To cell cycle, swing the APC/C

Biochimica et Biophysica Acta - Reviews on Cancer

Volumn 1786, Issue 1, 2008, Pages 49-59

  van Leuken, Renske ^a,b   Clijsters, Linda ^b   Wolthuis, Rob ^b  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

APC C; Cdc20; Cdh1; Cell cycle; Cyclin A; Cyclin B1; Cyclosome; Geminin; Mitosis; pRb; Securin

Indexed keywords

ANAPHASE PROMOTING COMPLEX; CYCLIN B1; PACLITAXEL;

CATALYSIS; CELL CYCLE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL SURVIVAL; DNA DAMAGE; ENZYME ACTIVITY; HUMAN; IN VITRO STUDY; MITOSIS; PRIORITY JOURNAL; PROPHASE; REVIEW; SPINDLE CELL; TUMOR CELL; UBIQUITINATION; X RAY CRYSTALLOGRAPHY;

CADHERINS; CDC2 PROTEIN KINASE; CELL CYCLE; CELL CYCLE PROTEINS; CYCLIN B; DNA DAMAGE; G2 PHASE; HUMANS; MITOTIC SPINDLE APPARATUS; MODELS, MOLECULAR; NEOPLASM PROTEINS; NEOPLASMS; S PHASE; UBIQUITIN-PROTEIN LIGASE COMPLEXES; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 51649096355     PISSN: 0304419X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbcan.2008.05.002     Document Type: Review

References (181)

1. Hershko A., and Ciechanover A. The ubiquitin system for protein degradation. Annu. Rev. Biochem. 61 (1992) 761-807
2. Reed S.I. Ratchets and clocks: the cell cycle, ubiquitylation and protein turnover. Nat. Rev., Mol. Cell Biol. 4 (2003) 855-864
3. Pagano M. Cell cycle regulation by the ubiquitin pathway. FASEB J. 11 (1997) 1067-1075
4. Hershko A., and Ciechanover A. The ubiquitin system. Annu. Rev. Biochem. 67 (1998) 425-479
5. Pickart C.M., and Eddins M.J. Ubiquitin: structures, functions, mechanisms. Biochim. Biophys. Acta 1695 (2004) 55-72
6. Scolnick D.M., and Halazonetis T.D. Chfr defines a mitotic stress checkpoint that delays entry into metaphase. Nature 406 (2000) 430-435
7. Brooks C.L., and Gu W. p53 ubiquitination: Mdm2 and beyond. Mol. Cell 21 (2006) 307-315
8. Nijman S.M., Luna-Vargas M.P., Velds A., Brummelkamp T.R., Dirac A.M., Sixma T.K., and Bernards R. A genomic and functional inventory of deubiquitinating enzymes. Cell 123 (2005) 773-786
9. Ovaa H., Kessler B.M., Rolen U., Galardy P.J., Ploegh H.L., and Masucci M.G. Activity-based ubiquitin-specific protease (USP) profiling of virus-infected and malignant human cells. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 2253-2258
10. Vodermaier H.C. APC/C and SCF: controlling each other and the cell cycle. Curr. Biol. 14 (2004) R787-R796
11. Harper J.W. A phosphorylation-driven ubiquitination switch for cell-cycle control. Trends Cell Biol. 12 (2002) 104-107
12. Yu H., Peters J.M., King R.W., Page A.M., Hieter P., and Kirschner M.W. Identification of a cullin homology region in a subunit of the anaphase-promoting complex. Science 279 (1998) 1219-1222
13. Leverson J.D., Joazeiro C.A., Page A.M., Huang H., Hieter P., and Hunter T. The APC11 RING-H2 finger mediates E2-dependent ubiquitination. Mol. Biol. Cell 11 (2000) 2315-2325
14. Tang Z., Li B., Bharadwaj R., Zhu H., Ozkan E., Hakala K., Deisenhofer J., and Yu H. APC2 Cullin protein and APC11 RING protein comprise the minimal ubiquitin ligase module of the anaphase-promoting complex. Mol. Biol. Cell 12 (2001) 3839-3851
15. Steen J.A., Steen H., Georgi A., Parker K., Springer M., Kirchner M., Hamprecht F., and Kirschner M.W. Different phosphorylation states of the anaphase promoting complex in response to antimitotic drugs: a quantitative proteomic analysis. Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 6069-6074
16. Townsley F.M., Aristarkhov A., Beck S., Hershko A., and Ruderman J.V. Dominant-negative cyclin-selective ubiquitin carrier protein E2-C/UbcH10 blocks cells in metaphase. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 2362-2367
17. Zachariae W., and Nasmyth K. Whose end is destruction: cell division and the anaphase-promoting complex. Genes Dev. 13 (1999) 2039-2058
18. Pines J. Mitosis: a matter of getting rid of the right protein at the right time. Trends Cell Biol. 16 (2006) 55-63
19. Visintin R., Prinz S., and Amon A. CDC20 and CDH1: a family of substrate-specific activators of APC-dependent proteolysis. Science 278 (1997) 460-463
20. Burton J.L., and Solomon M.J. 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 (2001) 2381-2395
21. Pfleger C.M., Lee E., and Kirschner M.W. Substrate recognition by the Cdc20 and Cdh1 components of the anaphase-promoting complex. Genes Dev. 15 (2001) 2396-2407
22. Yu H. Cdc20: a WD40 activator for a cell cycle degradation machine. Mol. Cell 27 (2007) 3-16
23. Peters J.M. The anaphase promoting complex/cyclosome: a machine designed to destroy. Nat. Rev., Mol. Cell Biol. 7 (2006) 644-656
24. Hwang L.H., Lau L.F., Smith D.L., Mistrot C.A., Hardwick K.G., Hwang E.S., Amon A., and Murray A.W. Budding yeast Cdc20: a target of the spindle checkpoint. Science 279 (1998) 1041-1044
25. De Antoni A., Pearson C.G., Cimini D., Canman J.C., Sala V., Nezi L., Mapelli M., Sironi L., Faretta M., Salmon E.D., and Musacchio A. The Mad1/Mad2 complex as a template for Mad2 activation in the spindle assembly checkpoint. Curr. Biol. 15 (2005) 214-215
26. Uhlmann F. The mechanism of sister chromatid cohesion. Exp. Cell Res. 296 (2004) 80-85
27. Di Fiore B., and 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 (2007) 425-437
28. Machida Y.J., and Dutta A. The APC/C inhibitor, Emi1, is essential for prevention of rereplication. Genes Dev. 21 (2007) 184-194
29. Verschuren E.W., Ban K.H., Masek M.A., Lehman N.L., and Jackson P.K. Loss of Emi1-dependent anaphase-promoting complex/cyclosome inhibition deregulates E2F target expression and elicits DNA damage-induced senescence. Mol. Cell. Biol. 27 (2007) 7955-7965
30. Reimann J.D., Gardner B.E., Margottin-Goguet F., and Jackson P.K. Emi1 regulates the anaphase-promoting complex by a different mechanism than Mad2 proteins. Genes Dev. 15 (2001) 3278-3285
31. Jaspersen S.L., Charles J.F., and Morgan D.O. Inhibitory phosphorylation of the APC regulator Hct1 is controlled by the kinase Cdc28 and the phosphatase Cdc14. Curr. Biol. 9 (1999) 227-236
32. Visintin R., Craig K., Hwang E.S., Prinz S., Tyers M., and Amon A. The phosphatase Cdc14 triggers mitotic exit by reversal of Cdk-dependent phosphorylation. Mol. Cell 2 (1998) 709-718
33. Margottin-Goguet F., Hsu J.Y., Loktev A., Hsieh H.M., Reimann J.D., and Jackson P.K. Prophase destruction of Emi1 by the SCF(BetaTrCP/Slimb) ubiquitin ligase activates the anaphase promoting complex to allow progression beyond prometaphase. Dev. Cell 6 (2003) 813-826
34. Lindqvist A., van Zon W., Karlsson Rosenthal C., and Wolthuis R.M. Cyclin B1-Cdk1 activation continues after centrosome separation to control mitotic progression. PLoS Biol. 5 (2007) e123
35. Jeganathan K.B., Malureanu L., and van Deursen J.M. The Rae1-Nup98 complex prevents aneuploidy by inhibiting securin degradation. Nature 438 (2005) 1036-1039
36. Zachariae W., Schwab M., Nasmyth K., and Seufert W. Control of cyclin ubiquitination by CDK-regulated binding of Hct1 to the anaphase promoting complex. Science 282 (1998) 1721-1724
37. Lukas C., Sorensen C.S., Kramer E., Santoni-Rugiu E., Lindeneg C., Peters J.M., Bartek J., and Lukas J. Accumulation of cyclin B1 requires E2F and cyclin-A-dependent rearrangement of the anaphase-promoting complex. Nature 401 (1999) 815-818
38. Engelbert D., Schnerch D., Baumgarten A., and Wasch R. The ubiquitin ligase APC(Cdh1) is required to maintain genome integrity in primary human cells. Oncogene 27 (2007) 907-917
39. Kramer E.R., Scheuringer N., Podtelejnikov A.V., Mann M., and Peters J.M. Mitotic regulation of the APC activator proteins CDC20 and CDH1. Mol. Biol. Cell 11 (2000) 1555-1569
40. Pfleger C.M., and Kirschner M.W. The KEN box: an APC recognition signal distinct from the D box targeted by Cdh1. Genes Dev. 14 (2000) 655-665
41. Bashir T., and Pagano M. Don't skip the G1 phase: how APC/CCdh1 keeps SCFSKP2 in check. Cell Cycle 3 (2004) 850-852
42. Den Elzen N., and Pines J. Cyclin A is destroyed in prometaphase and can delay chromosome alignment and anaphase. J. Cell Biol. 153 (2001) 121-136
43. Geley S., Kramer E., Gieffers C., Gannon J., Peters J.M., and Hunt T. 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 (2001) 137-148
44. Reis A., Levasseur M., Chang H.Y., Elliott D.J., and Jones K.T. The CRY box: a second APCcdh1-dependent degron in mammalian cdc20. EMBO Rep. 7 (2006) 1040-1045
45. Crane R., Kloepfer A., and Ruderman J.V. Requirements for the destruction of human aurora-A. J. Cell. Sci. 117 (2004) 5975-5983
46. Littlepage L.E., and 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 (2002) 2274-2285
47. Castro A., Vigneron S., Bernis C., Labbe J.C., and Lorca T. Xkid is degraded in a D-box, KEN-box, and A-box-independent pathway. Mol. Cell. Biol. 23 (2003) 4126-4138
48. Cox C.J., Dutta K., Petri E.T., Hwang W.C., Lin Y., Pascal S.M., and Basavappa R. The Regions of Securin and Cyclin B Proteins Recognized by the Ubiquitination Machinery Are Natively Unfolded. FEBS Lett. 527 (2002) 303-308
49. Yamano H., Tsurumi C., Gannon J., and 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 (1998) 5670-5678
50. Stegmeier F., Rape M., Draviam V.M., Nalepa G., Sowa M.E., Ang X.L., McDonald III E.R., Li M.Z., Hannon G.J., Sorger P.K., Kirschner M.W., Harper J.W., and Elledge S.J. Anaphase initiation is regulated by antagonistic ubiquitination and deubiquitination activities. Nature 446 (2007) 876-881
51. Rape M., Reddy S.K., and Kirschner M.W. The processivity of multiubiquitination by the APC determines the order of substrate degradation. Cell 124 (2006) 89-103
52. Hayes M.J., Kimata Y., Wattam S.L., Lindon C., Mao G., Yamano H., and Fry A.M. Early mitotic degradation of Nek2A depends on Cdc20-independent interaction with the APC/C. Nat. Cell Biol. 8 (2006) 607-614
53. Yamano H., Gannon J., Mahbubani H., and Hunt T. Cell Cycle-Regulated Recognition of the Destruction Box of Cyclin B by the APC/C in Xenopus Egg Extracts. Mol. Cell. 13 (2004) 137-147
54. Wolthuis R., Clay-Ferrace L., van Zon W., Yekezare M., Koop L., Ogink J., Medema R., and Pines J. Cdc20 and Cks direct the spindle checkpoint-independent destruction of cyclin A. Mol. Cell 30 (2008) 290-302
55. Vodermaier H.C., Gieffers C., Maurer-Stroh S., Eisenhaber F., and Peters J.M. TPR subunits of the anaphase-promoting complex mediate binding to the activator protein CDH1. Curr. Biol. 13 (2003) 1459-1468
56. Zachariae W., and Nasmyth K. TPR proteins required for anaphase progression mediate ubiquitination of mitotic B-type cyclins in yeast. Mol. Biol. Cell 7 (1996) 791-801
57. Kraft C., Vodermaier H.C., Maurer-Stroh S., Eisenhaber F., and Peters J.M. The WD40 propeller domain of Cdh1 functions as a destruction box receptor for APC/C substrates. Mol. Cell 18 (2005) 543-553
58. Ohi M.D., Feoktistova A., Ren L., Yip C., Cheng Y., Chen J.S., Yoon H.J., Wall J.S., Huang Z., Penczek P.A., Gould K.L., and Walz T. Structural organization of the anaphase-promoting complex bound to the mitotic activator slp1. Mol. Cell 28 (2007) 871-885
59. Schwab M., Neutzner M., Mocker D., and Seufert W. Yeast Hct1 recognizes the mitotic cyclin Clb2 and other substrates of the ubiquitin ligase APC. EMBO J. 20 (2001) 5165-5175
60. Thornton B.R., Ng T.M., Matyskiela M.E., Carroll C.W., Morgan D.O., and Toczyski D.P. An architectural map of the anaphase-promoting complex. Genes Dev. 20 (2006) 449-460
61. Carroll C.W., Enquist-Newman M., and Morgan D.O. The APC subunit Doc1 promotes recognition of the substrate destruction box. Curr. Biol. 15 (2005) 11-18
62. Passmore L.A., McCormack E.A., Au S.W., Paul A., Willison K.R., Harper J.W., and Barford D. Doc1 mediates the activity of the anaphase-promoting complex by contributing to substrate recognition. EMBO J. 22 (2003) 786-796
63. Wendt K.S., Vodermaier H.C., Jacob U., Gieffers C., Gmachl M., Peters J.M., Huber R., and Sondermann P. Crystal structure of the APC10/DOC1 subunit of the human anaphase-promoting complex. Nat. Struct. Biol 8 (2001) 784-788
64. W. van Zon, L. Clijsters, J. Ogink, and R. Wolthuis, unpublished observations.
65. Passmore L.A., and Barford D. Coactivator functions in a stoichiometric complex with anaphase-promoting complex/cyclosome to mediate substrate recognition. EMBO Rep. 6 (2005) 873-878
66. Passmore L.A., and Barford D. Getting into position: the catalytic mechanisms of protein ubiquitylation. Biochem. J. 379 (2004) 513-525
67. Eytan E., Moshe Y., Braunstein I., and Hershko A. Roles of the anaphase-promoting complex/cyclosome and of its activator Cdc20 in functional substrate binding. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 2081-2086
68. Gieffers C., Dube P., Harris J.R., Stark H., and Peters J.M. Three-dimensional structure of the anaphase-promoting complex. Mol. Cell 7 (2001) 907-913
69. Passmore L.A., Booth C.R., Venien-Bryan C., Ludtke S.J., Fioretto C., Johnson L.N., Chiu W., and Barford D. Structural analysis of the anaphase-promoting complex reveals multiple active sites and insights into polyubiquitylation. Mol. Cell 20 (2005) 855-866
70. Rodrigo-Brenni M.C., and Morgan D.O. Sequential E2s drive polyubiquitin chain assembly on APC targets. Cell 130 (2007) 127-139
71. Dube P., Herzog F., Gieffers C., Sander B., Riedel D., Muller S.A., Engel A., Peters J.M., and Stark H. Localization of the coactivator Cdh1 and the cullin subunit Apc2 in a cryo-electron microscopy model of vertebrate APC/C. Mol. Cell 20 (2005) 867-879
72. Thornton B.R., and Toczyski D.P. Precise destruction: an emerging picture of the APC. Genes Dev. 20 (2006) 3069-3078
73. Jackman M., Lindon C., Nigg E.A., and Pines J. Active cyclin B1-Cdk1 first appears on centrosomes in prophase. Nat. Cell. Biol. 5 (2003) 143-148
74. Rudner A.D., and Murray A.W. Phosphorylation by Cdc28 Activates the Cdc20-dependent activity of the anaphase-promoting complex. J. Cell. Biol. 149 (2000) 1377-1390
75. Lahav-Baratz S., Sudakin V., Ruderman J.V., and Hershko A. Reversible phosphorylation controls the activity of cyclosome-associated cyclin-ubiquitin ligase. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 9303-9307
76. Kraft C., Herzog F., Gieffers C., Mechtler K., Hagting A., Pines J., and Peters J.M. Mitotic regulation of the human anaphase-promoting complex by phosphorylation. EMBO J. 22 (2003) 6598-6609
77. Golan A., Yudkovsky Y., and Hershko A. The cyclin-ubiquitin ligase activity of cyclosome/APC is jointly activated by protein kinases Cdk1-cyclin B and Plk. J. Biol. Chem. 277 (2002) 15552-15557
78. Lenart P., Petronczki M., Steegmaier M., Di Fiore B., Lipp J.J., Hoffmann M., Rettig W.J., Kraut N., and Peters J.M. The small-molecule inhibitor BI 2536 reveals novel insights into mitotic roles of polo-like kinase 1. Curr. Biol. 17 (2007) 304-315
79. van Vugt M.A., van de Weerdt B.C., Vader G., Janssen H., Calafat J., Klompmaker R., Wolthuis R.M., and Medema R.H. 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 (2004) 36841-36854
80. Wasch R., and Cross F.R. APC-dependent proteolysis of the mitotic cyclin Clb2 is essential for mitotic exit. Nature 418 (2002) 556-562
81. Shteinberg M., Protopopov Y., Listovsky T., Brandeis M., and Hershko A. Phosphorylation of the cyclosome is required for its stimulation by Fizzy/cdc20. Biochem. Biophys. Res. Commun. 260 (1999) 193-198
82. Stewart E., Kobayashi H., Harrison D., and Hunt T. Destruction of Xenopus cyclins A and B2, but not B1, requires binding to p34cdc2. EMBO J. 13 (1994) 584-594
83. Gabellini D., Colaluca I.N., Vodermaier H.C., Biamonti G., Giacca M., Falaschi A., Riva S., and Peverali F.A. Early mitotic degradation of the homeoprotein HOXC10 is potentially linked to cell cycle progression. EMBO J. 22 (2003) 3715-3724
84. Fry A.M. The Nek2 protein kinase: a novel regulator of centrosome structure. Oncogene 21 (2002) 6184-6194
85. Amador V., Ge S., Santamaria P.G., Guardavaccaro D., and Pagano M. APC/C(Cdc20) controls the ubiquitin-mediated degradation of p21 in prometaphase. Mol. Cell 27 (2007) 462-473
86. Acquaviva C., Herzog F., Kraft C., and Pines J. The anaphase promoting complex/cyclosome is recruited to centromeres by the spindle assembly checkpoint. Nat. Cell Biol. 6 (2004) 892-898
87. Clute P., and Pines J. Temporal and spatial control of cyclin B1 destruction in metaphase. Nat. Cell Biol. 1 (1999) 82-87
88. Huang J.Y., and Raff J.W. The dynamic localisation of the Drosophila APC/C: evidence for the existence of multiple complexes that perform distinct functions and are differentially localised. J. Cell Sci. 115 (2002) 2847-2856
89. Pines J., and Lindon C. Proteolysis: anytime, any place, anywhere?. Nat. Cell Biol. 7 (2005) 731-735
90. az-Martinez L.A., and Yu H. Running on a treadmill: dynamic inhibition of APC/C by the spindle checkpoint. Cell Div. 2 (2007) 23
91. Fang G., Yu H., and Kirschner M.W. The checkpoint protein MAD2 and the mitotic regulator CDC20 form a ternary complex with the anaphase-promoting complex to control anaphase initiation. Genes Dev. 12 (1998) 1871-1883
92. Tang Z., Shu H., Oncel D., Chen S., and Yu H. Phosphorylation of Cdc20 by Bub1 provides a catalytic mechanism for APC/C inhibition by the spindle checkpoint. Mol. Cell 16 (2004) 387-397
93. Sudakin V., Chan G.K., and 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. (2001) 925-936
94. Millband D.N., and Hardwick K.G. Fission yeast Mad3p is required for Mad2p to inhibit the anaphase-promoting complex and localizes to kinetochores in a Bub1p-, Bub3p-, and Mph1p-dependent manner. Mol. Cell. Biol. 8 (2002) 2728-2742
95. Chung E., and Chen R.H. Phosphorylation of Cdc20 is required for its inhibition by the spindle checkpoint. Nat. Cell Biol. 5 (2003) 748-753
96. Luo X., Tang Z., Xia G., Wassmann K., Matsumoto T., Rizo J., and Yu H. The Mad2 spindle checkpoint protein has two distinct natively folded states. Nat. Struct. Mol. Biol. 11 (2004) 338-345
97. Hoffman D.B., Pearson C.G., Yen T.J., Howell B.J., and Salmon E.D. Microtubule-dependent changes in assembly of microtubule motor proteins and mitotic spindle checkpoint proteins at PtK1 kinetochores. Mol. Biol. Cell 12 (2001) 1995-2009
98. Wojcik E., Basto R., Serr M., Scaerou F., Karess R., and Hays T. Kinetochore dynein: its dynamics and role in the transport of the Rough deal checkpoint protein. Nat. Cell Biol. 3 (2001) 1001-1007
99. Howell B.J., McEwen B.F., Canman J.C., Hoffman D.B., Farrar E.M., Rieder C.L., and Salmon E.D. Cytoplasmic dynein/dynactin drives kinetochore protein transport to the spindle poles and has a role in mitotic spindle checkpoint inactivation. J. Cell Biol. 155 (2001) 1159-1172
100. Cimini D., Howell B., Maddox P., Khodjakov A., Degrassi F., and Salmon E.D. Merotelic kinetochore orientation is a major mechanism of aneuploidy in mitotic mammalian tissue cells. J. Cell Biol. 153 (2001) 517-527
101. Scaerou F., Aguilera I., Saunders R., Kane N., Blottiere L., and Karess R. The rough deal protein is a new kinetochore component required for accurate chromosome segregation in Drosophila. J. Cell Sci. 112 (1999) 3757-3768
102. Howell B.J., Hoffman D.B., Fang G., Murray A.W., and Salmon E.D. Visualization of Mad2 dynamics at kinetochores, along spindle fibers, and at spindle poles in living cells. J. Cell Biol. 150 (2000) 1233-1250
103. Rieder C.L., and Alexander S.P. Kinetochores are transported poleward along a single astral microtubule during chromosome attachment to the spindle in newt lung cells. J. Cell Biol. 110 (1990) 81-95
104. Griffis E.R., Stuurman N., and Vale R.D. Spindly, a novel protein essential for silencing the spindle assembly checkpoint, recruits dynein to the kinetochore. J. Cell Biol. 177 (2007) 1005-1015
105. Abrieu A., Kahana J.A., Wood K.W., and Cleveland D.W. CENP-E as an essential component of the mitotic checkpoint in vitro. Cell 102 (2000) 817-826
106. Mao Y., Desai A., and Cleveland D.W. Microtubule capture by CENP-E silences BubR1-dependent mitotic checkpoint signaling. J. Cell Biol. 170 (2005) 873-880
107. Mao Y., Abrieu A., and Cleveland D.W. Activating and silencing the mitotic checkpoint through CENP-E-dependent activation/inactivation of BubR1. Cell 114 (2003) 87-98
108. Chan G.K., Jablonski S.A., Sudakin V., Hittle J.C., and Yen T.J. Human BUBR1 is a mitotic checkpoint kinase that monitors CENP-E functions at kinetochores and binds the cyclosome/APC. J. Cell Biol. 146 (1999) 941-954
109. Habu T., Kim S.H., Weinstein J., and Matsumoto T. Identification of a MAD2-binding Protein, CMT2, and its role in mitosis. EMBO J. 21 (2002) 6419-6428 21
110. Xia G., Luo X., Habu T., Rizo J., Matsumoto T., and Yu H. Conformation-specific binding of P31(Comet) antagonizes the function of Mad2 in the Spindle checkpoint. EMBO J. 23 (2004) 3133-3143
111. Yang M., Li B., Tomchick D.R., Machius M., Rizo J., Yu H., and Luo X. p31comet blocks Mad2 activation through structural mimicry. Cell 131 (2007) 744-755
112. Reddy S.K., Rape M., Margansky W.A., and Kirschner M.W. Ubiquitination by the anaphase-promoting complex drives spindle checkpoint inactivation. Nature 446 (2007) 921-925
113. Hagting A., Den Elzen N., Vodermaier H.C., Waizenegger I.C., Peters J.M., and Pines J. 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 (2002) 1125-1137
114. Stemmann O., Gorr I.H., and Boos D. Anaphase topsy-turvy: Cdk1 a securin, separase a CKI. Cell Cycle 5 (2006) 11-13
115. Bembenek J., and Yu H. Regulation of the anaphase-promoting complex by the dual specificity phosphatase human Cdc14a. J. Biol. Chem. 276 (2001) 48237-48242
116. Yuan K., Hu H., Guo Z., Fu G., Shaw A.P., Hu R., and Yao X. Phospho-regulation of HsCdc14A By Polo-like kinase 1 is essential for mitotic progression. J. Biol. Chem. 282 (2007) 27414-27423
117. Jacobs H., Richter D., Venkatesh T., and Lehner C. Completion of mitosis requires neither fzr/rap nor fzr2, a male germline-specific Drosophila Cdh1 homolog. Curr. Biol. 12 (2002) 1435-1441
118. Keck J.M., Summers M.K., Tedesco D., Ekholm-Reed S., Chuang L.C., Jackson P.K., and Reed S.I. Cyclin E overexpression impairs progression through mitosis by inhibiting APC(Cdh1). J. Cell Biol. 178 (2007) 371-385 (2007)
119. Lindon C., and Pines J. Ordered proteolysis in anaphase inactivates Plk1 to contribute to proper mitotic exit in human cells. J. Cell Biol. 164 (2004) 233-241
120. DelSal G., Loda M., and Pagano M. Cell cycle and cancer: critical events at the G1 restriction point. Crit. Rev. Oncog. 7 (1996) 127-142
121. Bashir T., Dorrello N.V., Amador V., Guardavaccaro D., and Pagano M. Control of the SCF(Skp2-Cks1) ubiquitin ligase by the APC/C(Cdh1) ubiquitin ligase. Nature 428 (2004) 190-193
122. Ganoth D., Bornstein G., Ko T.K., Larsen B., Tyers M., Pagano M., and Hershko A. The cell-cycle regulatory protein Cks1 is required for SCF(Skp2)-mediated ubiquitinylation of p27. Nat. Cell Biol. 3 (2001) 321-324
123. Wei W., Ayad N.G., Wan Y., Zhang G.J., Kirschner M.W., and Kaelin Jr. W.G. Degradation of the SCF component Skp2 in cell-cycle phase G1 by the anaphase-promoting complex. Nature 428 (2004) 194-198
124. Agami R., and Bernards R. Distinct initiation and maintenance mechanisms cooperate to induce G1 cell cycle arrest in response to DNA damage. Cell 102 (2000) 55-66
125. Binne U.K., Classon M.K., Dick F.A., Wei W., Rape M., Kaelin Jr. W.G., Naar A.M., and Dyson N.J. Retinoblastoma protein and anaphase-promoting complex physically interact and functionally cooperate during cell-cycle exit. Nat. Cell Biol. 9 (2007) 225-232
126. Lukas J., Herzinger T., Hansen K., Moroni M.C., Resnitzky D., Helin K., Reed S.I., and Bartek J. Cyclin E-Induced S phase without activation of the PRb/E2F pathway. Genes Dev. 11 (1997) 1479-1492
127. Ji P., Jiang H., Rekhtman K., Bloom J., Ichetovkin M., Pagano M., and Zhu L. An Rb-Skp2-p27 pathway mediates acute cell cycle inhibition by Rb and is retained in a partial-penetrance Rb mutant. Mol. Cell 16 (2004) 47-58
128. Fay D.S., Keenan S., and Han M. fzr-1 and lin-35/Rb function redundantly to control cell proliferation in C. elegans as revealed by a nonbiased synthetic screen. Genes Dev. 16 (2002) 503-517
129. Sudo T., Ota Y., Kotani S., Nakao M., Takami Y., Takeda S., and Saya H. Activation of Cdh1-dependent APC is required for G1 cell cycle arrest and DNA damage-induced G2 checkpoint in vertebrate cells. EMBO J. 20 (2001) 6499-6508
130. Wirth K.G., Ricci R., Gimenez-Abian J.F., Taghybeeglu S., Kudo N.R., Jochum W., Vasseur-Cognet M., and Nasmyth K. Loss of the anaphase-promoting complex in quiescent cells causes unscheduled hepatocyte proliferation. Genes Dev. 18 (2004) 88-98
131. Tran K., Mahr J.A., Choi J., Teodoro J.G., Green M.R., and Spector D.H. Accumulation of substrates of the anaphase-promoting complex (APC) during human cytomegalovirus infection is associated with the phosphorylation of Cdh1 and the dissociation and relocalization of APC subunits. J. Virol. 82 (2008) 529-537
132. Teodoro J.G., Heilman D.W., Parker A.E., and Green M.R. The viral protein Apoptin associates with the anaphase-promoting complex to induce G2/M arrest and apoptosis in the absence of p53. Genes Dev. 18 (2004) 1952-1957
133. Sorensen C.S., Lukas C., Kramer E.R., Peters J.M., Bartek J., and Lukas J. Nonperiodic activity of the human anaphase-promoting complex-Cdh1 ubiquitin ligase results in continuous DNA synthesis uncoupled from mitosis. Mol. Cell. Biol. 20 (2000) 7613-7623
134. Fujita M., Yamada C., Goto H., Yokoyama N., Kuzushima K., Inagaki M., and Tsurumi T. Cell cycle regulation of human CDC6 protein. intracellular localization, interaction with the human Mcm complex, and CDC2 kinase-mediated hyperphosphorylation. J. Biol. Chem. 274 (1999) 25927-25932
135. Melixetian M., Ballabeni A., Masiero L., Gasparini P., Zamponi R., Bartek J., Lukas J., and Helin K. Loss of geminin induces rereplication in the presence of functional P53. J. Cell Biol. 165 (2004) 473-482
136. Mihaylov I.S., Kondo T., Jones L., Ryzhikov S., Tanaka J., Zheng J., Higa L.A., Minamino N., Cooley L., and Zhang H. Control of DNA replication and chromosome ploidy by geminin and cyclin A. Mol. Cell. Biol. 22 (2002) 1868-1880
137. Zhu W., Chen Y., and Dutta A. Rereplication by depletion of geminin is seen regardless of P53 status and activates a G2/M checkpoint. Mol. Cell. Biol. 24 (2004) 7140-7150
138. McGarry T.J., and Kirschner M.W. Geminin, an inhibitor of DNA replication, is degraded during mitosis. Cell 93 (1998) 1043-1053
139. Li A., and Blow J.J. Cdt1 downregulation by proteolysis and geminin inhibition prevents DNA re-replication in Xenopus. EMBO J. 24 (2005) 395-404
140. Saha P., Chen J., Thome K.C., Lawlis S.J., Hou Z.H., Hendricks M., Parvin J.D., and Dutta A. Human CDC6/Cdc18 associates with Orc1 and Cyclin-Cdk and is selectively eliminated from the nucleus at the onset of S phase. Mol. Cell. Biol. 18 (1998) 2758-2767
141. Jiang W., Wells N.J., and Hunter T. Multistep regulation of DNA replication by Cdk phosphorylation of HsCdc6. Proc. Natl. Acad. Sci. USA. 96 (1999) 6193-6198
142. Petersen B.O., Lukas J., Sorensen C.S., Bartek J., and Helin K. Phosphorylation of mammalian CDC6 by cyclin A/CDK2 regulates its subcellular localization. EMBO J. 18 (1999) 396-410
143. Coverley D., Pelizon C., Trewick S., and Laskey R.A. Chromatin-bound Cdc6 persists in S and G2 phases in human cells, while soluble Cdc6 is destroyed in a cyclin A-Cdk2 dependent process. J. Cell Sci. 113 (2000) 1929-1938
144. Li A., and Blow J.J. Non-proteolytic inactivation of geminin requires CDK-dependent ubiquitination. Nat. Cell Biol. 6 (2004) 260-267
145. Petersen B.O., Wagener C., Marinoni F., Kramer E.R., Melixetian M., Lazzerini Denchi E., Gieffers C., Matteucci C., Peters J.M., and Helin K. Cell cycle- and cell growth-regulated proteolysis of mammalian CDC6 is dependent on APC-CDH1. Genes Dev. 18 (2000) 2330-2343
146. Diffley J.F. Regulation of early events in chromosome replication. Curr. Biol. 14 (2004) R778-R786
147. Peters J.M. The anaphase-promoting complex: proteolysis in mitosis and beyond. Mol. Cell 9 (2002) 931-943
148. Mailand N., and Diffley J.F. CDKs promote DNA replication origin licensing in human cells by protecting Cdc6 from APC/C-dependent proteolysis. Cell 122 (2005) 915-926
149. Hsu J.Y., Reimann J.D., Sorensen C.S., Lukas J., and Jackson P.K. E2F-dependent accumulation of hEmi1 regulates S phase entry by inhibiting APC(Cdh1). Nat. Cell Biol. 4 (2002) 358-366
150. Sudo T., Ota Y., Kotani S., Nakao M., Takami Y., Takeda S., and Saya H. Activation of Cdh1-dependent APC is required for G1 cell cycle arrest and DNA damage-induced G2 checkpoint in vertebrate cells. EMBO J. 20 (2001) 6499-6508
151. Duursma A., and Agami R. p53-Dependent regulation of Cdc6 protein stability controls cellular proliferation. Mol. Cell. Biol. 25 (2005) 6937-6947
152. 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 (1997) 742-750
153. Coster G., Hayouka Z., Argaman L., Strauss C., Friedler A., Brandeis M., and Goldberg M. The DNA damage response mediator MDC1 directly interacts with the anaphase-promoting complex/cyclosome. J. Biol. Chem. 282 (2007) 32053-32064
154. Sudo T., Ueno N.T., and Saya H. Functional analysis of APC-Cdh1. Methods Mol. Biol. 281 (2004) 189-198
155. Grosskortenhaus R., and Sprenger F. Rca1 inhibits APC-Cdh1(Fzr) and is required to prevent cyclin degradation in G2. Dev. Cell 2 (2002) 29-40
156. Zielke N., Querings S., Grosskortenhaus R., Reis T., and Sprenger F. Molecular dissection of the APC/C inhibitor Rca1 shows a novel F-box-dependent function. EMBO Rep. 7 (2006) 1266-1272
157. Ferguson K.L., Vanderluit J.L., Hebert J.M., McIntosh W.C., Tibbo E., MacLaurin J.G., Park D.S., Wallace V.A., Vooijs M., McConnell S.K., and Slack R.S. Telencephalon-specific Rb knockouts reveal enhanced neurogenesis, survival and abnormal cortical development. EMBO J. 21 (2002) 3337-3346
158. MacPherson D., Sage J., Crowley D., Trumpp A., Bronson R.T., and Jacks T. Conditional mutation of Rb causes cell cycle defects without apoptosis in the central nervous system. Mol. Cell. Biol. 23 (2003) 1044-1053
159. Dannenberg J.H., van R.A., Schuijff L., and Te R.H. Ablation of the retinoblastoma gene family deregulates G(1) control causing immortalization and increased cell turnover under growth-restricting conditions. Genes Dev. 14 (2000) 3051-3064
160. Tanaka-Matakatsu M., Thomas B.J., and Du W. Mutation of the Apc1 homologue shattered disrupts normal eye development by disrupting G1 cell cycle arrest and progression through mitosis. Dev. Biol. 309 (2007) 222-235
161. Kitagawa M., Lee S.H., and McCormick F. Skp2 suppresses p53-dependent apoptosis by inhibiting p300. Mol. Cell 29 (2008) 217-231
162. Turnell A.S., and Mymryk J.S. Roles for the coactivators CBP and p300 and the APC/C E3 ubiquitin ligase in E1A-dependent cell transformation. Br. J. Cancer 95 (2006) 555-560
163. Turnell A.S., Stewart G.S., Grand R.J., Rookes S.M., Martin A., Yamano H., Elledge S.J., and Gallimore P.H. The APC/C and CBP/p300 cooperate to regulate transcription and cell-cycle progression. Nature 438 (2005) 690-695
164. Wang Q., Moyret-Lalle C., Couzon F., Surbiguet-Clippe C., Saurin J.C., Lorca T., Navarro C., and Puisieux A. Alterations of anaphase-promoting complex genes in human colon cancer cells. Oncogene 22 (2003) 1486-1490
165. Lasorella A., Iavarone A., and Israel M.A. Id2 specifically alters regulation of the cell cycle by tumor suppressor proteins. Mol. Cell. Biol. 16 (1996) 2570-2578
166. Lasorella A., Noseda M., Beyna M., Yokota Y., and Iavarone A. Id2 is a retinoblastoma protein target and mediates signalling by Myc oncoproteins. Nature 407 (2000) 592-598
167. Lasorella A., Stegmuller J., Guardavaccaro D., Liu G., Carro M.S., Rothschild G., Torre-Ubieta L., Pagano M., Bonni A., and Iavarone A. Degradation of Id2 by the anaphase-promoting complex couples cell cycle exit and axonal growth. Nature 442 (2006) 471-474
168. Lehman N.L., Tibshirani R., Hsu J.Y., Natkunam Y., Harris B.T., West R.B., Masek M.A., Montgomery K., van de Rijn M., and Jackson P.K. Oncogenic regulators and substrates of the anaphase promoting complex/cyclosome are frequently overexpressed in malignant tumors. Am. J. Pathol. 170 (2007) 1793-1805
169. Brito D.A., and Rieder C.L. Mitotic checkpoint slippage in humans occurs via cyclin B destruction in the presence of an active checkpoint. Curr. Biol. 16 (2006) 1194-1200
170. Rieder C.L., and Maiato H. Stuck in division or passing through: what happens when cells cannot satisfy the spindle assembly checkpoint. Dev. Cell 7 (2004) 637-651
171. Swanton C., Tomlinson I., and Downward J. Chromosomal instability, colorectal cancer and taxane resistance. Cell Cycle 5 (2006) 818-823
172. Swanton C., Marani M., Pardo O., Warne P.H., Kelly G., Sahai E., Elustondo F., Chang J., Temple J., Ahmed A.A., Brenton J.D., Downward J., and Nicke B. Regulators of mitotic arrest and ceramide metabolism are determinants of sensitivity to paclitaxel and other chemotherapeutic drugs. Cancer Cell 11 (2007) 498-512
173. Reinhardt H.C., Aslanian A.S., Lees J.A., and Yaffe M.B. p53-deficient cells rely on ATM- and ATR-mediated checkpoint signaling through the p38MAPK/MK2 pathway for survival after DNA damage. Cancer Cell 11 (2007) 175-189
174. Whitehurst A.W., Bodemann B.O., Cardenas J., Ferguson D., Girard L., Peyton M., Minna J.D., Michnoff C., Hao W., Roth M.G., Xie X.J., and White M.A. Synthetic lethal screen identification of chemosensitizer loci in cancer cells. Nature 446 (2007) 815-819
175. Xiao Z., Xue J., Semizarov D., Sowin T.J., Rosenberg S.H., and Zhang H. Novel indication for cancer therapy: Chk1 inhibition sensitizes tumor cells to antimitotics. Int. J. Cancer 115 (2005) 528-538
176. Tan T.T., Degenhardt K., Nelson D.A., Beaudoin B., Nieves-Neira W., Bouillet P., Villunger A., Adams J.M., and White E. Key roles of BIM-driven apoptosis in epithelial tumors and rational chemotherapy. Cancer Cell 7 (2005) 227-238
177. Li R., Moudgil T., Ross H.J., and Hu H.M. Apoptosis of non-small-cell lung cancer cell lines after paclitaxel treatment involves the BH3-only proapoptotic protein Bim. Cell Death Differ. 12 (2005) 292-303
178. Chen R.H. Dual inhibition of Cdc20 by the spindle checkpoint. J. Biomed. Sci. 14 (2007) 475-479
179. Dawson I.A., Roth S., and Artavanis-Tsakonas S. The Drosophila cell cycle gene fizzy is required for normal degradation of cyclins A and B during mitosis and has homology to the CDC20 gene of Saccharomyces cerevisiae. J. Cell Biol. 129 (1995) 725-737
180. Li M., York J.P., and Zhang P. Loss of Cdc20 causes a securin-dependent metaphase arrest in two-cell mouse embryos. Mol. Cell. Biol. 27 (2007) 3481-3488
181. Mondal G., Sengupta S., Panda C.K., Gollin S.M., Saunders W.S., and Roychoudhury S. Overexpression of Cdc20 leads to impairment of the spindle assembly checkpoint and aneuploidization in oral cancer. Carcinogenesis 28 (2007) 81-92