowska, I.J., and Schaaper, R.M. (2011) dnaX36 mutator of Escherichia coli: effects of the {tau} subunit of the DNA polymerase III holoenzyme on chromosomal DNA replication fidelity. J Bacteriol 193: 296-300.
30. Gietz, R.D., and Woods, R.A. (1998) Transformation of yeast by the lithium acetate/single stranded carrier DNA/PEG method. Methods Microbiol 26: 53-66.
31. +. Genetics 169: 77-89.
32. Greene, C.N., and Jinks-Robertson, S. (2001) Spontaneous frameshift mutations in Saccharomyces cerevisiae: accumulation during DNA replication and removal by proofreading and mismatch repair activities. Genetics 159: 65-75.
33. Grollman, A.P., and Moriya, M. (1993) Mutagenesis by 8-oxoguanine; an enemy within. Trends Genet 9: 246-249.
34. Guo, D., Wu, X., Rajpal, D.K., Taylor, J.S., and Wang, Z. (2001) Translesion synthesis by yeast DNA polymerase zeta from templates containing lesions of ultraviolet radiation and acetylaminofluorene. Nucleic Acids Res 29: 2875-2883.
35. Handa, T., Kanke, M., Takahashi, T.S., Nakagawa, T., and Masukata, H. (2012) DNA polymerization-independent functions of DNA polymerase epsilon in assembly and progression of the replisome in fission yeast. Mol Biol Cell 23: 3240-3253.
36. Haracska, L., Unk, I., Johnson, R.E., Johansson, E., Burgers, P.M., Prakash, S., and Prakash, L. (2001) Roles of yeast DNA polymerases delta and zeta and of REV1 in the bypass of abasic sites. Genes Dev 15: 945-954.
37. Harper, J.W., Adami, G.R., Wei, N., Keyomarsi, K., and Elledge, S.J. (1993) The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75: 805-813.
38. Henderson, S.T., and Petes, T.D. (1992) Instability of simple sequence DNA in Saccharomyces cerevisiae. Mol Cell Biol 12: 2749-2757.
39. Hokka, D., Maniwa, Y., Tane, S., Nishio, W., Yoshimura, M., Okita, Y., etal. (2013) Psf3 is a prognostic biomarker in lung adenocarcinoma. Lung Cancer 79: 77-82.
40. Iyer, R.R., Pluciennik, A., Burdett, V., and Modrich, P.L. (2006) DNA mismatch repair: functions and mechanisms. Chem Rev 106: 302-323.
41. Jaszczur, M., Flis, K., Rudzka, J., Kraszewska, J., Budd, M.E., Polaczek, P., etal. (2008) Dpb2p, a noncatalytic subunit of DNA polymerase epsilon, contributes to the fidelity of DNA replication in Saccharomyces cerevisiae. Genetics 178: 633-647.
42. Jiricny, J. (2006) The multifaceted mismatch-repair system. Nat Rev Mol Cell Biol 7: 335-345.
43. Johansson, E., and MacNeill, S.A. (2010) The eukaryotic replicative DNA polymerases take shape. Trends Biochem Sci 35: 339-347.
44. Johnson, A., and O'Donnell, M. (2005) Cellular DNA replicases: components and dynamics at the replication fork. Annu Rev Biochem 74: 283-315.
45. Johnson, R.E., Washington, M.T., Haracska, L., Prakash, S., and Prakash, L. (2000) Eukaryotic polymerases iota and zeta act sequentially to bypass DNA lesions. Nature 406: 1015-1019.
46. Kadyrova, L.Y., Mertz, T.M., Zhang, Y., Northam, M.R., Sheng, Z., Lobachev, K.S., etal. (2013) A reversible histone H3 acetylation cooperates with the mismatch repair and replicative polymerases in maintaining genome stability. PLoS Genet 9: e1003899.
47. Kamada, K. (2012) The GINS complex: structure and function. Subcell Biochem 62: 135-156.
48. Kamada, K., Kubota, Y., Arata, T., Shindo, Y., and Hanaoka, F. (2007) Structure of the human GINS complex and its assembly and functional interface in replication initiation. Nat Struct Mol Biol 14: 388-396.
49. Kanemaki, M., Sanchez-Diaz, A., Gambus, A., and Labib, K. (2003) Functional proteomic identification of DNA replication proteins by induced proteolysis in vivo. Nature 423: 720-724.
50. Kirchner, J.M., Tran, H., and Resnik, M.A. (2000) A DNA polymerase epsilon mutant that specifically causes+1 frameshift mutations within homonucleotide runs in yeast. Genetics 155: 1623-1632.
51. Kraszewska, J., Garbacz, M., Jonczyk, P., Fijalkowska, I.J., and Jaszczur, M. (2012) Defect of Dpb2p, a noncatalytic subunit of DNA polymerase ε, promotes error prone replication of undamaged chromosomal DNA in Saccharomyces cerevisiae. Mutat Res 737: 34-42.
52. Kroutil, L.C., Register, K., Bebenek, K., and Kunkel, T.A. (1996) Exonucleolytic proofreading during replication of repetitive DNA. Biochemistry 35: 1046-1053.
53. Kubota, Y., Takase, Y., Komori, Y., Hashimoto, Y., Arata, T., Kamimura, Y., etal. (2003) A novel ring-like complex of Xenopus proteins essential for the initiation of DNA replication. Genes Dev 17: 1141-1152.
54. Kunkel, T.A. (1986) Frameshift mutagenesis by eukaryotic DNA polymerases in vitro. J Biol Chem 261: 13581-13587.
55. Kunkel, T.A. (2011) Balancing eukaryotic replication asymmetry with replication fidelity. Curr Opin Chem Biol 15: 620-626.
56. Kunkel, T.A., and Bebenek, K. (2000) DNA replication fidelity. Annu Rev Biochem 69: 497-529.
57. Kunkel, T.A., and Erie, D.A. (2005) DNA mismatch repair. Annu Rev Biochem 74: 681-710.
58. Labib, K., and Gambus, A. (2007) A key role for the GINS complex at DNA replication forks. Trends Cell Biol 17: 271-278.
59. Lawrence, C.W. (2002) Cellular roles of DNA polymerase zeta and Rev1 protein. DNA Repair (Amst) 1: 425-435.
60. Lawrence, C.W. (2004) Cellular functions of DNA polymerase zeta and Rev1 protein. Adv Protein Chem 69: 167-203.
61. Leman, A.R., and Noguchi, E. (2013) The replication fork: understanding the eukaryotic replication machinery and the challenges to genome duplication. Genes 4: 1-32.
62. Lemoine, F.J., Degtyareva, N.P., Lobachev, K., and Petes, T.D. (2005) Chromosomal translocations in yeast induced by low levels of DNA polymerase: a model for chromosome fragile sites. Cell 120: 587-598.
63. Lemoine, F.J., Degtyareva, N.P., Kokoska, R.J., and Petes, T.D. (2008) Reduced levels of DNA polymerase delta induce chromosome fragile site instability in yeast. Mol Cell Biol 28: 5359-5368.
64. McHenry, C.S. (2011) DNA replicases from a bacterial perspective. Annu Rev Biochem 80: 403-436.
65. MacNeill, S.A. (2010) Structure and function of the GINS complex, a key component of the eukaryotic replisome. Biochem J 425: 489-500.
66. Marsischky, G.T., Filosi, N., Kane, M.F., and Kolodner, R. (1996) Redundancy of Saccharomyces cerevisiae MSH3 and MSH6 in MSH2-dependent mismatch repair. Genes Dev 10: 407-420.
67. Morrison, A., and Sugino, A. (1994) The 3′-5′ exonuclease of both DNA polymerases and participate in correcting errors of DNA replication in Saccharomyces cerevisiae. Mol Gen Genet 242: 289-296.
68. Morrison, A., Bell, J.B., Kunkel, T.A., and Sugino, A. (1991) Eukaryotic DNA polymerase amino acid sequence required for 3′-5′ exonuclease activity. Proc Natl Acad Sci USA 88: 9473-9477.
69. Morrison, A., Johnson, A.L., Johnston, L.H., and Sugino, A. (1993) Pathways correcting DNA replication errors in Saccharomyces cerevisiae. EMBO J 12: 1467-1473.
70. Moyer, S.E., Lewis, P.W., and Botchan, M.R. (2006) Isolation of the Cdc45/MCM2-7/GINS (CMG) complex, a candidate for the eukaryotic DNA replication for helicase. Proc Natl Acad Sci USA 103: 10236-10241.
71. Nagahama, Y., Ueno, M., Haraguchi, N., Mori, M., and Takakura, N. (2010) PSF3 marks malignant colon cancer and has a role in cancer cell proliferation. Biochem Biophys Res Commun 392: 150-154.
72. Nick McElhinny, S.A., Pavlov, Y.I., and Kunkel, T.A. (2006) Evidence for extrinsic exonucleolytic proofreading. Cell Cycle 5: 958-962.
73. 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.
74. Northam, M.R., Garg, P., Baitin, D.M., Burgers, P.M., and Shcherbakova, P.V. (2006) A novel function of DNA polymerase zeta regulated by PCNA. EMBO J 25: 4316-4325.
75. Northam, M.R., Robinson, H.A., Kochenova, O.V., and Shcherbakova, P.V. (2010) Participation of DNA polymerase ζ in replication of undamaged DNA in Saccharomyces cerevisiae. Genetics 184: 27-42.
76. O'Donnell, M. (2006) Replisome architecture and dynamics in Escherichia coli. J Biol Chem 281: 10653-10656.
77. Ohnishi, G., Endo, K., Doi, A., Fujita, A., Daigaku, Y., Nunoshiba, T., and Yamamoto, K. (2004) Spontaneous mutagenesis in haploid and diploid Saccharomyces cerevisiae. Biochem Biophys Res Commun 325: 928-933.
78. Onesti, S., and MacNeill, S.A. (2013) Structure and evolutionary origins of the CMG complex. Chromosoma 122: 47-53.
79. Pacek, M., Tutter, A.V., Kubota, Y., Takisawa, H., and Walter, J.C. (2006) Localization of MCM2-7, Cdc45, and GINS to the site of DNA unwinding during eukaryotic DNA replication. Mol Cell 21: 581-587.
80. Pai, C.C., Garcia, I., Wang, S.W., Cotterill, S., Macneill, S.A., and Kearsey, S.E. (2009) GINS inactivation phenotypes reveal two pathways for chromatin association of replicative alpha and epsilon DNA polymerases in fission yeast. Mol Biol Cell 20: 1213-1222.
81. Pavlov, Y.I., and Shcherbakova, P.V. (2010) DNA polymerases at the eukaryotic fork-20 years later. Mutat Res 685: 45-53.
82. Pavlov, Y.I., Newlon, C.S., and Kunkel, T.A. (2002) Yeast origins establish a strand bias for replicational mutagenesis. Mol Cell 10: 207-213.
83. Pavlov, Y.I., Maki, S., Maki, H., and Kunkel, T.A. (2004) Evidence for interplay among yeast replicative DNA polymerases alpha, delta and epsilon from studies of exonuclease and polymerase active site mutations. BMC Biol 2: 11.
84. Pham, P.T., Olson, M.W., McHenry, C.S., and Schaaper, R.M. (1998) The base substitution and frameshift fidelity of Escherichia coli DNA polymerase III holoenzyme in vitro. J Biol Chem 273: 23575-23584.
85. Pham, P.T., Olson, M.W., McHenry, C.S., and Schaaper, R.M. (1999) Mismatch extension by Escherichia coli DNA polymerase III holoenzyme. J Biol Chem 274: 3705-3710.
86. Pham, P.T., Zhao, W., and Schaaper, R.M. (2006) Mutator mutants of Escherichia coli carrying a defect in the DNA polymerase III subunit. Mol Microbiol 59: 1149-1161.
87. Prakash, S., and Prakash, L. (2002) Translesion DNA synthesis in eukaryotes: a one- or two-polymerase affair. Genes Dev 16: 1872-1883.
88. Prakash, S., Johnson, R.E., and Prakash, L. (2005) Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function. Annu Rev Biochem 74: 317-353.
89. Quah, S.K., von Borstel, R.C., and Hastings, P.J. (1980) The origin of spontaneous mutation in Saccharomyces cerevisiae. Genetics 96: 819-839.
90. Roche, H., Gietz, R.D., and Kunz, B.A. (1994) Specificity of the yeast rev3Δ antimutator and REV3 dependency of the mutator resulting from a defect (rad1Δ) in nucleotide excision repair. Genetics 137: 637-646.
91. Rose, M., Winston, F., and Hieter, P. (1990) Methods in Yeast Genetics: A Cold Spring Harbor Laboratory Course. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
92. Sabbioneda, S., Minesinger, B.K., Giannattasio, M., Plevani, P., Muzi-Falconi, M., and Jinks-Robertson, S. (2005) The 9-1-1 checkpoint clamp physically interacts with pol zeta and is partially required for spontaneous pol zeta-dependent mutagenesis in Saccharomyces cerevisiae. J Biol Chem 280: 38657-38665.
93. Sale, J.E., Lehmann, A.R., and Woodgate, R. (2012) Y-family DNA polymerases and their role in tolerance of cellular DNA damage. Nat Rev Mol Cell Biol 13: 141-152.
94. Schaaper, R.M., and Dunn, R.L. (1987) Spectra of spontaneous mutations in Escherichia coli strains defective in mismatch correction: the nature of in vivo DNA replication errors. Proc Natl Acad Sci USA 84: 6220-6224.
95. Schaaper, R.M., and Radman, M. (1989) The extreme mutator effect of Escherichia coli mutD5 results from saturation of mismatch repair by excessive DNA replication errors. EMBO J 8: 3511-3516.
96. Sengupta, S., van Deursen, F., de Piccoli, G., and Labib, K. (2013) Dpb2 integrates the leading-strand DNA polymerase into the eukaryotic replisome. Curr Biol 23: 543-552.
97. Shcherbakova, P.V., and Fijalkowska, I.J. (2006) Translesion synthesis DNA polymerases and control of genome stability. Front Biosci 11: 2496-2517.
98. Shcherbakova, P.V., and Kunkel, T.A. (1999) Mutator phenotypes conferred by MLH1 overexpresion and by heterozygosity for mlh1 mutations. Mol Cell Biol 19: 3177-3183.
99. Shcherbakova, P.V., Pavlov, Y.I., Chilkova, O., Rogozin, I.B., Johansson, E., and Kunkel, T.A. (2003) Unique error signature of the four-subunit yeast DNA polymerase epsilon. J Biol Chem 31: 43770-43780.
100. Shimizu, K., Hashimoto, K., Kirshner, J.M., Nakai, W., Nashikawa, H., Resnick, M.A., and Sugino, A. (2002) Fidelity of DNA polymerase epsilon holoenzyme from budding yeast Saccharomyces cerevisiae. J Biol Chem 277: 37422-37429.
101. Sia, E.A., Jinks-Robertson, S., and Petes, T.D. (1997) Genetic control of microsatellite stability. Mutat Res 383: 61-70.
102. Sikorski, R.S., and Hieter, P. (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19-27.
103. Simhadri, S., Kramata, P., Zajc, B., Sayer, J.M., Jerina, D.M., Hinkle, D.C., and Wei, C.S. (2002) Benzo[a]pyrene diol epoxide-deoxyguanosine adducts are accurately bypassed by yeast DNA polymerase zeta in vitro. Mutat Res 508: 137-145.
104. Streisinger, G., Okada, Y., Emrich, J., Newton, J., and Tsugita, A. (1966) Frameshift mutations and the genetic code. Cold Spring Harb Symp Quant Biol 31: 77-84.
105. Suzuki, M., Niimi, A., Limsirichaikul, S., Tomida, S., Miao Huang, Q., Izuta, S., etal. (2009) PCNA mono-ubiquitination and activation of translesion DNA polymerases by DNA polymerase α. J Biochem (Tokyo) 146: 13-21.
106. Takayama, Y., Kamimura, Y., Okawa, M., Muramatsu, S., Sugino, A., and Araki, H. (2003) GINS, a novel multiprotein complex required for chromosomal DNA replication in budding yeast. Genes Dev 17: 1153-1165.
107. Tran, H.T., Keen, J.D., Kricker, M., Resnick, M.A., and Gordenin, D.A. (1997) Hypermutability of homonucleotide runs in mismatch repair and DNA polymerase proofreading yeast mutants. Mol Cell Biol 17: 2859-2865.
108. Tran, H.T., Gordenin, D.A., and Resnik, M.A. (1999) The 3′-5′ exonuclease of DNA polymerases delta and epsilon and the 5′-3′ exonuclease Exo1 have major role in postreplication mutation avoidance in Saccharomyces cerevisiae. Mol Cell Biol 19: 2000-2007.
109. Wierdl, M., Dominska, M., and Petes, T.D. (1997) Microsatellite instability in yeast: dependence on the length of the microsatellite. Genetics 146: 769-779.
110. Zhong, X., Garg, P., Stith, C.M., Nick McElhinny, S.A., Kissling, G.E., Burgers, P.M., and Kunkel, T.A. (2006) The fidelity of DNA synthesis by yeast DNA polymerase zeta alone and with accessory proteins. Nucleic Acids Res 34: 4731-4742.