Mismatch repair-independent increase in spontaneous mutagenesis in yeast lacking non-essential subunits of DNA polymerase ε

PLoS Genetics

Volumn 6, Issue 11, 2010, Pages

  Aksenova, Anna ^a,e   Volkov, Kirill ^a,f   Maceluch, Jaroslaw ^a   Pursell, Zachary F ^b,g   Rogozin, Igor B ^c   Kunkel, Thomas A ^b   Pavlov, Youri I ^d   Johansson, Erik ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^e TUFTS UNIVERSITY   (United States)

^f GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^g TULANE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DNA DIRECTED DNA POLYMERASE; DNA DIRECTED DNA POLYMERASE BETA; DNA DIRECTED DNA POLYMERASE DELTA; DNA DIRECTED DNA POLYMERASE EPSILON; DNA DIRECTED DNA POLYMERASE ZETA; DPB3 PROTEIN; DPB4 PROTEIN; HOLOENZYME; NUCLEAR PROTEIN; PHOSPHODIESTERASE I; PROTEIN MLH1; PROTEIN MSH2; PROTEIN MSH6; PROTEIN PMS1; SPLEEN EXONUCLEASE; UNCLASSIFIED DRUG; DNA DIRECTED DNA POLYMERASE ALPHA; DNA DIRECTED DNA POLYMERASE GAMMA; DPB2 PROTEIN, S CEREVISIAE; EXONUCLEASE; PROTEIN SUBUNIT; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; DNA DEGRADATION; DNA PURIFICATION; DNA REPLICATION; ENZYME ACTIVITY; FRAMESHIFT MUTATION; GENE DELETION; GENE INTERACTION; GENE SEQUENCE; GENETIC STABILITY; GENOMIC INSTABILITY; IN VITRO STUDY; IN VIVO STUDY; MISMATCH REPAIR; MUTAGENESIS; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; OPEN READING FRAME; PROTEIN DNA INTERACTION; ENZYMOLOGY; FUNGAL GENE; GENETICS; METABOLISM; MUTATION; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE;

BASE SEQUENCE; DNA MISMATCH REPAIR; DNA POLYMERASE II; DNA POLYMERASE III; EXONUCLEASES; GENES, FUNGAL; HOLOENZYMES; MUTAGENESIS; MUTATION; PROTEIN BINDING; PROTEIN SUBUNITS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 78649701177     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1001209     Document Type: Article

References (71)

1. Bebenek K, Kunkel TA (2004) Functions of DNA polymerases. Adv Protein Chem 69: 137-165.
2. Garg P, Burgers PM (2005) DNA polymerases that propagate the eukaryotic DNA replication fork. Crit Rev Biochem Mol Biol 40: 115-128.
3. Jin YH, Obert R, Burgers PM, Kunkel TA, Resnick MA, et al. (2001) The 39-.59 exonuclease of DNA polymerase delta can substitute for the 59 flap endonuclease Rad27/Fen1 in processing Okazaki fragments and preventing genome instability. Proc Natl Acad Sci U S A 98: 5122-5127.
4. Jin YH, Ayyagari R, Resnick MA, Gordenin DA, Burgers PM (2003) Okazaki fragment maturation in yeast. II. Cooperation between the polymerase and 39-59-exonuclease activities of Pol delta in the creation of a ligatable nick. J Biol Chem 278: 1626-1633.
5. Garg P, Stith CM, Sabouri N, Johansson E, Burgers PM (2004) Idling by DNA polymerase delta maintains a ligatable nick during lagging-strand DNA replication. Genes Dev 18: 2764-2773.
6. Nick McElhinny SA, Gordenin DA, Stith CM, Burgers PM, Kunkel TA (2008) Division of labor at the eukaryotic replication fork. Mol Cell 30: 137-144.
7. Pursell ZF, Isoz I, Lundstrom EB, Johansson E, Kunkel TA (2007) Yeast DNA polymerase epsilon participates in leading-strand DNA replication. Science 317: 127-130.
8. Shcherbakova PV, Pavlov YI (1996) 3′->5′ exonucleases of DNA polymerases epsilon and delta correct base analog induced DNA replication errors on opposite DNA strands in Saccharomyces cerevisiae. Genetics 142: 717-726.
9. Morrison A, Sugino A (1994) The 3′->5′ exonucleases of both DNA polymerases delta and epsilon participate in correcting errors of DNA replication in Saccharomyces cerevisiae. Mol Gen Genet 242: 289-296.
10. Karthikeyan R, Vonarx EJ, Straffon AF, Simon M, Faye G, et al. (2000) Evidence from mutational specificity studies that yeast DNA polymerases delta and epsilon replicate different DNA strands at an intracellular replication fork. J Mol Biol 299: 405-419.
11. Pavlov YI, Frahm C, Nick McElhinny SA, Niimi A, Suzuki M, et al. (2006) Evidence that errors made by DNA polymerase alpha are corrected by DNA polymerase delta. Curr Biol 16: 202-207.
12. Pavlov YI, Shcherbakova PV (2010) DNA polymerases at the eukaryotic fork-20 years later. Mutat Res 685: 45-53.
13. Kunkel TA, Burgers PM (2008) Dividing the workload at a eukaryotic replication fork. Trends Cell Biol 18: 521-527.
14. Burgers PM (2008) Polymerase dynamics at the eukaryotic DNA replication fork. J Biol Chem 284: 4041-4045.
15. Budzowska M, Kanaar R (2009) Mechanisms of dealing with DNA damageinduced replication problems. Cell Biochem Biophys 53: 17-31.
16. Lopes M, Foiani M, Sogo JM (2006) Multiple mechanisms control chromosome integrity after replication fork uncoupling and restart at irreparable UV lesions. Mol Cell 21: 15-27.
17. Karras GI, Jentsch S (2010) The RAD6 DNA damage tolerance pathway operates uncoupled from the replication fork and is functional beyond S phase. Cell 141: 255-267.
18. Daigaku Y, Davies AA, Ulrich HD (2010) Ubiquitin-dependent DNA damage bypass is separable from genome replication. Nature 465: 951-955.
19. Pomerantz RT, O'Donnell M (2008) The replisome uses mRNA as a primer after colliding with RNA polymerase. Nature 456: 762-766.
20. Chilkova O, Jonsson BH, Johansson E (2003) The quaternary structure of DNA polymerase epsilon from Saccharomyces cerevisiae. J Biol Chem 278: 14082-14086.
21. Araki H, Hamatake RK, Johnston LH, Sugino A (1991) DPB2, the gene encoding DNA polymerase II subunit B, is required for chromosome replication in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 88: 4601-4605.
22. Feng W, Rodriguez-Menocal L, Tolun G, D'Urso G (2003) Schizosacchromyces pombe Dpb2 binds to origin DNA early in S phase and is required for chromosomal DNA replication. Mol Biol Cell 14: 3427-3436.
23. Kesti T, McDonald WH, Yates JR, III, Wittenberg C (2004) Cell cycledependent phosphorylation of the DNA polymerase epsilon subunit, Dpb2, by the Cdc28 cyclin-dependent protein kinase. J Biol Chem 279: 14245-14255.
24. Jaszczur M, Flis K, Rudzka J, Kraszewska J, Budd ME, et al. (2008) Dpb2p, a noncatalytic subunit of DNA polymerase epsilon, contributes to the fidelity of DNA replication in Saccharomyces cerevisiae. Genetics 178: 633-647.
25. Jaszczur M, Rudzka J, Kraszewska J, Flis K, Polaczek P, et al. (2009) Defective interaction between Pol2p and Dpb2p, subunits of DNA polymerase epsilon, contributes to a mutator phenotype in Saccharomyces cerevisiae. Mutat Res 669: 27-35.
26. Araki H, Hamatake RK, Morrison A, Johnson AL, Johnston LH, et al. (1991) Cloning DPB3, the gene encoding the third subunit of DNA polymerase II of Saccharomyces cerevisiae. Nucleic Acids Res 19: 4867-4872.
27. Northam MR, Garg P, Baitin DM, Burgers PM, Shcherbakova PV (2006) A novel function of DNA polymerase zeta regulated by PCNA. EMBO J 25: 4316-4325.
28. Li Y, Pursell ZF, Linn S (2000) Identification and cloning of two histone fold motif-containing subunits of HeLa DNA polymerase epsilon. J Biol Chem 275: 31554.
29. Tsubota T, Maki S, Kubota H, Sugino A, Maki H (2003) Double-stranded DNA binding properties of Saccharomyces cerevisiae DNA polymerase epsilon and of the Dpb3p-Dpb4p subassembly. Genes Cells 8: 873-888.
30. Iida T, Araki H (2004) Noncompetitive counteractions of DNA polymerase epsilon and ISW2/yCHRAC for epigenetic inheritance of telomere position effect in Saccharomyces cerevisiae. Mol Cell Biol 24: 217-227.
31. Tackett AJ, Dilworth DJ, Davey MJ, O'Donnell M, Aitchison JD, et al. (2005) Proteomic and genomic characterization of chromatin complexes at a boundary. J Cell Biol 169: 35-47.
32. Asturias FJ, Cheung IK, Sabouri N, Chilkova O, Wepplo D, et al. (2006) Structure of Saccharomyces cerevisiae DNA polymerase epsilon by cryoelectron microscopy. Nat Struct Mol Biol 13: 35-43.
33. Shcherbakova PV, Kunkel TA (1999) Mutator phenotypes conferred by MLH1 overexpression and by heterozygosity for mlh1 mutations. Mol Cell Biol 19: 3177-3183.
34. Tran HT, Keen JD, Kricker M, Resnick MA, Gordenin DA (1997) Hypermutability of homonucleotide runs in mismatch repair and DNA polymerase proofreading yeast mutants. Mol Cell Biol 17: 2859-2865.
35. Tran HT, Gordenin DA, Resnick MA (1999) The 3′->5′ exonucleases of DNA polymerases delta and epsilon and the 5′->3′ exonuclease Exo1 have major roles in postreplication mutation avoidance in Saccharomyces cerevisiae. Mol Cell Biol 19: 2000-2007.
36. Kirchner JM, Tran H, Resnick MA (2000) A DNA polymerase epsilon mutant that specifically causes +1 frameshift mutations within homonucleotide runs in yeast. Genetics 155: 1623-1632.
37. Dang W, Kagalwala MN, Bartholomew B (2007) The Dpb4 subunit of ISW2 is anchored to extranucleosomal DNA. J Biol Chem 282: 19418-19425.
38. Gangaraju VK, Prasad P, Srour A, Kagalwala MN, Bartholomew B (2009) Conformational changes associated with template commitment in ATPdependent chromatin remodeling by ISW2. Mol Cell 35: 58-69.
39. Bebenek K, Kunkel TA (1995) Analyzing fidelity of DNA polymerases. Methods Enzymol 262: 217-232.
40. Shcherbakova PV, Pavlov YI, Chilkova O, Rogozin IB, Johansson E, et al. (2003) Unique error signature of the four-subunit yeast DNA polymerase epsilon. J Biol Chem 278: 43770-43780.
41. Lawrence CW (2004) Cellular functions of DNA polymerase zeta and Rev1 protein. Adv Protein Chem 69: 167-203.
42. Northam MR, Robinson HA, Kochenova OV, Shcherbakova PV (2009) Participation of DNA Polymerase {zeta} in Replication of Undamaged DNA in Saccharomyces cerevisiae. Genetics 184: 27-42.
43. Zhong X, Garg P, Stith CM, Nick McElhinny SA, Kissling GE, et al. (2006) The fidelity of DNA synthesis by yeast DNA polymerase zeta alone and with accessory proteins. Nucleic Acids Res 34: 4731-4742.
44. Pavlov YI, Shcherbakova PV, Kunkel TA (2001) In vivo consequences of putative active site mutations in yeast DNA polymerases alpha, epsilon, delta, and zeta. Genetics 159: 47-64.
45. Harfe BD, Jinks-Robertson S (2000) DNA mismatch repair and genetic instability. Annu Rev Genet 34: 359-399.
46. Tran HT, Degtyareva NP, Gordenin DA, Resnick MA (1999) Genetic factors affecting the impact of DNA polymerase delta proofreading activity on mutation avoidance in yeast. Genetics 152: 47-59.
47. Huang ME, Rio AG, Galibert MD, Galibert F (2002) Pol32, a subunit of Saccharomyces cerevisiae DNA polymerase delta, suppresses genomic deletions and is involved in the mutagenic bypass pathway. Genetics 160: 1409-1422.
48. Chilkova O, Stenlund P, Isoz I, Stith CM, Grabowski P, et al. (2007) The eukaryotic leading and lagging strand DNA polymerases are loaded onto primerends via separate mechanisms but have comparable processivity in the presence of PCNA. Nucleic Acids Res 35: 6588-6597.
49. Kokoska RJ, Stefanovic L, DeMai J, Petes TD (2000) Increased rates of genomic deletions generated by mutations in the yeast gene encoding DNA polymerase delta or by decreases in the cellular levels of DNA polymerase delta. Mol Cell Biol 20: 7490-7504.
50. Xie Y, Counter C, Alani E (1999) Characterization of the repeat-tract instability and mutator phenotypes conferred by a Tn3 insertion in RFC1, the large subunit of the yeast clamp loader. Genetics 151: 499-509.
51. Niimi A, Limsirichaikul S, Yoshida S, Iwai S, Masutani C, et al. (2004) Palm mutants in DNA polymerases alpha and eta alter DNA replication fidelity and translesion activity. Mol Cell Biol 24: 2734-2746.
52. Chen C, Umezu K, Kolodner RD (1998) Chromosomal rearrangements occur in S. cerevisiae rfa1 mutator mutants due to mutagenic lesions processed by double-strand-break repair. Mol Cell 2: 9-22.
53. Yang Y, Sterling J, Storici F, Resnick MA, Gordenin DA (2008) Hypermutability of damaged single-strand DNA formed at double-strand breaks and uncapped telomeres in yeast Saccharomyces cerevisiae. PLoS Genet 4: e1000264. doi:10.1371/journal.pgen.1000264.
54. Jin YH, Garg P, Stith CM, Al-Refai H, Sterling JF, et al. (2005) The multiple biological roles of the 3′->5′ exonuclease of Saccharomyces cerevisiae DNA polymerase delta require switching between the polymerase and exonuclease domains. Mol Cell Biol 25: 461-471.
55. Swan MK, Johnson RE, Prakash L, Prakash S, Aggarwal AK (2009) Structural basis of high-fidelity DNA synthesis by yeast DNA polymerase delta. Nat Struct Mol Biol 16: 979-986.
56. Gutierrez PJ, Wang TS (2003) Genomic instability induced by mutations in Saccharomyces cerevisiae POL1. Genetics 165: 65-81.
57. Tran HT, Gordenin DA, Resnick MA (1996) The prevention of repeatassociated deletions in Saccharomyces cerevisiae by mismatch repair depends on size and origin of deletions. Genetics 143: 1579-1587.
58. Kunkel TA, Erie DA (2005) DNA mismatch repair. Annu Rev Biochem 74: 681-710.
59. Mojas N, Lopes M, Jiricny J (2007) Mismatch repair-dependent processing of methylation damage gives rise to persistent single-stranded gaps in newly replicated DNA. Genes Dev 21: 3342-3355.
60. Lehner K, Jinks-Robertson S (2009) The mismatch repair system promotes DNA polymerase zeta-dependent translesion synthesis in yeast. Proc Natl Acad Sci U S A 106: 5749-5754.
61. Delbos F, Aoufouchi S, Faili A, Weill JC, Reynaud CA (2007) DNA polymerase eta is the sole contributor of A/T modifications during immunoglobulin gene hypermutation in the mouse. J Exp Med 204: 17-23.
62. Albertson TM, Ogawa M, Bugni JM, Hays LE, Chen Y, et al. (2009) DNA polymerase {varepsilon} and {delta} proofreading suppress discrete mutator and cancer phenotypes in mice. Proc Natl Acad Sci U S A.
63. Goldstein AL, McCusker JH (1999) Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15: 1541-1553.
64. Pavlov YI, Maki S, Maki H, Kunkel TA (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.
65. Morrison A, Bell JB, Kunkel TA, Sugino A (1991) Eukaryotic DNA polymerase amino acid sequence required for 3′->5′ exonuclease activity. Proc Natl Acad Sci U S A 88: 9473-9477.
66. Jin YH, Obert R, Burgers PM, Kunkel TA, Resnick MA, et al. (2001) The 3′->5′ exonuclease of DNA polymerase delta can substitute for the 5′ flap endonuclease Rad27/Fen1 in processing Okazaki fragments and preventing genome instability. Proc Natl Acad Sci U S A 98: 5122-5127.
67. Pavlov YI, Mian IM, Kunkel TA (2003) Evidence for preferential mismatch repair of lagging strand DNA replication errors in yeast. Curr Biol 13: 744-748.
68. Shcherbakova PV, Noskov VN, Pshenichnov MR, Pavlov YI (1996) Base analog 6-N-hydroxylaminopurine mutagenesis in the yeast Saccharomyces cerevisiae is controlled by replicative DNA polymerases. Mutat Res 369: 33-44.
69. Adams WT, Skopek TR (1987) Statistical test for the comparison of samples from mutational spectra. J Mol Biol 194: 391-396.
70. Khromov-Borisov NN, Rogozin IB, Pegas Henriques JA, de Serres FJ (1999) Similarity pattern analysis in mutational distributions. Mutat Res 430: 55-74.
71. Kokoska RJ, McCulloch SD, Kunkel TA (2003) The efficiency and specificity of apurinic/apyrimidinic site bypass by human DNA polymerase eta and Sulfolobus solfataricus Dpo4. J Biol Chem 278: 50537-50545.