The role of Cdc6 in ensuring complete genome licensing and S phase checkpoint activation

Journal of Cell Biology

Volumn 165, Issue 2, 2004, Pages 181-190

  Oehlmann, Maren ^a   Score, Alan J ^a   Blow, J Julian ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Cdc6; Chk1; DNA replication; Replication licensing; Xenopus

Indexed keywords

CELL CYCLE PROTEIN; CELL CYCLE PROTEIN 6; CHECKPOINT KINASE 2; MINICHROMOSOME MAINTENANCE PROTEIN; PROTEIN MCM2 7; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CYCLE S PHASE; CELL DIFFERENTIATION; CELL DIVISION; CELLULAR DISTRIBUTION; CHROMOSOME DUPLICATION; DNA REPLICATION; EXTRACT; GENE LIBRARY; GENOME ANALYSIS; NONHUMAN; PRIORITY JOURNAL; RECEPTOR AFFINITY; XENOPUS;

ANIMALS; APHIDICOLIN; CELL CYCLE PROTEINS; CHROMATIN; DNA REPLICATION; DNA-BINDING PROTEINS; ENZYME ACTIVATION; ENZYME INHIBITORS; FEMALE; GENOME; HUMANS; MALE; MODELS, GENETIC; NUCLEAR PROTEINS; OOCYTES; ORIGIN RECOGNITION COMPLEX; PROTEIN BINDING; PROTEIN KINASES; PROTEIN STRUCTURE, QUATERNARY; PROTEIN SUBUNITS; REPLICATION ORIGIN; S PHASE; SACCHAROMYCES CEREVISIAE PROTEINS; SPERMATOZOA; XENOPUS LAEVIS;

ANIMALIA;

EID: 2142808749     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200311044     Document Type: Article

References (61)

1. Alexandrow, M.G., and J.L. Hamlin. 2004. Cdc6 chromatin affinity is unaffected by serine-54 phosphorylation, S-phase progression, and overexpression of cyclin A. Mol. Cell. Biol. 24:1614-1627.
2. Baum, B., H. Nishitani, S. Yanow, and P. Nurse. 1998. Cdc18 transcription and proteolysis couple S phase to passage through mitosis. EMBO J. 17:5689-5698.
3. Blow, J.J. 2001. Control of chromosomal DNA replication in the early Xenopus embryo. EMBO J. 20:3293-3297.
4. Blow, J.J., P.J. Gillespie, D. Francis, and D.A. Jackson. 2001. Replication origins in Xenopus egg extract are 5-15 kilobases apart and are activated in clusters that fire at different times. J. Cell Biol 152:15-25.
5. Blow, J.J., and B. Hodgson. 2002. Replication licensing-defining the proliferative state? Trends Cell Biol. 12:72-78.
6. Brown, G.W., P.V. Jallepalli, B.J. Huneycutt, and T.J. Kelly. 1997. Interaction of the S phase regulator cdc18 with cyclin-dependent kinase in fission yeast. Proc. Natl. Acad. Sci. USA. 94:6142-6147.
7. Calzada, A., M. Sacristan, E. Sanchez, and A. Bueno. 2001. Cdc6 cooperates with Sic1 and Hct1 to inactivate mitotic cyclin-dependent kinases. Nature. 412:355-358.
8. Chong, J.P., H.M. Mahbubani, C.Y. Khoo, and J.J Blow. 1995. Purification of an MCM-containing complex as a component of the DNA replication licensing system. Nature. 375:418-421.
9. Chong, J.P., P. Thömmes, A. Rowles, H.M. Mahbubani, and J.J. Blow. 1997. Characterization of the Xenopus replication licensing system. Methods Enzymol. 283:549-564.
10. Clay-Farrace, L., C. Pelizon, D. Santamaria, J. Pines, and R.A. Laskey. 2003. Human replication protein Cdc6 prevents mitosis through a checkpoint mechanism that implicates Chk1. EMBO J. 22:704-712.
11. Coleman, T.R., P.B. Carpenter, and W.G. Dunphy. 1996. The Xenopus Cdc6 protein is essential for the initiation of a single round of DNA replication in cell-free extracts. Cell. 87:53-63.
12. Coverley, D., C. Pelizon, S. Trewick, and R.A. Laskey. 2000. Chromatin-bound Cdc6 persists in S and G(2) phases in human cells, while soluble Cdc6 is destroyed in a cyclin A-cdk2 dependent process. J. Cell Sci. 113:1929-1938.
13. Donovan, S., J. Harwood, L.S. Drury, and J.F. Diffley. 1997. Cdc6p-dependent loading of Mcm proteins onto pre-replicative chromatin in budding yeast. Proc. Natl. Acad. Sci. USA. 94:5611-5616.
14. Drury, L.S., G. Perkins, and J.F.X. Diffley. 1997. The Cdc4/34/53 pathway targets Cdc6p for proteolysis in budding yeast. EMBO J. 16:5966-5976.
15. Drury, L.S., G. Perkins, and J.F.X. Diffley. 2000. The cyclin-dependent kinase Cdc28p regulates distinct modes of Cdc6p proteolysis during the budding yeast cell cycle. Curr. Biol. 10:231-240.
16. Edwards, M.C., A.V. Tutter, C. Cvetic, C.H. Gilbert, T.A. Prokhorova, and J.C. Walter. 2002. MCM2-7 complexes bind chromatin in a distributed pattern surrounding the origin recognition complex in Xenopus egg extracts. J. Biol. Chem. 277:33049-33057.
17. Elsasser, S., F. Lou, B. Wang, J.L. Campbell, and A. Jong. 1996. Interaction between yeast Cdc6 protein and B-type cyclin/Cdc28 kinases. Mol. Biol. Cell. 7:1723-1735.
18. Elsasser, S., Y. Chi, P. Yang, and J.L. Campbell. 1999. Phosphorylation controls timing of Cdc6p destruction: a biochemical analysis. Mol. Biol. Cell. 10:3263-3277.
19. Fletcher, R.J., B.E. Bishop, R.P. Leon, R.A. Sclafani, C.M. Ogata, and X.S. Chen. 2003. The structure and function of MCM from archaeal M. Thermoautotrophicum. Nat. Struct. Biol. 10:160-167.
20. Frolova, N.S., N. Schek, N. Tikhmyanova, and T.R. Coleman. 2002. Xenopus Cdc6 performs separate functions in initiating DNA replication. Mol. Biol. Cell. 13:1298-1312.
21. Fujita, M., Y. Ishimi, H. Nakamura, T. Kiyono, and T. Tsurumi. 2002. Nuclear organization of DNA replication initiation proteins in mammalian cells. J. Biol. Chem. 277:10354-10361.
22. Furstenthal, L., B.K. Kaiser, C. Swanson, and P.K. Jackson. 2001a. Cyclin E uses Cdc6 as a chromatin-associated receptor required for DNA replication. J. Cell Biol. 152:1267-1278.
23. Furstenthal, L., C. Swanson, B.K. Kaiser, A.G. Eldridge, and P.K. Jackson. 2001b. Triggering ubiquitination of a CDK inhibitor at origins of DNA replication. Nat. Cell Biol. 3:715-722.
24. Gillespie, P.J., and J.J. Blow. 2000. Nucleoplasmin-mediated chromatin remodelling is required for Xenopus sperm nuclei to become licensed for DNA replication. Nucleic Acids Res. 28:472-480.
25. Gillespie, P.J., A. Li, and J.J. Blow. 2001. Reconstitution of licensed replication origins on Xenopus sperm nuclei using purified proteins. BMC Biochem. 2:15.
26. Guo, Z., A. Kumagai, S.X. Wang, and W.G. Dunphy. 2000. Requirement for Atr in phosphorylation of Chk1 and cell cycle regulation in response to DNA replication blocks and UV-damaged DNA in Xenopus egg extracts. Genes Dev. 14:2745-2756.
27. Hodgson, B., A. Li, S. Tada, and J.J. Blow. 2002. Geminin becomes activated as an inhibitor of Cdt1/RLF-B following nuclear import. Curr. Biol. 12:678-683.
28. Hua, X.H., and J. Newport. 1998. Identification of a preinitiation step in DNA replication that is independent of origin recognition complex and cdc6, but dependent on cdk2. J. Cell Biol. 140:271-281.
29. Hyrien, O., K. Marheineke, and A. Goldar. 2003. Paradoxes of eukaryotic DNA replication: MCM proteins and the random completion problem. Bioessays. 25:116-125.
30. Jallepalli, P.V., G.W. Brown, M. Muzi-Falconi, D. Tien, and T.J. Kelly. 1997. Regulation of the replication initiator protein p65(cdc18) by CDK phosphorylation. Genes Dev. 11:2767-2779.
31. Jares, P., and J.J. Blow. 2000. Xenopus Cdc7 function is dependent on licensing but not on XORC, XCdc6, or CDK activity and is required for XCdc45 loading. Genes Dev. 14:1528-1540.
32. Kominami, K., and T. Toda. 1997. Fission yeast WD-repeat protein popl regulates genome ploidy through ubiquitin-proteasome-mediated degradation of the CDK inhibitor Rum1 and the S-phase initiator Cdc18. Genes Dev. 11:1548-1560.
33. Kumagai, A., Z. Guo, K.H. Emami, S.X. Wang, and W.G. Dunphy. 1998. The Xenopus Chk1 protein kinase mediates a caffeine-sensitive pathway of checkpoint control in cell-free extracts. J. Cell Biol. 142:1559-1569.
34. Labib, K., and J.F. Diffley. 2001. Is the MCM2-7 complex the eukaryotic DNA replication fork helicase? Curr. Opin. Genet. Dev. 11:64-70.
35. Li, A., and J.J. Blow. 2001. The origin of CDK regulation. Nat. Cell Biol. 3:E182-E184.
36. Li, A., and J.J. Blow. 2004. Non-proteolytic inactivation of geminin requires CDK-dependent ubiquitination. Nat. Cell Biol. 6:260-267.
37. Liu, Q., S. Guntuku, X.S. Cui, S. Matsuoka, D. Cortez, K. Tamai, G. Luo, S. Carattini-Rivera, F. DeMayo, A. Bradley, et al. 2000. Chk1 is an essential kinase that is regulated by Atr and required for the G(2)/M DNA damage checkpoint. Genes Dev. 14:1448-1459.
38. Mahaffey, D.T., C. Gorbea, and M. Rechsteiner. 2003. Evidence that DNA replication is not regulated by ubiquitin-dependent proteolysis in Xenopus egg extract. Exp. Cell Res. 288:225-234.
39. Mahbubani, H.M., J.P. Chong, S. Chevalier, P. Thömmes, and J.J. Blow. 1997. Cell cycle regulation of the replication licensing system: involvement of a Cdk-dependent inhibitor. J. Cell Biol. 136:125-135.
40. Maiorano, D., J. Moreau, and M. Mechali. 2000. XCDT1 is required for the assembly of pre-replicative complexes in Xenopus laevis. Nature. 404:622-625.
41. McGarry, T.J., and M.W. Kirschner. 1998. Geminin, an inhibitor of DNA replication, is degraded during mitosis. Cell. 93:1043-1053.
42. Meijer, L., A. Borgne, O. Mulner, J.P.J. Chong, J.J. Blow, N. Inagaki, M. Inagaki, J.G. Delcros, and J.P. Moulinoux. 1997. Biochemical and cellular effects of roscovitine, a potent and selective inhibitor of the cyclin-dependent kinases cdc2, cdk2 and cdk5. Eur. J. Biochem. 243:527-536.
43. Mendez, J., and B. Stillman. 2000. Chromatin association of human origin recognition complex, Cdc6, and minichromosome maintenance proteins during the cell cycle: Assembly of prereplication complexes in late mitosis. Mol. Cell. Biol. 20:8602-8612.
44. Mizushima, T., N. Takahashi, and B. Stillman. 2000. Cdc6p modulates the structure and DNA binding activity of the origin recognition complex in vitro. Genes Dev. 14:1631-1641.
45. Murakami, H., S.K. Yanow, D. Griffiths, M. Nakanishi, and P. Nurse. 2002. Maintenance of replication forks and the S-phase checkpoint by Cdc18p and Orp1p. Nat. Cell Biol. 4:384-388.
46. Nishitani, H., and Z. Lygerou. 2002. Control of DNA replication licensing in a cell cycle. Genes Cells. 7:523-534.
47. Pelizon, C., M.A. Madine, P. Romanowski, and R.A. Laskey. 2000. Unphosphorylatable mutants of Cdc6 disrupt its nuclear export but still support DNA replication once per cell cycle. Genes Dev. 14:2526-2533.
48. Petersen, B.O., J. Lukas, C.S. Sorensen, J. Bartek, and K. Helin. 1999. Phosphorylation of mammalian CDC6 by cyclin A/CDK2 regulates its subcellular localization. EMBO J. 18:396-410.
49. Petersen, B.O., C. Wagener, F. Marinoni, E.R. Kramer, M. Melixetian, E.L. Denchi, C. Gieffers, C. Matteucci, J.M. Peters, and K. Helin. 2000. Cell cycle-and cell growth-regulated proteolysis of mammalian CDC6 is dependent on APC-CDH1. Genes Dev. 14:2330-2343.
50. Prokhorova, T.A., and J.J. Blow. 2000. Sequential MCM/P1 subcomplex assembly is required to form a heterohexamer with replication licensing activity. J. Biol. Chem. 275:2491-2498.
51. Rowles, A., J.P. Chong, L. Brown, M. Howell, G.I. Evan, and J.J. Blow. 1996. Interaction between the origin recognition complex and the replication licensing system in Xenopus. Cell. 87:287-296.
52. Rowles, A., S. Tada, and J.J. Blow. 1999. Changes in association of the Xenopus origin recognition complex with chromatin on licensing of replication origins. J. Cell Sci. 112:2011-2018.
53. Saha, P., J.J. Chen, K.C. Thome, S.J. Lawlis, Z.H. Hou, M. Hendricks, J.D. Parvin, and A. Dutta. 1998. Human CDC6/Cdc18 associates with Orcl and cyclin-cdk and is selectively eliminated from the nucleus at the onset of S phase. Mol. Cell. Biol. 18:2758-2767.
54. Santocanale, C., and J.F. Diffley. 1998. A Mec1- and Rad53-dependent checkpoint controls late-firing origins of DNA replication. Nature. 395:615-618.
55. Shirahige, K., Y. Hori, K. Shiraishi, M. Yamashita, K. Takahashi, C. Obuse, T. Tsurimoto, and H. Yoshikawa. 1998. Regulation of DNA-replication origins during cell-cycle progression. Nature. 395:618-621.
56. Sun, W.H., T.R. Coleman, and M.L. DePamphilis. 2002. Cell cycle-dependent regulation of the association between origin recognition proteins and somatic cell chromatin. EMBO J. 21:1437-1446.
57. Tada, S., J.P.J. Chong, H.M. Mahbubani, and J.J. Blow. 1999. The RLF-B component of the replication licensing system is distinct from Cdc6 and functions after Cdc6 binds to chromatin. Curr. Biol. 9:211-214.
58. Tada, S., A. Li, D. Maiorano, M. Mechali, and J.J. Blow. 2001. Repression of origin assembly in metaphase depends on inhibition of RLF-B/Cdt1 by geminin. Nat. Cell Biol. 3:107-113.
59. Thömmes, P., Y. Kubota, H. Takisawa, and J.J. Blow. 1997. The RLF-M component of the replication licensing system forms complexes containing all six MCM/P1 polypeptides. EMBO J. 16:3312-3319.
60. Wohlschlegel, J.A., B.T. Dwyer, S.K. Dhar, C. Cvetic, J.C. Walter, and A. Dutta. 2000. Inhibition of eukaryotic replication by geminin binding to Cdt1. Science. 290:2309-2312.
61. You, Z., K. Harvey, L. Kong, and J. Newport. 2002. Xic1 degradation in Xenopus egg extracts is coupled to initiation of DNA replication. Genes Dev. 16:1182-1194.