Interphase APC/C-Cdc20 inhibition by cyclin A2-Cdk2 ensures efficient mitotic entry

Nature Communications

Volumn 7, Issue , 2016, Pages

  Hein, Jamin B ^a   Nilsson, Jakob ^a  

^a University of Copenhagen   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ANAPHASE PROMOTING COMPLEX; CELL CYCLE PROTEIN 20; CYCLIN A2; CYCLIN B1; CYCLIN DEPENDENT KINASE 2; CCNA2 PROTEIN, HUMAN; CCNB1 PROTEIN, HUMAN; CDC20 PROTEIN, HUMAN; CDK2 PROTEIN, HUMAN;

CELLS AND CELL COMPONENTS; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC ANALYSIS; INHIBITION; INHIBITOR;

ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; FEMALE; HUMAN; HUMAN CELL; INTERPHASE; MITOSIS; POSITIVE FEEDBACK; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; CELL CYCLE G2 PHASE; HELA CELL LINE; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; WESTERN BLOTTING;

ANAPHASE-PROMOTING COMPLEX-CYCLOSOME; BLOTTING, WESTERN; CDC20 PROTEINS; CYCLIN A2; CYCLIN B1; CYCLIN-DEPENDENT KINASE 2; G2 PHASE; HELA CELLS; HUMANS; INTERPHASE; MITOSIS; PHOSPHORYLATION;

EID: 84960912526     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10975     Document Type: Article

References (41)

1. Pines, J. Cubism and the cell cycle: the many faces of the APC/C. Nat. Rev. Mol. Cell Biol. 12, 427-438 (2011).
2. Nilsson, J. Cdc20 control of cell fate during prolonged mitotic arrest: Do Cdc20 protein levels affect cell fate in response to antimitotic compounds? Bioessays 33, 903-909 (2011).
3. Gong, D. et al. Cyclin A2 regulates nuclear-envelope breakdown and the nuclear accumulation of cyclin B1. Curr. Biol. 17, 85-91 (2007).
4. Gong, D. & Ferrell, J. E. The roles of cyclin A2, B1, and B2 in early and late mitotic events. Mol. Biol. Cell 21, 3149-3161 (2010).
5. Gavet, O. & Pines, J. Progressive activation of CyclinB1-Cdk1 coordinates entry to mitosis. Dev. Cell 18, 533-543 (2010).
6. Fung, T. K., Ma, H. T. & Poon, R. Y. C. Specialized roles of the two mitotic cyclins in somatic cells: cyclin A as an activator of M phase-promoting factor. Mol. Biol. Cell 18, 1861-1873 (2007).
7. De Boer, L. et al. Cyclin A/cdk2 coordinates centrosomal and nuclear mitotic events. Oncogene 27, 4261-4268 (2008).
8. Kimata, Y., Baxter, J. E., Fry, A. M. & Yamano, H. A role for the Fizzy/Cdc20 family of proteins in activation of the APC/C distinct from substrate recruitment. Mol. Cell 32, 576-583 (2008).
9. Chang, L., Zhang, Z., Yang, J., McLaughlin, S. H. & Barford, D. Molecular architecture and mechanism of the anaphase-promoting complex. Nature 513, 388-393 (2014).
10. Clute, P. & Pines, J. Temporal and spatial control of cyclin B1 destruction in metaphase. Nat. Cell Biol. 1, 82-87 (1999).
11. Geley, S. et al. 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 (2001).
12. Elzen, den, N. & Pines, J. Cyclin A is destroyed in prometaphase and can delay chromosome alignment and anaphase. J. Cell Biol. 153, 121-136 (2001).
13. Di Fiore, B. & Pines, J. Defining the role of Emi1 in the DNA replicationsegregation cycle. Chromosoma 117, 333-338 (2008).
14. Kraft, C. et al. Mitotic regulation of the human anaphase-promoting complex by phosphorylation. EMBO J. 22, 6598-6609 (2003).
15. Rudner, A. D. & Murray, A. W. Phosphorylation by Cdc28 activates the Cdc20-dependent activity of the anaphase-promoting complex. J. Cell Biol. 149, 1377-1390 (2000).
16. Kramer, E. R., Scheuringer, N., Podtelejnikov, A. V., Mann, M. & Peters, J. M. Mitotic regulation of the APC activator proteins CDC20 and CDH1. Mol. Biol. Cell 11, 1555-1569 (2000).
17. Shteinberg, M., Protopopov, Y., Listovsky, T., Brandeis, M. & Hershko, A. Phosphorylation of the cyclosome is required for its stimulation by Fizzy/cdc20. Biochem. Biophys. Res. Commun. 260, 193-198 (1999).
18. Fang, G., Yu, H. & Kirschner, M. W. Direct binding of CDC20 protein family members activates the anaphase-promoting complex in mitosis and G1. Mol. Cell 2, 163-171 (1998).
19. Kramer, E. R., Gieffers, C., Hölzl, G., Hengstschläger, M. & Peters, J. M. Activation of the human anaphase-promoting complex by proteins of the CDC20/Fizzy family. Curr. Biol. 8, 1207-1210 (1998).
20. Lara-Gonzalez, P., Westhorpe, F. G. & Taylor, S. S. The spindle assembly checkpoint. Curr. Biol. 22, R966-R980 (2012).
21. Labit, H. et al. Dephosphorylation of Cdc20 is required for its C-box-dependent activation of the APC/C. EMBO J. 31, 3351-3362 (2012).
22. D'Angiolella, V., Mari, C., Nocera, D., Rametti, L. & Grieco, D. The spindle checkpoint requires cyclin-dependent kinase activity. Genes Dev. 17, 2520-2525 (2003).
23. Yudkovsky, Y., Shteinberg, M., Listovsky, T., Brandeis, M. & Hershko, A. Phosphorylation of Cdc20/fizzy negatively regulates the mammalian cyclosome/APC in the mitotic checkpoint. Biochem. Biophys. Res. Commun. 271, 299-304 (2000).
24. Weinstein, J. Cell cycle-regulated expression, phosphorylation, and degradation of p55Cdc. A mammalian homolog of CDC20/Fizzy/slp1. J. Biol. Chem. 272, 28501-28511 (1997).
25. Elowe, S. et al. Uncoupling of the spindle-checkpoint and chromosomecongression functions of BubR1. J. Cell Sci. 123, 84-94 (2010).
26. Huang, H. et al. Phosphorylation sites in BubR1 that regulate kinetochore attachment, tension, and mitotic exit. J. Cell Biol. 183, 667-680 (2008).
27. Pines, J. & Hunter, T. Human cyclins A and B1 are differentially located in the cell and undergo cell cycle-dependent nuclear transport. J. Cell Biol. 115, 1-17 (1991).
28. Di Fiore, B. et al. The ABBA motif binds APC/C activators and is shared by APC/C substrates and regulators. Dev. Cell 32, 358-372 (2015).
29. Ohtoshi, A., Maeda, T., Higashi, H., Ashizawa, S. & Hatakeyama, M. Human p55(CDC)/Cdc20 associates with cyclin A and is phosphorylated by the cyclin A-Cdk2 complex. Biochem. Biophys. Res. Commun. 268, 530-534 (2000).
30. Spencer, S. L. et al. The proliferation-quiescence decision is controlled by a bifurcation in CDK2 activity at mitotic exit. Cell 155, 369-383 (2013).
31. Schmitz, M. H. A. et al. Live-cell imaging RNAi screen identifies PP2AB55alpha and importin-beta1 as key mitotic exit regulators in human cells. Nat. Cell Biol. 12, 886-893 (2010).
32. Jackman, M., Lindon, C., Nigg, E. A. & Pines, J. Active cyclin B1-Cdk1 first appears on centrosomes in prophase. Nat. Cell Biol. 5, 143-148 (2003).
33. Sudakin, V., Chan, G. K. & Yen, T. J. Checkpoint inhibition of the APC/C in HeLa cells is mediated by a complex of BUBR1, BUB3, CDC20, and MAD2. J. Cell Biol. 154, 925-936 (2001).
34. Rodriguez-Bravo, V. et al. Nuclear pores protect genome integrity by assembling a premitotic and mad1-dependent anaphase inhibitor. Cell 156, 1017-1031 (2014).
35. Nilsson, J., Yekezare, M., Minshull, J. & Pines, J. The APC/C maintains the spindle assembly checkpoint by targeting Cdc20 for destruction. Nat. Cell Biol. 10, 1411-1420 (2008).
36. Lischetti, T., Zhang, G., Sedgwick, G. G., Bolanos-Garcia, V. M. & Nilsson, J. The internal Cdc20 binding site in BubR1 facilitates both spindle assembly checkpoint signalling and silencing. Nat. Commun. 5, 5563 (2014).
37. Hein, J. B. & Nilsson, J. Stable MCC binding to the APC/C is required for a functional spindle assembly checkpoint. EMBO Rep. 15, 264-272 (2014).
38. Matsusaka, T., Enquist-Newman, M., Morgan, D. O. & Pines, J. Co-activator independent differences in how the metaphase and anaphase APC/C recognise the same substrate. Biol. Open 3, 904-912 (2014).
39. Yang, Q. & Ferrell, J. E. The Cdk1-APC/C cell cycle oscillator circuit functions as a time-delayed, ultrasensitive switch. Nat. Cell Biol. 15, 519-525 (2013).
40. Akopyan, K. et al. Assessing kinetics from fixed cells reveals activation of the mitotic entry network at the S/G2 transition. Mol. Cell 53, 843-853 (2014).
41. Mejlvang, J. et al. New histone supply regulates replication fork speed and PCNA unloading. J. Cell Biol. 204, 29-43 (2014).