The spindle checkpoint, APC/CCdc20, and APC/CCdh1 play distinct roles in connecting mitosis to S phase

Journal of Cell Biology

Volumn 201, Issue 7, 2013, Pages 1013-1026

  Clijsters, Linda ^a   Ogink, Janneke ^a   Wolthuis, Rob ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN 20; CELL CYCLE PROTEIN 6; CYCLIN B1; GEMININ; REPLICATION LICENSING FACTOR CDT1; SECURIN;

ARTICLE; CELL CYCLE S PHASE; CELL PROLIFERATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; M PHASE CELL CYCLE CHECKPOINT; METAPHASE; MITOSIS; PRIORITY JOURNAL; PROMETAPHASE; PROTEIN DEGRADATION; SISTER CHROMATID;

CADHERINS; CELL CYCLE PROTEINS; CELL LINE, TUMOR; CYCLIN B1; HUMANS; M PHASE CELL CYCLE CHECKPOINTS; MITOSIS; NUCLEAR PROTEINS; S PHASE; UBIQUITIN-PROTEIN LIGASE COMPLEXES;

ANIMALIA;

EID: 84880011165     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201211019     Document Type: Article

References (44)

1. Amador, V., S. Ge, P.G. Santamaría, D. Guardavaccaro, and M. Pagano. 2007. APC/C(Cdc20) controls the ubiquitin-mediated degradation of p21 in prometaphase. Mol. Cell. 27:462-473. http://dx.doi.org/10.1016/j.molcel.2007.06.013
2. Arias, E.E., and J.C. Walter. 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. http://dx.doi.org/10.1101/gad.1255805
3. Arias, E.E., and J.C. Walter. 2007. Strength in numbers: preventing rereplication via multiple mechanisms in eukaryotic cells. Genes Dev. 21:497-518. http://dx.doi.org/10.1101/gad.1508907
4. Ballabeni, A., M. Melixetian, R. Zamponi, L. Masiero, F. Marinoni, and K. Helin. 2004. Human geminin promotes pre-RC formation and DNA replication by stabilizing CDT1 in mitosis. EMBO J. 23:3122-3132. http://dx.doi.org/10.1038/sj.emboj.7600314
5. Brinkley, B.R., R.P. Zinkowski, W.L. Mollon, F.M. Davis, M.A. Pisegna, M. Pershouse, and P.N. Rao. 1988. Movement and segregation of kinetochores experimentally detached from mammalian chromosomes. Nature. 336:251-254. http://dx.doi.org/10.1038/336251a0
6. Brito, D.A., and C.L. Rieder. 2006. Mitotic checkpoint slippage in humans occurs via cyclin B destruction in the presence of an active checkpoint. Curr. Biol. 16:1194-1200. http://dx.doi.org/10.1016/j.cub.2006.04.043
7. Clute, P., and J. Pines. 1999. Temporal and spatial control of cyclin B1 destruction in metaphase. Nat. Cell Biol. 1:82-87. http://dx.doi.org/10.1038/10049
8. Colombo, S.L., M. Palacios-Callender, N. Frakich, J. De Leon, C.A. Schmitt, L. Boorn, N. Davis, and S. Moncada. 2010. Anaphase-promoting complex/ cyclosome-Cdh1 coordinates glycolysis and glutaminolysis with transition to S phase in human T lymphocytes. Proc. Natl. Acad. Sci. USA. 107:18868-18873. http://dx.doi.org/10.1073/pnas.1012362107
9. Di Fiore, B., and J. Pines. 2007. Emi1 is needed to couple DNA replication with mitosis but does not regulate activation of the mitotic APC/C. J. Cell Biol. 177:425-437. http://dx.doi.org/10.1083/jcb.200611166
10. Diffley, J.F. 2004. Regulation of early events in chromosome replication. Curr. Biol. 14:R778-R786. http://dx.doi.org/10.1016/j.cub.2004.09.019
11. Duursma, A.M., and R. Agami. 2005. CDK-dependent stabilization of Cdc6: linking growth and stress signals to activation of DNA replication. Cell Cycle. 4:1725-1728. http://dx.doi.org/10.4161/cc.4.12.2193
12. Emanuele, M.J., A. Ciccia, A.E. Elia, and S.J. Elledge. 2011. Proliferating cell nuclear antigen (PCNA)-associated KIAA0101/PAF15 protein is a cell cycle-regulated anaphase-promoting complex/cyclosome substrate. Proc. Natl. Acad. Sci. USA. 108:9845-9850. http://dx.doi.org/10.1073/pnas.1106136108
13. Engelbert, D., D. Schnerch, A. Baumgarten, and R. Wäsch. 2008. The ubiquitin ligase APC(Cdh1) is required to maintain genome integrity in primary human cells. Oncogene. 27:907-917. http://dx.doi.org/10.1038/sj.onc.1210703
14. Floyd, S., J. Pines, and C. Lindon. 2008. APC/C Cdh1 targets aurora kinase to control reorganization of the mitotic spindle at anaphase. Curr. Biol. 18:1649-1658. http://dx.doi.org/10.1016/j.cub.2008.09.058
15. García-Higuera, I., E. Manchado, P. Dubus, M. Cañamero, J. Méndez, S. Moreno, and M. Malumbres. 2008. Genomic stability and tumour suppression by the APC/C cofactor Cdh1. Nat. Cell Biol. 10:802-811. http://dx.doi.org/10.1038/ncb1742
16. Geng, Y., Q. Yu, E. Sicinska, M. Das, J.E. Schneider, S. Bhattacharya, W.M. Rideout, R.T. Bronson, H. Gardner, and P. Sicinski. 2003. Cyclin E ablation in the mouse. Cell. 114:431-443. http://dx.doi.org/10.1016/S0092-8674(03)00645-7
17. Gurden, M.D., A.J. Holland, W. van Zon, A. Tighe, M.A. Vergnolle, D.A. Andres, H.P. Spielmann, M. Malumbres, R.M. Wolthuis, D.W. Cleveland, and S.S. Taylor. 2010. Cdc20 is required for the post-anaphase, KENdependent degradation of centromere protein F. J. Cell Sci. 123:321-330. http://dx.doi.org/10.1242/jcs.062075
18. Hagting, A., N. Den Elzen, H.C. Vodermaier, I.C. Waizenegger, J.M. Peters, and J. Pines. 2002. Human securin proteolysis is controlled by the spindle checkpoint and reveals when the APC/C switches from activation by Cdc20 to Cdh1. J. Cell Biol. 157:1125-1137. http://dx.doi.org/10.1083/jcb.200111001
19. Hall, J.R., H.O. Lee, B.D. Bunker, E.S. Dorn, G.C. Rogers, R.J. Duronio, and J.G. Cook. 2008. Cdt1 and Cdc6 are destabilized by rereplication-induced DNA damage. J. Biol. Chem. 283:25356-25363. http://dx.doi.org/10.1074/jbc.M802667200
20. Hames, R.S., S.L. Wattam, H. Yamano, R. Bacchieri, and A.M. Fry. 2001. APC/ C-mediated destruction of the centrosomal kinase Nek2A occurs in early mitosis and depends upon a cyclin A-type D-box. EMBO J. 20:7117- 7127. http://dx.doi.org/10.1093/emboj/20.24.7117
21. Harley, M.E., L.A. Allan, H.S. Sanderson, and P.R. Clarke. 2010. Phosphorylation of Mcl-1 by CDK1-cyclin B1 initiates its Cdc20-dependent destruction during mitotic arrest. EMBO J. 29:2407-2420. http://dx.doi.org/10.1038/emboj.2010.112
22. Hermand, D., and P. Nurse. 2007. Cdc18 enforces long-term maintenance of the S phase checkpoint by anchoring the Rad3-Rad26 complex to chromatin. Mol. Cell. 26:553-563. http://dx.doi.org/10.1016/j.molcel.2007.04.014
23. Hochegger, H., D. Dejsuphong, E. Sonoda, A. Saberi, E. Rajendra, J. Kirk, T. Hunt, and S. Takeda. 2007. An essential role for Cdk1 in S phase control is revealed via chemical genetics in vertebrate cells. J. Cell Biol. 178:257-268. http://dx.doi.org/10.1083/jcb.200702034
24. Honey, S., and B. Futcher. 2007. Roles of the CDK phosphorylation sites of yeast Cdc6 in chromatin binding and rereplication. Mol. Biol. Cell. 18:1324-1336. http://dx.doi.org/10.1091/mbc.E06-06-0544
25. Ibarra, A., E. Schwob, and J. Méndez. 2008. Excess MCM proteins protect human cells from replicative stress by licensing backup origins of replication. Proc. Natl. Acad. Sci. USA. 105:8956-8961. http://dx.doi.org/10.1073/pnas.0803978105
26. Li, A., and J.J. Blow. 2004. Non-proteolytic inactivation of geminin requires CDK-dependent ubiquitination. Nat. Cell Biol. 6:260-267. http://dx.doi.org/10.1038/ncb1100
27. Mailand, N., and J.F. Diffley. 2005. CDKs promote DNA replication origin licensing in human cells by protecting Cdc6 from APC/C-dependent proteolysis. Cell. 122:915-926. http://dx.doi.org/10.1016/j.cell.2005.08.013
28. Maiorano, D., L. Krasinska, M. Lutzmann, and M. Mechali. 2005. Recombinant Cdt1 induces rereplication of G2 nuclei in Xenopus egg extracts. Curr. Biol. 15:146-153. http://dx.doi.org/10.1016/j.cub.2004.12.002
29. McGarry, T.J., and M.W. Kirschner. 1998. Geminin, an inhibitor of DNA replication, is degraded during mitosis. Cell. 93:1043-1053. http://dx.doi.org/10.1016/S0092-8674(00)81209-X
30. Melixetian, M., A. Ballabeni, L. Masiero, P. Gasparini, R. Zamponi, J. Bartek, J. Lukas, and K. Helin. 2004. Loss of Geminin induces rereplication in the presence of functional p53. J. Cell Biol. 165:473-482. http://dx.doi.org/10.1083/jcb.200403106
31. Narbonne-Reveau, K., S. Senger, M. Pal, A. Herr, H.E. Richardson, M. Asano, P. Deak, and M.A. Lilly. 2008. APC/CFzr/Cdh1 promotes cell cycle progression during the Drosophila endocycle. Development. 135:1451- 1461. http://dx.doi.org/10.1242/dev.016295
32. Nishitani, H., S. Taraviras, Z. Lygerou, and T. Nishimoto. 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. http://dx.doi.org/10.1074/jbc.M105406200
33. Petersen, B.O., C. Wagener, F. Marinoni, E.R. Kramer, M. Melixetian, E. Lazzerini 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. http://dx.doi.org/10.1101/gad.832500
34. Piatti, S., T. Böhm, J.H. Cocker, J.F. Diffley, and K. Nasmyth. 1996. Activation of S-phase-promoting CDKs in late G1 defines a "point of no return" after which Cdc6 synthesis cannot promote DNA replication in yeast. Genes Dev. 10:1516-1531. http://dx.doi.org/10.1101/gad.10.12.1516
35. Pines, J. 2006. Mitosis: a matter of getting rid of the right protein at the right time. Trends Cell Biol. 16:55-63. http://dx.doi.org/10.1016/j.tcb.2005.11.006
36. Rialland, M., F. Sola, and C. Santocanale. 2002. Essential role of human CDT1 in DNA replication and chromatin licensing. J. Cell Sci. 115:1435-1440.
37. Sakaue-Sawano, A., H. Kurokawa, T. Morimura, A. Hanyu, H. Hama, H. Osawa, S. Kashiwagi, K. Fukami, T. Miyata, H. Miyoshi, et al. 2008. Visualizing spatiotemporal dynamics of multicellular cell-cycle progression. Cell. 132:487-498. http://dx.doi.org/10.1016/j.cell.2007.12.033
38. Senga, T., U. Sivaprasad, W. Zhu, J.H. Park, E.E. Arias, J.C. Walter, and A. Dutta. 2006. PCNA is a cofactor for Cdt1 degradation by CUL4/DDB1- mediated N-terminal ubiquitination. J. Biol. Chem. 281:6246-6252. http://dx.doi.org/10.1074/jbc.M512705200
39. Skaar, J.R., and M. Pagano. 2008. Cdh1: a master G0/G1 regulator. Nat. Cell Biol. 10:755-757. http://dx.doi.org/10.1038/ncb0708-755
40. van Leuken, R., L. Clijsters, and R. Wolthuis. 2008. To cell cycle, swing the APC/C. Biochim. Biophys. Acta. 1786:49-59.
41. van Zon, W., J. Ogink, B. ter Riet, R.H. Medema, H. te Riele, and R.M. Wolthuis. 2010. The APC/C recruits cyclin B1-Cdk1-Cks in prometaphase before D box recognition to control mitotic exit. J. Cell Biol. 190:587-602. http://dx.doi.org/10.1083/jcb.200912084
42. Wolthuis, R., L. Clay-Farrace, W. van Zon, M. Yekezare, L. Koop, J. Ogink, R. Medema, and J. Pines. 2008. Cdc20 and Cks direct the spindle checkpoint- independent destruction of cyclin A. Mol. Cell. 30:290-302. http://dx.doi.org/10.1016/j.molcel.2008.02.027
43. Xouri, G., A. Squire, M. Dimaki, B. Geverts, P.J. Verveer, S. Taraviras, H. Nishitani, A.B. Houtsmuller, P.I. Bastiaens, and Z. Lygerou. 2007. Cdt1 associates dynamically with chromatin throughout G1 and recruits Geminin onto chromatin. EMBO J. 26:1303-1314. http://dx.doi.org/10.1038/sj.emboj.7601597
44. Zielke, N., S. Querings, C. Rottig, C. Lehner, and F. Sprenger. 2008. The anaphase- promoting complex/cyclosome (APC/C) is required for rereplication control in endoreplication cycles. Genes Dev. 22:1690-1703. http://dx.doi.org/10.1101/gad.469108