DNA replication and homologous recombination factors: Acting together to maintain genome stability

Chromosoma

Volumn 122, Issue 5, 2013, Pages 401-413

  Aze, Antoine ^a   Zhou, Jin Chuan ^a   Costa, Alessandro ^a   Costanzo, Vincenzo ^a  

^a London Research Institute   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CLASPIN; DNA DIRECTED DNA POLYMERASE ALPHA; DNA DIRECTED DNA POLYMERASE DELTA; DNA DIRECTED DNA POLYMERASE EPSILON; DNA PRIMASE; MINICHROMOSOME MAINTENANCE PROTEIN 2; MINICHROMOSOME MAINTENANCE PROTEIN 3; MINICHROMOSOME MAINTENANCE PROTEIN 4; MINICHROMOSOME MAINTENANCE PROTEIN 5; MINICHROMOSOME MAINTENANCE PROTEIN 6; MINICHROMOSOME MAINTENANCE PROTEIN 7; MRE11 PROTEIN; PROTEIN CDC45; PROTEIN CTF4; PROTEIN GINS; PROTEIN MRC1; PROTEIN RAD15; UNCLASSIFIED DRUG;

CATALYSIS; DNA REPAIR; DNA REPLICATION; DNA STRAND BREAKAGE; DNA TEMPLATE; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVATION; GENE CONSTRUCT; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION; HUMAN; NONHUMAN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REPLISOME; REVIEW; SIGNAL TRANSDUCTION; TIGHT JUNCTION;

CELL CYCLE PROTEINS; DNA; DNA HELICASES; DNA REPLICATION; EUKARYOTIC CELLS; GENES, DUPLICATE; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION;

EID: 84885844201     PISSN: 00095915     EISSN: 14320886     Source Type: Journal    
DOI: 10.1007/s00412-013-0411-3     Document Type: Review

References (123)

1. Abe T, Sugimura K, Hosono Y, Takami Y, Akita M, Yoshimura A, Tada S, Nakayama T, Murofushi H, Okumura K, Takeda S, Horikoshi M, Seki M, Enomoto T (2011) The histone chaperone facilitates chromatin transcription (FACT) protein maintains normal replication fork rates. J Biol Chem 286:30504-30512
2. Alcasabas AA, Osborn AJ, Bachant J, Hu F, Werler PJ, Bousset K, Furuya K, Diffley JF, Carr AM, Elledge SJ (2001) Mrc1 transduces signals of DNA replication stress to activate Rad53. Nat Cell Biol 3:958-965
3. Arias EE, Walter JC (2007) Strength in numbers: preventing rereplication via multiple mechanisms in eukaryotic cells. Genes Dev 21:497-518
4. Asturias FJ, Cheung IK, Sabouri N, Chilkova O, Wepplo D, Johansson E (2006) Structure of Saccharomyces cerevisiae DNA polymerase epsilon by cryo-electron microscopy. Nat Struct Mol Biol 13:35-43
5. Augustin MA, Huber R, Kaiser JT (2001) Crystal structure of a DNA-dependent RNA polymerase (DNA primase). Nat Struct Biol 8:57-61
6. Baranovskiy AG, Babayeva ND, Liston VG, Rogozin IB, Koonin EV, Pavlov YI, Vassylyev DG, Tahirov TH (2008) X-ray structure of the complex of regulatory subunits of human DNA polymerase delta. Cell Cycle 7:3026-3036
7. Barry ER, Lovett JE, Costa A, Lea SM, Bell SD (2009) Intersubunit allosteric communication mediated by a conserved loop in the MCM helicase. Proc Natl Acad Sci U S A 106:1051-1056
8. Bermudez VP, Farina A, Raghavan V, Tappin I, Hurwitz J (2011) Studies on human DNA polymerase epsilon and GINS complex and their role in DNA replication. J Biol Chem 286:28963-28977
9. Bochman ML, Schwacha A (2008) The Mcm2-7 complex has in vitro helicase activity. Mol Cell 31:287-293
10. Bochman ML, Schwacha A (2010) The Saccharomyces cerevisiae Mcm6/2 and Mcm5/3 ATPase active sites contribute to the function of the putative Mcm2-7 'gate'. Nucleic Acids Res 38:6078-6088
11. Boos D, Frigola J, Diffley JF (2012) Activation of the replicative DNA helicase:breaking up is hard to do. Curr Opin Cell Biol 24:423-430
12. Botchan M, Berger J (2010) DNA replication: making two forks from one prereplication complex. Mol Cell 40:860-861
13. Brewster AS, Wang G, Yu X, Greenleaf WB, Carazo JM, Tjajadia M, Klein MG, Chen XS (2008) Crystal structure of a near-full-length archaeal MCM: functional insights for an AAA + hexameric helicase. Proc Natl Acad Sci U S A 105:20191-20196
14. Bruck I, Kaplan DL (2013) Cdc45 Protein-single-stranded DNA interaction is important for stalling the helicase during replication stress. J Biol Chem 288:7550-7563
15. Bruning JB, Shamoo Y (2004) Structural and thermodynamic analysis of human PCNA with peptides derived from DNA polymerase-delta p66 subunit and flap endonuclease-1. Structure 12:2209-2219
16. Buis J, Wu Y, Deng Y, Leddon J, Westfield G, Eckersdorff M, Sekiguchi JM, Chang S, Ferguson DO (2008) Mre11 nuclease activity has essential roles in DNA repair and genomic stability distinct from ATM activation. Cell 135:85-96
17. Chang YP, Wang G, Bermudez V, Hurwitz J, Chen XS (2007) Crystal structure of the GINS complex and functional insights into its role in DNA replication. Proc Natl Acad Sci U S A 104:12685-12690
18. Cho WH, Kang YH, An YY, Tappin I, Hurwitz J, Lee JK (2013) Human Tim-Tipin complex affects the biochemical properties of the replicative DNA helicase and DNA polymerases. Proc Natl Acad Sci U S A 110:2523-2527
19. Choi JM, Lim HS, Kim JJ, Song OK, Cho Y (2007) Crystal structure of the human GINS complex. Genes Dev 21:1316-1321
20. Chong JP, Hayashi MK, Simon MN, Xu RM, Stillman B (2000) A double-hexamer archaeal minichromosome maintenance protein is an ATP-dependent DNA helicase. Proc Natl Acad Sci U S A 97:1530-1535
21. Chou DM, Elledge SJ (2006) Tipin and Timeless form a mutually protective complex required for genotoxic stress resistance and checkpoint function. Proc Natl Acad Sci U S A 103:18143-18147
22. Cimprich KA, Cortez D (2008) ATR: an essential regulator of genome integrity. Nat Rev Mol Cell Biol 9:616-627
23. Costa A, Ilves I, Tamberg N, Petojevic T, Nogales E, Botchan MR, Berger JM (2011) The structural basis for MCM2-7 helicase activation by GINS and Cdc45. Nat Struct Mol Biol 18:471-477
24. Costanzo V, Gautier J (2003) Single-strand DNA gaps trigger an ATR- and Cdc7-dependent checkpoint. Cell Cycle 2:17
25. Costanzo V, Gautier J (2004) Xenopus cell-free extracts to study DNA damage checkpoints. Methods Mol Biol 241:255-267
26. Costanzo V, Robertson K, Bibikova M, Kim E, Grieco D, Gottesman M, Carroll D, Gautier J (2001) Mre11 protein complex prevents double-strand break accumulation during chromosomal DNA replication. Mol Cell 8:137-147
27. Costanzo V, Chaudhuri J, Fung JC, Moran JV (2009) Dealing with dangerous accidents: DNA double-strand breaks take centre stage. Symposium on Genome Instability and DNA Repair. EMBO Rep 10:837-842
28. Cotta-Ramusino C, Fachinetti D, Lucca C, Doksani Y, Lopes M, Sogo J, Foiani M (2005) Exo1 processes stalled replication forks and counteracts fork reversal in checkpoint-defective cells. Mol Cell 17:153-159
29. D'Amours D, Jackson SP (2002) The Mre11 complex: at the crossroads of dna repair and checkpoint signalling. Nat Rev Mol Cell Biol 3:317-327
30. De Falco M, Ferrari E, De Felice M, Rossi M, Hubscher U, Pisani FM (2007) The human GINS complex binds to and specifically stimulates human DNA polymerase alpha-primase. EMBO Rep 8:99-103
31. Deem A, Keszthelyi A, Blackgrove T, Vayl A, Coffey B, Mathur R, Chabes A, Malkova A (2011) Break-induced replication is highly inaccurate. PLoS Biology 9:e1000594
32. Dua R, Levy DL, Campbell JL (1998) Role of the putative zinc finger domain of Saccharomyces cerevisiae DNA polymerase epsilon in DNA replication and the S/M checkpoint pathway. J Biol Chem 273:30046-30055
33. Dua R, Levy DL, Campbell JL (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
34. Errico A, Costanzo V (2012) Mechanisms of replication fork protection: a safeguard for genome stability. Crit Rev Biochem Mol Biol 47:222-235
35. Errico A, Costanzo V, Hunt T (2007) Tipin is required for stalled replication forks to resume DNA replication after removal of aphidicolin in Xenopus egg extracts. Proc Natl Acad Sci U S A 104:14929-14934
36. Errico A, Cosentino C, Rivera T, Losada A, Schwob E, Hunt T, Costanzo V (2009) Tipin/Tim1/And1 protein complex promotes Pol alpha chromatin binding and sister chromatid cohesion. EMBO J 28:3681-3692
37. Feng W, 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
38. Fletcher RJ, Bishop BE, Leon RP, Sclafani RA, Ogata CM, Chen XS (2003) The structure and function of MCM from archaeal M. thermoautotrophicum. Nat Struct Biol 10:160-167
39. Frick DN, Richardson CC (2001) DNA primases. Annu Rev Biochem 70:39-80
40. Fu YV, Yardimci H, Long DT, Ho TV, Guainazzi A, Bermudez VP, Hurwitz J, van Oijen A, Scharer OD, Walter JC (2011) Selective bypass of a lagging strand roadblock by the eukaryotic replicative DNA helicase. Cell 146:931-941
41. Gambus A, Jones RC, Sanchez-Diaz A, Kanemaki M, van Deursen F, Edmondson RD, 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
42. Gambus A, van Deursen F, Polychronopoulos D, Foltman M, Jones RC, Edmondson RD, Calzada A, Labib K (2009) A key role for Ctf4 in coupling the MCM2-7 helicase to DNA polymerase alpha within the eukaryotic replisome. EMBO J 28:2992-3004
43. Gerik KJ, Li X, Pautz A, Burgers PM (1998) Characterization of the two small subunits of Saccharomyces cerevisiae DNA polymerase delta. J Biol Chem 273:19747-19755
44. Hashimoto Y, Ray Chaudhuri A, Lopes M, Costanzo V (2010) Rad51 protects nascent DNA from Mre11-dependent degradation and promotes continuous DNA synthesis. Nat Struct Mol Biol 17:1305-1311
45. Hashimoto Y, Puddu F, Costanzo V (2011) RAD51- and MRE11-dependent reassembly of uncoupled CMG helicase complex at collapsed replication forks. Nat Struct Mol Biol 19:17-24
46. Hicks WM, Kim M, Haber JE (2010) Increased mutagenesis and unique mutation signature associated with mitotic gene conversion. Science 329:82-85
47. Hogg M, Johansson E (2012) DNA Polymerase epsilon. Subcell Biochem 62:237-257
48. Ilves I, Petojevic T, Pesavento JJ, Botchan MR (2010) Activation of the MCM2-7 helicase by association with Cdc45 and GINS proteins. Mol Cell 37:247-258
49. Ilves I, Tamberg N, Botchan MR (2012) Checkpoint kinase 2 (Chk2) inhibits the activity of the Cdc45/MCM2-7/GINS (CMG) replicative helicase complex. Proc Natl Acad Sci U S A 109:13163-13170
50. Im JS, Ki SH, Farina A, Jung DS, Hurwitz J, Lee JK (2009) Assembly of the Cdc45-Mcm2-7-GINS complex in human cells requires the Ctf4/And-1, RecQL4, and Mcm10 proteins. Proc Natl Acad Sci U S A 106:15628-15632
51. Jensen RB, Carreira A, Kowalczykowski SC (2010) Purified human BRCA2 stimulates RAD51-mediated recombination. Nature 467:678-683
52. Johansson E, Macneill SA (2010) The eukaryotic replicative DNA polymerases take shape. Trends Biochem Sci 35:339-347
53. Kamada K (2012) The GINS Complex: structure and function. Subcell Biochem 62:135-156
54. Kamada K, Kubota Y, Arata T, Shindo Y, 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
55. Kamimura Y, Tak YS, Sugino A, Araki H (2001) Sld3, which interacts with Cdc45 (Sld4), functions for chromosomal DNA replication in Saccharomyces cerevisiae. EMBO J 20:2097-2107
56. Kang YH, Galal WC, Farina A, Tappin I, Hurwitz J (2012) Properties of the human Cdc45/Mcm2-7/GINS helicase complex and its action with DNA polymerase epsilon in rolling circle DNA synthesis. Proc Natl Acad Sci U S A 109:6042-6047
57. Kanke M, Kodama Y, Takahashi TS, Nakagawa T, Masukata H (2012) Mcm10 plays an essential role in origin DNA unwinding after loading of the CMG components. EMBO J 31:2182-2194
58. Kelman Z, Lee JK, Hurwitz J (1999) The single minichromosome maintenance protein of Methanobacterium thermoautotrophicum DeltaH contains DNA helicase activity. Proc Natl Acad Sci U S A 96:14783-14788
59. Kesti T, Flick K, Keranen S, Syvaoja JE, Wittenberg C (1999) DNA polymerase epsilon catalytic domains are dispensable for DNA replication, DNA repair, and cell viability. Mol Cell 3:679-685
60. Kilkenny ML, De Piccoli G, Perera RL, Labib K, Pellegrini L (2012) A conserved motif in the C-terminal tail of DNA polymerase alpha tethers primase to the eukaryotic replisome. J Biol Chem 287:23740-23747
61. Klinge S, Nunez-Ramirez R, Llorca O, Pellegrini L (2009) 3D architecture of DNA Pol alpha reveals the functional core of multi-subunit replicative polymerases. EMBO J 28:1978-1987
62. Krastanova I, Sannino V, Amenitsch H, Gileadi O, Pisani FM, Onesti S (2012) Structural and functional insights into the DNA replication factor Cdc45 reveal an evolutionary relationship to the DHH family of phosphoesterases. J Biol Chem 287:4121-4128
63. Labib K (2010) How do Cdc7 and cyclin-dependent kinases trigger the initiation of chromosome replication in eukaryotic cells? Genes Dev 24:1208-1219
64. Lambert S, Mizuno K, Blaisonneau J, Martineau S, Chanet R, Freon K, Murray JM, Carr AM, Baldacci G (2010) Homologous recombination restarts blocked replication forks at the expense of genome rearrangements by template exchange. Mol Cell 39:346-359
65. Lao-Sirieix SH, Nookala RK, Roversi P, Bell SD, Pellegrini L (2005a) Structure of the heterodimeric core primase. Nat Struct Mol Biol 12:1137-1144
66. Lao-Sirieix SH, Pellegrini L, Bell SD (2005b) The promiscuous primase. Trends Genet: TIG 21:568-572
67. Lee J, Kumagai A, Dunphy WG (2003) Claspin, a Chk1-regulatory protein, monitors DNA replication on chromatin independently of RPA, ATR, and Rad17. Mol Cell 11:329-340
68. Li H, Xie B, Zhou Y, Rahmeh A, Trusa S, Zhang S, Gao Y, Lee EY, Lee MY (2006) Functional roles of p12, the fourth subunit of human DNA polymerase delta. J Biol Chem 281:14748-14755
69. Li Z, Santangelo TJ, Cubonova L, Reeve JN, Kelman Z (2010) Affinity purification of an archaeal DNA replication protein network. mBio 1
70. Li Z, Pan M, Santangelo TJ, Chemnitz W, Yuan W, Edwards JL, Hurwitz J, Reeve JN, Kelman Z (2011) A novel DNA nuclease is stimulated by association with the GINS complex. Nucleic Acids Res 39:6114-6123
71. Lindahl T, Barnes DE (2000) Repair of endogenous DNA damage. Cold Spring Harb Symp Quant Biol 65:127-133
72. Liu L, Mo J, Rodriguez-Belmonte EM, Lee MY (2000) Identification of a fourth subunit of mammalian DNA polymerase delta. J Biol Chem 275:18739-18744
73. Liu S, Bekker-Jensen S, Mailand N, Lukas C, Bartek J, Lukas J (2006) Claspin operates downstream of TopBP1 to direct ATR signaling towards Chk1 activation. Mol Cell Biol 26:6056-6064
74. Llorente B, Smith CE, Symington LS (2008) Break-induced replication: what is it and what is it for? Cell Cycle 7:859-864
75. Lou H, Komata M, Katou Y, Guan Z, Reis CC, Budd M, Shirahige K, Campbell JL (2008) Mrc1 and DNA polymerase epsilon function together in linking DNA replication and the S phase checkpoint. Mol Cell 32:106-117
76. Lovett ST, Clark AJ (1984) Genetic analysis of the recJ gene of Escherichia coli K-12. J Bacteriol 157:190-196
77. Lu X, Tan CK, Zhou JQ, You M, Carastro LM, Downey KM, So AG (2002) Direct interaction of proliferating cell nuclear antigen with the small subunit of DNA polymerase delta. J Biol Chem 277:24340-24345
78. Lydeard JR, Jain S, Yamaguchi M, Haber JE (2007) Break-induced replication and telomerase-independent telomere maintenance require Pol32. Nature 448:820-823
79. Lydeard JR, Lipkin-Moore Z, Sheu YJ, Stillman B, Burgers PM, Haber JE (2010) Break-induced replication requires all essential DNA replication factors except those specific for pre-RC assembly. Genes Dev 24:1133-1144
80. Lyubimov AY, Strycharska M, Berger JM (2011) The nuts and bolts of ring-translocase structure and mechanism. Curr Opin Struct Biol 21:240-248
81. Lyubimov AY, Costa A, Bleichert F, Botchan MR, Berger JM (2012) ATP-dependent conformational dynamics underlie the functional asymmetry of the replicative helicase from a minimalist eukaryote. Proc Natl Acad Sci U S A 109:11999-12004
82. Macneill S (2012) Composition and dynamics of the eukaryotic replisome: a brief overview. Subcell Biochem 62:1-17
83. Makarova KS, Koonin EV, Kelman Z (2012) The CMG (CDC45/RecJ, MCM, GINS) complex is a conserved component of the DNA replication system in all archaea and eukaryotes. Biol Direct 7:7
84. Marinsek N, Barry ER, Makarova KS, Dionne I, Koonin EV, Bell SD (2006) GINS, a central nexus in the archaeal DNA replication fork. EMBO Rep 7:539-545
85. Meng X, Zhou Y, Zhang S, Lee EY, Frick DN, Lee MY (2009) DNA damage alters DNA polymerase delta to a form that exhibits increased discrimination against modified template bases and mismatched primers. Nucleic Acids Res 37:647-657
86. Meng X, Zhou Y, Lee EY, Lee MY, Frick DN (2010) The p12 subunit of human polymerase delta modulates the rate and fidelity of DNA synthesis. Biochemistry 49:3545-3554
87. Miles J, Formosa T (1992) Evidence that POB1, a Saccharomyces cerevisiae protein that binds to DNA polymerase alpha, acts in DNA metabolism in vivo. Mol Cell Biol 12:5724-5735
88. Mizuno K, Lambert S, Baldacci G, Murray JM, Carr AM (2009) Nearby inverted repeats fuse to generate acentric and dicentric palindromic chromosomes by a replication template exchange mechanism. Genes Dev 23:2876-2886
89. Mizuno K, Miyabe I, Schalbetter SA, Carr AM, Murray JM (2013) Recombination-restarted replication makes inverted chromosome fusions at inverted repeats. Nature 493:246-249
90. Moyer SE, Lewis PW, Botchan MR (2006) Isolation of the Cdc45/Mcm2-7/GINS (CMG) complex, a candidate for the eukaryotic DNA replication fork helicase. Proc Natl Acad Sci U S A 103:10236-10241
91. Muramatsu S, Hirai K, Tak YS, Kamimura Y, Araki H (2010) CDK-dependent complex formation between replication proteins Dpb11, Sld2, Pol (epsilon}, and GINS in budding yeast. Genes Dev 24:602-612
92. Nedelcheva MN, Roguev A, Dolapchiev LB, Shevchenko A, Taskov HB, Shevchenko A, Stewart AF, Stoynov SS (2005) Uncoupling of unwinding from DNA synthesis implies regulation of MCM helicase by Tof1/Mrc1/Csm3 checkpoint complex. J Mol Biol 347:509-521
93. Netz DJ, Stith CM, Stumpfig M, Kopf G, Vogel D, Genau HM, Stodola JL, Lill R, Burgers PM, Pierik AJ (2012) Eukaryotic DNA polymerases require an iron-sulfur cluster for the formation of active complexes. Nat Chem Biol 8:125-132
94. Neuwald AF, Aravind L, Spouge JL, Koonin EV (1999) AAA+: A class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res 9:27-43
95. 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
96. Nunez-Ramirez R, Klinge S, Sauguet L, Melero R, Recuero-Checa MA, Kilkenny M, Perera RL, Garcia-Alvarez B, Hall RJ, Nogales E, Pellegrini L, Llorca O (2011) Flexible tethering of primase and DNA Pol alpha in the eukaryotic primosome. Nucleic Acids Res 39:8187-8199
97. Nuutinen T, Tossavainen H, Fredriksson K, Pirila P, Permi P, Pospiech H, Syvaoja JE (2008) The solution structure of the amino-terminal domain of human DNA polymerase epsilon subunit B is homologous to C-domains of AAA+ proteins. Nucleic Acids Res 36:5102-5110
98. Osborn AJ, Elledge SJ (2003) Mrc1 is a replication fork component whose phosphorylation in response to DNA replication stress activates Rad53. Genes Dev 17:1755-1767
99. Pellegrini L (2012) The Pol alpha-Primase complex. Subcell Biochem 62:157-169
100. Pellegrini L, Venkitaraman A (2004) Emerging functions of BRCA2 in DNA recombination. Trends Biochem Sci 29:310-316
101. Pellegrini L, Yu DS, Lo T, Anand S, Lee M, Blundell TL, Venkitaraman AR (2002) Insights into DNA recombination from the structure of a RAD51-BRCA2 complex. Nature 420:287-293
102. Podust VN, Chang LS, Ott R, Dianov GL, 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
103. 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
104. Remus D, Beuron F, Tolun G, Griffith JD, Morris EP, Diffley JF (2009) Concerted loading of Mcm2-7 double hexamers around DNA during DNA replication origin licensing. Cell 139:719-730
105. Reynolds N, Watt A, Fantes PA, MacNeill SA (1998) Cdm1, the smallest subunit of DNA polymerase d in the fission yeast Schizosaccharomyces pombe, is non-essential for growth and division. Curr Genet 34:250-258
106. San Filippo J, Sung P, Klein H (2008) Mechanism of eukaryotic homologous recombination. Annu Rev Biochem 77:229-257
107. Sanchez-Pulido L, Ponting CP (2011) Cdc45: the missing RecJ ortholog in eukaryotes? Bioinformatics 27:1885-1888
108. Schlacher K, Christ N, Siaud N, Egashira A, Wu H, Jasin M (2011) Double-strand break repair-independent role for BRCA2 in blocking stalled replication fork degradation by MRE11. Cell 145:529-542
109. Segurado M, Diffley JF (2008) Separate roles for the DNA damage checkpoint protein kinases in stabilizing DNA replication forks. Genes Dev 22:1816-1827
110. Su X, Bernal JA, Venkitaraman AR (2008) Cell-cycle coordination between DNA replication and recombination revealed by a vertebrate N-end rule degron-Rad51. Nat Struct Mol Biol 15:1049-1058
111. 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
112. Szyjka SJ, Viggiani CJ, Aparicio OM (2005) Mrc1 is required for normal progression of replication forks throughout chromatin in S. cerevisiae. Mol Cell 19:691-697
113. Tahirov TH, Makarova KS, Rogozin IB, Pavlov YI, Koonin EV (2009) Evolution of DNA polymerases: an inactivated polymerase-exonuclease module in Pol epsilon and a chimeric origin of eukaryotic polymerases from two classes of archaeal ancestors. Biol Direct 4:11
114. Tanaka H, Katou Y, Yagura M, Saitoh K, Itoh T, Araki H, Bando M, Shirahige K (2009) Ctf4 coordinates the progression of helicase and DNA polymerase alpha. Genes Cells: Devoted Mol Cell Mech 14:807-820
115. Tercero JA, Labib K, Diffley JF (2000) DNA synthesis at individual replication forks requires the essential initiation factor Cdc45p. EMBO J 19:2082-2093
116. Tourriere H, Versini G, Cordon-Preciado V, Alabert C, Pasero P (2005) Mrc1 and Tof1 promote replication fork progression and recovery independently of Rad53. Mol Cell 19:699-706
117. van Deursen F, Sengupta S, De Piccoli G, Sanchez-Diaz A, Labib K (2012) Mcm10 associates with the loaded DNA helicase at replication origins and defines a novel step in its activation. EMBO J 31:2195-2206
118. Vijayraghavan S, Schwacha A (2012) The eukaryotic mcm2-7 replicative helicase. Subcell Biochem 62:113-134
119. Vos SM, Tretter EM, Schmidt BH, Berger JM (2011) All tangled up: how cells direct, manage and exploit topoisomerase function. Nat Rev Mol Cell Biol 12:827-841
120. Waga S, Stillman B (1994) Anatomy of a DNA replication fork revealed by reconstitution of SV40 DNA replication in vitro. Nature 369:207-212
121. Winkler DD, Luger K (2011) The histone chaperone FACT: structural insights and mechanisms for nucleosome reorganization. J Biol Chem 286:18369-18374
122. Yardimci H, Loveland AB, Habuchi S, van Oijen AM, Walter JC (2010) Uncoupling of sister replisomes during eukaryotic DNA replication. Mol Cell 40:834-840
123. Zegerman P, Diffley JF (2007) Phosphorylation of Sld2 and Sld3 by cyclin-dependent kinases promotes DNA replication in budding yeast. Nature 445:281-285