DNA polymerases that propagate the eukaryotic DNA replication fork

Critical Reviews in Biochemistry and Molecular Biology

Volumn 40, Issue 2, 2005, Pages 115-128

  Garg, Parie ^a   Burgers, Peter M J ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

DNA polymerase; DNA replication; FEN1; Nuclease; Okazaki fragment; PCNA; Replication fork

Indexed keywords

CYCLINE; DEOXYRIBONUCLEASE; DNA DIRECTED DNA POLYMERASE ALPHA; DNA DIRECTED DNA POLYMERASE DELTA; DNA DIRECTED DNA POLYMERASE EPSILON; DNA POLYMERASE; DNA PRIMASE; ENDONUCLEASE; ENDONUCLEASE FEN1; HELICASE; OKAZAKI FRAGMENT; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; PRIMER DNA; PRIMER RNA; UNCLASSIFIED DRUG;

DNA NICK TRANSLATION; DNA REPLICATION; DNA STRAND; ENZYME ACTIVITY; EUKARYOTE; MODEL; NONHUMAN; PRIORITY JOURNAL; REVIEW; RNA DEGRADATION; RNA TRANSLATION;

ANIMALS; CHROMOSOMES; DNA PRIMASE; DNA REPLICATION; DNA-DIRECTED DNA POLYMERASE; EUKARYOTIC CELLS; HUMANS;

EUKARYOTA;

EID: 18044384092     PISSN: 10409238     EISSN: None     Source Type: Journal    
DOI: 10.1080/10409230590935433     Document Type: Review

References (132)

1. Aparicio, O.M., Stout, A.M., and Bell, S.P. 1999. Differential assembly of Cdc45p and DNA polymerases at early and late origins of DNA replication. Proc Natl Acad Sci USA 96:9130-9135.
2. Aparicio, O.M., Weinstein, D.M., and Bell, S.P. 1997. Components and dynamics of DNA replication complexes in S. cerevisiae-redistribution of MCM proteins and Cdc45p during S phase. Cell 91:59-69.
3. Araki, H., Hamatake, R.K., Johnston, L.H., and Sugino, A. 1991a. 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.
4. Araki, H., Hamatake, R.K., Morrison, A., Johnson, A.L., Johnston, L.H., and Sugino, A. 1991b. Cloning DPB3, the gene encoding the third subunit of DNA polymerase II of Saccharomyces cerevisiae. Nucleic Acids Res 19:4867-4872.
5. Araki, H., Leem, S.H., Phongdara, A., and Sugino, A. 1995. Dpb11, which interacts with DNA polymerase (IIepsilon) in Saccharomyces cerevisiae, has a dual role in S-phase progression and at a cell cycle checkpoint. Proc Natl Acad Sci USA 92:11791-11795.
6. Arezi, B., Kirk, B.W., Copeland, W.C., and Kuchta, R.D. 1999. Interactions of DNA with human DNA primase monitored with photoactivatable cross-linking agents: implications for the role of the p58 subunit. Biochemistry 38:12899-12907.
7. Arezi, B. and Kuchta, R. D. 2000. Eukaryotic DNA primase. Trends Biochem Sci25:572-576.
8. Ayyagari, R., Gomes, X.V., Gordenin, D.A., and Burgers, P.M. 2003. Okazaki fragment maturation in yeast. I. Distribution of functions between FEN1 AND DNA2. J Biol Chem 278:1618-1625.
9. Bae, S.H., Bae, K.H., Kim, J.A., and Seo, Y.S. 2001. RPA governs endonuclease switching during processing of Okazaki fragments in eukaryotes. Nature 412:456-461.
10. Bedford, E., Tabor, S., and Richardson, C.C. 1997. The thioredoxin binding domain of bacteriophage T7 DNA polymerase confers processivity on Escherichia coli DNA polymerase I. Proc Natl Acad Sci USA 94:479-484.
11. Bell, S.P. and Dutta, A. 2002. DNA replication in eukaryotic cells. Annu Rev Biochem 71:333-374.
12. Bell, S.P. and Stillman, B. 1992. ATP-dependent recognition of eukaryotic origins of DNA replication by a multiprotein complex. Nature 357:128-134.
13. Bermudez, V.P., MacNeill, S.A., Tappin, I., and Hurwitz, J. 2002. The influence of the Cdc27 subunit on the properties of the Schizosaccharomyces pombe DNA polymerase delta. J Biol Chem 277:36853-36862.
14. Budd, M.E. and Campbell, J.L. 1997. A yeast replicative helicase, Dna2 helicase, interacts with yeast FEN-1 nuclease in carrying out its essential function. Mol Cell Biol 17:2136-2142.
15. Budd, M.E., Choe, W., and Campbell, J.L. 2000. The nuclease activity of the yeast DNA2 protein, which is related to the RecB-like nucleases, is essential in vivo. J Biol Chem 275:16518-16529.
16. Budd, M.E., Choe, W.-C., and Campbell, J. 1995. DNA2 Encodes a DNA helicase essential for replication of eukaryotic chromosomes. J Biol Chem 270:26766-26769.
17. Burgers, P.M. and Gerik, K.J. 1998. Structure and processivity of two forms of Saccharomyces cerevisiae DNA polymerase delta. J Biol Chem 273:19756-19762.
18. Burgers, P.M., Koonin, E.V., Bruford, E., Blanco, L., Burtis, K.C., Christman, M.F., Copeland, W.C., Friedberg, E.C., Hanaoka, F., Hinkle, D.C., et al. 2001. Eukaryotic DNA polymerases: proposal for a revised nomenclature. J Biol Chem 276:43487-43490.
19. Burgers, P.M.J. 1991. Saccharomyces cerevisiae Replication factor C. II. Formation and activity of complexes with the proliferating cell nuclear antigen and with DNA polymerases delta and epsilon. J Biol Chem 266:22698-22706.
20. Chilkova, O., Jonsson, B.H., and Johansson, E. 2003. The quaternary structure of DNA polymerase epsilon from Saccharomyces cerevisiae. J Biol Chem 278:14082-14086.
21. Collins, K.L. and Kelly, T.J. 1991. Effects of T antigen and replication protein A on the initiation of DNA synthesis by DNA polymerase alpha-primase. Mol Cell Biol 11:2108-2115.
22. Derbyshire, V., Freemont, P.S., Sanderson, M.R., Beese, L., Friedman, J.M., Joyce, C.M., and Steitz, T.A. 1988. Genetic and crystallographic studies of the 3′-5′-exonucleolytic site of DNA polymerase I. Science 240:199-201.
23. Desdouets, C., Santocanale, C., Drury, L.S., Perkins, G., Foiani, M., Plevani, P., and Diffley, J.F. 1998. Evidence for a Cdc6p-independent mitotic resetting event involving DNA polymerase alpha. EMBO J 17:4139-4146.
24. Diede, S.J. and Gottschling, D.E. 1999. Telomerase-mediated telomere addition in vivo requires DNA primase and DNA polymerases alpha and delta. Cell 23:723-733.
25. Dionne, I., Nookala, R.K., Jackson, S.P., Doherty, A.J., and Bell, S.D. 2003. A heterotrimeric PCNA in the hyperthermophilic archaeon Sulfolobus solfataricus. Mol Cell 11:275-282.
26. Doublie, S., Tabor, S., Long, A.M., Richardson, C.C., and Ellenberger, T. 1998. Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 A resolution. Nature 391:251-258.
27. Dua, R., Edwards, S., Levy, D.L., and Campbell, J.L. 2000. Subunit interactions within the Saccharomyces cerevisiae DNA polymerase epsilon pol epsilon) complex. Demonstration of a dimeric pol epsilon. J Biol Chem 275:28816-28825.
28. Dua, R., Levy, D.L., and Campbell, J.L. 1999. Analysis of the essential functions of the C-terminal protein/protein interaction domain of Saccharomyces cerevisiae pol epsilon and its unexpected ability to support growth in the absence of the DNA polymerase domain. J Biol Chem 274:22283-22288.
29. Dua, R., Levy, D.L., Li, C.M., Snow, P.M., and Campbell, J.L. 2002. In vivo reconstitution of Saccharomyces cerevisiae DNA polymerase epsilon in insect cells. Purification and characterization. J Biol Chem 277:7889-7896.
30. Edwards, S., Li, C.M., Levy, D.L., Brown, J., Snow, P.M., and Campbell, J.L. 2003. Saccharomyces cerevisiae DNA polymerase epsilon and polymerase sigma interact physically and functionally, suggesting a role for polymerase epsilon in sister chromatid cohesion. Mol Cell Biol 23:2733-2748.
31. Eissenberg, J.C., Ayyagari, R., Gomes, X.V., and Burgers, P. 1997. Mutations in yeast proliferating cell nuclear antigen define distinct sites for interaction with DNA polymerase delta and DNA polymerase epsilon. Mol Cell Biol 17:6367-6378.
32. Feng, W. and D'Urso, G. 2001. 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 21:4495-4504.
33. Feng, W., Rodriguez-Menocal, L., Tolun, G., and 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.
34. Fien, K., Cho, Y.S., Lee, J.K., Raychaudhuri, S., Tappin, I., and Hurwitz, J. 2004. Primer utilization by DNA polymerase alpha-primase is influenced by its interaction with Mcm10p. J Biol Chem 279:16144-16153.
35. Franklin, M.C., Wang, J., and Steitz, T.A. 2001. Structure of the replicating complex of a pol alpha family DNA polymerase. Cell 105:657-667.
36. Frick, D.N. and Richardson, C.C. 2001. DNA primases. Annu Rev Biochem 70:39-80.
37. Fukui, T., Yamauchi, K., Muroya, T., Akiyama, M., Maki, H., Sugino, A., and Waga, S. 2004. Distinct roles of DNA polymerases delta and epsilon at the replication fork in Xenopus egg extracts. Genes Cell 9:179-191.
38. Fuss, J. and Linn, S. 2002. Human DNA polymerase epsilon colocalizes with proliferating cell nuclear antigen and DNA replication late, but not early, in S phase. J Biol Chem 277:8658-8666.
39. Garg, P., Stith, C.M., Sabouri, N., Johansson, E., and Burgers, P.M. 2004. Idling by DNA polymerase delta maintains a ligatable nick during lagging-strand DNA replication. Genes Dev 18:2764-2773.
40. Gerik, K.J., Gary, S.L., and Burgers, P.M. 1997. Overproduction and affinity purification of Saccharomyces cerevisiae replication factor C. J Biol Chem 272:1256-1262.
41. Gerik, K.J., Li, X., Pautz, A., and Burgers, P.M. 1998. Characterization of the two small subunits of Saccharomyces cerevisiae DNA polymerase delta. J Biol Chem 273:19747-19755.
42. Gomes, X.V. and Burgers, P.M. 2001. ATP utilization by yeast replication factor C. I. ATP-mediated interaction with DNA and with proliferating cell nuclear antigen. J Biol Chem 276:34768-34775.
43. Gomes, X.V. and Burgers, P.M.J. 2000. Two modes of FEN1 binding to PCNA regulated by DNA. EMBO J 19:3811-3821.
44. Gomes, X.V., Schmidt, S.L., and Burgers, P.M. 2001. ATP utilization by yeast replication factor C. II. Multiple stepwise ATP binding events are required to load proliferating cell nuclear antigen onto primed DNA. J Biol Chem 276:34776-34783.
45. Hamatake, R.K., Hasegawa, H., Clark, A.B., Bebenek, K., Kunkel, T.A., and Sugino, A. 1990. Purification and characterization of DNA polymerase Il from the yeast Saccharomyces cerevisiae. Identification of the catalytic core and a possible holoenzyme form. J Biol Chem 265:4072-4083.
46. Hashimoto, H., Nishioka, M., Fujiwara, S., Takagi, M., Imanaka, T., Inoue, T., and Kai, Y. 2001. Crystal structure of DNA polymerase from hyperthermophilic archaeon Pyrococcus kodakaraensis KOD1. J Mol Biol 306:469-477.
47. Hopfner, K.P., Eichinger, A., Engh, R.A., Laue, F., Ankenbauer, W., Huber, R., and Angerer, B. 1999. Crystal structure of a thermostable type B DNA polymerase from Thermococcus gorgonarius. Proc Natl Acad Sci USA 96:3600-3605.
48. Huang, M.E., Le Douarin, B., Henry, C., and Galibert, F. 1999. The Saccharomyces cerevisiae protein YJR043C Pol32) interacts with the catalytic subunit of DNA polymerase alpha and is required for cell cycle progression in G2/M. Mol Gen Genet 260:541-550.
49. Huang, M.E., Rio, A.G., Galibert, M.D., and 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.
50. Hubscher, U., Maga, G., and Spadari, S. 2002. Eukaryotic DNA polymerases. Annu Rev Biochem 71:133-163.
51. Hughes, D.A., MacNeill, S.A., and Fantes, P.A. 1992. Molecular cloning and sequence analysis of cdc27+ required for the G2-M transition in the fission yeast Schizosaccharomyces pombe. Mol Gen Genet 231:401-410.
52. Hughes, P., Tratner, I., Ducoux, M., Piard, K., and Baldacci, G. 1999. Isolation and identification of the third subunit of mammalian DNA polymerase delta by PCNA-affinity chromatography of mouse FM3A cell extracts. Nucleic Acids Res 27:2108-2114.
53. Ishimi, Y., Claude, A., Bullock, P., and Hurwitz, J. 1988. Complete enzymatic synthesis of DNA containing the SV40 origin of replication. J Biol Chem 263:19723-19733.
54. Jin, Y.H., Ayyagari, R., Resnick, M.A., Gordenin, D.A., and Burgers, P.M. 2003. Okazaki fragment maturation in yeast. II. Cooperation between the polymerase and 3′-5′-exonuclease activities of Pol delta in the creation of a ligatable nick. J Biol Chem 278:1626-1633.
55. Jin, Y.H., Garg, P., Stith, C.M., Al Refai, H., Sterling, J., Weston, L., Kunkel, T., Resnick, M.A., Burgers, P.M., and Gordenin, D.A. 2005. The multiple biological roles for the 3′-5′-exonuclease of DNA polymerase d require switching between the polymerase and exonuclease domains. Mol Cell Biol 25:461-171.
56. Jin, Y.H., Obert, R., Burgers, P.M., Kunkel, TA., Resnick, M.A., and Gordenin, D.A. 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 USA 98:5122-5127.
57. Johansson, E., Garg, P., and Burgers, P.M. 2004. The Pol32 subunit of DNA polymerase delta contains separable domains for processive replication and proliferating cell nuclear antigen PCNA) binding. J Biol Chem 279:1907-1915.
58. Johansson, E., Majka, J., and Burgers, P.M. 2001. Structure of DNA polymerase delta from Saccharomyces cerevisiae. J Biol Chem 276:43824-43828.
59. Kao, H.I., Veeraraghavan, J., Polaczek, P., Campbell, J.L., and Bambara, R.A. 2004. On the roles of Saccharomyces cerevisiae Dna2p and Flap endonuclease 1 in Okazaki fragment processing. J Biol Chem 279:15014-15024.
60. Karthikeyan, R., Vonarx, E.J., Straffon, A.F., Simon, M., Faye, G., and Kunz, B.A. 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.
61. Kearsey, S. E. and Cotterill, S. 2003. Enigmatic variations: divergent modes of regulating eukaryotic DNA replication. Mol Cell 12:1067-1075.
62. Kesti, T., Flick, K., Keranen, S., Syvaoja, J.E., and Wittenberg, C. 1999. DNA polymerase epsilon catalytic domains are dispensable for DNA replication, DNA repair, and cell viability. Mol Cell 3:679-685.
63. Kolesky, S.E., Ouhammouch, M., and Geiduschek, E.P. 2002. The mechanism of transcriptional activation by the topologically DNA-linked sliding clamp of bacteriophage T4. J Mol Biol 321:767-784.
64. Labib, K., Tercero, J.A., and Diffley, J.F. 2000. Uninterrupted MCM2-7 function required for DNA replication fork progression. Science 288:1643-1647.
65. Lee, K.M., Kim, D.W., Bae, S.H., Kim, J.A., Ryu, G.H., Kwon, Y.N., Kim, K.A., Koo, H.S., and Seo, Y.S. 2000. The endonuclease activity of the yeast Dna2 enzyme is essential in vivo. Nucleic Acids Res 28:2873-2881.
66. Lee, M.Y.W.T., Tan, C.-K., Downey, K.M., and So, A.G. 1984. Further studies on calf thymus DNA polymerase δ purified to homogeneity by a new procedure. Biochemistry 23:1906-1913.
67. Li, Y., Korolev, S., and Waksman, G. 1998. Crystal structures of open and closed forms of binary and ternary complexes of the large fragment of Thermus aquaticus DNA polymerase I: structural basis for nucleotide incorporation. EMBO J 17:7514-7525.
68. Liu, L., Mo, J., Rodriguez-Belmonte, E.M., and Lee, M.Y. 2000. Identification of a fourth subunit of mammalian DNA polymerase delta. J Biol Chem 275:18739-18744.
69. Lu, X., Tan, C.K., Zhou, J.Q., You, M., Carastro, L.M., Downey, K.M., and So, A.G. 2002. Direct interaction of proliferating cell nuclear antigen with the small subunit of DNA polymerase delta. J Biol Chem 277:24340-24345.
70. MacNeill, S.A., Baldacci, G., Burgers, P.M., and Hubscher, U. 2001. A unified nomenclature for the subunits of eukaryotic DNA polymerase delta. Trends Biochem Sci 26:16-17.
71. MacNeill, S.A., Moreno, S., Reynolds, N., Nurse, P., and Fantes, RA. 1996. The fission yeast Cdc1 protein, a homologue of the small subunit of DMA polymerase delta, binds to Pol3 and Cdc27. EMBO J 15:4613-4628.
72. Maga, G., Stucki, M., Spadari, S., and Hubscher, U. 2000. DNA polymerase switching: I. Replication factor C displaces DNA polymerase alpha prior to PCNA loading. J Mol Biol 295:791-801.
73. Maga, G., Villani, G., Tillement, V., Stucki, M., Locatelli, G.A., Frouin, I., Spadari, S., and Hubscher, U. 2001. Okazaki fragment processing: modulation of the strand displacement activity of DNA polymerase delta by the concerted action of replication protein A, proliferating cell nuclear antigen, and flap endonuclease-1. Proc Natl Acad Sci USA 98:14298-14303.
74. Majka, J. and Burgers, P.M. 2004. The PCNA-RFC families of DNA clamps and clamp loaders. Progr Nucl Acids Res Mol Biol 78:227-260.
75. Maki, S., Hashimoto, K., Ohara, T., and Sugino, A. 1998. DNA polymerase II epsilon) of Saccharomyces cerevisiae dissociates from the DNA template by sensing single-stranded DNA. J Biol Chem 273:21332-21341.
76. Masumoto, H., Muramatsu, S., Kamimura, Y., and Araki, H. 2002. S-Cdk-dependent phosphorylation of Sld2 essential for chromosomal DNA replication in budding yeast. Nature 415:651-655.
77. Masumoto, H., Sugino, A., and Araki, H. 2000. Dpb11 controls the association between DNA polymerases alpha and epsilon and the autonomously replicating sequence region of budding yeast. Mol Cell Biol 20:2809-2817.
78. Matsunaga, F., Norais, C., Forterre, P., and Myllykallio, H. 2003. Identification of short 'eukaryotic' Okazaki fragments synthesized from a prokaryotic replication origin. EMBO Rep 4:154-158.
79. McConnell, M., Miller, H., Mozzherin, D.J., Quamina, A., Tan, C.K., Downey, K.M., and Fisher, P.A. 1996. The mammalian DNA polymerase delta-proliferating cell nuclear antigen-template-primer complex: molecular characterization by direct binding. Biochemistry 35:8268-8274.
80. Melendy, T. and Stillman, B. 1993. An interaction between replication protein A and SV40 T antigen appears essential for primosome assembly during SV40 DNA replication. J Biol Chem 268:3389-3395.
81. Mimura, S., Masuda, T., Matsui, T., and Takisawa, H. 2000. Central role for cdc45 in establishing an initiation complex of DNA replication in Xenopus egg extracts. Genes Cells 5:439-452.
82. Mo, J., Liu, L., Leon, A., Mazloum, N., and Lee, M.Y. 2000. Evidence that DNA polymerase delta isolated by immunoaffinity chromatography exhibits high-molecular weight characteristics and is associated with the KIAA0039 protein and RPA. Biochemistry 39:7245-7254.
83. Morrison, A., Araki, H., Clark, A.B., Hamatake, R. K., and Sugino, A. 1990. A third essential DNA polymerase in S. cerevisiae. Cell 62:1143-1151.
84. Mossi, R., Keller, R.C., Ferrari, E., and Hubscher, U. 2000. DNA polymerase switching: II. Replication factor C abrogates primer synthesis by DNA polymerase alpha at a critical length. J Mol Biol 295:803-814.
85. Mozzherin, D.J., Tan, C.K., Downey, K.M., and Fisher, P.A. 1999. Architecture of the active DNA polymerase delta proliferating cell nuclear antigen template-primer complex. J Biol Chem 274:19862-19867.
86. Murante, R.S., Rust, L., and Bambara, R.A. 1995. Calf 5′ to 3′ exo/endonuclease must slide from a 5′ end of the substrate to perform structure-specific cleavage. J Biol Chem 270:30377-30383.
87. Muzi-Falconi, M., Giannattasio, M., Foiani, M., and Plevani, P. 2003. The DNA polymerase alpha-primase complex: multiple functions and interactions. Scientific World Journal 3:21-33.
88. Nasheuer, H.P., Moore, A., Wahl, A.F., and Wang, T.S. 1991. Cell cycle-dependent phosphorylation of human DNA polymerase alpha. J Biol Chem 266:7893-7903.
89. Navas, T.A., Zhou, Z., and Elledge, S.J. 1995. DNA polymerase epsilon links the DNA replication machinery to the S phase checkpoint. Cell 80:29-39.
90. Nethanel, T., Zlotkin, T., and Kaufmann, G. 1992. Assembly of simian virus 40 Okazaki pieces from DNA primers is reversibly arrested by ATP depletion. J Virol 66:6634-6640.
91. Ohya, T., Kawasaki, Y., Hiraga, S., Kanbara, S., Nakajo, K., Nakashima, N., Suzuki, A., and Sugino, A. 2002. The DNA polymerase domain of polepsilon) is required for rapid, efficient, and highly accurate chromosomal DNA replication, telomere length maintenance, and normal cell senescence in Saccharomyces cerevisiae. J Biol Chem 277:28099-28108.
92. Ohya, T., Maki, S., Kawasaki, Y., and Sugino, A. 2000. Structure and function of the fourth subunit Dpb4p) of DNA polymerase epsilon in Saccharomyces cerevisiae. Nucleic Acids Res 28:3846-3852.
93. Pavlov, Y.I., Shcherbakova, P.V., and Kunkel, T.A. 2001. In vivo consequences of putative active site mutations in yeast DNA polymerases alpha, epsilon, delta, and zeta. Genetics 9:47-64.
94. Podust, V., Mikhailov, V., Georgaki, A., and Hubscher, U. 1992. DNA polymerase delta and epsilon holoenzymes from calf thymus. Chromosoma 102:41.
95. Podust, V.N., Chang, L.S., Ott, R., Dianov, G.L., and Fanning, E. 2002. Reconstitution of human DNA polymerase delta using recombinant baculoviruses: the p12 subunit potentiates DNA polymerizing activity of the four-subunit enzyme. J Biol Chem 277:3894-3901.
96. Pospiech, H. and Syvaoja, J.E. 2003. DNA polymerase epsilon-more than a polymerase. Scientific World Journal 3:87-104.
97. Prelich, G., Tan, C.K., Kostura, M., Mathews, M.B., So, A.G., Downey, K.M., and Stillman, B. 1987. Functional identity of proliferating cell nuclear antigen and a DNA polymerase-delta auxiliary protein. Nature 326:517-520.
98. Raghuraman, M.K., Winzeler, E.A., Collingwood, D., Hunt, S., Wodicka, L., Conway, A., Lockhart, D.J., Davis, R.W., Brewer, B.J., and Fangman, W.L. 2001. Replication dynamics of the yeast genome. Science 294:115-121.
99. Resnick, M.A. 1978. Similar responses to ionizing radiation of fungal and vertebrate cells and the importance of DNA doublestrand breaks. J Theor Biol 71:339-346.
100. Resnick, M.A. and Martin, P. 1976. The repair of double-strand breaks in the nuclear DNA of Saccharomyces cerevisiae and its genetic control. Mol Gen Genet 143:119-129.
101. Ricke, R.M. and Bielinsky, A.K. 2004. Mcm10 Regulates the Stability and Chromatin Association of DNA Polymerase-alpha. Mol Cell 16:173-185.
102. Rodriguez, A.C., Park, H.W., Mao, C., and Beese, L.S. 2000. Crystal structure of a pol alpha family DNA polymerase from the hyperthermophilic archaeon Thermococcus sp. 9 degrees N-7. J Mol Biol 299:447-462.
103. Santocanale, C., Foiani, M., Lucchini, G., and Plevani, P. 1993. The isolated 48,000-dalton subunit of yeast DNA primase is sufficient for RNA primer synthesis. J Biol Chem 268:1343-1348.
104. Sawyer, S.L., Cheng, I.H., Chai, W., and Tye, B.K. 2004. Mcm10 and Cdc45 cooperate in origin activation in Saccharomyces cerevisiae J Mol Biol 340:195-202.
105. Shcherbakova, P.V., Noskov, V.N., Pshenichnov, M.R., and Pavlov, Y.I. 1996. Base analog 6-N-hydroxylaminopurine mutagenesis in the yeast Saccharomyces cerevisiae is controlled by replicative DNA polymerases. Mutat Res 369:33-44.
106. Shcherbakova, P.V. and Pavlov, Y.I. 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.
107. Shibahara, K. and Stillman, B. 1999. Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell 96:575-585.
108. Shikata, K., Ohta, S., Yamada, K., Obuse, C., Yoshikawa, H., and Tsurimoto, T. 2001. The human homologue of fission Yeast cdc27, p66, is a component of active human DNA polymerase delta. J Biochem 129:699-708.
109. Sogo, J.M., Lopes, M., and Foiani, M. 2002. Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects.[see comment]. Science 297:599-602.
110. Spiga, M.G. and D'Urso, G. 2004. Identification and cloning of two putative subunits of DNA polymerase epsilon in fission yeast. Nucleic Acids Res 32:4945-4953.
111. Sporbert, A., Gahl, A., Ankerhold, R., Leonhardt, H., and Cardoso, M.C. 2002. DNA polymerase clamp shows little turnover at established replication sites but sequential de novo assembly at adjacent origin clusters. Mol Cell 10:1355-1365.
112. Sun, Y.B., Jiang, Y.Q., Zhang, P., Zhang, S.J., Zhou, Y., Li, B.Q., Toomey, N.L., and Lee, M.Y. 1997. Expression and characterization of the small subunit of human DNA polymerase delta. J Biol Chem 272:13013-13018.
113. 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.
114. Tan, C.K., Castillo, C., So, A.G., and Downey, K.M. 1986. An auxiliary protein for DNA polymerase delta from fetal calf thymus. J Biol Chem 261:12310-12316.
115. Tong, A.M., Lesage, G., Bader, G.D., Ding, H., Xu, H., Xin, X., Young, J., Berriz, G.F., Brost, R.L., Chang, M., et al. 2004. Global mapping of the yeast genetic interaction network. Science 303:808-813.
116. Tratner, I., Piard, K., Grenon, M., Perderiset, M., and Baldacci, G. 1997. PCNA and DNA polymerase delta catalytic subunit from Schizosaccharomyces pombe do not interact directly. Biochem Biophys Res Commun 231:321-328.
117. Tsubota, T., Maki, S., Kubota, H., Sugino, A., and 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.
118. Tsurimoto, T., Melendy, T., and Stillman, B. 1990. Sequential initiation of lagging and leading strand synthesis by two different polymerase complexes at the SV40 DNA replication origin. Nature 346:534-539.
119. Tsurimoto, T. and Stillman, B. 1991. Replication factors required for SV40 DNA replication in vitro. II. Switching of DNA polymerase alpha and delta during initiation of leading and lagging strand synthesis. J Biol Chem 266:1961-1968.
120. Uchiyama, M., Griffiths, D., Arai, K., and Masai, H. 2001. Essential role of Sna41/Cdc45 in loading of DNA polymerase alpha onto minichromosome maintenance proteins in fission yeast. J Biol Chem 276:26189-26196.
121. Waga, S. and Stillman, B. 1998. The DNA replication fork in eukaryotic cells. Annu Rev Biochem 67:721-751.
122. Warbrick, E. 2000. The puzzle of PCNAs many partners. Bioessays 22:997-1006.
123. Wintersberger, U. and Wintersberger, E. 1970. Studies on deoxyribonucleic acid polymerases from yeast. 1. Parial purification and properties of two DNA polymerases from mitochondria-free cell extracts. Eur J Biochem 13:11-19.
124. Zerbe, L.K. and Kuchta, R.D. 2002. The p58 subunit of human DNA primase is important for primer initiation, elongation, and counting. Biochemistry 41:4891-4900.
125. Zhang, P., Mo, J.Y., Perez, A., Leon, A., Liu, L., Mazloum, N., Xu, H., and Lee, M.Y. 1999. Direct interaction of proliferating cell nuclear antigen with the p125 catalytic subunit of mammalian DNA polymerase delta. J Biol Chem 274:26647-26653.
126. Zhang, S.J., Zeng, X.R., Zhang, P., Toomey, N.L., Chuang, R.Y., Chang, L.S., and Lee, M.Y. 1995. A conserved region in the amino terminus of DNA polymerase delta is involved in proliferating cell nuclear antigen binding. J Biol Chem 270:7988-7992.
127. Zhao, Y., Jeruzalmi, D., Moarefi, I., Leighton, L., Lasken, R., and Kuriyan, J. 1999. Crystal structure of an archaebacterial DNA polymerase. Structure Fold Des 7:1189-1199.
128. Zhou, J.Q., He, H., Tan, C.K., Downey, K.M., and So, A.G. 1997. The small subunit is required for functional interaction of DNA polymerase delta with the proliferating cell nuclear antigen. Nucleic Acids Res 25:1094-1099.
129. Zlotkin, T., Kaufmann, G., Jiang, Y., Lee, M.Y., Ditto, L., Syvaoja, J., Dornreiter, I., Fanning, E., and Nethanel, T. 1996. DNA polymerase epsilon may be dispensable for SV40- but not cellular-DNA replication. EMBO J 15:2298-2305.
130. Zou, L. and Stillman, B. 2000. Assembly of a complex containing Cdc45p, replication protein A, and Mcm2p at replication origins controlled by S-phase cyclin-dependent kinases and Cdc7p-Dbf4p kinase. Mol Cell Biol 20:3086-3096.
131. Zuo, S., Bermudez, V., Zhang, G., Kelman, Z., and Hurwitz, J. 2000. Structure and activity associated with multiple forms of Schizosaccharomyces pombe DNA polymerase delta. J Biol Chem 275:5153-5162.
132. Zuo, S.J., Gibbs, E., Kelman, Z., Wang, T., Odonnell, M., Macneill, S.A., and Hurwitz, J. 1997. Dna polymerase delta isolated from schizosaccharomyces pombe contains five subunits. Proc Natl Acad Sci USA 94:11244-11249.