The APC/C recruits cyclin B1-Cdk1-Cks in prometaphase before D box recognition to control mitotic exit

Journal of Cell Biology

Volumn 190, Issue 4, 2010, Pages 587-602

  Van Zon, Wouter ^a   Ogink, Janneke ^a   Ter Riet, Bas ^a   Medema, René H ^a,b   Te Riele, Hein ^a   Wolthuis, Rob M F ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ANAPHASE PROMOTING COMPLEX; CELL CYCLE PROTEIN 20; CELL PROTEIN; CHECKPOINT KINASE 1; CHECKPOINT KINASE 2; CYCLIN A; CYCLIN B1; CYCLIN DEPENDENT KINASE 1; D BOX PROTEIN; PROTEIN SUBUNIT; UNCLASSIFIED DRUG; CARRIER PROTEIN; CDC20 PROTEIN, HUMAN; CELL CYCLE PROTEIN; CKS1B PROTEIN, HUMAN; CYCLIN DEPENDENT KINASE; HYBRID PROTEIN; NOCODAZOLE; PROTEIN BINDING; PROTEIN KINASE INHIBITOR; PURINE DERIVATIVE; ROSCOVITINE; SECURIN; TUBULIN MODULATOR; TUMOR PROTEIN; UBIQUITIN; UBIQUITIN PROTEIN LIGASE;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL CYCLE REGULATION; CONTROLLED STUDY; CYTOKINESIS; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; METAPHASE; MITOSIS; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROMETAPHASE; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN STABILITY; UBIQUITINATION; ANIMAL; CELL LINE; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; RNA INTERFERENCE;

ANAPHASE-PROMOTING COMPLEX-CYCLOSOME; ANIMALS; CARRIER PROTEINS; CDC2 PROTEIN KINASE; CDC2-CDC28 KINASES; CDC20 PROTEINS; CELL CYCLE PROTEINS; CELL LINE; CYCLIN A; CYCLIN B1; CYCLIN-DEPENDENT KINASES; HUMANS; MITOSIS; NEOPLASM PROTEINS; NOCODAZOLE; PHOSPHORYLATION; PROMETAPHASE; PROTEIN BINDING; PROTEIN KINASE INHIBITORS; PURINES; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; SECURIN; TUBULIN MODULATORS; UBIQUITIN; UBIQUITIN-PROTEIN LIGASE COMPLEXES;

EID: 77955855320     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200912084     Document Type: Article

References (61)

1. Arooz, T., C.H. Yam, W.Y. Siu, A. Lau, K.K. Li, and R.Y. Poon. 2000. On the concentrations of cyclins and cyclin-dependent kinases in extracts of cultured human cells. Biochemistry. 39:9494-9501. doi:10.1021/bi0009643 (Pubitemid 30626339)
2. Bentley, A.M., G. Normand, J. Hoyt, and R.W. King. 2007. Distinct sequence elements of cyclin B1 promote localization to chromatin, centrosomes, and kinetochores during mitosis. Mol. Biol. Cell. 18:4847-4858. doi:10.1091/mbc.E06-06-0539
3. Burton, J.L., and M.J. Solomon. 2001. D box and KEN box motifs in budding yeast Hsl1p are required for APC-mediated degradation and direct binding to Cdc20p and Cdh1p. Genes Dev. 15:2381-2395. doi:10.1101/gad.917901
4. Burton, J.L., V. Tsakraklides, and M.J. Solomon. 2005. Assembly of an APC-Cdh1-substrate complex is stimulated by engagement of a destruction box. Mol. Cell. 18:533-542. doi:10.1016/j.molcel.2005.04.022
5. 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.
6. Chesnel, F., F. Bazile, A. Pascal, and J.Z. Kubiak. 2007. Cyclin B2/cyclin-dependent kinase1 dissociation precedes CDK1 Thr-161 dephosphorylation upon M-phase promoting factor inactivation in Xenopus laevis cell-free extract. Int. J. Dev. Biol. 51:297-305. doi:10.1387/ijdb.072292fc (Pubitemid 46997589)
7. Clute, P., and J. Pines. 1999. Temporal and spatial control of cyclin B1 destruction in metaphase. Nat. Cell Biol. 1:82-87. doi:10.1038/10049 (Pubitemid 129501948)
8. den Elzen, N., and J. Pines. 2001. Cyclin A is destroyed in prometaphase and can delay chromosome alignment and anaphase. J. Cell Biol. 153:121-136. doi:10.1083/jcb.153.1.121
9. Donovan, P.J., and S.I. Reed. 2003. Germline exclusion of Cks1 in the mouse reveals a metaphase I role for Cks proteins in male and female meiosis. Cell Cycle. 2:275-276.
10. Draviam, V.M., S. Orrechia, M. Lowe, R. Pardi, and J. Pines. 2001. The localization of human cyclins B1 and B2 determines CDK1 substrate specificity and neither enzyme requires MEK to disassemble the Golgi apparatus. J. Cell Biol. 152:945-958. doi:10.1083/jcb.152.5.945
11. Eytan, E., Y. Moshe, I. Braunstein, and A. Hershko. 2006. Roles of the anaphase-promoting complex/cyclosome and of its activator Cdc20 in functional substrate binding. Proc. Natl. Acad. Sci. USA. 103:2081-2086. doi:10.1073/pnas.0510695103 (Pubitemid 43271626)
12. Ge, S., J.R. Skaar, and M. Pagano. 2009. APC/C- and Mad2-mediated degradation of Cdc20 during spindle checkpoint activation. Cell Cycle. 8: 167-171.
13. Geley, S., E. Kramer, C. Gieffers, J. Gannon, J.M. Peters, and T. Hunt. 2001. Anaphase-promoting complex/cyclosome-dependent proteolysis of human cyclin A starts at the beginning of mitosis and is not subject to the spindle assembly checkpoint. J. Cell Biol. 153:137-148. doi:10.1083/jcb.153.1.137
14. 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. doi:10.1083/jcb.200111001
15. Hayes, M.J., Y. Kimata, S.L. Wattam, C. Lindon, G. Mao, H. Yamano, and A.M. Fry. 2006. Early mitotic degradation of Nek2A depends on Cdc20-independent interaction with the APC/C. Nat. Cell Biol. 8:607-614. doi:10.1038/ncb1410
16. Herzog, F., I. Primorac, P. Dube, P. Lenart, B. Sander, K. Mechtler, H. Stark, and J.M. Peters. 2009. Structure of the anaphase-promoting complex/cyclosome interacting with a mitotic checkpoint complex. Science. 323: 1477-1481. doi:10.1126/science.1163300
17. Hilioti, Z., Y.S. Chung, Y. Mochizuki, C.F. Hardy, and O. Cohen-Fix. 2001. The anaphase inhibitor Pds1 binds to the APC/C-associated protein Cdc20 in a destruction box-dependent manner. Curr. Biol. 11:1347-1352. doi:10.1016/S0960-9822(01)00399-2 (Pubitemid 32835875)
18. Huang, H.C., J. Shi, J.D. Orth, and T.J. Mitchison. 2009. Evidence that mitotic exit is a better cancer therapeutic target than spindle assembly. Cancer Cell. 16:347-358.
19. Inui, N., K. Kitagawa, S. Miwa, T. Hattori, K. Chida, H. Nakamura, and M. Kitagawa. 2003. High expression of Cks1 in human non-small cell lung carcinomas. Biochem. Biophys. Res. Commun. 303:978-984. doi:10.1016/S0006- 291X(03)00469-8
20. Keller, U.B., J.B. Old, F.C. Dorsey, J.A. Nilsson, L. Nilsson, K.H. MacLean, L. Chung, C. Yang, C. Spruck, K. Boyd, et al. 2007. Myc targets Cks1 to provoke the suppression of p27Kip1, proliferation and lymphomagenesis. EMBO J. 26:2562-2574. doi:10.1038/sj.emboj.7601691
21. Kimata, Y., J.E. Baxter, A.M. Fry, and H. Yamano. 2008. A role for the Fizzy/Cdc20 family of proteins in activation of the APC/C distinct from substrate recruitment. Mol. Cell. 32:576-583. doi:10.1016/j.molcel.2008.09.023
22. Kitajima, S., Y. Kudo, I. Ogawa, T. Bashir, M. Kitagawa, M. Miyauchi, M. Pagano, and T. Takata. 2004. Role of Cks1 overexpression in oral squamous cell carcinomas: cooperation with Skp2 in promoting p27 degradation. Am. J. Pathol. 165:2147-2155.
23. Kops, G.J. 2008. The kinetochore and spindle checkpoint in mammals. Front. Biosci. 13:3606-3620. doi:10.2741/2953
24. Kraft, C., H.C. Vodermaier, S. Maurer-Stroh, F. Eisenhaber, and J.M. Peters. 2005. The WD40 propeller domain of Cdh1 functions as a destruction box receptor for APC/C substrates. Mol. Cell. 18:543-553. doi:10.1016/j.molcel.2005. 04.023 (Pubitemid 40726231)
25. Kulukian, A., J.S. Han, and D.W. Cleveland. 2009. Unattached kinetochores catalyze production of an anaphase inhibitor that requires a Mad2 template to prime Cdc20 for BubR1 binding. Dev. Cell. 16:105-117. doi:10.1016/j.devcel.2008. 11.005
26. Lens, S.M., R.M.F. Wolthuis, R. Klompmaker, J. Kauw, R. Agami, T. Brummelkamp, G. Kops, and R.H. Medema. 2003. Survivin is required for a sustained spindle checkpoint arrest in response to lack of tension. EMBO J. 22:2934-2947. doi:10.1093/emboj/cdg307
27. Lindqvist, A., W. van Zon, C. Karlsson Rosenthal, and R.M.F. Wolthuis. 2007. Cyclin B1-Cdk1 activation continues after centrosome separation to control mitotic progression. PLoS Biol. 5:e123. doi:10.1371/journal.pbio.0050123
28. Lindqvist, A., V. Rodríguez-Bravo, and R.H. Medema. 2009. The decision to enter mitosis: feedback and redundancy in the mitotic entry network. J. Cell Biol. 185:193-202. doi:10.1083/jcb.200812045
29. Martinsson-Ahlzén, H.S., V. Liberal, B. Grünenfelder, S.R. Chaves, C.H. Spruck, and S.I. Reed. 2008. Cyclin-dependent kinase-associated proteins Cks1 and Cks2 are essential during early embryogenesis and for cell cycle progression in somatic cells. Mol. Cell. Biol. 28:5698-5709. doi:10.1128/MCB.01833-07
30. Masuda, T.A., H. Inoue, K. Nishida, H. Sonoda, Y. Yoshikawa, Y. Kakeji, T. Utsunomiya, and M. Mori. 2003. Cyclin-dependent kinase 1 gene expression is associated with poor prognosis in gastric carcinoma. Clin. Cancer Res. 9:5693-5698.
31. Matyskiela, M.E., and D.O. Morgan. 2009. Analysis of activator-binding sites on the APC/C supports a cooperative substrate-binding mechanism. Mol. Cell. 34:68-80. doi:10.1016/j.molcel.2009.02.027
32. Nilsson, J., M. Yekezare, J. Minshull, and J. Pines. 2008. The APC/C maintains the spindle assembly checkpoint by targeting Cdc20 for destruction. Nat. Cell Biol. 10:1411-1420. doi:10.1038/ncb1799
33. Nishiyama, A., K. Tachibana, Y. Igarashi, H. Yasuda, N. Tanahashi, K. Tanaka, K. Ohsumi, and T. Kishimoto. 2000. A nonproteolytic function of the proteasome is required for the dissociation of Cdc2 and cyclin B at the end of M phase. Genes Dev. 14:2344-2357. doi:10.1101/gad.823200
34. Ohtoshi, A., T. Maeda, H. Higashi, S. Ashizawa, and M. Hatakeyama. 2000. Human p55(CDC)/Cdc20 associates with cyclin A and is phosphorylated by the cyclin A-Cdk2 complex. Biochem. Biophys. Res. Commun. 268:530-534. doi:10.1006/bbrc.2000.2167 (Pubitemid 30119656)
35. Passmore, L.A., and D. Barford. 2005. Coactivator functions in a stoichiometric complex with anaphase-promoting complex/cyclosome to mediate substrate recognition. EMBO Rep. 6:873-878. doi:10.1038/sj.embor.7400482
36. Patra, D., and W.G. Dunphy. 1996. Xe-p9, a Xenopus Suc1/Cks homolog, has multiple essential roles in cell cycle control. Genes Dev. 10:1503-1515. doi:10.1101/gad.10.12.1503
37. Patra, D., and W.G. Dunphy. 1998. Xe-p9, a Xenopus Suc1/Cks protein, is essential for the Cdc2-dependent phosphorylation of the anaphase- promoting complex at mitosis. Genes Dev. 12:2549-2559. doi:10.1101/gad.12.16.2549
38. Patra, D., S.X. Wang, A. Kumagai, and W.G. Dunphy. 1999. The xenopus Suc1/Cks protein promotes the phosphorylation of G(2)/M regulators. J. Biol. Chem. 274:36839-36842. doi:10.1074/jbc.274.52.36839 (Pubitemid 30016748) (Pubitemid 129513854)
39. Pines, J. 1996. Cell cycle: reaching for a role for the Cks proteins. Curr. Biol. 6:1399-1402. doi:10.1016/S0960-9822(96)00741-5
40. Pines, J. 2006. Mitosis: a matter of getting rid of the right protein at the right time. Trends Cell Biol. 16:55-63. doi:10.1016/j.tcb.2005.11.006
41. Pines, J., and T. Hunter. 1994. The differential localization of human cyclins A and B is due to a cytoplasmic retention signal in cyclin B. EMBO J. 13:3772-3781. (Pubitemid 24275023)
42. Rape, M., S.K. Reddy, and M.W. Kirschner. 2006. The processivity of multiubiquitination by the APC determines the order of substrate degradation. Cell. 124:89-103. doi:10.1016/j.cell.2005.10.032
43. Sczaniecka, M.M., and K.G. Hardwick. 2008. The spindle checkpoint: how do cells delay anaphase onset? SEB Exp Biol Ser. 59:243-256.
44. Shapira, M., O. Ben-Izhak, S. Linn, B. Futerman, I. Minkov, and D.D. Hershko. 2005. The prognostic impact of the ubiquitin ligase subunits Skp2 and Cks1 in colorectal carcinoma. Cancer. 103:1336-1346. doi:10.1002/cncr.20917
45. Shteinberg, M., and A. Hershko. 1999. Role of Suc1 in the activation of the cyclosome by protein kinase Cdk1/cyclin B. Biochem. Biophys. Res. Commun. 257:12-18. doi:10.1006/bbrc.1999.0409
46. Stegmeier, F., M. Rape, V.M. Draviam, G. Nalepa, M.E. Sowa, X.L. Ang, E.R. McDonald III, M.Z. Li, G.J. Hannon, P.K. Sorger, et al. 2007. Anaphase initiation is regulated by antagonistic ubiquitination and deubiquitination activities. Nature. 446:876-881. doi:10.1038/nature05694
47. Stewart, E., H. Kobayashi, D. Harrison, and T. Hunt. 1994. Destruction of Xenopus cyclins A and B2, but not B1, requires binding to p34cdc2. EMBO J. 13:584-594. (Pubitemid 24979436) (Pubitemid 24050672)
48. Sudakin, V., M. Shteinberg, D. Ganoth, J. Hershko, and A. Hershko. 1997. Binding of activated cyclosome to p13(suc1). Use for affinity purification. J. Biol. Chem. 272:18051-18059. doi:10.1074/jbc.272.29.18051
49. Sullivan, M., and D.O. Morgan. 2007. Finishing mitosis, one step at a time. Nat. Rev. Mol. Cell Biol. 8:894-903. doi:10.1038/nrm2276
50. Sullivan, M., L. Holt, and D.O. Morgan. 2008. Cyclin-specific control of ribosomal DNA segregation. Mol. Cell. Biol. 28:5328-5336. doi:10.1128/MCB.00235- 08
51. Surana, U., H. Robitsch, C. Price, T. Schuster, I. Fitch, A.B. Futcher, and K. Nasmyth. 1991. The role of CDC28 and cyclins during mitosis in the budding yeast S. cerevisiae. Cell. 65:145-161. doi:10.1016/0092-8674(91)90416-V (Pubitemid 121001222)
52. Thornton, B.R., and D.P. Toczyski. 2003. Securin and B-cyclin/CDK are the only essential targets of the APC. Nat. Cell Biol. 5:1090-1094. doi:10.1038/ncb1066
53. van 't Veer, L.J., H. Dai, M.J. van de Vijver, Y.D. He, A.A. Hart, M. Mao, H.L. Peterse, K. van der Kooy, M.J. Marton, A.T. Witteveen, et al. 2002. Gene expression profiling predicts clinical outcome of breast cancer. Nature. 415:530-536. doi:10.1038/415530a
54. van Leuken, R., L. Clijsters, and R. Wolthuis. 2008. To cell cycle, swing the APC/C. Biochim. Biophys. Acta. 1786:49-59.
55. van Vugt, M.A., B.C. van de Weerdt, G. Vader, H. Janssen, J. Calafat, R. Klompmaker, R.M. Wolthuis, and R.H. Medema. 2004. Polo-like kinase-1 is required for bipolar spindle formation but is dispensable for anaphase promoting complex/Cdc20 activation and initiation of cytokinesis. J. Biol. Chem. 279:36841-36854. doi:10.1074/jbc.M313681200
56. van Zon, W., and R.M.F. Wolthuis. 2010. Cyclin A and Nek2A: APC/C-Cdc20 substrates invisible to the mitotic spindle checkpoint. Biochem. Soc. Trans. 38:72-77. doi:10.1042/BST0380072
57. Wolf, F., C. Wandke, N. Isenberg, and S. Geley. 2006. Dose-dependent effects of stable cyclin B1 on progression through mitosis in human cells. EMBO J. 25:2802-2813. doi:10.1038/sj.emboj.7601163
58. 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. doi:10.1016/j.molcel.2008.02.027
59. Yamano, H., J. Gannon, H. Mahbubani, and T. Hunt. 2004. Cell cycle-regulated recognition of the destruction box of cyclin B by the APC/C in Xenopus egg extracts. Mol. Cell. 13:137-147. doi:10.1016/S1097-2765(03)00480-5 (Pubitemid 38117122)
60. Yanagida, M. 2005. Basic mechanism of eukaryotic chromosome segregation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 360:609-621. doi:10.1098/rstb.2004. 1615 (Pubitemid 41529658)
61. Yu, H. 2007. Cdc20: a WD40 activator for a cell cycle degradation machine. Mol. Cell. 27:3-16. doi:10.1016/j.molcel.2007.06.009