Function of TopBP1 in genome stability

Sub-Cellular Biochemistry

Volumn 50, Issue , 2010, Pages 119-141

  Sokka, Miiko ^b   Parkkinen, Sinikka ^b   Pospiech, Helmut ^b   Syväoja, Juhani E ^a  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b NONE

Author keywords

BRCT; Checkpoint; DNA damage response; Replication; TopBP1

Indexed keywords

EUKARYOTA; METAZOA;

ADENOSINE DIPHOSPHATE RIBOSE; CARRIER PROTEIN; DNA BINDING PROTEIN; NUCLEAR PROTEIN; TOPBP1 PROTEIN, HUMAN;

DNA DAMAGE; DNA REPLICATION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GENOMIC INSTABILITY; HUMAN; MEIOSIS; METABOLISM; MITOSIS; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION; ULTRAVIOLET RADIATION;

ADENOSINE DIPHOSPHATE RIBOSE; CARRIER PROTEINS; DNA DAMAGE; DNA REPLICATION; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; GENOMIC INSTABILITY; HUMANS; MEIOSIS; MITOSIS; NUCLEAR PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; ULTRAVIOLET RAYS;

EID: 77952980297     PISSN: 03060225     EISSN: None     Source Type: Journal    
DOI: 10.1007/978-90-481-3471-7_7     Document Type: Article

References (97)

1. Abraham, R. T. (2001) Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev, 15, 2177–2196.
2. Adhikary, S. and Eilers, M. (2005) Transcriptional regulation and transformation by Myc proteins. Nat Rev Mol Cell Biol, 6, 635–645.
3. Albert, T., Wells, J., Funk, J. O., Pullner, A., Raschke, E. E., Stelzer, G., Meisterernst, M., Farnham, P. J., and Eick, D. (2001) The chromatin structure of the dual c-myc promoter P1/P2 is regulated by separate elements. J Biol Chem, 276, 20482–20490.
4. Araki, H., Leem, S. H., Phongdara, A., and Sugino, A. (1995) Dpb11, which interacts with DNA polymerase II(epsilon) 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.
5. Benard, M., Maric, C., and Pierron, G. (2001) DNA replication-dependent formation of joint DNA molecules in Physarum polycephalum. Mol Cell, 7, 971–980.
6. Boner, W. and Morgan, I. M. (2002) Novel cellular interacting partners of the human papillo-mavirus 16 transcription/replication factor E2. Vi r us Re s, 90, 113–118.
7. Boner, W., Taylor, E. R., Tsirimonaki, E., Yamane, K., Campo, M. S., and Morgan, I. M. (2002) A Functional interaction between the human papillomavirus 16 transcription/replication factor E2 and the DNA damage response protein TopBP1. J Biol Chem, 277, 22297–22303.
8. Celeste, A., Petersen, S., Romanienko, P. J., Fernandez-Capetillo, O., Chen, H. T., Sedelnikova, O. A., Reina-San-Martin, B., Coppola, V., Meffre, E., Difilippantonio, M. J., Redon, C., Pilch, D. R., Olaru, A., Eckhaus, M., Camerini-Otero, R. D., Tessarollo, L., Livak, F., Manova, K., Bonner, W. M., Nussenzweig, M. C., and Nussenzweig, A. (2002) Genomic instability in mice lacking histone H2AX. Science, 296, 922–927.
9. Chaplet, M., Rai, R., Jackson-Bernitsas, D., Li, K., and Lin, S. Y. (2006) BRIT1/MCPH1: a guardian of genome and an enemy of tumors. Cell Cycle, 5, 2579–2583.
10. Choi, J. H., Lindsey-Boltz, L. A., and Sancar, A. (2007) Reconstitution of a human ATR-mediated checkpoint response to damaged DNA. Proc Natl Acad Sci USA, 104, 13301–13306.
11. Choi, J. H., Lindsey-Boltz, L. A., and Sancar, A. (2009) Cooperative activation of the ATR checkpoint kinase by TopBP1 and damaged DNA. Nucleic Acids Res, 37, 1501–1509.
12. Cimprich, K. A. and Cortez, D. (2008) ATR: an essential regulator of genome integrity. Nat Rev Mol Cell Biol, 9, 616–627.
13. de Nigris, F., Mega, T., Berger, N., Barone, M. V., Santoro, M., Viglietto, G., Verde, P., and Fusco, A. (2001) Induction of ETS-1 and ETS-2 transcription factors is required for thyroid cell transformation. Cancer Res, 61, 2267–2275.
14. Delacroix, S., Wagner, J. M., Kobayashi, M., Yamamoto, K., and Karnitz, L. M. (2007) The Rad9-Hus1-Rad1 (9-1-1) clamp activates checkpoint signaling via TopBP1. Genes Dev, 21, 1472–1477.
15. Dittmer, J. (2003) The biology of the Ets1 proto-oncogene. Mol Cancer, 2, 29.
16. Donaldson, M. M., Boner, W., and Morgan, I. M. (2007) TopBP1 regulates human papillomavirus type 16 E2 interaction with chromatin. J Virol, 81, 4338–4342.
17. Dutertre, S., Cazales, M., Quaranta, M., Froment, C., Trabut, V., Dozier, C., Mirey, G., Bouche, J. P., Theis-Febvre, N., Schmitt, E., Monsarrat, B., Prigent, C., and Ducommun, B. (2004) Phosphorylation of CDC25B by Aurora-A at the centrosome contributes to the G2-M transition. J Cell Sci, 117, 2523–2531.
18. Garcia, V., Furuya, K., and Carr, A. M. (2005) Identification and functional analysis of TopBP1 and its homologs. DNA Repair (Amst), 4, 1227–1239.
19. Going, J. J., Nixon, C., Dornan, E. S., Boner, W., Donaldson, M. M., and Morgan, I. M. (2007) Aberrant expression of TopBP1 in breast cancer. Histopathology, 50, 418–424.
20. Greer, D. A., Besley, B. D., Kennedy, K. B., and Davey, S. (2003) hRad9 rapidly binds DNA containing double-strand breaks and is required for damage-dependent topoisomerase II beta binding protein 1 focus formation. Cancer Res, 63, 4829–4835.
21. Hallstrom, T. C. and Nevins, J. R. (2003) Specificity in the activation and control of transcription factor E2F-dependent apoptosis. Proc Natl Acad Sci USA, 100, 10848–10853.
22. Ham, J., Dostatni, N., Gauthier, J. M., and Yaniv, M. (1991) The papillomavirus E2 protein: a factor with many talents. Trends Biochem Sci, 16, 440–444.
23. Hantschel, O. and Superti-Furga, G. (2004) Regulation of the c-Abl and Bcr-Abl tyrosine kinases. Nat Rev Mol Cell Biol, 5, 33–44.
24. Hashimoto, Y. and Takisawa, H. (2003) Xenopus Cut5 is essential for a CDK-dependent process in the initiation of DNA replication. EMBO J, 22, 2526–2535.
25. Hashimoto, Y., Tsujimura, T., Sugino, A., and Takisawa, H. (2006) The phosphorylated C-terminal domain of Xenopus Cut5 directly mediates ATR-dependent activation of Chk1. Genes Cells, 11, 993–1007.
26. Herold, S., Hock, A., Herkert, B., Berns, K., Mullenders, J., Beijersbergen, R., Bernards, R., and Eilers, M. (2008) Miz1 and HectH9 regulate the stability of the checkpoint protein, TopBP1. EMBO J, 27, 2851–2861.
27. Herold, S., Wanzel, M., Beuger, V., Frohme, C., Beul, D., Hillukkala, T., Syvaoja, J., Saluz, H. P., Haenel, F., and Eilers, M. (2002) Negative regulation of the mammalian UV response by Myc through association with Miz-1. Mol Cell, 10, 509–521.
28. Honda, Y., Tojo, M., Matsuzaki, K., Anan, T., Matsumoto, M., Ando, M., Saya, H., and Nakao, M. (2002) Cooperation of HECT-domain ubiquitin ligase hHYD and DNA topoisomerase IIbinding protein for DNA damage response. J Biol Chem, 277, 3599-3605.
29. Hu, B., Zhou, X. Y., Wang, X., Zeng, Z. C., Iliakis, G., and Wang, Y. (2001) The radioresis-tance to killing of A1–5 cells derives from activation of the Chk1 pathway. J Biol Chem, 276, 17693–17698.
30. Huyton, T., Bates, P. A., Zhang, X., Sternberg, M. J., and Freemont, P. S. (2000) The BRCA1 C-terminal domain: structure and function. Mutat Res, 460, 319–332.
31. Jackman, M., Lindon, C., Nigg, E. A., and Pines, J. (2003) Active cyclin B1-Cdk1 first appears on centrosomes in prophase. Nat Cell Biol, 5, 143–148.
32. Jeon, Y., Lee, K. Y., Ko, M. J., Lee, Y. S., Kang, S., and Hwang, D. S. (2007) Human TopBP1 participates in cyclin E/CDK2 activation and preinitiation complex assembly during G1/S transition. J Biol Chem, 282, 14882–14890.
33. Karppinen, S. M., Erkko, H., Reini, K., Pospiech, H., Heikkinen, K., Rapakko, K., Syvaoja, J. E., and Winqvist, R. (2006) Identification of a common polymorphism in the TopBP1 gene associated with hereditary susceptibility to breast and ovarian cancer. Eur J Cancer, 42, 2647–2652.
34. Kim, J. E., McAvoy, S. A., Smith, D. I., and Chen, J. (2005) Human TopBP1 ensures genome integrity during normal S phase. Mol Cell Biol, 25, 10907–10915.
35. Kramer, A., Lukas, J., and Bartek, J. (2004) Checking out the centrosome. Cell Cycle, 3, 1390–1393.
36. Kubota, Y., Takase, Y., Komori, Y., Hashimoto, Y., Arata, T., Kamimura, Y., Araki, H., and Takisawa, H. (2003) A novel ring-like complex of Xenopus proteins essential for the initiation of DNA replication. Genes Dev, 17, 1141–1152.
37. Kumagai, A., Lee, J., Yoo, H. Y., and Dunphy, W. G. (2006) TopBP1 activates the ATR-ATRIP complex. Cell, 124, 943–955.
38. Lee, J., Kumagai, A., and Dunphy, W. G. (2007) The Rad9-Hus1-Rad1 checkpoint clamp regulates interaction of TopBP1 with ATR. J Biol Chem, 282, 28036–28044.
39. Liu, K., Lin, F. T., Ruppert, J. M., and Lin, W. C. (2003) Regulation of E2F1 by BRCT domain-containing protein TopBP1. Mol Cell Biol, 23, 3287–3304.
40. Liu, K., Luo, Y., Lin, F. T., and Lin, W. C. (2004) TopBP1 recruits Brg1/Brm to repress E2F1-induced apoptosis, a novel pRb-independent and E2F1-specific control for cell survival. Genes Dev, 18, 673–686.
41. Liu, K., Paik, J. C., Wang, B., Lin, F. T., and Lin, W. C. (2006) Regulation of TopBP1 oligomerization by Akt/PKB for cell survival. EMBO J, 25, 4795–4807.
42. Lou, Z., Minter-Dykhouse, K., Franco, S., Gostissa, M., Rivera, M. A., Celeste, A., Manis, J. P., van Deursen, J., Nussenzweig, A., Paull, T. T., Alt, F. W., and Chen, J. (2006) MDC1 maintains genomic stability by participating in the amplification of ATM-dependent DNA damage signals. Mol Cell, 21, 187–200.
43. Lupardus, P. J. and Cimprich, K. A. (2006) Phosphorylation of Xenopus Rad1 and Hus1 defines a readout for ATR activation that is independent of Claspin and the Rad9 carboxy terminus. Mol Biol Cell, 17, 1559–1569.
44. Makiniemi, M., Hillukkala, T., Tuusa, J., Reini, K., Vaara, M., Huang, D., Pospiech, H., Majuri, I., Westerling, T., Makela, T. P., and Syvaoja, J. E. (2001) BRCT domain-containing protein TopBP1 functions in DNA replication and damage response. J Biol Chem, 276, 30399–30406.
45. Manke, I. A., Lowery, D. M., Nguyen, A., and Yaffe, M. B. (2003) BRCT repeats as phosphopeptide-binding modules involved in protein targeting. Science, 302, 636–639.
46. 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.
47. Matsuno, K., Kumano, M., Kubota, Y., Hashimoto, Y., and Takisawa, H. (2006) The N-terminal noncatalytic region of Xenopus RecQ4 is required for chromatin binding of DNA polymerase alpha in the initiation of DNA replication. Mol Cell Biol, 26, 4843–4852.
48. Mordes, D. A., Glick, G. G., Zhao, R., and Cortez, D. (2008) TopBP1 activates ATR through ATRIP and a PIKK regulatory domain. Genes Dev, 22, 1478–1489.
49. Morishima, K., Sakamoto, S., Kobayashi, J., Izumi, H., Suda, T., Matsumoto, Y., Tauchi, H., Ide, H., Komatsu, K., and Matsuura, S. (2007) TopBP1 associates with NBS1 and is involved in homologous recombination repair. Biochem Biophys Res Commun, 362, 872–879.
50. Morris, J. S., Nixon, C., Bruck, A., Nasir, L., Morgan, I. M., and Philbey, A. W. (2008) Immunohistochemical expression of TopBP1 in feline mammary neoplasia in relation to histological grade, Ki67, ERα and p53. Ve t J, 175, 218–226.
51. Morris, J. S., Nixon, C., King, O. J., Morgan, I. M., and Philbey, A. W. (2009) Expression of TopBP1 in canine mammary neoplasia in relation to histological type, Ki67, ERα and p53. Ve t J, 179, 422–429.
52. Nasheuer, H. P., Pospiech, H., and Syväoja, J. (2007) Progress towards the anatomy of the eukaryotic DNA replication fork. In: Lankenau, D. H. (Ed.) Genome Integrity: Facets and Perspectives, Genome Dynamics & Stability, Vol. 1, Springer, Berlin-Heidelberg-NewYork, pp. 27–68.
53. Nasheuer, H. P., Smith, R., Bauerschmidt, C., Grosse, F., and Weisshart, K. (2002) Initiation of eukaryotic DNA replication: regulation and mechanisms. Prog Nucleic Acid Res Mol Biol, 72, 41–94.
54. Parrilla-Castellar, E. R., Arlander, S. J., and Karnitz, L. (2004) Dial 9–1-1 for DNA damage: the Rad9-Hus1-Rad1 (9–1-1) clamp complex. DNA Repair (Amst), 3, 1009–1014.
55. Parrilla-Castellar, E. R. and Karnitz, L. M. (2003) Cut5 is required for the binding of Atr and DNA polymerase alpha to genotoxin-damaged chromatin. J Biol Chem, 278, 45507–45511.
56. Perera, D., Perez-Hidalgo, L., Moens, P. B., Reini, K., Lakin, N., Syvaoja, J. E., San-Segundo, P. A., and Freire, R. (2004) TopBP1 and ATR colocalization at meiotic chromosomes: role of TopBP1/Cut5 in the meiotic recombination checkpoint. Mol Biol Cell, 15, 1568–1579.
57. Pharoah, P. D., Antoniou, A., Bobrow, M., Zimmern, R. L., Easton, D. F., and Ponder, B. A. (2002) Polygenic susceptibility to breast cancer and implications for prevention. Nat Genet, 31, 33–36.
58. Polager, S. and Ginsberg, D. (2008) E2F - at the crossroads of life and death. Trends Cell Biol, 18, 528–535.
59. Reini, K., Uitto, L., Perera, D., Moens, P. B., Freire, R., and Syvaoja, J. E. (2004) TopBP1 localises to centrosomes in mitosis and to chromosome cores in meiosis. Chromosoma, 112, 323–330.
60. Rogakou, E. P., Pilch, D. R., Orr, A. H., Ivanova, V. S., and Bonner, W. M. (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem, 273, 5858–5868.
61. Roussel, M. F., Davis, J. N., Cleveland, J. L., Ghysdael, J., and Hiebert, S. W. (1994) Dual control of myc expression through a single DNA binding site targeted by ets family proteins and E2F-1. Oncogene, 9, 405–415.
62. Saka, Y., Fantes, P., Sutani, T., McInerny, C., Creanor, J., and Yanagida, M. (1994a) Fission yeast cut5 links nuclear chromatin and M phase regulator in the replication checkpoint control. EMBO J, 13, 5319–5329.
63. Saka, Y., Fantes, P., and Yanagida, M. (1994b) Coupling of DNA replication and mitosis by fission yeast rad4/cut5. J Cell Sci Suppl, 18, 57–61.
64. Sangrithi, M. N., Bernal, J. A., Madine, M., Philpott, A., Lee, J., Dunphy, W. G., and Venkitaraman, A. R. (2005) Initiation of DNA replication requires the RECQL4 protein mutated in Rothmund-Thomson syndrome. Cell, 121, 887–898.
65. Schmidt, U., Wollmann, Y., Franke, C., Grosse, F., Saluz, H. P., and Hanel, F. (2008) Characterization of the interaction between the human DNA topoisomerase IIbeta-binding protein 1 (TopBP1) and the cell division cycle 45 (Cdc45) protein. Biochem J, 409, 169–177.
66. Scully, R., Chen, J., Ochs, R. L., Keegan, K., Hoekstra, M., Feunteun, J., and Livingston, D. M. (1997) Dynamic changes of BRCA1 subnuclear location and phosphorylation state are initiated by DNA damage. Cell, 90, 425–435.
67. Sjottem, E., Rekdal, C., Svineng, G., Johnsen, S. S., Klenow, H., Uglehus, R. D., and Johansen, T. (2007) The ePHD protein SPBP interacts with TopBP1 and together they co-operate to stimulate Ets1-mediated transcription. Nucleic Acids Res, 35, 6648–6662.
68. Sorensen, C. S., Hansen, L. T., Dziegielewski, J., Syljuasen, R. G., Lundin, C., Bartek, J., and Helleday, T. (2005) The cell-cycle checkpoint kinase Chk1 is required for mammalian homologous recombination repair. Nat Cell Biol, 7, 195–201.
69. St Onge, R. P., Besley, B. D., Pelley, J. L., and Davey, S. (2003) A role for the phosphorylation of hRad9 in checkpoint signaling. J Biol Chem, 278, 26620–26628.
70. Stanley, M. A., Pett, M. R., and Coleman, N. (2007) HPV: from infection to cancer. Biochem Soc Trans, 35, 1456–1460.
71. Stevens, C. and La Thangue, N. B. (2004) The emerging role of E2F-1 in the DNA damage response and checkpoint control. DNA Repair (Amst), 3, 1071–1079.
72. Syljuasen, R. G., Sorensen, C. S., Hansen, L. T., Fugger, K., Lundin, C., Johansson, F., Helleday, T., Sehested, M., Lukas, J., and Bartek, J. (2005) Inhibition of human Chk1 causes increased initiation of DNA replication, phosphorylation of ATR targets, and DNA breakage. Mol Cell Biol, 25, 3553–3562.
73. Tanaka, S., Tak, Y. S., and Araki, H. (2007a) The role of CDK in the initiation step of DNA replication in eukaryotes. Cell Div, 2, 16.
74. Tanaka, S., Umemori, T., Hirai, K., Muramatsu, S., Kamimura, Y., and Araki, H. (2007b) CDK-dependent phosphorylation of Sld2 and Sld3 initiates DNA replication in budding yeast. Nature, 445, 328–332.
75. Thelen, M. P., Venclovas, C., and Fidelis, K. (1999) A sliding clamp model for the Rad1 family of cell cycle checkpoint proteins. Cell, 96, 769–770.
76. Toledo, L. I., Murga, M., Gutierrez-Martinez, P., Soria, R., and Fernandez-Capetillo, O. (2008) ATR signaling can drive cells into senescence in the absence of DNA breaks. Genes Dev, 22, 297–302.
77. Usskilat, C., Skerka, C., Saluz, H. P., and Hanel, F. (2006) The transcription factor Egr-1 is a regulator of the human TopBP1 gene. Gene, 380, 144–150
78. van Hatten, R. A., Tutter, A. V., Holway, A. H., Khederian, A. M., Walter, J. C., and Michael, W. M. (2002) The Xenopus Xmus101 protein is required for the recruitment of Cdc45 to origins of DNA replication. J Cell Biol, 159, 541–547.
79. Wilsker, D., Petermann, E., Helleday, T., and Bunz, F. (2008) Essential function of Chk1 can be uncoupled from DNA damage checkpoint and replication control. Proc Natl Acad Sci USA, 105, 20752–20757.
80. Wollmann, Y., Schmidt, U., Wieland, G. D., Zipfel, P. F., Saluz, H. P., and Hanel, F. (2007) The DNA topoisomerase IIbeta binding protein 1 (TopBP1) interacts with poly (ADP-ribose) polymerase (PARP-1). J Cell Biochem, 102, 171–182.
81. Woodhouse, B. C. and Dianov, G. L. (2008) Poly ADP-ribose polymerase-1: an international molecule of mystery. DNA Repair (Amst), 7, 1077–1086.
82. Wright, R. H., Dornan, E. S., Donaldson, M. M., and Morgan, I. M. (2006) TopBP1 contains a transcriptional activation domain suppressed by two adjacent BRCT domains. Biochem J, 400, 573–582.
83. Xu, Z. X., Timanova-Atanasova, A., Zhao, R. X., and Chang, K. S. (2003) PML colocalizes with and stabilizes the DNA damage response protein TopBP1. Mol Cell Biol, 23, 4247–4256.
84. Yamamoto, R. R., Axton, J. M., Yamamoto, Y., Saunders, R. D., Glover, D. M., and Henderson, D. S. (2000) The Drosophila mus101 gene, which links DNA repair, replication and condensation of heterochromatin in mitosis, encodes a protein with seven BRCA1 C-terminus domains. Genetics, 156, 711–721.
85. Yamane, K., Chen, J., and Kinsella, T. J. (2003) Both DNA topoisomerase II-binding protein 1 and BRCA1 regulate the G2-M cell cycle checkpoint. Cancer Res, 63, 3049–3053.
86. Yamane, K., Kawabata, M., and Tsuruo, T. (1997) A DNA-topoisomerase-II-binding protein with eight repeating regions similar to DNA-repair enzymes and to a cell-cycle regulator. Eur J Biochem, 250, 794–799.
87. Yamane, K. and Tsuruo, T. (1999) Conserved BRCT regions of TopBP1 and of the tumor suppressor BRCA1 bind strand breaks and termini of DNA. Oncogene, 18, 5194–5203.
88. Yamane, K., Wu, X., and Chen, J. (2002) A DNA damage-regulated BRCT-containing protein, TopBP1, is required for cell survival. Mol Cell Biol, 22, 555–566.
89. Yan, S., Lindsay, H. D., and Michael, W. M. (2006) Direct requirement for Xmus101 in ATR-mediated phosphorylation of Claspin bound Chk1 during checkpoint signaling. J Cell Biol, 173, 181–186.
90. Yang, S. Z., Lin, F. T., and Lin, W. C. (2008) MCPH1/BRIT1 cooperates with E2F1 in the activation of checkpoint, DNA repair and apoptosis. EMBO Rep, 9, 907–915.
91. Yoo, H. Y., Kumagai, A., Shevchenko, A., Shevchenko, A., and Dunphy, W. G. (2007) Ataxia-telangiectasia mutated (ATM)-dependent activation of ATR occurs through phosphorylation of TopBP1 by ATM. J Biol Chem, 282, 17501–17506.
92. Yoshida, K. (2007) Geminin organizes the molecular platform to balance cellular proliferation and differentiation. Front Biosci, 12, 2984–2992.
93. Yoshida, K. and Inoue, I. (2004) Expression of MCM10 and TopBP1 is regulated by cell proliferation and UV irradiation via the E2F transcription factor. Oncogene, 23, 6250–6260.
94. Yu, X., Chini, C. C., He, M., Mer, G., and Chen, J. (2003) The BRCT domain is a phospho-protein binding domain. Science, 302, 639–642.
95. Zegerman, P. and Diffley, J. F. (2007) Phosphorylation of Sld2 and Sld3 by cyclin-dependent kinases promotes DNA replication in budding yeast. Nature, 445, 281–285.
96. Zeng, L., Hu, Y., and Li, B. (2005) Identification of TopBP1 as a c-Abl-interacting protein and a repressor for c-Abl expression. J Biol Chem, 280, 29374–29380.
97. Zou, H. and Rothstein, R. (1997) Holliday junctions accumulate in replication mutants via a RecA homolog-independent mechanism. Cell, 90, 87–96.