Dynamic interactions of high Cdt1 and geminin levels regulate S phase in early Xenopus embryos

Development

Volumn 139, Issue 1, 2011, Pages 63-74

  Kisielewska, Jolanta ^a   Julian Blow, J ^b  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Cdt1:geminin; DNA replication; Xenopus embryos

Indexed keywords

GEMININ; REPLICATION LICENSING FACTOR CDT1;

ARTICLE; BLASTULA; CELL CYCLE ARREST; CELL CYCLE S PHASE; CELLULAR DISTRIBUTION; CHROMOSOME BREAKAGE; DNA DAMAGE; EMBRYO; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; XENOPUS;

EID: 82855176832     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.068676     Document Type: Article

References (76)

1. Arias, E. E. and Walter, J. C. (2005). Replication-dependent destruction of Cdt1 limits DNA replication to a single round per cell cycle in Xenopus egg extracts. Genes Dev. 19, 114-126.
2. Arias, E. E. and Walter, J. C. (2006). PCNA functions as a molecular platform to trigger Cdt1 destruction and prevent re-replication. Nat. Cell Biol. 8, 84-90.
3. Bell, S. P. (2002). The origin recognition complex: from simple origins to complex functions. Genes Dev. 16, 659-672.
4. Bell, S. P. and Dutta, A. (2001). DNA replication in eukaryotic cells. Annu. Rev. Biochem. 71, 333-374.
5. Blow, J. J. and Dutta, A. (2005). Preventing re-replication of chromosomal DNA. Nat. Rev. Mol. Cell Biol. 6, 476-486.
6. Bulavin, D. V., Demidenko, Z. N., Phillips, C., Moody, S. A. and Fornance, A. J. (2003). Phosphorylation of Xenopus Cdc25C at Ser285 interferes with ability to activate a DNA damage replication checkpoint in pre-midblastula embryos. Cell Cycle 2, 263-266.
7. Cardoso, M. C., Sporbert, A. and Leonhardt, H. (1999). Structure and function in the nucleus: subnuclear trafficking of DNA replication factors. J. Cell Biochem. S32/33, 15-23.
8. Chong, J. P., Thömmes, P., Rowles, A., Mahbubani, H. M. and Blow, J. J. (1997). Characterization of the Xenopus replication licensing system. Methods Enzymol. 283, 549-564.
9. Clute, P. and Masui, Y. (1997). Microtubule dependence of chromosome cycles in Xenopus laevis blastomeres under the influence of a DNA synthesis inhibitor, aphidicolin. Dev. Biol. 185, 1-13.
10. Conn, C. W., Lewellyn, A. L. and Maller, J. L. (2004). The DNA damage checkpoint in embryonic cell cycles is dependent on the DNA-to-cytoplasmic ratio. Dev. Cell 7, 275-281.
11. Davidson, I. F., Li, A. and Blow, J. J. (2006). Deregulated replication licensing causes DNA fragmentation consistent with head-to-tail fork collision. Mol. Cell 24, 433-443.
12. De Marco, V., Gillespie, P. J., Li, A., Karantzelis, N., Christodoulou, E., Klompmaker, R., van Gerven, S., Fish, A., Petoukhov, M. V., Iliou, M. S. et al. (2009). Quaternary structure of the human Cdt1-Geminin complex regulates DNA replication licensing. Proc. Natl. Acad. Sci. USA 106, 19807-19812.
13. Del Bene, F., Tessmar-Raible, K. and Wittbrodt, J. (2004). Direct interaction of geminin and Six3 in eye development. Nature 427, 745-749.
14. DePamphilis, M. L. (2005). Cell cycle dependent regulation of the origin recognition complex. Cell Cycle 4, 70-79.
15. Dimitrova, D. S., Prokhorova, T. A., Blow, J. J., Todorov, I. T. and Gilbert, D. M. (2002). Mammalian nuclei become licensed for DNA replication during late telophase. J. Cell Sci. 115, 51-59.
16. Evrin, C., Clarke, P., Zech, J., Lurz, R., Sun, J., Uhle, S., Li, H., Stillman, B. and Speck, C. (2009). A double-hexameric MCM2-7 complex is loaded onto origin DNA during licensing of eukaryotic DNA replication. Proc. Natl. Acad. Sci. USA 106, 20240-20245.
17. Ferenbach, A., Li, A., Brito-Martins, M. and Blow, J. J. (2005). Functional domains of the Xenopus replication licensing factor Cdt1. Nucleic Acids Res. 33, 316-324.
18. Ferrell, J. E. J. (1999). Xenopus oocyte maturation: new lessons from a good egg. BioEssays 21, 833-842.
19. Gillespie, P. J., Li, A. and Blow, J. J. (2001). Reconstitution of licensed replication origins on Xenopus sperm nuclei using purified proteins. BMC Biochem. 2, 15.
20. Gillespie, P. J., Khudoli, G. A., Stewart, G., Swedlow, J. R. and Blow, J. J. (2007). ELYS/MEL-28 chromatin association coordinates nuclear pore complex assembly and replication licensing. Curr. Biol. 17, 1657-1662.
21. Harlow, E. and Lane, D. (1988). In Antibodies: A Laboratory Manual, pp. 522-523. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
22. Hartley, R. S., Rempel, R. E. and Maller, J. L. (1996). In vivo regulation of the early embryonic cell cycle in Xenopus. Dev. Biol. 173, 408-419.
23. Hodgson, B., Li, A., Tada, S. and Blow, J. J. (2002). Geminin becomes activated as an inhibitor of Cdt1/RLF-B following nuclear import. Curr. Biol. 12, 678-683.
24. Hu, J. and Xiong, Y. (2006). An evolutionarily conserved function of proliferating cell nuclear antigen for Cdt1 degradation by the Cul4-Ddb1 ubiquitin ligase in response to DNA damage. J. Biol. Chem. 281, 3753-3756.
25. Jin, J., Arias, E. E., Chen, J., Harper, J. W. and Walter, J. C. (2006). A family of diverse Cul4-Ddb1-interacting proteins includes Cdt2, which is required for S phase destruction of the replication factor Cdt1. Mol. Cell 23, 709-721.
26. Kerns, S. L., Torke, S. J., Benjamin, J. M. and McGarry, T. J. (2007). Geminin prevents rereplication during Xenopus development. J. Biol. Chem. 282, 5514-5521.
27. Khokha, M. K., Chung, C., Bustamante, E. L., Gaw, L. W., Trott, K. A., Yeh, J., Lim, N., Lin, J. C., Taverner, N., Amaya, E. et al. (2002). Techniques and probes for the study of Xenopus tropicalis development. Dev. Dyn. 225, 499-510.
28. Khudoli, G. A., Gillespie, P. J., Stewart, G., Andersen, J. S., Swedlow, J. R. and Blow, J. J. (2008). Temporal profiling of the chromatin proteome reveals system-wide responses to replication inhibition. Curr. Biol. 18, 838-843.
29. Kim, M. Y., Jeong, B. C., Lee, J. H., Kee, H. J., Kook, H., Kim, N. S., Kim, J. H., Kim, J. K., Ahn, K. J. and Kim, K. K. (2006). A repressor complex, AP4 transcription factor and geminin, negatively regulates expression of target genes in nonneuronal cells. Proc. Natl. Acad. Sci. USA 103, 13074-13079.
30. Kisielewska, J., Lu, P. and Whitaker, M. (2005). GFP-PCNA as an S-phase marker in embryos during the first and subsequent cell cycles. Biol. Cell 97, 221-229.
31. Kisielewska, J., Philipova, R., Huang, J.-Y. and Whitaker, M. (2009). MAP kinase dependent cyclinE/cdk2 activity promotes DNA replication in early sea urchin embryos. Dev. Biol. 334, 383-394.
32. Lavery, D. L. and Hoppler, S. (2008). Analysis of gene expression in Xenopus embryos. Methods Mol. Biol. 469, 335-361.
33. Lee, H. O., Zacharek, S. J. and Duronio, R. J. (2010). Cell type-dependent requirement for PIP box-regulated Cdt1 destruction during S phase. Mol. Biol. Cell 21, 3639-3653.
34. Leibovici, M., Monod, G., Géraudie, J., Bravo, R. and Méchali, M. (1992). Nuclear distribution of PCNA during embryonic development in Xenopus laevis: a reinvestigation of early cell cycles. J. Cell Sci. 102, 63-69.
35. Lemaire, P., Garrett, N. and Gurdon, J. B. (1995). Expression cloning of Siamois, a Xenopus homeobox gene expressed in dorsal-vegetal cells of blastulae and able to induce a complete secondary axis. Cell 81, 85-94.
36. Leonhardt, H., Rahn, H. P., Weinzierl, P., Sporbert, A., Cremer, T., Zink, D. and Cardoso, M. C. (2000). Dynamics of DNA replication factories in living cells. J. Cell Biol. 149, 271-279.
37. Li, A. and Blow, J. J. (2004). Non-proteolytic inactivation of geminin requires CDK-dependent ubiquitination. Nat. Cell Biol. 6, 260-267.
38. Li, A. and Blow, J. J. (2005). Cdt1 downregulation by proteolysis and geminin inhibition prevents DNA re-replication in Xenopus. EMBO J. 24, 395-404.
39. Liu, E., Li, X., Yan, F., Zhao, Q. and Wu, X. (2004). Cyclin-dependent kinases phosphorylate human Cdt1 and induce its degradation. J. Biol. Chem. 279, 17283-17288.
40. Luo, L. and Kessel, M. (2004). Geminin coordinates cell cycle and developmental control. Cell Cycle 3, 711-714.
41. Lutzmann, M., Maiorano, D. and Mechali, M. (2006). A Cdt1-geminin complex licenses chromatin for DNA replication and prevents re-replication during S phase in Xenopus. EMBO J. 25, 5764-5774.
42. Machida, Y. J. and Dutta, A. (2005). Cellular checkpoint mechanisms monitoring proper initiation of DNA replication. J. Biol. Chem. 280, 6253-6256.
43. Maiorano, D., Moreau, J. and Méchali, M. (2000). XCDT1 is required for the assembly of pre-replicative complexes in Xenopus laevis. Nature 404, 622-625.
44. Maiorano, D., Rul, W. and Mechali, M. (2004). Cell cycle regulation of the licensing activity of Cdt1 in Xenopus laevis. Exp. Cell Res. 295, 138-149.
45. Maiorano, D., Krasinska, L., Lutzman, M. and Mechali, M. (2005). Recombinant Cdt1 induces rereplication of G2 nuclei in Xenopus egg extract. Curr. Biol. 15, 146-153.
46. McCleland, M. L., Shermoen, A. W. and O'Farrell, P. H. (2009). DNA replication times the cell cycle and contributes to the mid-blastula transition in Drosophila embryos. J. Cell Biol. 187, 7-14.
47. McGarry, T. J. (2002). Geminin deficiency causes a Chk1-dependent G2 arrest in Xenopus. Mol. Biol. Cell 13, 3662-3671.
48. McGarry, T. J. and Kirshner, M. W. (1998). Geminin, an inhibitor of DNA replication, is degraded during mitosis. Cell 93, 1043-1053.
49. Melixetian, M., Ballabeni, A., Masiero, L., Gasparini, P., Zamponi, R., Bartek, J., Lukas, J. and Helin, K. (2004). Loss of Geminin induces rereplication in the presence of functional p53. J. Cell Biol. 165, 473-482.
50. Menut, S., Lemaitre, J.-M., Hair, A. and Mechali, M. (1999). DNA replication and chromatin assembly using Xenopus eggs and embryos. In Advances in Molecular Biology: A Comparative Methods Approach to the Study of Oocytes and Embryos, pp. 196-226. Oxford, UK: Oxford University Press.
51. Mihaylov, I. S., Kondo, T., Jones, L., Ryzhikov, S., Tanaka, J., Zheng, J., Higa, L. A., Minamino, N. and Cooley, L., Zhang, H. (2002). Control of DNA replication by chromosome ploidy by geminin anf cyclin A. Mol. Cell. Biol. 22, 1868-1880.
52. Newport, J. and Kirshner, M. W. (1982). A major developmental transition in early Xenopus embryos: I. Characterization and Timing of cellular changes at the midblastula stage. Cell 30, 675-686.
53. Nishitani, H., Lygerou, Z., Nishimoto, T. and Nurse, P. (2000). The Cdt1 protein is required to license DNA for replication in fission yeast. Nature 404, 625-628.
54. Nishitani, H., Taraviras, S., Lygerou, Z. and Nishimoto, T. (2001). The human licensing factor for DNA replication Cdt1 accumulates in G1 and is destabilized after initiation of S-phase. J. Biol. Chem. 276, 44905-44911.
55. Nishitani, H., Sugimoto, N., Roukos, V., Nakanishi, Y., Saijo, M., Obuse, C., Tsurimoto, T., Nakayama, K. I., Nakayama, K., Fujita, M. et al. (2006). Two E3 ubiquitin ligases, SCF-Skp2 and DDB1-Cul4, target human Cdt1 for proteolysis. EMBO J. 25, 1126-1136.
56. Ode, K. L., Fujimoto, K., Kubota, Y. and Takisawa, H. (2011). Inter-origin cooperativity of geminin action establishes an all-or-none switch for replication origin licensing. Genes Cells 16, 380-396.
57. Oehlmann, M., Score, A. J. and Blow, J. J. (2004). The role of Cdc6 in ensuring complete genome licensing and S phase checkpoint activation. J. Cell Biol. 165, 181-190.
58. Papanayotou, C., Mey, A., Birot, A. M., Saka, Y., Boast, S., Smith, J. C., Samarut, J. and Stern, C. D. (2008). A mechanism regulating the onset of Sox2 expression in the embryonic neural plate. PLoS Biol. 6, e2.
59. Pefani, D. E., Dimaki, M., Spella, M., Karantzelis, N., Mitsiki, E., Kyrousi, C., Symeonidou, I. E., Perrakis, A., Taraviras, S. and Lygerou, Z. (2011). Idas, a novel phylogenetically conserved geminin-related protein, binds to geminin and is required for cell cycle progression. J. Biol. Chem. 286, 23234-23246.
60. Pitulescu, M., Kessel, M. and Luo, L. (2005). The regulation of embryonic patterning and DNA replication by geminin. Cell. Mol. Life Sci. 62, 1425-1433.
61. Quinn, L. M., Herr, A., McGarry, T. J. and Richardson, H. (2001). The Drosophila geminin homolog: roles for geminin in limiting DNA replication, in anaphase and in neurogenesis. Genes Dev. 15, 2741-2754.
62. Remus, D., Beuron, F., Tolun, G., Griffith, J. D., Morris, E. P. and Diffley, J. F. (2009). Concerted loading of Mcm2-7 double hexamers around DNA during DNA replication origin licensing. Cell 139, 719-730.
63. Sasaki, T. and Gilbert, D. M. (2007). The many faces of the origin recognition complex. Curr. Opin. Cell Biol. 19, 337-343.
64. Senga, T., Sivaprasad, U., Zhu, W., Park, J. H., Arias, E. E., Walter, J. C. and Dutta, A. (2006). PCNA is a cofactor for Cdt1 degradation by CUL4/DDB1- mediated N-terminal ubiquitination. J. Biol. Chem. 281, 6246-6252.
65. Seo, S. and Kroll, K. L. (2006). Chromatin connections that regulate transcription at the transition from proliferation to differentiation. Cell Cycle 5, 374-380.
66. Seo, S., Herr, A., Lim, J.-W., Richardson, G. A., Richardson, H. and Kroll, K. L. (2005). Geminin regulates neuronal differentiation by antagonizing Brg1 activity. Genes Dev. 19, 1723-1734.
67. Shreeram, S., Sparks, A., Lane, D. P. and Blow, J. J. (2002). Cell type-specific responses of human cells to inhibition of replication licensing. Oncogene 21, 6624-6632.
68. Sugimoto, N., Tatsumi, Y., Tsurumi, T., Matsukage, A., Kiyono, T., Nishitani, H. and Fujita, M. (2004). Cdt1 phosphorylation by cyclinA-dependent kinases negatively regulates its function without affecting geminin binding. J. Biol. Chem. 279, 19691-19697.
69. Tada, S., Li, A., Maiorano, D., Mechali, M. and Blow, J. J. (2001). Repression of origin assembly in metaphase depends on inhibition of RLF-B/Cdt1 by geminin. Nat. Cell Biol. 3, 107-113.
70. Tchang, F. and Mechali, M. (1999). Nuclear import of p53 during Xenopus Laevis early development in relation to DNA replication and DNA repair. Exp. Cell Res. 251, 46-56.
71. Tsakraklides, V. and Bell, S. P. (2010). Dynamics of pre-replicative complex assembly. J. Biol. Chem. 285, 9437-9443.
72. Vaziri, C., Saxena, S., Jeon, Y., Lee, C., Murata, K., Machida, Y., Wagle, N., Hwang, D. S. and Dutta, A. (2003). A p-53-depandent checkpoint pathway prevents rereplication. Mol. Cell 11, 997-1008.
73. Whittaker, A. J., Royzman, I. and Orr-Weaver, T. L. (2000). Drosophila double parked: a conserved, essential replication protein that colocalizes with the origin recognition complex and links DNA replication with mitosis and the down- regulation of S phase transcripts. Genes Dev. 14, 1765-1776.
74. Wohlschlegel, J. A., Dwyer, B. T., Dhar, S. K., Cvetic, C., Walter, J. C. and Dutta, A. (2000). Inhibition of eucaryotic DNA replication by geminin binding to Cdt1. Science 290, 2309-2312.
75. Wohlschlegel, J. A., Kutok, J. L., Weng, A. P. and Dutta, A. (2002). Expression of geminin as a marker of cell proliferation in normal tissues and malignances. Am. J. Pathol. 161, 267-273.
76. Yoshida, K., Takisawa, H. and Kubota, Y. (2005). Intrinsic nuclear import activity of geminin is essential to prevent re-initiation of DNA replication in Xenopus eggs. Genes Cells 10, 63-73.