Balancing eukaryotic replication asymmetry with replication fidelity

Current Opinion in Chemical Biology

Volumn 15, Issue 5, 2011, Pages 620-626

  Kunkel, Thomas A ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED DNA POLYMERASE ALPHA; DNA DIRECTED DNA POLYMERASE DELTA; DNA DIRECTED DNA POLYMERASE EPSILON; DNA DIRECTED DNA POLYMERASE GAMMA; LEUCINE; METHIONINE; OKAZAKI FRAGMENT;

AMINO ACID SUBSTITUTION; BASE MISPAIRING; CATALYSIS; CELL CYCLE S PHASE; CHROMOSOME STRUCTURE; DNA REPLICATION; DNA SYNTHESIS; ENZYME STRUCTURE; EUKARYOTE; GENOMIC INSTABILITY; MISMATCH REPAIR; MUTAGENESIS; POLYMERIZATION; PROTEIN FUNCTION; REVIEW; SEQUENCE HOMOLOGY;

ANIMALS; BASE SEQUENCE; DEOXYRIBONUCLEOTIDES; DNA; DNA DAMAGE; DNA POLYMERASE I; DNA POLYMERASE II; DNA POLYMERASE III; DNA REPAIR; DNA REPLICATION; EUKARYOTA; GENOMIC INSTABILITY; HUMANS; MOLECULAR SEQUENCE DATA; SACCHAROMYCES CEREVISIAE; SUBSTRATE SPECIFICITY;

EUKARYOTA;

EID: 80053562457     PISSN: 13675931     EISSN: 18790402     Source Type: Journal    
DOI: 10.1016/j.cbpa.2011.07.025     Document Type: Review

References (51)

1. Kunkel T.A. Evolving views of DNA replication (in)fidelity. Cold Spring Harb Symp Quant Biol 2009, 74:91-101.
2. Drake J.W. The distribution of rates of spontaneous mutation over viruses, prokaryotes, and eukaryotes. Ann N Y Acad Sci 1999, 870:100-107.
3. Yao N.Y., O'Donnell M. Replisome structure and conformational dynamics underlie fork progression past obstacles. Curr Opin Cell Biol 2009, 21:336-343.
4. Burgers P.M. Polymerase dynamics at the eukaryotic DNA replication fork. J Biol Chem 2009, 284:4041-4045.
5. Johansson E., Macneill S.A. The eukaryotic replicative DNA polymerases take shape. Trends Biochem Sci 2010, 35:339-347.
6. Hashimoto K., Shimizu K., Nakashima N., Sugino A. Fidelity of DNA polymerase delta holoenzyme from Saccharomyces cerevisiae: the sliding clamp proliferating cell nuclear antigen decreases its fidelity. Biochemistry 2003, 42:14207-14213.
7. Fortune J.M., Pavlov Y.I., Welch C.M., Johansson E., Burgers P.M., Kunkel T.A. Saccharomyces cerevisiae DNA polymerase delta: high fidelity for base substitutions but lower fidelity for single- and multi-base deletions. J Biol Chem 2005, 280:29980-29987.
8. Shcherbakova P.V., Pavlov Y.I., Chilkova O., Rogozin I.B., Johansson E., Kunkel T.A. Unique error signature of the four-subunit yeast DNA polymerase epsilon. J Biol Chem 2003, 278:43770-43780.
9. Kunkel T.A., Burgers P.M. Dividing the workload at a eukaryotic replication fork. Trends Cell Biol 2008, 18:521-527.
10. Pavlov Y.I., Shcherbakova P.V. DNA polymerases at the eukaryotic fork-20 years later. Mutat Res 2010, 685:45-53.
11. Niimi A., Limsirichaikul S., Yoshida S., Iwai S., Masutani C., Hanaoka F., Kool E.T., Nishiyama Y., Suzuki M. Palm mutants in DNA polymerases alpha and eta alter DNA replication fidelity and translesion activity. Mol Cell Biol 2004, 24:2734-2746.
12. Li L., Murphy K.M., Kanevets U., Reha-Krantz L.J. Sensitivity to phosphonoacetic acid: a new phenotype to probe DNA polymerase delta in Saccharomyces cerevisiae. Genetics 2005, 170:569-580.
13. Venkatesan R.N., Hsu J.J., Lawrence N.A., Preston B.D., Loeb L.A. Mutator phenotypes caused by substitution at a conserved motif A residue in eukaryotic DNA polymerase delta. J Biol Chem 2006, 281:4486-4494.
14. 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.
15. Pursell Z.F., Isoz I., Lundstrom E.B., Johansson E., Kunkel T.A. Yeast DNA polymerase epsilon participates in leading-strand DNA replication. Science 2007, 317:127-130.
16. 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 2008, 30:137-144.
17. 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 U S A 2010, 107:17674-17679.
18. Shcherbakova P.V., Pavlov Y.I. 3'-->5' exonucleases of DNA polymerases epsilon and delta correct base analog induced DNA replication errors on opposite DNA strands in Saccharomyces cerevisiae. Genetics 1996, 142:717-726.
19. Pavlov Y.I., Frahm C., Nick McElhinny S.A., Niimi A., Suzuki M., Kunkel T.A. Evidence that errors made by DNA polymerase alpha are corrected by DNA polymerase delta. Curr Biol 2006, 16:202-207.
20. Korona D.A., Lecompte K.G., Pursell Z.F. The high fidelity and unique error signature of human DNA polymerase {varepsilon}. Nucleic Acids Res 2011, 39:1763-1773.
21. Schmitt M.W., Matsumoto Y., Loeb L.A. High fidelity and lesion bypass capability of human DNA polymerase delta. Biochimie 2009, 91:1163-1172.
22. Karras G.I., Jentsch S. The RAD6 DNA damage tolerance pathway operates uncoupled from the replication fork and is functional beyond S phase. Cell 2010, 141:255-267.
23. Traut T.W. Physiological concentrations of purines and pyrimidines. Mol Cell Biochem 1994, 140:1-22.
24. Chabes A., Georgieva B., Domkin V., Zhao X., Rothstein R., Thelander L. Survival of DNA damage in yeast directly depends on increased dNTP levels allowed by relaxed feedback inhibition of ribonucleotide reductase. Cell 2003, 112:391-401.
25. Kumar D., Viberg J., Nilsson A.K., Chabes A. Highly mutagenic and severely imbalanced dNTP pools can escape detection by the S-phase checkpoint. Nucleic Acids Res 2010, 38:3975-3983.
26. Kumar D., Abdulovic A.L., Viberg J., Nilsson A.K., Kunkel T.A., Chabes A. Mechanisms of mutagenesis in vivo due to imbalanced dNTP pools. Nucleic Acids Res 2011, 39:1360-1371.
27. Pursell Z.F., Kunkel T.A. DNA polymerase epsilon: a polymerase of unusual size (and complexity). Prog Nucleic Acid Res Mol Biol 2008, 82:101-145.
28. Nick McElhinny S.A., Watts B., Kumar D., Watt D.L., Lundström E.-B., Burgers P.M.J., Johansson E., Chabes A., Kunkel T.A. Abundant ribonucleotide incorporation into DNA by yeast replicative polymerases. Proc Natl Acad Sci U S A 2010, 107:4949-4954.
29. Joyce C.M. Choosing the right sugar: how polymerases select a nucleotide substrate. Proc Natl Acad Sci U S A 1997, 94:1619-1622.
30. Nick McElhinny S.A., Kumar D., Clark A.B., Watt D.L., Watts B.E., Lundstrom E.B., Johansson E., Chabes A., Kunkel T.A. Genome instability due to ribonucleotide incorporation into DNA. Nat Chem Biol 2010, 6:774-781.
31. Clark A.B., Lujan S.A., Kissling G.E., Kunkel TA Mismatch repair-independent tandem repeat sequence instability resulting from ribonucleotide incorporation by DNA polymerase epsilon. DNA Repair 2011, 10:476-482.
32. Kim N., Huang S.Y., Williams J.S., Li Y.C., Clark A.B., Cho J.E., Kunkel T.A., Pommier Y., Jinks-Robertson S. Mutagenic processing of ribonucleotides in DNA by yeast topoisomerase I. Science 2011, 332:1561-1564.
33. Cerritelli S.M., Crouch R.J. Ribonuclease H: the enzymes in eukaryotes. FEBS J 2009, 276:1494-1505.
34. Watt D.L., Arana M.E., Johansson E., Burgers P.M., Kunkel T.A. Replication of ribonucleotide containing DNA templates by yeast replicative polymerases. DNA Repair 2011, 10:897-902.
35. Schaaper R.M. Base selection, proofreading, and mismatch repair during DNA replication in Escherichia coli. J Biol Chem 1993, 268:23762-23765.
36. Iyer R.R., Pluciennik A., Burdett V., Modrich P.L. DNA mismatch repair: functions and mechanisms. Chem Rev 2006, 106:302-323.
37. Umar A., Buermeyer A.B., Simon J.A., Thomas D.C., Clark A.B., Liskay R.M., Kunkel T.A. Requirement for PCNA in DNA mismatch repair at a step preceding DNA resynthesis. Cell 1996, 87:65-73.
38. Pavlov Y.I., Mian I.M., Kunkel T.A. Evidence for preferential mismatch repair of lagging strand DNA replication errors in yeast. Curr Biol 2003, 13:744-748.
39. Nick McElhinny S.A., Kissling G.E., Kunkel T.A. Differential correction of lagging-strand replication errors made by DNA polymerases {alpha} and {delta}. Proc Natl Acad Sci U S A 2010, 107:21070-21075.
40. Kadyrov F.A., Genschel J., Fang Y., Penland E., Edelmann W., Modrich P. A possible mechanism for exonuclease 1-independent eukaryotic mismatch repair. Proc Natl Acad Sci U S A 2009, 106:8495-8500.
41. Johnson R.E., Kovvali G.K., Prakash L., Prakash S. Requirement of the yeast RTH1 5' to 3' exonuclease for the stability of simple repetitive DNA. Science 1995, 269:238-240.
42. Wagner R., Meselson M. Repair tracts in mismatched DNA heteroduplexes. Proc Natl Acad Sci U S A 1976, 73:4135-4139.
43. Li F., Tian L., Gu L., Li G.M. Evidence that nucleosomes inhibit mismatch repair in eukaryotic cells. J Biol Chem 2009, 284:33056-33061.
44. Javaid S., Manohar M., Punja N., Mooney A., Ottesen J.J., Poirier M.G., Fishel R. Nucleosome remodeling by hMSH2-hMSH6. Mol Cell 2009, 36:1086-1094.
45. Gorman J., Plys A.J., Visnapuu M.L., Alani E., Greene E.C. Visualizing one-dimensional diffusion of eukaryotic DNA repair factors along a chromatin lattice. Nat Struct Mol Biol 2010, 17:932-938.
46. Kadyrova L.Y., Blanko E.R., Kadyrov F.A. CAF-I-dependent control of degradation of the discontinuous strands during mismatch repair. Proc Natl Acad Sci U S A 2011, 108:2753-2758.
47. Svejstrup J.Q. The interface between transcription and mechanisms maintaining genome integrity. Trends Biochem Sci 2010, 35:333-338.
48. Drake J.W. General antimutators are improbable. J Mol Biol 1993, 229:8-13.
49. Loeb L.A., Monnat R.J. DNA polymerases and human disease. Nat Rev Genet 2008, 9:594-604.
50. DePamphilis M. DNA Replication and Human Disease. Cold Spring Harbor Monograph 2006, vol. 46.
51. Albertson T.M., Ogawa M., Bugni J.M., Hays L.E., Chen Y., Wang Y., Treuting P.M., Heddle J.A., Goldsby R.E., Preston B.D. DNA polymerase epsilon and delta proofreading suppress discrete mutator and cancer phenotypes in mice. Proc Natl Acad Sci U S A 2009, 106:17101-17104.