Re-replication induced by geminin depletion occurs from G2 and is enhanced by checkpoint activation

Journal of Cell Science

Volumn 125, Issue 10, 2012, Pages 2436-2445

  Klotz Noack, Kathleen ^a   McIntosh, Debbie ^a   Schurch, Nicholas ^a   Pratt, Norman ^b   Blow, J Julian ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b NINEWELLS HOSPITAL   (United Kingdom)

Author keywords

Deep sequencing; DNA replication; Geminin; Re replication; Replication licensing

Indexed keywords

ATM PROTEIN; ATR PROTEIN; CHECKPOINT KINASE 1; DNA; GEMININ; REPLICATION LICENSING FACTOR CDT1;

ARTICLE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL DEATH; CELL LINE; CELL PROLIFERATION; CELL SYNCHRONIZATION; CONTROLLED STUDY; DNA RE-REPLICATION; DNA REPLICATION; DNA SEQUENCE; ECHIDNA; FLOW CYTOMETRY; G2 PHASE CELL CYCLE CHECKPOINT; GENOME; HUMAN; HUMAN CELL; M PHASE CELL CYCLE CHECKPOINT; MITOSIS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL;

CELL CYCLE CHECKPOINTS; CELL CYCLE PROTEINS; CELL LINE, TUMOR; CELLS; DNA REPLICATION; G2 PHASE; GEMININ; HUMANS; MINICHROMOSOME MAINTENANCE COMPLEX COMPONENT 2; NUCLEAR PROTEINS; S PHASE;

ANIMALIA;

EID: 84864822578     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.100883     Document Type: Article

References (52)

1. 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.
2. Arias, E. E. and Walter, J. C. (2007). Strength in numbers: preventing rereplication via multiple mechanisms in eukaryotic cells. Genes Dev. 21, 497-518.
3. Ballabeni, A., Melixetian, M., Zamponi, R., Masiero, L., Marinoni, F. and Helin, K. (2004). Human geminin promotes pre-RC formation and DNA replication by stabilizing CDT1 in mitosis. EMBO J. 23, 3122-3132.
4. Blow, J. J. and Dutta, A. (2005). Preventing re-replication of chromosomal DNA. Nat. Rev. Mol. Cell Biol. 6, 476-486.
5. Blow, J. J. and Gillespie, P. J. (2008). Replication licensing and cancer--a fatal entanglement? Nat. Rev. Cancer 8, 799-806.
6. Blow, J. J., Ge, X. Q. and Jackson, D. A. (2011). How dormant origins promote complete genome replication. Trends Biochem. Sci. 36, 405-414.
7. 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.
8. De Marco, V., Gillespie, P. J., Li, A., Karantzelis, N., Christodoulou, E., Klompmaker, R., van Gerwen, 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.
9. DePamphilis, M. L., Blow, J. J., Ghosh, S., Saha, T., Noguchi, K. and Vassilev, A. (2006). Regulating the licensing of DNA replication origins in metazoa. Curr. Opin. Cell Biol. 18, 231-239.
10. Ding, Q. and MacAlpine, D. M. (2010). Preferential re-replication of Drosophila heterochromatin in the absence of geminin. PLoS Genet. 6, e1001112.
11. 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.
12. Gambus, A., Khoudoli, G. A., Jones, R. C. and Blow, J. J. (2011). MCM2-7 form double hexamers at licensed origins in Xenopus egg extract. J. Biol. Chem. 286, 11855-11864.
13. Ge, X. Q. and Blow, J. J. (2010). Chk1 inhibits replication factory activation but allows dormant origin firing in existing factories. J. Cell Biol. 191, 1285-1297.
14. Ge, X. Q., Jackson, D. A. and Blow, J. J. (2007). Dormant origins licensed by excess Mcm2-7 are required for human cells to survive replicative stress. Genes Dev. 21, 3331-3341.
15. 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.
16. Green, B. M. and Li, J. J. (2005). Loss of rereplication control in Saccharomyces cerevisiae results in extensive DNA damage. Mol. Biol. Cell 16, 421-432.
17. Green, B. M., Morreale, R. J., Ozaydin, B., Derisi, J. L. and Li, J. J. (2006). Genome-wide mapping of DNA synthesis in Saccharomyces cerevisiae reveals that mechanisms preventing reinitiation of DNA replication are not redundant. Mol. Biol. Cell 17, 2401-2414.
18. Green, B. M., Finn, K. J. and Li, J. J. (2010). Loss of DNA replication control is a potent inducer of gene amplification. Science 329, 943-946.
19. Hall, J. R., Lee, H. O., Bunker, B. D., Dorn, E. S., Rogers, G. C., Duronio, R. J. and Cook, J. G. (2008). Cdt1 and Cdc6 are destabilized by rereplication-induced DNA damage. J. Biol. Chem. 283, 25356-25363.
20. 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.
21. Kisielewska, J. and Blow, J. J. (2012). Dynamic interactions of high Cdt1 and geminin levels regulate S phase in early Xenopus embryos. Development 139, 63-74.
22. Lee, A. Y., Liu, E. and Wu, X. (2007). The Mre11/Rad50/Nbs1 complex plays an important role in the prevention of DNA rereplication in mammalian cells. J. Biol. Chem. 282, 32243-32255.
23. Lee, H. O., Zacharek, S. J., Xiong, Y. and Duronio, R. J. (2010). Cell type-dependent requirement for PIP box-regulated Cdt1 destruction during S phase. Mol. Biol. Cell 21, 3639-3653.
24. Li, A. and Blow, J. J. (2004). Non-proteolytic inactivation of geminin requires CDKdependent ubiquitination. Nat. Cell Biol. 6, 260-267.
25. 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.
26. Li, X., Zhao, Q., Liao, R., Sun, P. and Wu, X. (2003). The SCF(Skp2) ubiquitin ligase complex interacts with the human replication licensing factor Cdt1 and regulates Cdt1 degradation. J. Biol. Chem. 278, 30854-30858.
27. Lin, J. J. and Dutta, A. (2007). ATR pathway is the primary pathway for activating G2/M checkpoint induction after re-replication. J. Biol. Chem. 282, 30357-30362.
28. Lin, J. J., Milhollen, M. A., Smith, P. G., Narayanan, U. and Dutta, A. (2010). NEDD8-targeting drug MLN4924 elicits DNA rereplication by stabilizing Cdt1 in S phase, triggering checkpoint activation, apoptosis, and senescence in cancer cells. Cancer Res. 70, 10310-10320.
29. Liu, E., Lee, A. Y., Chiba, T., Olson, E., Sun, P. and Wu, X. (2007). The ATRmediated S phase checkpoint prevents rereplication in mammalian cells when licensing control is disrupted. J. Cell Biol. 179, 643-657.
30. Lu, J., Li, F., Murphy, C. S., Davidson, M. W. and Gilbert, D. M. (2010). G2 phase chromatin lacks determinants of replication timing. J. Cell Biol. 189, 967-980.
31. Lutzmann, M., Maiorano, D. and Méchali, M. (2006). A Cdt1-geminin complex licenses chromatin for DNA replication and prevents rereplication during S phase in Xenopus. EMBO J. 25, 5764-5774.
32. Maiorano, D., Krasinska, L., Lutzmann, M. and Mechali, M. (2005). Recombinant Cdt1 induces rereplication of G2 nuclei in Xenopus egg extracts. Curr. Biol. 15, 146-153.
33. McGarry, T. J. and Kirschner, M. W. (1998). Geminin, an inhibitor of DNA replication, is degraded during mitosis. Cell 93, 1043-1053.
34. 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.
35. Mihaylov, I. S., Kondo, T., Jones, L., Ryzhikov, S., Tanaka, J., Zheng, J., Higa, L. A., Minamino, N., Cooley, L. and Zhang, H. (2002). Control of DNA replication and chromosome ploidy by geminin and cyclin A. Mol. Cell. Biol. 22, 1868-1880.
36. Milhollen, M. A., Narayanan, U., Soucy, T. A., Veiby, P. O., Smith, P. G. and Amidon, B. (2011). Inhibition of NEDD8-activating enzyme induces rereplication and apoptosis in human tumor cells consistent with deregulating CDT1 turnover. Cancer Res. 71, 3042-3051.
37. Nishitani, H., Lygerou, Z. and Nishimoto, T. (2004). Proteolysis of DNA replication licensing factor Cdt1 in S-phase is performed independently of geminin through its N-terminal region. J. Biol. Chem. 279, 30807-30816.
38. 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.
39. 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.
40. 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.
41. Soucy, T. A., Smith, P. G., Milhollen, M. A., Berger, A. J., Gavin, J. M., Adhikari, S., Brownell, J. E., Burke, K. E., Cardin, D. P., Critchley, S. et al. (2009). An inhibitor of NEDD8-activating enzyme as a new approach to treat cancer. Nature 458, 732-736.
42. Sugimoto, N., Tatsumi, Y., Tsurumi, T., Matsukage, A., Kiyono, T., Nishitani, H. and Fujita, M. (2004). Cdt1 phosphorylation by cyclin A-dependent kinases negatively regulates its function without affecting geminin binding. J. Biol. Chem. 279, 19691-19697.
43. Tada, S., Li, A., Maiorano, D., Méchali, 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.
44. Thomer, M., May, N. R., Aggarwal, B. D., Kwok, G. and Calvi, B. R. (2004). Drosophila double-parked is sufficient to induce re-replication during development and is regulated by cyclin E/CDK2. Development 131, 4807-4818.
45. van Koningsbruggen, S., Gierlinski, M., Schofield, P., Martin, D., Barton, G. J., Ariyurek, Y., den Dunnen, J. T. and Lamond, A. I. (2010). High-resolution wholegenome sequencing reveals that specific chromatin domains from most human chromosomes associate with nucleoli. Mol. Biol. Cell 21, 3735-3748.
46. Vaziri, C., Saxena, S., Jeon, Y., Lee, C., Murata, K., Machida, Y., Wagle, N., Hwang, D. S. and Dutta, A. (2003). A p53-dependent checkpoint pathway prevents rereplication. Mol. Cell 11, 997-1008.
47. Wohlschlegel, J. A., Dwyer, B. T., Dhar, S. K., Cvetic, C., Walter, J. C. and Dutta, A. (2000). Inhibition of eukaryotic DNA replication by geminin binding to Cdt1. Science 290, 2309-2312.
48. Yang, V. S., Carter, S. A., Hyland, S. J., Tachibana-Konwalski, K., Laskey, R. A. and Gonzalez, M. A. (2011). Geminin escapes degradation in G1 of mouse pluripotent cells and mediates the expression of Oct4, Sox2, and Nanog. Curr. Biol. 21, 692-699.
49. Zhong, W., Feng, H., Santiago, F. E. and Kipreos, E. T. (2003). CUL-4 ubiquitin ligase maintains genome stability by restraining DNA-replication licensing. Nature 423, 885-889.
50. Zhu, W. and Dutta, A. (2006). An ATR- and BRCA1-mediated Fanconi anemia pathway is required for activating the G2/M checkpoint and DNA damage repair upon rereplication. Mol. Cell. Biol. 26, 4601-4611.
51. Zhu, W. and DePamphilis, M. L. (2009). Selective killing of cancer cells by suppression of geminin activity. Cancer Res. 69, 4870-4877.
52. Zhu, W., Chen, Y. and Dutta, A. (2004). Rereplication by depletion of geminin is seen regardless of p53 status and activates a G2/M checkpoint. Mol. Cell. Biol. 24, 7140-7150.