Cubism and the cell cycle: The many faces of the APC/C

Nature Reviews Molecular Cell Biology

Volumn 12, Issue 7, 2011, Pages 427-438

  Pines, Jonathon ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANAPHASE PROMOTING COMPLEX;

CELL CYCLE; DNA REPLICATION; MITOSIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN STRUCTURE; REVIEW; UBIQUITINATION;

ANIMALS; CELL CYCLE; CELL CYCLE PROTEINS; HUMANS; MITOSIS; MITOTIC SPINDLE APPARATUS; MODELS, BIOLOGICAL; UBIQUITIN-PROTEIN LIGASE COMPLEXES;

EID: 79959555511     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm3132     Document Type: Review

References (140)

1. Coudreuse, D. & Nurse, P. Driving the cell cycle with a minimal CDK control network. Nature 468, 1074-1079 (2010).
2. Noton, E. & Diffley, J. F. 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 (2000). (Pubitemid 30105438)
3. Amon, A., Irniger, S. & Nasmyth, K. Closing the cell cycle circle in yeast: G2 cyclin proteolysis initiated at mitosis persists until the activation of G1 cyclins in the next cycle. Cell 77, 1037-1050 (1994). (Pubitemid 24208863)
4. Musacchio, A. & Salmon, E. D. The spindle-assembly checkpoint in space and time. Nature Rev. Mol. Cell Biol. 8, 379-393 (2007). (Pubitemid 46643240)
5. Pesin, J. A. & Orr-Weaver, T. L. Regulation of APC/C activators in mitosis and meiosis. Annu. Rev. Cell Dev. Biol. 24, 475-499 (2008).
6. Verlhac, M. H., Terret, M. E. & Pintard, L. Control of the oocyte-to-embryo transition by the ubiquitin-proteolytic system in mouse and C. elegans. Curr. Opin. Cell Biol. 22, 758-763 (2010).
7. Schreiber, A. et al. Structural basis for the subunit assembly of the anaphase-promoting complex. Nature 470, 227-232 (2011).
8. Vodermaier, H. C., Gieffers, C., Maurer-Stroh, S., Eisenhaber, F. & Peters, J. M. TPR subunits of the anaphase-promoting complex mediate binding to the activator protein CDH1. Curr. Biol. 13, 1459-1468 (2003). (Pubitemid 37078402)
9. Thornton, B. R. et al. An architectural map of the anaphase-promoting complex. Genes Dev. 20, 449-460 (2006). (Pubitemid 43244399)
10. Gmachl, M., Gieffers, C., Podtelejnikov, A. V., Mann, M. & Peters, J. M. The RING-H2 finger protein APC11 and the E2 enzyme UBC4 are sufficient to ubiquitinate substrates of the anaphase-promoting complex. Proc. Natl Acad. Sci. USA 97, 8973-8978 (2000). (Pubitemid 30626658)
11. Tang, Z. et al. APC2 cullin protein and APC11 RING protein comprise the minimal ubiquitin ligase module of the anaphase-promoting complex. Mol. Biol. Cell 12, 3839-3851 (2001). (Pubitemid 34001077)
12. Ohi, M. D. et al. Structural organization of the anaphase-promoting complex bound to the mitotic activator Slp1. Mol. Cell 28, 871-885 (2007). (Pubitemid 350217056)
13. Passmore, L. A. et al. Structural analysis of the anaphase-promoting complex reveals multiple active sites and insights into polyubiquitylation. Mol. Cell 20, 855-866 (2005). (Pubitemid 41814875)
14. Herzog, F. et al. Structure of the anaphase-promoting complex/cyclosome interacting with a mitotic checkpoint complex. Science 323, 1477-1481 (2009).
15. Gieffers, C., Dube, P., Harris, J. R., Stark, H. & Peters, J. M. Three-dimensional structure of the anaphase-promoting complex. Mol. Cell 7, 907-913 (2001). (Pubitemid 32436450)
16. da Fonseca, P. C. A. et al. Structures of APC/CCdh1 with substrates identify Cdh1 and Apc10 as the D-box co-receptor. Nature 470, 274-278 (2011).
17. Buschhorn, B. A. et al. Substrate binding on the APC/C occurs between the coactivator Cdh1 and the processivity factor Doc1. Nature Struct. Mol. Biol. 18, 6-13 (2011).
18. Carroll, C. W. & Morgan, D. O. The Doc1 subunit is a processivity factor for the anaphase-promoting complex. Nature Cell Biol. 4, 880-887 (2002). (Pubitemid 35331363)
19. Carroll, C. W., Enquist-Newman, M. & Morgan, D. O. The APC subunit Doc1 promotes recognition of the substrate destruction box. Curr. Biol. 15, 11-18 (2005).
20. Passmore, L. A. et al. Doc1 mediates the activity of the anaphase-promoting complex by contributing to substrate recognition. EMBO J. 22, 786-796 (2003). (Pubitemid 36227781)
21. Passmore, L. A. & Barford, D. Coactivator functions in a stoichiometric complex with anaphase-promoting complex/cyclosome to mediate substrate recognition. EMBO Rep. 6, 873-878 (2005). (Pubitemid 43108679)
22. Matyskiela, M. E. & Morgan, D. O. Analysis of activator-binding sites on the APC/C supports a cooperative substrate-binding mechanism. Mol. Cell 34, 68-80 (2009).
23. Izawa, D. & Pines, J. How APC/C-Cdc20 changes its substrate specificity in mitosis. Nature Cell Biol. 13, 223-233 (2011). References 22 and 23 provide biochemical evidence that the APC/C binds substrates through a bipartite degron receptor involving a co-activator.
24. Mailand, N. & Diffley, J. F. CDKs promote DNA replication origin licensing in human cells by protecting Cdc6 from APC/C-dependent proteolysis. Cell 122, 915-926 (2005). (Pubitemid 41345208)
25. Holt, L. J., Krutchinsky, A. N. & Morgan, D. O. Positive feedback sharpens the anaphase switch. Nature 454, 353-357 (2008).
26. Rodier, G., Coulombe, P., Tanguay, P. L., Boutonnet, C. & Meloche, S. Phosphorylation of Skp2 regulated by CDK2 and Cdc14B protects it from degradation by APCCdh1 in G1 phase. EMBO J. 27, 679-691 (2008). (Pubitemid 351273128)
27. Choi, E. et al. BubR1 acetylation at prometaphase is required for modulating APC/C activity and timing of mitosis. EMBO J. 28, 2077-2089 (2009).
28. Yamano, H., Tsurumi, C., Gannon, J. & Hunt, T. The role of the destruction box and its neighbouring lysine residues in cyclin B for anaphase ubiquitin-dependent proteolysis in fission yeast: defining the D-box receptor. EMBO J. 17, 5670-5678 (1998). (Pubitemid 28445978)
29. King, R. W., Glotzer, M. & Kirschner, M. W. Mutagenic analysis of the destruction signal of mitotic cyclins and structural characterization of ubiquitinated intermediates. Mol. Biol. Cell 7, 1343-1357 (1996). (Pubitemid 26304198)
30. Jin, L., Williamson, A., Banerjee, S., Philipp, I. & Rape, M. Mechanism of ubiquitin-chain formation by the human anaphase-promoting complex. Cell 133, 653-665 (2008). (Pubitemid 351636306)
31. Summers, M. K., Pan, B., Mukhyala, K. & Jackson, P. K. The unique N terminus of the UbcH10 E2 enzyme controls the threshold for APC activation and enhances checkpoint regulation of the APC. Mol. Cell 31, 544-556 (2008).
32. Williamson, A. et al. Identification of a physiological E2 module for the human anaphase-promoting complex. Proc. Natl Acad. Sci. USA 106, 18213-18218 (2009).
33. Rodrigo-Brenni, M. C., Foster, S. A. & Morgan, D. O. Catalysis of lysine 48-specific ubiquitin chain assembly by residues in E2 and ubiquitin. Mol. Cell 39, 548-559 (2010).
34. Garnett, M. J. et al. UBE2S elongates ubiquitin chains on APC/C substrates to promote mitotic exit. Nature Cell Biol. 11, 1363-1369 (2009).
35. Wu, T. et al. UBE2S drives elongation of K11-linked ubiquitin chains by the anaphase-promoting complex. Proc. Natl Acad. Sci. USA 107, 1355-1360 (2010).
36. Seino, H., Kishi, T., Nishitani, H. & Yamao, F. Two ubiquitin-conjugating enzymes, UbcP1/Ubc4 and UbcP4/Ubc11, have distinct functions for ubiquitination of mitotic cyclin. Mol. Cell. Biol. 23, 3497-3505 (2003). (Pubitemid 36539182)
37. Mathe, E. et al. The E2-C vihar is required for the correct spatiotemporal proteolysis of cyclin B and itself undergoes cyclical degradation. Curr. Biol. 14, 1723-1733 (2004). (Pubitemid 39301161)
38. Townsley, F. M., Aristarkhov, A., Beck, S., Hershko, A. & Ruderman, J. V. Dominant-negative cyclin-selective ubiquitin carrier protein E2-C/UbcH10 blocks cells in metaphase. Proc. Natl Acad. Sci. USA 94, 2362-2367 (1997). (Pubitemid 27136880)
39. Rape, M. & Kirschner, M. W. Autonomous regulation of the anaphase-promoting complex couples mitosis to S-phase entry. Nature 432, 588-595 (2004). (Pubitemid 39626259)
40. Kirkpatrick, D. S. et al. Quantitative analysis of in vitro ubiquitinated cyclin B1 reveals complex chain topology. Nature Cell Biol. 8, 700-710 (2006).
41. Nasmyth, K. Segregating sister genomes: the molecular biology of chromosome separation. Science 297, 559-565 (2002). (Pubitemid 34815333)
42. McGarry, T. J. & Kirschner, M. W. Geminin, an inhibitor of DNA replication, is degraded during mitosis. Cell 93, 1043-1053 (1998). (Pubitemid 28280797)
43. Littlepage, L. E. & Ruderman, J. V. Identification of a new APC/C recognition domain, the A box, which is required for the Cdh1-dependent destruction of the kinase Aurora-A during mitotic exit. Genes Dev. 16, 2274-2285 (2002). (Pubitemid 35013090)
44. Lindon, C. & Pines, J. Ordered proteolysis in anaphase inactivates Plk1 to contribute to proper mitotic exit in human cells. J. Cell Biol. 164, 233-241 (2004). (Pubitemid 38133943)
45. Castro, A. et al. The D-Box-activating domain (DAD) is a new proteolysis signal that stimulates the silent D-Box sequence of Aurora-A. EMBO Rep. 3, 1209-1214 (2002). (Pubitemid 36105012)
46. 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). (Pubitemid 30437613)
47. Kraft, C. et al. Mitotic regulation of the human anaphase-promoting complex by phosphorylation. EMBO J. 22, 6598-6609 (2003). (Pubitemid 38009606)
48. 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). (Pubitemid 29351806)
49. Rudner, A. D., Hardwick, K. G. & Murray, A. W. Cdc28 activates exit from mitosis in budding yeast. J. Cell Biol. 149, 1361-1376 (2000). (Pubitemid 30437612)
50. Cross, F. R. Two redundant oscillatory mechanisms in the yeast cell cycle. Dev. Cell 4, 741-752 (2003). (Pubitemid 36564903)
51. Kotani, S. et al. PKA and MPF-activated Polo-like kinase regulate anaphase-promoting complex activity and mitosis progression. Mol. Cell 1, 371-380 (1998). (Pubitemid 128378885)
52. Reimann, J. D. et al. Emi1 is a mitotic regulator that interacts with Cdc20 and inhibits the anaphase promoting complex. Cell 105, 645-655 (2001). (Pubitemid 32524117)
53. Hansen, D. V., Loktev, A. V., Ban, K. H. & Jackson, P. K. Plk1 regulates activation of the anaphase promoting complex by phosphorylating and triggering SCF?TrCP-dependent destruction of the APC inhibitor Emi1. Mol. Biol. Cell 15, 5623-5634 (2004). (Pubitemid 39564753)
54. Moshe, Y., Boulaire, J., Pagano, M. & Hershko, A. Role of Polo-like kinase in the degradation of early mitotic inhibitor 1, a regulator of the anaphase promoting complex/cyclosome. Proc. Natl Acad. Sci. USA 101, 7937-7942 (2004). (Pubitemid 38698032)
55. Di Fiore, B. & Pines, J. 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 (2007). (Pubitemid 46718272)
56. Lenart, P. et al. The small-molecule inhibitor BI 2536 reveals novel insights into mitotic roles of Polo-like kinase 1. Curr. Biol. 17, 304-315 (2007).
57. 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). Evidence that CDC20 may have additional properties in activating the APC/C, aside from forming a degron receptor.
58. Saha, A. & Deshaies, R. J. Multimodal activation of the ubiquitin ligase SCF by Nedd8 conjugation. Mol. Cell 32, 21-31 (2008).
59. Duda, D. M. et al. Structural insights into NEDD8 activation of cullin-RING ligases: conformational control of conjugation. Cell 134, 995-1006 (2008).
60. Gavet, O. & Pines, J. Activation of Cyclin B1-Cdk1 synchronizes events in the nucleus and the cytoplasm at mitosis. J. Cell Biol. 189, 247-259 (2010).
61. Wolthuis, R. et al. Cdc20 and Cks direct the spindle checkpoint- independent destruction of cyclin A. Mol. Cell 30, 290-302 (2008). (Pubitemid 351615313)
62. Geley, S. et al. APC/C-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).
63. Di Fiore, B. & Pines, J. How cyclin A destruction escapes the spindle assembly checkpoint. J. Cell Biol. 190, 501-509 (2010).
64. den Elzen, N. & Pines, J. Cyclin A is destroyed in prometaphase and can delay chromosome alignment and anaphase. J. Cell Biol. 153, 121-136 (2001).
65. Rieder, C. L., Cole, R. W., Khodjakov, A. & Sluder, G. The checkpoint delaying anaphase in response to chromosome monoorientation is mediated by an inhibitory signal produced by unattached kinetochores. J. Cell Biol. 130, 941-948 (1995).
66. Zich, J. & Hardwick, K. G. Getting down to the phosphorylated nuts and bolts of spindle checkpoint signalling. Trends Biochem. Sci. 35, 18-27 (2010).
67. De Antoni, A. et al. The Mad1/Mad2 complex as a template for Mad2 activation in the spindle assembly checkpoint. Curr. Biol. 15, 214-225 (2005). (Pubitemid 40205701)
68. Kulukian, A., Han, J. S. & Cleveland, D. W. Unattached kinetochores catalyze production of an anaphase inhibitor that requires a Mad2 template to prime Cdc20 for BubR1 binding. Dev. Cell 16, 105-117 (2009).
69. Fang, G. Checkpoint protein BubR1 acts synergistically with Mad2 to inhibit anaphase-promoting complex. Mol. Biol. Cell 13, 755-766 (2002). (Pubitemid 34250344)
70. 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). (Pubitemid 34286173)
71. Burton, J. L. & Solomon, M. J. Mad3p, a pseudosubstrate inhibitor of APCCdc20 in the spindle assembly checkpoint. Genes Dev. 21, 655-667 (2007). (Pubitemid 46440288)
72. King, E. M., van der Sar, S. J. & Hardwick, K. G. Mad3 KEN boxes mediate both Cdc20 and Mad3 turnover, and are critical for the spindle checkpoint. PLoS ONE 2, e342 (2007).
73. Reddy, S. K., Rape, M., Margansky, W. A. & Kirschner, M. W. Ubiquitination by the anaphase-promoting complex drives spindle checkpoint inactivation. Nature 446, 921-925 (2007). (Pubitemid 46633168)
74. Stegmeier, F. et al. Anaphase initiation is regulated by antagonistic ubiquitination and deubiquitination activities. Nature 446, 876-881 (2007).
75. Pan, J. & Chen, R. H. Spindle checkpoint regulates Cdc20p stability in Saccharomyces cerevisiae. Genes Dev. 18, 1439-1451 (2004). (Pubitemid 38780630)
76. Nilsson, J., Yekezare, M., Minshull, J. & Pines, J. The APC/C maintains the spindle assembly checkpoint by targeting Cdc20 for destruction. Nature Cell Biol. 10, 1411-1420 (2008).
77. Ge, S., Skaar, J. R. & Pagano, M. APC/C- and Mad2-mediated degradation of Cdc20 during spindle checkpoint activation. Cell Cycle 8, 167-171 (2009).
78. Song, M. S. et al. The tumour suppressor RASSF1A regulates mitosis by inhibiting the APC-Cdc20 complex. Nature Cell Biol. 6, 129-37 (2004). (Pubitemid 38425712)
79. Jeganathan, K. B., Malureanu, L. & van Deursen, J. M. The Rae1-Nup98 complex prevents aneuploidy by inhibiting securin degradation. Nature 438, 1036-1039 (2005). (Pubitemid 43093978)
80. Tommasi, S. et al. Tumor susceptibility of Rassf1a knockout mice. Cancer Res. 65, 92-98 (2005). (Pubitemid 40070799)
81. Wang, Q. et al. BUBR1 deficiency results in abnormal megakaryopoiesis. Blood 103, 1278-1285 (2004). (Pubitemid 38168638)
82. Dobles, M., Liberal, V., Scott, M. L., Benezra, R. & Sorger, P. K. Chromosome missegregation and apoptosis in mice lacking the mitotic checkpoint protein Mad2. Cell 101, 635-645 (2000).
83. Hayes, M. J. et al. Early mitotic degradation of Nek2A depends on Cdc20-independent interaction with the APC/C. Nature Cell Biol. 8, 607-614 (2006). (Pubitemid 43827354)
84. Gabellini, D. et al. Early mitotic degradation of the homeoprotein HOXC10 is potentially linked to cell cycle progression. EMBO J. 22, 3715-3724 (2003). (Pubitemid 36898348)
85. Clute, P. & Pines, J. Temporal and spatial control of cyclin B1 destruction in metaphase. Nature Cell Biol. 1, 82-87 (1999). (Pubitemid 129501948)
86. Acquaviva, C., Herzog, F., Kraft, C. & Pines, J. The anaphase promoting complex/cyclosome is recruited to centromeres by the spindle assembly checkpoint. Nature Cell Biol. 6, 892-898 (2004). (Pubitemid 39207254)
87. Huang, J. & Raff, J. W. The disappearance of cyclin B at the end of mitosis is regulated spatially in Drosophila cells. EMBO J. 18, 2184-2195 (1999). (Pubitemid 29179175)
88. Manchado, E. et al. Targeting mitotic exit leads to tumor regression in vivo: modulation by Cdk1, Mastl, and the PP2A/B55, phosphatase. Cancer Cell 18, 641-654 (2010).
89. Li, M., York, J. P. & Zhang, P. Loss of Cdc20 causes a securin-dependent metaphase arrest in two-cell mouse embryos. Mol. Cell. Biol. 27, 3481-3488 (2007). (Pubitemid 46685222)
90. Huang, H. C., Shi, J., Orth, J. D. & Mitchison, T. J. Evidence that mitotic exit is a better cancer therapeutic target than spindle assembly. Cancer Cell 16, 347-358 (2009).
91. Chow, J. P., Poon, R. Y. & Ma, H. T. Inhibitory phosphorylation of CDK1 as a compensatory mechanism for mitosis exit. Mol. Cell. Biol. 31, 1478-1491 (2011).
92. Baumgarten, A. J., Felthaus, J. & Wasch, R. Strong inducible knockdown of APC/CCdc20 does not cause mitotic arrest in human somatic cells. Cell Cycle 8, 643-646 (2009).
93. Kraft, C., Vodermaier, H. C., Maurer-Stroh, S., Eisenhaber, F. & Peters, J. M. The WD40 propeller domain of Cdh1 functions as a destruction box receptor for APC/C substrates. Mol. Cell 18, 543-553 (2005). (Pubitemid 40726231)
94. Hagting, A. et al. 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 (2002). (Pubitemid 34847784)
95. Sigl, R. et al. Loss of the mammalian APC/C activator FZR1 shortens G1 and lengthens S phase but has little effect on exit from mitosis. J. Cell Sci. 122, 4208-4217 (2009).
96. Garcia-Higuera, I. et al. Genomic stability and tumour suppression by the APC/C cofactor Cdh1. Nature Cell Biol. 10, 802-811 (2008).
97. Floyd, S., Pines, J. & Lindon, C. APC/C Cdh1 targets Aurora kinase to control reorganization of the mitotic spindle at anaphase. Curr. Biol. 18, 1649-1658 (2008).
98. Sigrist, S. J. & Lehner, C. F. Drosophila Fizzy-related down-regulates mitotic cyclins and is required for cell proliferation arrest and entry into endocycles. Cell 90, 671-681 (1997). (Pubitemid 27357959)
99. Blanco, M. A., Sanchez-Diaz, A., de Prada, J. M. & Moreno, S. APCste9/srw1 promotes degradation of mitotic cyclins in G1 and is inhibited by cdc2 phosphorylation. EMBO J. 19, 3945-3955 (2000). (Pubitemid 30608534)
100. Schwab, M., Lutum, A. S. & Seufert, W. Yeast Hct1 is a regulator of Clb2 cyclin proteolysis. Cell 90, 683-693 (1997). (Pubitemid 27357960)
101. Visintin, R., Prinz, S. & Amon, A. CDC20 and CDH1: a family of substrate-specific activators of APC-dependent proteolysis. Science 278, 460-463 (1997). (Pubitemid 27454429)
102. DAmours, D. & Amon, A. At the interface between signaling and executing anaphase-Cdc14 and the FEAR network. Genes Dev. 18, 2581-2595 (2004). (Pubitemid 39453097)
103. Rape, M., Reddy, S. K. & Kirschner, M. W. The processivity of multiubiquitination by the APC determines the order of substrate degradation. Cell 124, 89-103 (2006). (Pubitemid 43069312)
104. Bashir, T., Dorrello, N. V., Amador, V., Guardavaccaro, D. & Pagano, M. Control of the SCFSkp2-Cks1 ubiquitin ligase by the APC/CCdh1 ubiquitin ligase. Nature 428, 190-193 (2004). (Pubitemid 38374316)
105. Wei, W. et al. Degradation of the SCF component Skp2 in cell-cycle phase G1 by the anaphase-promoting complex. Nature 428, 194-198 (2004). (Pubitemid 38374317)
106. Kominami, K., Seth-Smith, H. & Toda, T. Apc10 and Ste9/Srw1, two regulators of the APC-cyclosome, as well as the CDK inhibitor Rum1 are required for G1 cell-cycle arrest in fission yeast. EMBO J. 17, 5388-5399 (1998). (Pubitemid 28427052)
107. Kitamura, K., Maekawa, H. & Shimoda, C. Fission yeast Ste9, a homolog of Hct1/Cdh1 and Fizzy-related, is a novel negative regulator of cell cycle progression during G1-phase. Mol. Biol. Cell 9, 1065-1080 (1998). (Pubitemid 28457300)
108. Wasch, R. & Cross, F. R. APC-dependent proteolysis of the mitotic cyclin Clb2 is essential for mitotic exit. Nature 418, 556-562 (2002). (Pubitemid 34851404)
109. Jorgensen, P., Nishikawa, J. L., Breitkreutz, B. J. & Tyers, M. Systematic identification of pathways that couple cell growth and division in yeast. Science 297, 395-400 (2002). (Pubitemid 34790768)
110. Sudo, T. et al. Activation of Cdh1-dependent APC is required for G1 cell cycle arrest and DNA damage-induced G2 checkpoint in vertebrate cells. EMBO J. 20, 6499-6508 (2001). (Pubitemid 33078722)
111. Mocciaro, A. et al. Vertebrate cells genetically deficient for Cdc14A or Cdc14B retain DNA damage checkpoint proficiency but are impaired in DNA repair. J. Cell Biol. 189, 631-639 (2010).
112. Bassermann, F. et al. The Cdc14B-Cdh1-Plk1 axis controls the G2 DNA-damage-response checkpoint. Cell 134, 256-267 (2008). (Pubitemid 352010329)
113. Matsumoto, T. A fission yeast homolog of cdc20/p55cdc/Fizzy is required for recovery from DNA damage and genetically interacts with p34cdc2. Mol. Cell. Biol. 17, 742-750 (1997).
114. Jaspersen, S. L., Charles, J. F. & Morgan, D. O. Inhibitory phosphorylation of the APC regulator Hct1 is controlled by the kinase Cdc28 and the phosphatase Cdc14. Curr. Biol. 9, 227-236 (1999). (Pubitemid 29139305)
115. Zachariae, W., Schwab, M., Nasmyth, K. & Seufert, W. Control of cyclin ubiquitination by CDK-regulated binding of Hct1 to the anaphase promoting complex. Science 282, 1721-1724 (1998). (Pubitemid 28549290)
116. Reber, A., Lehner, C. F. & Jacobs, H. W. Terminal mitoses require negative regulation of Fzr/Cdh1 by Cyclin A, preventing premature degradation of mitotic cyclins and String/Cdc25. Development 133, 3201-3211 (2006). (Pubitemid 44404343)
117. Lukas, C. et al. Accumulation of cyclin B1 requires E2F and cyclin-A-dependent rearrangement of the anaphase-promoting complex. Nature 401, 815-818 (1999).
118. Hsu, J. Y., Reimann, J. D., Sorensen, C. S., Lukas, J. & Jackson, P. K. E2F-dependent accumulation of hEmi1 regulates S phase entry by inhibiting APCCdh1. Nature Cell Biol. 4, 358-366 (2002). (Pubitemid 34521031)
119. Machida, Y. J. & Dutta, A. The APC/C inhibitor, Emi1, is essential for prevention of rereplication. Genes Dev. 21, 184-194 (2007). (Pubitemid 46155812)
120. Martinez, J. S., Jeong, D. E., Choi, E., Billings, B. M. & Hall, M. C. Acm1 is a negative regulator of the CDH1-dependent anaphase-promoting complex/cyclosome in budding yeast. Mol. Cell. Biol. 26, 9162-9176 (2006). (Pubitemid 44904413)
121. Grosskortenhaus, R. & Sprenger, F. Rca1 inhibits APC-Cdh1Fzr and is required to prevent cyclin degradation in G2. Dev. Cell 2, 29-40 (2002). (Pubitemid 34065904)
122. Ostapenko, D., Burton, J. L., Wang, R. & Solomon, M. J. Pseudosubstrate inhibition of the anaphase-promoting complex by Acm1: regulation by proteolysis and Cdc28 phosphorylation. Mol. Cell. Biol. 28, 4653-4664 (2008).
123. Enquist-Newman, M., Sullivan, M. & Morgan, D. O. Modulation of the mitotic regulatory network by APC-dependent destruction of the Cdh1 inhibitor Acm1. Mol. Cell 30, 437-446 (2008). (Pubitemid 351672373)
124. Miller, J. J. et al. Emi1 stably binds and inhibits the anaphase-promoting complex/cyclosome as a pseudosubstrate inhibitor. Genes Dev. 20, 2410-2420 (2006). (Pubitemid 44320389)
125. Tang, W. et al. Emi2-mediated inhibition of E2-substrate ubiquitin transfer by the APC/C through a D-Box-independent mechanism. Mol. Biol. Cell 21, 2589-2597 (2010).
126. Walker, A., Acquaviva, C., Matsusaka, T., Koop, L. & Pines, J. UbcH10 has a rate-limiting role in G1 phase but might not act in the spindle checkpoint or as part of an autonomous oscillator. J. Cell Sci. 121, 2319-2326 (2008).
127. Zielke, N., Querings, S., Rottig, C., Lehner, C. & Sprenger, F. The anaphase-promoting complex/ cyclosome (APC/C) is required for rereplication control in endoreplication cycles. Genes Dev. 22, 1690-1703 (2008). (Pubitemid 351846847)
128. Lee, H. et al. Mouse emi1 has an essential function in mitotic progression during early embryogenesis. Mol. Cell. Biol. 26, 5373-5381 (2006). (Pubitemid 44036206)
129. Geng, Y. et al. Cyclin E ablation in the mouse. Cell 114, 431-443 (2003). (Pubitemid 37100992)
130. Wirth, K. G. et al. Loss of the anaphase-promoting complex in quiescent cells causes unscheduled hepatocyte proliferation. Genes Dev. 18, 88-98 (2004). (Pubitemid 38090690)
131. Konishi, Y., Stegmuller, J., Matsuda, T., Bonni, S. & Bonni, A. Cdh1-APC controls axonal growth and patterning in the mammalian brain. Science 303, 1026-1030 (2004). (Pubitemid 38209709)
132. van Roessel, P., Elliott, D. A., Robinson, I. M., Prokop, A. & Brand, A. H. Independent regulation of synaptic size and activity by the anaphase-promoting complex. Cell 119, 707-718 (2004). (Pubitemid 39535757)
133. Yang, Y. et al. A Cdc20-APC ubiquitin signaling pathway regulates presynaptic differentiation. Science 326, 575-578 (2009).
134. Malureanu, L. A. et al. BubR1 N terminus acts as a soluble inhibitor of cyclin B degradation by APC/CCdc20 in interphase. Dev. Cell 16, 118-131 (2009).
135. Maciejowski, J. et al. Mps1 directs the assembly of Cdc20 inhibitory complexes during interphase and mitosis to control M phase timing and spindle checkpoint signaling. J. Cell Biol. 190, 89-100 (2010).
136. Hwang, L. H. & Murray, A. W. A novel yeast screen for mitotic arrest mutants identifies DOC1, a new gene involved in cyclin proteolysis. Mol. Biol. Cell 8, 1877-1887 (1997). (Pubitemid 27451108)
137. Hershko, A. & Ciechanover, A. The ubiquitin system. Annu. Rev. Biochem. 67, 425-479 (1998). (Pubitemid 28411135)
138. Pines, J. Mitosis: a matter of getting rid of the right protein at the right time. Trends Cell Biol. 16, 55-63 (2006). (Pubitemid 43077095)
139. Uhlmann, F., Lottspeich, F. & Nasmyth, K. Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1. Nature 400, 37-42 (1999). (Pubitemid 29315102)
140. Hauf, S., Waizenegger, I. C. & Peters, J. M. Cohesin cleavage by separase required for anaphase and cytokinesis in human cells. Science 293, 1320-1323 (2001). (Pubitemid 32777422)