Cdc14p resets the competency of replication licensing by dephosphorylating multiple initiation proteins during mitotic exit in budding yeast

Journal of Cell Science

Volumn 123, Issue 22, 2010, Pages 3933-3943

  Zhai, Yuanliang ^a   Yung, Philip Y K ^a   Huo, Lin ^a   Liang, Chun ^a  

^a HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

Author keywords

Budding yeast; Cdc14p phosphatase; Cell cycle; DNA replication; Replication licensing; Replication initiation proteins

Indexed keywords

CELL CYCLE PROTEIN 6; CYCLIN DEPENDENT KINASE; INITIATION FACTOR; PHOSPHOPROTEIN PHOSPHATASE CDC14;

ARTICLE; BUDDING; CELL CYCLE; CONTROLLED STUDY; DEPHOSPHORYLATION; DNA REPLICATION; ENZYME ACTIVITY; ENZYME SUBSTRATE; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SACCHAROMYCES CEREVISIAE;

CELL CYCLE; CELL CYCLE PROTEINS; CELL NUCLEUS; DNA REPLICATION; DNA, FUNGAL; MITOSIS; PHOSPHORYLATION; PROTEIN TYROSINE PHOSPHATASES; REPLICATION ORIGIN; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EUKARYOTA; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

EID: 78349244870     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.075366     Document Type: Article

References (53)

1. Amon, A. (2008). A decade of Cdc14-A personal perspective delivered on 9 July 2007 at the 32nd FEBS congress in Vienna, Austria. FEBS J. 275, 5774-5784.
2. Archambault, V., Li, C. X., Tackett, A. J., Wasch, R., Chait, B. T., Rout, M. P. and Cross, F. R. (2003). Genetic and biochemical evaluation of the importance of Cdc6 in regulating mitotic exit. Mol. Biol. Cell 14, 4592-4604.
3. Arias, E. E. and Walter, J. C. (2007). Strength in numbers: preventing rereplication via multiple mechanisms in eukaryotic cells. Genes Dev. 21, 497-518.
4. Azzam, R., Chen, S. L., Shou, W., Mah, A. S., Alexandru, G., Nasmyth, K., Annan, R. S., Carr, S. A. and Deshaies, R. J. (2004). Phosphorylation by cyclin B-Cdk underlies release of mitotic exit activator Cdc14 from the nucleolus. Science 305, 516-519.
5. Bell, S. P. and Dutta, A. (2002). DNA replication in eukaryotic cells. Annu. Rev. Biochem. 71, 333-374.
6. Bishop, A. C., Ubersax, J. A., Petsch, D. T., Matheos, D. P., Gray, N. S., Blethrow, J., Shimizu, E., Tsien, J. Z., Schultz, P. G., Rose, M. D. et al. (2000). A chemical switch for inhibitor-sensitive alleles of any protein kinase. Nature 407, 395-401.
7. Bloom, J. and Cross, F. R. (2007). Novel role for Cdc14 sequestration: Cdc14 dephosphorylates factors that promote DNA replication. Mol. Biol. Cell 27, 842-853.
8. Cheng, X., Xu, Z., Wang, J. F., Zhai, Y. L, Lu, Y. J. and Liang, C. (2010). ATP-dependent pre-replicative complex assembly is facilitated by Adk1p in budding yeast. J. Biol. Chem. 285, 29974-29980.
9. Clemente-Blanco, A., Mayan-Santos, M., Schneider, D. A., Machin, F., Jarmuz, A., Tschochner, H. and Aragon, L. (2009). Cdc14 inhibits transcription by RNA polymerase I during anaphase. Nature 458, 219-222.
10. Dahmann, C., Diffley, J. F. and Nasmyth, K. A. (1995). S-phase-promoting cyclin-dependent kinases prevent re-replication by inhibiting the transition of replication origins to a pre-replicative state. Curr. Biol. 5, 1257-1269.
11. Devault, A., Gueydon, E. and Schwob, E. (2008). Interplay between S-cyclin-dependent kinase and Dbf4-dependent kinase in controlling DNA replication through phosphorylation of yeast Mcm4 N-terminal domain. Mol. Biol. Cell 19, 2267-2277.
12. Diffley, J. F. X. (2004). Regulation of early events in chromosome replication. Curr. Biol. 14, R778-R786.
13. Dohmen, R. J., Wu, P. and Varshavsky, A. (1994). Heat-inducible degron: A method for constructing temperature-sensitive mutants. Science 263, 1273-1276.
14. Dulev, S., de Renty, C., Mehta, R., Minkov, I., Schwob, E. and Strunnikov, A. (2009). Essential global role of CDC14 in DNA synthesis revealed by chromosome underreplication unrecognized by checkpoints in cdc14 mutants. Proc. Natl. Acad. Sci. USA 106, 14466-14471.
15. Hall, M. C., Jeong, D. E., Henderson, J. T., Choi, E., Bremmer, S. C., Iliuk, A. B. and Charbonneau, H. (2008). Cdc28 and Cdc14 control stability of the anaphase-promoting complex inhibitor Acm1. J. Biol. Chem. 283, 10396-10407.
16. Hardy, C. F. J. (1996). Characterization of an essential Orc2p-associated factor that plays a role in DNA replication. Mol. Biol. Cell 16, 1832-1841.
17. Hogan, E. and Koshland, D. (1992). Addition of extra origins of replication to a minichromosome suppresses its mitotic loss in cdc6 and cdc14 mutants of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 89, 3098-3102.
18. Hook, S. S., Lin, J. J. and Dutta, A. (2007). Mechanisms to control rereplication and implications for cancer. Curr. Opin. Cell Biol. 19, 663-671.
19. Janke, C., Magiera, M. M., Rathfelder, N., Taxis, C., Reber, S., Maekawa, H., Moreno-Borchart, A., Doenges, G., Schwob, E., Schiebel, E. et al. (2004). A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21, 947-962.
20. Jaspersen, S. L. and Morgan, D. O. (2000). Cdc14 activates Cdc15 to promote mitotic exit in budding yeast. Curr. Biol. 10, 615-618.
21. Jaspersen, S. L., Charles, J. F., Tinker-Kulberg, R. L. and Morgan, D. O. (1998). A late mitotic regulatory network controlling cyclin destruction in Saccharomyces cerevisiae. Mol. Biol. Cell 9, 2803-2817.
22. Jaspersen, S. L., Charles, J. F. and Morgan, D. O. (1999). Inhibitory phosphorylation of the APC regulator Hct1 is controlled by the kinase Cdc28 and the phosphatase Cdc14. Curr. Biol. 9, 227-236.
23. Kinoshita, E., Kinoshita-Kikuta, E. and Koike, T. (2009). Separation and detection of large phosphoproteins using Phos-tag SDS-PAGE. Nat. Protoc. 4, 1513-1521.
24. Kroll, E. S., Hyland, K. M., Hieter, P. and Li, J. J. (1996). Establishing genetic interactions by a synthetic dosage lethality phenotype. Genetics 143, 95-102.
25. Lengronne, A. and Schwob, E. (2002). The yeast CDK inhibitor Sic1 prevents genomic instability by promoting replication origin licensing in late G1. Mol. Cell 9, 1067-1078.
26. Liang, C. and Stillman, B. (1997). Persistent initiation of DNA replication and chromatin-bound MCM proteins during the cell cycle in cdc6 mutants. Genes Dev. 11, 3375-3386.
27. Liku, M. E., Nguyen, V. Q., Rosales, A. W., Irie, K. and Li, J. J. (2005). CDK phosphorylation of a novel NLS-NES module distributed between two subunits of the Mcm2-7 complex prevents chromosomal rereplication. Mol. Biol. Cell 16, 5026-5039.
28. Longtine, M. S., McKenzie, A., III, Demarini, D. J., Shah, N. G., Wach, A., Brachat, A., Philippsen, P. and Pringle, J. R. (1998). Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961.
29. Loo, S., Fox, C. A., Rine, J., Kobayashi, R., Stillman, B. and Bell, S. (1995). The origin recognition complex in silencing, cell cycle progression, and DNA replication. Mol. Biol. Cell 6, 741-756.
30. Lu, Y. and Cross, F. (2009). Mitotic exit in the absence of separase activity. Mol. Biol. Cell 20, 1576-1591.
31. Ma, L. J., Zhai, Y. L., Feng, D. R., Chan, T. C., Lu, J. L., Fu, X. R., Wang, J. F., Chen, Y. H., Li, J. N., Xu, K. and Liang, C. (2010). Identification of novel factors involved in or regulating initiation of DNA replication by a phenotypic screen in Saccharomyces cerevisiae. Cell Cycle (in press).
32. Machin, F., Torres-Rosell, J., De Piccoli, G., Carballo, J. A., Cha, R. S., Jarmuz, A. and Aragon, L. (2006). Transcription of ribosomal genes can cause nondisjunction. J. Cell Biol. 173, 893-903.
33. Makise, M., Takehara, M., Kuniyasu, A., Matsui, N., Nakayama, H. and Mizushima, T. (2009). Linkage between phosphorylation of the origin recognition complex and its ATP binding activity in Saccharomyces cerevisiae. J. Biol. Chem. 284, 3396-3407.
34. Miller, C. T., Gabrielse, C., Chen, Y. C. and Weinreich, M. (2009). Cdc7p-Dbf4p regulates mitotic exit by inhibiting polo kinase. PLoS Genet. 5, e1000498.
35. Mimura, S., Seki, T., Tanaka, S. and Diffley, J. F. X. (2004). Phosphorylation-dependent binding of mitotic cyclins to Cdc6 contributes to DNA replication control. Nature 431, 1118-1123.
36. Nguyen, V. Q., Co, C., Irie, K. and Li, J. J. (2000). Clb/Cdc28 kinases promote nuclear export of the replication initiator proteins Mcm2-7. Curr. Biol. 10, 195-205.
37. Nguyen, V. Q., Co, C. and Li, J. J. (2001). Cyclin-dependent kinases prevent DNA rereplication through multiple mechanisms. Nature 411, 1068-1073.
38. Noton, E. A. and Diffley, J. F. X. (2000). CDK inactivation is the only essential function of the APC/C and the mitotic exit network proteins for origin resetting during mitosis. Mol. Cell 5, 85-95.
39. Pereira, G., Manson, C., Grindlay, J. and Schiebel, E. (2002). Regulation of the Bfa1p-Bub2p complex at spindle pole bodies by the cell cycle phosphatase Cdc14p. J. Cell Biol. 157, 367-379.
40. Perkins, G., Drury, L. S. and Diffley, J. F. X. (2001). Separate SCFCDC4 recognition elements target Cdc6 for proteolysis in S phase and mitosis. EMBO J. 20, 4836-4845.
41. Piatti, S., Lengauer, C. and Nasmyth, K. (1995). Cdc6 is an unstable protein whose de novo synthesis in G1 is important for the onset of S phase and for preventing a 'reductional' anaphase in the budding yeast Saccharomyces cerevisiae. EMBO J. 14, 3788-3799.
42. Sanchez-Diaz, A., Kanemaki, M., Marchesi, V. and Labib, K. (2004). Rapid depletion of budding yeast proteins by fusion to a heat-inducible degron. Sci. STKE 2004.
43. Shima, N., Alcaraz, A., Liachko, I., Buske, T. R., Andrews, C. A., Munroe, R. J., Hartford, S. A., Tye, B. K. and Schimenti, J. C. (2007). A viable allele of Mcm4 causes chromosome instability and mammary adenocarcinomas in mice. Nat. Genet. 39, 93-98.
44. Stegmeier, F. and Amon, A. (2004). Closing mitosis: the functions of the Cdc14 phosphatase and its regulation. Annu. Rev. Genet. 38, 203-232.
45. Sullivan, M. and Morgan, D. O. (2007). Finishing mitosis, one step at a time. Nat. Rev. Mol. Cell Biol. 8, 894-903.
46. Tye, B. K. (1999). Minichromosome maintenance as a genetic assay for defects in DNA replication. Methods 18, 329-334.
47. Ubersax, J. A., Woodbury, E. L., Quang, P. N., Paraz, M., Blethrow, J. D., Shah, K., Shokat, K. M. and Morgan, D. O. (2003). Targets of the cyclin-dependent kinase Cdk1. Nature 425, 859-864.
48. Verma, R., Annan, R. S., Huddleston, M. J., Carr, S. A., Reynard, G. and Deshaies R. J. (1997). Phosphoregulation of Sic1p by G1 Cdk required for its degradation and entry into S phase. Science 278, 455-460.
49. Visintin, R., Craig, K., Hwang, E. S., Prinz, S., Tyers, M. and Amon, A. (1998). The phosphatase Cdc14 triggers mitotic exit by reversal of Cdk-dependent phosphorylation. Mol. Cell 2, 709-718.
50. Wang, J. F., Wu, R. T., Lu, Y. J. and Liang, C. (2010). Ctf4p facilitates Mcm10p to promote DNA replication in budding yeast. Biochem. Biophys. Res. Commun. 395, 336-341.
51. Yuste-Rojas, M. and Cross, F. R. (2000). Mutations in CDC14 results in high sensitivity to cyclin gene dosage in Saccharomyces cerevisiae. Mol. Gen. Genet. 263, 60-72.
52. Zhang, Y., Yu, Z., Fu, X. and Liang, C. (2002). Noc3p, a bHLH protein, plays an integral role in the initiation of DNA replication in budding yeast. Cell 109, 849-860.
53. Zou, L., Mitchell, J. and Stillman, B. (1997). CDC45, a novel yeast gene that functions with the origin recognition complex and Mcm proteins in initiation of DNA replication. Mol. Cell. Biol. 17, 553-563.