Functional characterization of Anaphase Promoting Complex/Cyclosome (APC/C) E3 ubiquitin ligases in tumorigenesis

Biochimica et Biophysica Acta - Reviews on Cancer

Volumn 1845, Issue 2, 2014, Pages 277-293

  Zhang, Jinfang ^a   Wan, Lixin ^a   Dai, Xiangpeng ^a   Sun, Yi ^b   Wei, Wenyi ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

APC C E3 ligase; Cell cycle progression; Mouse model; Tumorigenesis; Ubiquitin ligase; Ubiquitin proteasome system

Indexed keywords

ANAPHASE PROMOTING COMPLEX; ANAPHASE PROMOTING COMPLEX SUBUNIT 10; ANAPHASE PROMOTING COMPLEX SUBUNIT 2; BUB1 RELATED PROTEIN; BUB3 PROTEIN; EARLY MITOTIC INHIBITOR 1; ENZYME INHIBITOR; FIZZY RELATED PROTEIN; PROTEIN MAD2; RING FINGER PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; UVOMORULIN;

CARCINOGENESIS; CELL CYCLE REGULATION; CELL FUNCTION; CELL MATURATION; CELL PROLIFERATION; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME REGULATION; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

APC/C E3 LIGASE; CELL CYCLE PROGRESSION; MOUSE MODEL; TUMORIGENESIS; UBIQUITIN LIGASE; UBIQUITIN-PROTEASOME SYSTEM;

ANAPHASE-PROMOTING COMPLEX-CYCLOSOME; ANIMALS; CARCINOGENESIS; CELL TRANSFORMATION, NEOPLASTIC; HUMANS; MICE; MITOSIS; NEOPLASMS; PROTEASOME ENDOPEPTIDASE COMPLEX; SIGNAL TRANSDUCTION; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84895984956     PISSN: 0304419X     EISSN: 18792561     Source Type: Journal    
DOI: 10.1016/j.bbcan.2014.02.001     Document Type: Review

References (288)

1. Hershko A., Ciechanover A. The ubiquitin system. Annu. Rev. Biochem. 1998, 67:425-479.
2. Varshavsky A. The ubiquitin system, an immense realm. Annu. Rev. Biochem. 2012, 81:167-176.
3. Eldridge A.G., O'Brien T. Therapeutic strategies within the ubiquitin proteasome system. Cell Death Differ. 2010, 17:4-13.
4. Hoeller D., Dikic I. Targeting the ubiquitin system in cancer therapy. Nature 2009, 458:438-444.
5. Nalepa G., Rolfe M., Harper J.W. Drug discovery in the ubiquitin-proteasome system. Nat. Rev. Drug Discov. 2006, 5:596-613.
6. Pickart C.M. Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 2001, 70:503-533.
7. Nakayama K.I., Nakayama K. Ubiquitin ligases: cell-cycle control and cancer. Nat. Rev. Cancer 2006, 6:369-381.
8. Nagy V., Dikic I. Ubiquitin ligase complexes: from substrate selectivity to conjugational specificity. Biol. Chem. 2010, 391:163-169.
9. Deshaies R.J., Joazeiro C.A. RING domain E3 ubiquitin ligases. Annu. Rev. Biochem. 2009, 78:399-434.
10. Petroski M.D., Deshaies R.J. Function and regulation of cullin-RING ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 2005, 6:9-20.
11. Bedford L., Lowe J., Dick L.R., Mayer R.J., Brownell J.E. Ubiquitin-like protein conjugation and the ubiquitin-proteasome system as drug targets. Nat. Rev. Drug Discov. 2011, 10:29-46.
12. Skaar J.R., Pagano M. Control of cell growth by the SCF and APC/C ubiquitin ligases. Curr. Opin. Cell Biol. 2009, 21:816-824.
13. Rotin D., Kumar S. Physiological functions of the HECT family of ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 2009, 10:398-409.
14. Metzger M.B., Hristova V.A., Weissman A.M. HECT and RING finger families of E3 ubiquitin ligases at a glance. J. Cell Sci. 2012, 125:531-537.
15. Kulathu Y., Komander D. Atypical ubiquitylation - the unexplored world of polyubiquitin beyond Lys48 and Lys63 linkages. Nat. Rev. Mol. Cell Biol. 2012, 13:508-523.
16. Komander D., Rape M. The ubiquitin code. Annu. Rev. Biochem. 2012, 81:203-229.
17. Schwarz L.A., Patrick G.N. Ubiquitin-dependent endocytosis, trafficking and turnover of neuronal membrane proteins. Mol. Cell. Neurosci. 2012, 49:387-393.
18. Ulrich H.D., Walden H. Ubiquitin signalling in DNA replication and repair. Nat. Rev. Mol. Cell Biol. 2010, 11:479-489.
19. Acconcia F., Sigismund S., Polo S. Ubiquitin in trafficking: the network at work. Exp. Cell Res. 2009, 315:1610-1618.
20. Baboshina O.V., Haas A.L. Novel multiubiquitin chain linkages catalyzed by the conjugating enzymes E2EPF and RAD6 are recognized by 26S proteasome subunit 5. J. Biol. Chem. 1996, 271:2823-2831.
21. Cardozo T., Pagano M. The SCF ubiquitin ligase: insights into a molecular machine. Nat. Rev. Mol. Cell Biol. 2004, 5:739-751.
22. Karin M., Ben-Neriah Y. Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity. Annu. Rev. Immunol. 2000, 18:621-663.
23. Wertz I.E., Dixit V.M. Signaling to NF-kappaB: regulation by ubiquitination. Cold Spring Harb. Perspect. Biol. 2010, 2:a003350.
24. Skaug B., Jiang X., Chen Z.J. The role of ubiquitin in NF-kappaB regulatory pathways. Annu. Rev. Biochem. 2009, 78:769-796.
25. Haglund K., Dikic I. Ubiquitylation and cell signaling. EMBO J. 2005, 24:3353-3359.
26. Hayden M.S., Ghosh S. Shared principles in NF-kappaB signaling. Cell 2008, 132:344-362.
27. Ikeda F., Dikic I. Atypical ubiquitin chains: new molecular signals. 'Protein modifications: beyond the usual suspects' review series. EMBO Rep. 2008, 9:536-542.
28. Wu K., Kovacev J., Pan Z.Q. Priming and extending: a UbcH5/Cdc34 E2 handoff mechanism for polyubiquitination on a SCF substrate. Mol. Cell 2010, 37:784-796.
29. Rape M. Assembly of k11-linked ubiquitin chains by the anaphase-promoting complex. Subcell. Biochem. 2010, 54:107-115.
30. Wickliffe K.E., Williamson A., Meyer H.J., Kelly A., Rape M. K11-linked ubiquitin chains as novel regulators of cell division. Trends Cell Biol. 2011, 21:656-663.
31. Ye Y., Rape M. Building ubiquitin chains: E2 enzymes at work. Nat. Rev. Mol. Cell Biol. 2009, 10:755-764.
32. Walczak H., Iwai K., Dikic I. Generation and physiological roles of linear ubiquitin chains. BMC Biol. 2012, 10:23.
33. Iwai K., Tokunaga F. Linear polyubiquitination: a new regulator of NF-kappaB activation. EMBO Rep. 2009, 10:706-713.
34. Harper J.W., Burton J.L., Solomon M.J. The anaphase-promoting complex: it's not just for mitosis any more. Genes Dev. 2002, 16:2179-2206.
35. Jin J., Cardozo T., Lovering R.C., Elledge S.J., Pagano M., Harper J.W. Systematic analysis and nomenclature of mammalian F-box proteins. Genes Dev. 2004, 18:2573-2580.
36. Ang X.L., Wade Harper J. SCF-mediated protein degradation and cell cycle control. Oncogene 2005, 24:2860-2870.
37. Jia L., Sun Y. SCF E3 ubiquitin ligases as anticancer targets. Curr. Cancer Drug Targets 2011, 11:347-356.
38. Frescas D., Pagano M. Deregulated proteolysis by the F-box proteins SKP2 and beta-TrCP: tipping the scales of cancer. Nat. Rev. Cancer 2008, 8:438-449.
39. Welcker M., Clurman B.E. FBW7 ubiquitin ligase: a tumour suppressor at the crossroads of cell division, growth and differentiation. Nat. Rev. Cancer 2008, 8:83-93.
40. Lau A.W., Fukushima H., Wei W. The Fbw7 and betaTRCP E3 ubiquitin ligases and their roles in tumorigenesis. Front. Biosci. 2012, 17:2197-2212.
41. Lipkowitz S., Weissman A.M. RINGs of good and evil: RING finger ubiquitin ligases at the crossroads of tumour suppression and oncogenesis. Nat. Rev. Cancer 2011, 11:629-643.
42. Barford D. Structural insights into anaphase-promoting complex function and mechanism. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 2011, 366:3605-3624.
43. Foe I., Toczyski D. Structural biology: a new look for the APC. Nature 2011, 470:182-183.
44. McLean J.R., Chaix D., Ohi M.D., Gould K.L. State of the APC/C: organization, function, and structure. Crit. Rev. Biochem. Mol. Biol. 2011, 46:118-136.
45. Peters J.M. The anaphase promoting complex/cyclosome: a machine designed to destroy. Nat. Rev. Mol. Cell Biol. 2006, 7:644-656.
46. Schreiber A., Stengel F., Zhang Z., Enchev R.I., Kong E.H., Morris E.P., Robinson C.V., da Fonseca P.C., Barford D. Structural basis for the subunit assembly of the anaphase-promoting complex. Nature 2011, 470:227-232.
47. Buschhorn B.A., Petzold G., Galova M., Dube P., Kraft C., Herzog F., Stark H., Peters J.M. Substrate binding on the APC/C occurs between the coactivator Cdh1 and the processivity factor Doc1. Nat. Struct. Mol. Biol. 2011, 18:6-13.
48. Jin L., Williamson A., Banerjee S., Philipp I., Rape M. Mechanism of ubiquitin-chain formation by the human anaphase-promoting complex. Cell 2008, 133:653-665.
49. 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., Walz T. Structural organization of the anaphase-promoting complex bound to the mitotic activator Slp1. Mol. Cell 2007, 28:871-885.
50. Thornton B.R., Ng T.M., Matyskiela M.E., Carroll C.W., Morgan D.O., Toczyski D.P. An architectural map of the anaphase-promoting complex. Genes Dev. 2006, 20:449-460.
51. 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. 2003, 13:1459-1468.
52. da Fonseca P.C., Kong E.H., Zhang Z., Schreiber A., Williams M.A., Morris E.P., Barford D. Structures of APC/C(Cdh1) with substrates identify Cdh1 and Apc10 as the D-box co-receptor. Nature 2011, 470:274-278.
53. 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 2000, 11:1555-1569.
54. Kraft C., Herzog F., Gieffers C., Mechtler K., Hagting A., Pines J., Peters J.M. Mitotic regulation of the human anaphase-promoting complex by phosphorylation. EMBO J. 2003, 22:6598-6609.
55. Yu H. Regulation of APC-Cdc20 by the spindle checkpoint. Curr. Opin. Cell Biol. 2002, 14:706-714.
56. Yu H. Cdc20: a WD40 activator for a cell cycle degradation machine. Mol. Cell 2007, 27:3-16.
57. Bharadwaj R., Yu H. The spindle checkpoint, aneuploidy, and cancer. Oncogene 2004, 23:2016-2027.
58. Musacchio A., Salmon E.D. The spindle-assembly checkpoint in space and time. Nat. Rev. Mol. Cell Biol. 2007, 8:379-393.
59. Musacchio A. Spindle assembly checkpoint: the third decade. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 2011, 366:3595-3604.
60. Lara-Gonzalez P., Westhorpe F.G., Taylor S.S. The spindle assembly checkpoint. Curr. Biol. 2012, 22:R966-R980.
61. Howell B.J., Hoffman D.B., Fang G., Murray A.W., Salmon E.D. Visualization of Mad2 dynamics at kinetochores, along spindle fibers, and at spindle poles in living cells. J. Cell Biol. 2000, 150:1233-1250.
62. Howell B.J., Moree B., Farrar E.M., Stewart S., Fang G., Salmon E.D. Spindle checkpoint protein dynamics at kinetochores in living cells. Curr. Biol. 2004, 14:953-964.
63. Shah J.V., Botvinick E., Bonday Z., Furnari F., Berns M., Cleveland D.W. Dynamics of centromere and kinetochore proteins; implications for checkpoint signaling and silencing. Curr. Biol. 2004, 14:942-952.
64. Vink M., Simonetta M., Transidico P., Ferrari K., Mapelli M., De Antoni A., Massimiliano L., Ciliberto A., Faretta M., Salmon E.D., Musacchio A. In vitro FRAP identifies the minimal requirements for Mad2 kinetochore dynamics. Curr. Biol. 2006, 16:755-766.
65. Hardwick K.G., Weiss E., Luca F.C., Winey M., Murray A.W. Activation of the budding yeast spindle assembly checkpoint without mitotic spindle disruption. Science 1996, 273:953-956.
66. Abrieu A., Magnaghi-Jaulin L., Kahana J.A., Peter M., Castro A., Vigneron S., Lorca T., Cleveland D.W., Labbe J.C. Mps1 is a kinetochore-associated kinase essential for the vertebrate mitotic checkpoint. Cell 2001, 106:83-93.
67. Chung E., Chen R.H. Spindle checkpoint requires Mad1-bound and Mad1-free Mad2. Mol. Biol. Cell 2002, 13:1501-1511.
68. De Antoni A., Pearson C.G., Cimini D., Canman J.C., Sala V., Nezi L., Mapelli M., Sironi L., Faretta M., Salmon E.D., Musacchio A. The Mad1/Mad2 complex as a template for Mad2 activation in the spindle assembly checkpoint. Curr. Biol. 2005, 15:214-225.
69. Morrow C.J., Tighe A., Johnson V.L., Scott M.I., Ditchfield C., Taylor S.S. Bub1 and aurora B cooperate to maintain BubR1-mediated inhibition of APC/CCdc20. J. Cell Sci. 2005, 118:3639-3652.
70. Kim S., Yu H. Mutual regulation between the spindle checkpoint and APC/C. Semin. Cell Dev. Biol. 2011, 22:551-558.
71. Michaelis C., Ciosk R., Nasmyth K. Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell 1997, 91:35-45.
72. Nasmyth K. Disseminating the genome: joining, resolving, and separating sister chromatids during mitosis and meiosis. Annu. Rev. Genet. 2001, 35:673-745.
73. Lukas C., Sorensen C.S., Kramer E., Santoni-Rugiu E., Lindeneg C., Peters J.M., Bartek J., Lukas J. Accumulation of cyclin B1 requires E2F and cyclin-A-dependent rearrangement of the anaphase-promoting complex. Nature 1999, 401:815-818.
74. Keck J.M., Summers M.K., Tedesco D., Ekholm-Reed S., Chuang L.C., Jackson P.K., Reed S.I. Cyclin E overexpression impairs progression through mitosis by inhibiting APC(Cdh1). J. Cell Biol. 2007, 178:371-385.
75. Lau A.W., Inuzuka H., Fukushima H., Wan L., Liu P., Gao D., Sun Y., Wei W. Regulation of APC(Cdh1) E3 ligase activity by the Fbw7/cyclin E signaling axis contributes to the tumor suppressor function of Fbw7. Cell Res. 2013, 23:947-961.
76. 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. 2002, 16:2274-2285.
77. Stewart S., Fang G. Destruction box-dependent degradation of aurora B is mediated by the anaphase-promoting complex/cyclosome and Cdh1. Cancer Res. 2005, 65:8730-8735.
78. Nguyen H.G., Chinnappan D., Urano T., Ravid K. Mechanism of aurora-B degradation and its dependency on intact KEN and A-boxes: identification of an aneuploidy-promoting property. Mol. Cell. Biol. 2005, 25:4977-4992.
79. Yamada M., Watanabe K., Mistrik M., Vesela E., Protivankova I., Mailand N., Lee M., Masai H., Lukas J., Bartek J. ATR-Chk1-APC/CCdh1-dependent stabilization of Cdc7-ASK (Dbf4) kinase is required for DNA lesion bypass under replication stress. Genes Dev. 2013, 27:2459-2472.
80. Zhao W.M., Fang G. Anillin is a substrate of anaphase-promoting complex/cyclosome (APC/C) that controls spatial contractility of myosin during late cytokinesis. J. Biol. Chem. 2005, 280:33516-33524.
81. 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 2008, 30:437-446.
82. Song L., Rape M. Regulated degradation of spindle assembly factors by the anaphase-promoting complex. Mol. Cell 2010, 38:369-382.
83. Li R., Wan B., Zhou J., Wang Y., Luo T., Gu X., Chen F., Yu L. APC/C(Cdh1) targets brain-specific kinase 2 (BRSK2) for degradation via the ubiquitin-proteasome pathway. PLoS ONE 2012, 7:e45932.
84. Qi W., Yu H. KEN-box-dependent degradation of the Bub1 spindle checkpoint kinase by the anaphase-promoting complex/cyclosome. J. Biol. Chem. 2007, 282:3672-3679.
85. Simpson-Lavy K.J., Sajman J., Zenvirth D., Brandeis M. APC/CCdh1 specific degradation of Hsl1 and Clb2 is required for proper stress responses of S. cerevisiae. Cell Cycle 2009, 8:3003-3009.
86. Visintin C., Tomson B.N., Rahal R., Paulson J., Cohen M., Taunton J., Amon A., Visintin R. APC/C-Cdh1-mediated degradation of the Polo kinase Cdc5 promotes the return of Cdc14 into the nucleolus. Genes Dev. 2008, 22:79-90.
87. Petersen B.O., Wagener C., Marinoni F., Kramer E.R., Melixetian M., Lazzerini Denchi E., Gieffers C., Matteucci C., Peters J.M., Helin K. Cell cycle- and cell growth-regulated proteolysis of mammalian CDC6 is dependent on APC-CDH1. Genes Dev. 2000, 14:2330-2343.
88. Huang J.N., Park I., Ellingson E., Littlepage L.E., Pellman D. Activity of the APC(Cdh1) form of the anaphase-promoting complex persists until S phase and prevents the premature expression of Cdc20p. J. Cell Biol. 2001, 154:85-94.
89. Hyun S.Y., Sarantuya B., Lee H.J., Jang Y.J. APC/C(Cdh1)-dependent degradation of Cdc20 requires a phosphorylation on CRY-box by Polo-like kinase-1 during somatic cell cycle. Biochem. Biophys. Res. Commun. 2013, 436:12-18.
90. Donzelli M., Squatrito M., Ganoth D., Hershko A., Pagano M., Draetta G.F. Dual mode of degradation of Cdc25 A phosphatase. EMBO J. 2002, 21:4875-4884.
91. Sugimoto N., Kitabayashi I., Osano S., Tatsumi Y., Yugawa T., Narisawa-Saito M., Matsukage A., Kiyono T., Fujita M. Identification of novel human Cdt1-binding proteins by a proteomics approach: proteolytic regulation by APC/CCdh1. Mol. Biol. Cell 2008, 19:1007-1021.
92. Gurden M.D., Holland A.J., van Zon W., Tighe A., Vergnolle M.A., Andres D.A., Spielmann H.P., Malumbres M., Wolthuis R.M., Cleveland D.W., Taylor S.S. Cdc20 is required for the post-anaphase, KEN-dependent degradation of centromere protein F. J. Cell Sci. 2010, 123:321-330.
93. Benanti J.A., Matyskiela M.E., Morgan D.O., Toczyski D.P. Functionally distinct isoforms of Cik1 are differentially regulated by APC/C-mediated proteolysis. Mol. Cell 2009, 33:581-590.
94. Seki A., Fang G. CKAP2 is a spindle-associated protein degraded by APC/C-Cdh1 during mitotic exit. J. Biol. Chem. 2007, 282:15103-15113.
95. Hong K.U., Park Y.S., Seong Y.S., Kang D., Bae C.D., Park J. Functional importance of the anaphase-promoting complex-Cdh1-mediated degradation of TMAP/CKAP2 in regulation of spindle function and cytokinesis. Mol. Cell. Biol. 2007, 27:3667-3681.
96. Bashir T., Dorrello N.V., Amador V., Guardavaccaro D., Pagano M. Control of the SCF(Skp2-Cks1) ubiquitin ligase by the APC/C(Cdh1) ubiquitin ligase. Nature 2004, 428:190-193.
97. Gao D., Inuzuka H., Korenjak M., Tseng A., Wu T., Wan L., Kirschner M., Dyson N., Wei W. Cdh1 regulates cell cycle through modulating the claspin/Chk1 and the Rb/E2F1 pathways. Mol. Biol. Cell 2009, 20:3305-3316.
98. Bassermann F., Frescas D., Guardavaccaro D., Busino L., Peschiaroli A., Pagano M. The Cdc14B-Cdh1-Plk1 axis controls the G2 DNA-damage-response checkpoint. Cell 2008, 134:256-267.
99. Hadjihannas M.V., Bernkopf D.B., Bruckner M., Behrens J. Cell cycle control of Wnt/beta-catenin signalling by conductin/axin2 through CDC20. EMBO Rep. 2012, 13:347-354.
100. den Elzen N., Pines J. Cyclin A is destroyed in prometaphase and can delay chromosome alignment and anaphase. J. Cell Biol. 2001, 153:121-136.
101. Geley S., Kramer E., Gieffers C., Gannon J., Peters J.M., 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. 2001, 153:137-148.
102. Clute P., Pines J. Temporal and spatial control of cyclin B1 destruction in metaphase. Nat. Cell Biol. 1999, 1:82-87.
103. Liot C., Seguin L., Siret A., Crouin C., Schmidt S., Bertoglio J. APC(cdh1) mediates degradation of the oncogenic Rho-GEF Ect2 after mitosis. PLoS ONE 2011, 6:e23676.
104. Budhavarapu V.N., White E.D., Mahanic C.S., Chen L., Lin F.T., Lin W.C. Regulation of E2F1 by APC/C Cdh1 via K11 linkage-specific ubiquitin chain formation. Cell Cycle 2012, 11:2030-2038.
105. Ping Z., Lim R., Bashir T., Pagano M., Guardavaccaro D. APC/C (Cdh1) controls the proteasome-mediated degradation of E2F3 during cell cycle exit. Cell Cycle 2012, 11:1999-2005.
106. Sun J., Karoulia Z., Wong E.Y., Ahmed M., Itoh K., Xu P.X. The phosphatase-transcription activator EYA1 is targeted by anaphase-promoting complex/Cdh1 for degradation at M-to-G1 transition. Mol. Cell. Biol. 2013, 33:927-936.
107. Lai F., Hu K., Wu Y., Tang J., Sang Y., Cao J., Kang T. Human KIAA1018/FAN1 nuclease is a new mitotic substrate of APC/C(Cdh1). Chin. J. Cancer 2012, 31:440-448.
108. Woodbury E.L., Morgan D.O. Cdk and APC activities limit the spindle-stabilizing function of Fin1 to anaphase. Nat. Cell Biol. 2007, 9:106-112.
109. Park H.J., Costa R.H., Lau L.F., Tyner A.L., Raychaudhuri P. Anaphase-promoting complex/cyclosome-CDH1-mediated proteolysis of the forkhead box M1 transcription factor is critical for regulated entry into S phase. Mol. Cell. Biol. 2008, 28:5162-5171.
110. McGarry T.J., Kirschner M.W. Geminin, an inhibitor of DNA replication, is degraded during mitosis. Cell 1998, 93:1043-1053.
111. Fu A.K., Hung K.W., Fu W.Y., Shen C., Chen Y., Xia J., Lai K.O., Ip N.Y. APC(Cdh1) mediates EphA4-dependent downregulation of AMPA receptors in homeostatic plasticity. Nat. Neurosci. 2011, 14:181-189.
112. Colombo S.L., Palacios-Callender M., Frakich N., Carcamo S., Kovacs I., Tudzarova S., Moncada S. Molecular basis for the differential use of glucose and glutamine in cell proliferation as revealed by synchronized HeLa cells. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:21069-21074.
113. Takahashi A., Imai Y., Yamakoshi K., Kuninaka S., Ohtani N., Yoshimoto S., Hori S., Tachibana M., Anderton E., Takeuchi T., Shinkai Y., Peters G., Saya H., Hara E. DNA damage signaling triggers degradation of histone methyltransferases through APC/C(Cdh1) in senescent cells. Mol. Cell 2012, 45:123-131.
114. Li L., Zhou Y., Wang G.F., Liao S.C., Ke Y.B., Wu W., Li X.H., Zhang R.L., Fu Y.C. Anaphase-promoting complex/cyclosome controls HEC1 stability. Cell Prolif. 2011, 44:1-9.
115. Kim A.H., Puram S.V., Bilimoria P.M., Ikeuchi Y., Keough S., Wong M., Rowitch D., Bonni A. A centrosomal Cdc20-APC pathway controls dendrite morphogenesis in postmitotic neurons. Cell 2009, 136:322-336.
116. Lasorella A., Stegmuller J., Guardavaccaro D., Liu G., Carro M.S., Rothschild G., de la Torre-Ubieta L., Pagano M., Bonni A., Iavarone A. Degradation of Id2 by the anaphase-promoting complex couples cell cycle exit and axonal growth. Nature 2006, 442:471-474.
117. Ko N., Nishihama R., Tully G.H., Ostapenko D., Solomon M.J., Morgan D.O., Pringle J.R. Identification of yeast IQGAP (Iqg1p) as an anaphase-promoting-complex substrate and its role in actomyosin-ring-independent cytokinesis. Mol. Biol. Cell 2007, 18:5139-5153.
118. Gutierrez G.J., Tsuji T., Chen M., Jiang W., Ronai Z.A. Interplay between Cdh1 and JNK activity during the cell cycle. Nat. Cell Biol. 2010, 12:686-695.
119. Feine O., Zur A., Mahbubani H., Brandeis M. Human kid is degraded by the APC/C(Cdh1) but not by the APC/C(Cdc20). Cell Cycle 2007, 6:2516-2523.
120. Sedgwick G.G., Hayward D.G., Di Fiore B., Pardo M., Yu L., Pines J., Nilsson J. Mechanisms controlling the temporal degradation of Nek2A and Kif18A by the APC/C-Cdc20 complex. EMBO J. 2013, 32:303-314.
121. Teng F.Y., Tang B.L. APC/C regulation of axonal growth and synaptic functions in postmitotic neurons: the Liprin-alpha connection. Cell. Mol. Life Sci. 2005, 62:1571-1578.
122. 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 2004, 119:707-718.
123. Harley M.E., Allan L.A., Sanderson H.S., Clarke P.R. Phosphorylation of Mcl-1 by CDK1-cyclin B1 initiates its Cdc20-dependent destruction during mitotic arrest. EMBO J. 2010, 29:2407-2420.
124. Kimata Y., Trickey M., Izawa D., Gannon J., Yamamoto M., Yamano H. A mutual inhibition between APC/C and its substrate Mes1 required for meiotic progression in fission yeast. Dev. Cell 2008, 14:446-454.
125. Nishimura K., Oki T., Kitaura J., Kuninaka S., Saya H., Sakaue-Sawano A., Miyawaki A., Kitamura T. APC(CDH1) targets MgcRacGAP for destruction in the late M phase. PLoS ONE 2013, 8:e63001.
126. Huang N.J., Zhang L., Tang W., Chen C., Yang C.S., Kornbluth S. The Trim39 ubiquitin ligase inhibits APC/CCdh1-mediated degradation of the Bax activator MOAP-1. J. Cell Biol. 2012, 197:361-367.
127. Cui Y., Cheng X., Zhang C., Zhang Y., Li S., Wang C., Guadagno T.M. Degradation of the human mitotic checkpoint kinase Mps1 is cell cycle-regulated by APC-cCdc20 and APC-cCdh1 ubiquitin ligases. J. Biol. Chem. 2010, 285:32988-32998.
128. Doucet C., Gutierrez G.J., Lindon C., Lorca T., Lledo G., Pinset C., Coux O. Multiple phosphorylation events control mitotic degradation of the muscle transcription factor Myf5. BMC Biochem. 2005, 6:27.
129. Lu L., Hu S., Wei R., Qiu X., Lu K., Fu Y., Li H., Xing G., Li D., Peng R., He F., Zhang L. HECT type ubiquitin ligase NEDL2 is degraded by APC/C-Cdh1 and its tight regulation maintains the metaphase to anaphase transition. J. Biol. Chem. 2013, 288:35637-35650.
130. Hayes M.J., Kimata Y., Wattam S.L., Lindon C., Mao G., Yamano H., Fry A.M. Early mitotic degradation of Nek2A depends on Cdc20-independent interaction with the APC/C. Nat. Cell Biol. 2006, 8:607-614.
131. Hames R.S., Wattam S.L., Yamano H., Bacchieri R., Fry A.M. APC/C-mediated destruction of the centrosomal kinase Nek2A occurs in early mitosis and depends upon a cyclin A-type D-box. EMBO J. 2001, 20:7117-7127.
132. Yang Y., Kim A.H., Yamada T., Wu B., Bilimoria P.M., Ikeuchi Y., de la Iglesia N., Shen J., Bonni A. A Cdc20-APC ubiquitin signaling pathway regulates presynaptic differentiation. Science 2009, 326:575-578.
133. Klitzing C., Huss R., Illert A.L., Froschl A., Wotzel S., Peschel C., Bassermann F., Duyster J. APC/C(Cdh1)-mediated degradation of the F-box protein NIPA is regulated by its association with Skp1. PLoS ONE 2011, 6:e28998.
134. Wang Y., Zhan Q. Cell cycle-dependent expression of centrosomal ninein-like protein in human cells is regulated by the anaphase-promoting complex. J. Biol. Chem. 2007, 282:17712-17719.
135. Ostapenko D., Solomon M.J. Anaphase promoting complex-dependent degradation of transcriptional repressors Nrm1 and Yhp1 in Saccharomyces cerevisiae. Mol. Biol. Cell 2011, 22:2175-2184.
136. Lim H.J., Dimova N.V., Tan M.K., Sigoillot F.D., King R.W., Shi Y. The G2/M regulator histone demethylase PHF8 is targeted for degradation by the anaphase-promoting complex containing CDC20. Mol. Cell. Biol. 2013, 33:4166-4180.
137. Lindon C., Pines J. Ordered proteolysis in anaphase inactivates Plk1 to contribute to proper mitotic exit in human cells. J. Cell Biol. 2004, 164:233-241.
138. Herrero-Mendez A., Almeida A., Fernandez E., Maestre C., Moncada S., Bolanos J.P. The bioenergetic and antioxidant status of neurons is controlled by continuous degradation of a key glycolytic enzyme by APC/C-Cdh1. Nat. Cell Biol. 2009, 11:747-752.
139. Wu S., Wang W., Kong X., Congdon L.M., Yokomori K., Kirschner M.W., Rice J.C. Dynamic regulation of the PR-Set7 histone methyltransferase is required for normal cell cycle progression. Genes Dev. 2010, 24:2531-2542.
140. Naoe H., Araki K., Nagano O., Kobayashi Y., Ishizawa J., Chiyoda T., Shimizu T., Yamamura K., Sasaki Y., Saya H., Kuninaka S. The anaphase-promoting complex/cyclosome activator Cdh1 modulates Rho GTPase by targeting p190 RhoGAP for degradation. Mol. Cell. Biol. 2010, 30:3994-4005.
141. Amador V., Ge S., Santamaria P.G., Guardavaccaro D., Pagano M. APC/C(Cdc20) controls the ubiquitin-mediated degradation of p21 in prometaphase. Mol. Cell 2007, 27:462-473.
142. Zhang L., Park C.H., Wu J., Kim H., Liu W., Fujita T., Balasubramani M., Schreiber E.M., Wang X.F., Wan Y. Proteolysis of Rad17 by Cdh1/APC regulates checkpoint termination and recovery from genotoxic stress. EMBO J. 2010, 29:1726-1737.
143. Cho H.J., Lee E.H., Han S.H., Chung H.J., Jeong J.H., Kwon J., Kim H. Degradation of human RAP80 is cell cycle regulated by Cdc20 and Cdh1 ubiquitin ligases. Mol. Cancer Res. 2012, 10:615-625.
144. Zhao W.M., Coppinger J.A., Seki A., Cheng X.L., Yates J.R., Fang G. RCS1, a substrate of APC/C, controls the metaphase to anaphase transition. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:13415-13420.
145. Chun A.C., Kok K.H., Jin D.Y. REV7 is required for anaphase-promoting complex-dependent ubiquitination and degradation of translesion DNA polymerase REV1. Cell Cycle 2013, 12:365-378.
146. Karamysheva Z., Diaz-Martinez L.A., Crow S.E., Li B., Yu H. Multiple anaphase-promoting complex/cyclosome degrons mediate the degradation of human Sgo1. J. Biol. Chem. 2009, 284:1772-1780.
147. Christensen K.L., Brennan J.D., Aldridge C.S., Ford H.L. Cell cycle regulation of the human Six1 homeoprotein is mediated by APC(Cdh1). Oncogene 2007, 26:3406-3414.
148. Stegmuller J., Konishi Y., Huynh M.A., Yuan Z., Dibacco S., Bonni A. Cell-intrinsic regulation of axonal morphogenesis by the Cdh1-APC target SnoN. Neuron 2006, 50:389-400.
149. Wei W., Ayad N.G., Wan Y., Zhang G.J., Kirschner M.W., Kaelin W.G. Degradation of the SCF component Skp2 in cell-cycle phase G1 by the anaphase-promoting complex. Nature 2004, 428:194-198.
150. Wang R., Li K.M., Zhou C.H., Xue J.L., Ji C.N., Chen J.Z. Cdc20 mediates D-box-dependent degradation of Sp100. Biochem. Biophys. Res. Commun. 2011, 415:702-706.
151. Jeng J.C., Lin Y.M., Lin C.H., Shih H.M. Cdh1 controls the stability of TACC3. Cell Cycle 2009, 8:3529-3536.
152. Ke P.Y., Kuo Y.Y., Hu C.M., Chang Z.F. Control of dTTP pool size by anaphase promoting complex/cyclosome is essential for the maintenance of genetic stability. Genes Dev. 2005, 19:1920-1933.
153. Ke P.Y., Hu C.M., Chang Y.C., Chang Z.F. Hiding human thymidine kinase 1 from APC/C-mediated destruction by thymidine binding. FASEB J. 2007, 21:1276-1284.
154. Ohoka N., Sakai S., Onozaki K., Nakanishi M., Hayashi H. Anaphase-promoting complex/cyclosome-cdh1 mediates the ubiquitination and degradation of TRB3. Biochem. Biophys. Res. Commun. 2010, 392:289-294.
155. Ichim G., Mola M., Finkbeiner M.G., Cros M.P., Herceg Z., Hernandez-Vargas H. The histone acetyltransferase component TRRAP is targeted for destruction during the cell cycle. Oncogene 2013, 33:181-192.
156. Rape M., Kirschner M.W. Autonomous regulation of the anaphase-promoting complex couples mitosis to S-phase entry. Nature 2004, 432:588-595.
157. Cotto-Rios X.M., Jones M.J., Busino L., Pagano M., Huang T.T. APC/CCdh1-dependent proteolysis of USP1 regulates the response to UV-mediated DNA damage. J. Cell Biol. 2011, 194:177-186.
158. Irniger S., Nasmyth K. The anaphase-promoting complex is required in G1 arrested yeast cells to inhibit B-type cyclin accumulation and to prevent uncontrolled entry into S-phase. J. Cell Sci. 1997, 110(Pt 13):1523-1531.
159. Puram S.V., Bonni A. Novel functions for the anaphase-promoting complex in neurobiology. Semin. Cell Dev. Biol. 2011, 22:586-594.
160. Hu D., Qiao X., Wu G., Wan Y. The emerging role of APC/CCdh1 in development. Semin. Cell Dev. Biol. 2011, 22:579-585.
161. Wasch R., Robbins J.A., Cross F.R. The emerging role of APC/CCdh1 in controlling differentiation, genomic stability and tumor suppression. Oncogene 2010, 29:1-10.
162. Manchado E., Eguren M., Malumbres M. The anaphase-promoting complex/cyclosome (APC/C): cell-cycle-dependent and -independent functions. Biochem. Soc. Trans. 2010, 38:65-71.
163. Konishi Y., Stegmuller J., Matsuda T., Bonni S., Bonni A. Cdh1-APC controls axonal growth and patterning in the mammalian brain. Science 2004, 303:1026-1030.
164. Li M., Shin Y.H., Hou L., Huang X., Wei Z., Klann E., Zhang P. The adaptor protein of the anaphase promoting complex Cdh1 is essential in maintaining replicative lifespan and in learning and memory. Nat. Cell Biol. 2008, 10:1083-1089.
165. Golan A., Yudkovsky Y., Hershko A. The cyclin-ubiquitin ligase activity of cyclosome/APC is jointly activated by protein kinases Cdk1-cyclin B and Plk. J. Biol. Chem. 2002, 277:15552-15557.
166. Chung E., Chen R.H. Phosphorylation of Cdc20 is required for its inhibition by the spindle checkpoint. Nat. Cell Biol. 2003, 5:748-753.
167. Tang Z., Shu H., Oncel D., Chen S., Yu H. Phosphorylation of Cdc20 by Bub1 provides a catalytic mechanism for APC/C inhibition by the spindle checkpoint. Mol. Cell 2004, 16:387-397.
168. 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. 2000, 271:299-304.
169. Zachariae W., Schwab M., Nasmyth K., Seufert W. Control of cyclin ubiquitination by CDK-regulated binding of Hct1 to the anaphase promoting complex. Science 1998, 282:1721-1724.
170. Mailand N., Diffley J.F. CDKs promote DNA replication origin licensing in human cells by protecting Cdc6 from APC/C-dependent proteolysis. Cell 2005, 122:915-926.
171. Lin H.K., Wang G., Chen Z., Teruya-Feldstein J., Liu Y., Chan C.H., Yang W.L., Erdjument-Bromage H., Nakayama K.I., Nimer S., Tempst P., Pandolfi P.P. Phosphorylation-dependent regulation of cytosolic localization and oncogenic function of Skp2 by Akt/PKB. Nat. Cell Biol. 2009, 11:420-432.
172. Gao D., Inuzuka H., Tseng A., Chin R.Y., Toker A., Wei W. Phosphorylation by Akt1 promotes cytoplasmic localization of Skp2 and impairs APCCdh1-mediated Skp2 destruction. Nat. Cell Biol. 2009, 11:397-408.
173. Hoyt M.A., Totis L., Roberts B.T. S. cerevisiae genes required for cell cycle arrest in response to loss of microtubule function. Cell 1991, 66:507-517.
174. Li R., Murray A.W. Feedback control of mitosis in budding yeast. Cell 1991, 66:519-531.
175. Chen R.H., Waters J.C., Salmon E.D., Murray A.W. Association of spindle assembly checkpoint component XMAD2 with unattached kinetochores. Science 1996, 274:242-246.
176. Taylor S.S., McKeon F. Kinetochore localization of murine Bub1 is required for normal mitotic timing and checkpoint response to spindle damage. Cell 1997, 89:727-735.
177. Taylor S.S., Ha E., McKeon F. The human homologue of Bub3 is required for kinetochore localization of Bub1 and a Mad3/Bub1-related protein kinase. J. Cell Biol. 1998, 142:1-11.
178. Hagting A., Den Elzen N., Vodermaier H.C., Waizenegger I.C., Peters J.M., 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. 2002, 157:1125-1137.
179. 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 2009, 16:105-117.
180. Fang G. Checkpoint protein BubR1 acts synergistically with Mad2 to inhibit anaphase-promoting complex. Mol. Biol. Cell 2002, 13:755-766.
181. 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. 2001, 154:925-936.
182. Herzog F., Primorac I., Dube P., Lenart P., Sander B., Mechtler K., Stark H., Peters J.M. Structure of the anaphase-promoting complex/cyclosome interacting with a mitotic checkpoint complex. Science 2009, 323:1477-1481.
183. Hwang L.H., Lau L.F., Smith D.L., Mistrot C.A., Hardwick K.G., Hwang E.S., Amon A., Murray A.W. Budding yeast Cdc20: a target of the spindle checkpoint. Science 1998, 279:1041-1044.
184. Kim S.H., Lin D.P., Matsumoto S., Kitazono A., Matsumoto T. Fission yeast Slp1: an effector of the Mad2-dependent spindle checkpoint. Science 1998, 279:1045-1047.
185. Han J.S., Holland A.J., Fachinetti D., Kulukian A., Cetin B., Cleveland D.W. Catalytic assembly of the mitotic checkpoint inhibitor BubR1-Cdc20 by a Mad2-induced functional switch in Cdc20. Mol. Cell 2013, 51:92-104.
186. Chow C., Wong N., Pagano M., Lun S.W., Nakayama K.I., Nakayama K., Lo K.W. Regulation of APC/CCdc20 activity by RASSF1A-APC/CCdc20 circuitry. Oncogene 2012, 31:1975-1987.
187. Song M.S., Song S.J., Ayad N.G., Chang J.S., Lee J.H., Hong H.K., Lee H., Choi N., Kim J., Kim H., Kim J.W., Choi E.J., Kirschner M.W., Lim D.S. The tumour suppressor RASSF1A regulates mitosis by inhibiting the APC-Cdc20 complex. Nat. Cell Biol. 2004, 6:129-137.
188. Reimann J.D., Gardner B.E., Margottin-Goguet F., Jackson P.K. Emi1 regulates the anaphase-promoting complex by a different mechanism than Mad2 proteins. Genes Dev. 2001, 15:3278-3285.
189. Miller J.J., Summers M.K., Hansen D.V., Nachury M.V., Lehman N.L., Loktev A., Jackson P.K. Emi1 stably binds and inhibits the anaphase-promoting complex/cyclosome as a pseudosubstrate inhibitor. Genes Dev. 2006, 20:2410-2420.
190. 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 APC(Cdh1). Nat. Cell Biol. 2002, 4:358-366.
191. Shoji S., Yoshida N., Amanai M., Ohgishi M., Fukui T., Fujimoto S., Nakano Y., Kajikawa E., Perry A.C. Mammalian Emi2 mediates cytostatic arrest and transduces the signal for meiotic exit via Cdc20. EMBO J. 2006, 25:834-845.
192. Liu J., Grimison B., Lewellyn A.L., Maller J.L. The anaphase-promoting complex/cyclosome inhibitor Emi2 is essential for meiotic but not mitotic cell cycles. J. Biol. Chem. 2006, 281:34736-34741.
193. Tung J.J., Hansen D.V., Ban K.H., Loktev A.V., Summers M.K., Adler J.R., Jackson P.K. A role for the anaphase-promoting complex inhibitor Emi2/XErp1, a homolog of early mitotic inhibitor 1, in cytostatic factor arrest of Xenopus eggs. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:4318-4323.
194. Ohe M., Kawamura Y., Ueno H., Inoue D., Kanemori Y., Senoo C., Isoda M., Nakajo N., Sagata N. Emi2 inhibition of the anaphase-promoting complex/cyclosome absolutely requires Emi2 binding via the C-terminal RL tail. Mol. Biol. Cell 2010, 21:905-913.
195. Pfleger C.M., Salic A., Lee E., Kirschner M.W. Inhibition of Cdh1-APC by the MAD2-related protein MAD2L2: a novel mechanism for regulating Cdh1. Genes Dev. 2001, 15:1759-1764.
196. Chen J., Fang G. MAD2B is an inhibitor of the anaphase-promoting complex. Genes Dev. 2001, 15:1765-1770.
197. 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. 2006, 26:9162-9176.
198. 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. 2008, 28:4653-4664.
199. Martinez J.S., Hall H., Bartolowits M.D., Hall M.C. Acm1 contributes to nuclear positioning by inhibiting Cdh1-substrate interactions. Cell Cycle 2012, 11:384-394.
200. Kimata Y., Kitamura K., Fenner N., Yamano H. Mes1 controls the meiosis I to meiosis II transition by distinctly regulating the anaphase-promoting complex/cyclosome coactivators Fzr1/Mfr1 and Slp1 in fission yeast. Mol. Biol. Cell 2011, 22:1486-1494.
201. Burton J.L., Solomon M.J. Mad3p, a pseudosubstrate inhibitor of APCCdc20 in the spindle assembly checkpoint. Genes Dev. 2007, 21:655-667.
202. Clarke D.J., Segal M., Andrews C.A., Rudyak S.G., Jensen S., Smith K., Reed S.I. S-phase checkpoint controls mitosis via an APC-independent Cdc20p function. Nat. Cell Biol. 2003, 5:928-935.
203. Wan L., Zou W., Gao D., Inuzuka H., Fukushima H., Berg A.H., Drapp R., Shaik S., Hu D., Lester C., Eguren M., Malumbres M., Glimcher L.H., Wei W. Cdh1 regulates osteoblast function through an APC/C-independent modulation of Smurf1. Mol. Cell 2011, 44:721-733.
204. Tang Z., Li B., Bharadwaj R., Zhu H., Ozkan E., Hakala K., Deisenhofer J., Yu H. APC2 cullin protein and APC11 RING protein comprise the minimal ubiquitin ligase module of the anaphase-promoting complex. Mol. Biol. Cell 2001, 12:3839-3851.
205. Yu H., Peters J.M., King R.W., Page A.M., Hieter P., Kirschner M.W. Identification of a cullin homology region in a subunit of the anaphase-promoting complex. Science 1998, 279:1219-1222.
206. Wirth K.G., Ricci R., Gimenez-Abian J.F., Taghybeeglu S., Kudo N.R., Jochum W., Vasseur-Cognet M., Nasmyth K. Loss of the anaphase-promoting complex in quiescent cells causes unscheduled hepatocyte proliferation. Genes Dev. 2004, 18:88-98.
207. Kuczera T., Stilling R.M., Hsia H.E., Bahari-Javan S., Irniger S., Nasmyth K., Sananbenesi F., Fischer A. The anaphase promoting complex is required for memory function in mice. Learn. Mem. 2010, 18:49-57.
208. Van Valen P. Oligosyndactylism, an early embryonic lethal in the mouse. J. Embryol. Exp. Morphol. 1966, 15:119-124.
209. Magnuson T., Epstein C.J. Oligosyndactyly: a lethal mutation in the mouse that results in mitotic arrest very early in development. Cell 1984, 38:823-833.
210. Pravtcheva D.D., Wise T.L. A transgene-induced mitotic arrest mutation in the mouse allelic with oligosyndactylism. Genetics 1996, 144:1747-1756.
211. Pravtcheva D.D., Wise T.L. Disruption of Apc10/Doc1 in three alleles of oligosyndactylism. Genomics 2001, 72:78-87.
212. Yamanaka H., Hashimoto N., Koyama K., Nakagawa H., Nakamura Y., Noguchi K. Expression of Apc2 during mouse development. Brain Res. Gene Expr. Patterns 2002, 1:107-114.
213. Gieffers C., Peters B.H., Kramer E.R., Dotti C.G., Peters J.M. Expression of the CDH1-associated form of the anaphase-promoting complex in postmitotic neurons. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:11317-11322.
214. Kuczera T., Stilling R.M., Hsia H.E., Bahari-Javan S., Irniger S., Nasmyth K., Sananbenesi F., Fischer A. The anaphase promoting complex is required for memory function in mice. Learn. Mem. 2011, 18:49-57.
215. Almeida A., Bolanos J.P., Moreno S. Cdh1/Hct1-APC is essential for the survival of postmitotic neurons. J. Neurosci. 2005, 25:8115-8121.
216. Stewart A.D., Stewart J. Studies on syndrome of diabetes insipidus associated with oligosyndactyly in mice. Am. J. Physiol. 1969, 217:1191-1198.
217. Kato T., Daigo Y., Aragaki M., Ishikawa K., Sato M., Kaji M. Overexpression of CDC20 predicts poor prognosis in primary non-small cell lung cancer patients. J. Surg. Oncol. 2012, 106:423-430.
218. Chang D.Z., Ma Y., Ji B., Liu Y., Hwu P., Abbruzzese J.L., Logsdon C., Wang H. Increased CDC20 expression is associated with pancreatic ductal adenocarcinoma differentiation and progression. J. Hematol. Oncol. 2012, 5:15.
219. Rajkumar T., Sabitha K., Vijayalakshmi N., Shirley S., Bose M.V., Gopal G., Selvaluxmy G. Identification and validation of genes involved in cervical tumourigenesis. BMC Cancer 2011, 11:80.
220. Marucci G., Morandi L., Magrini E., Farnedi A., Franceschi E., Miglio R., Calo D., Pession A., Foschini M.P., Eusebi V. Gene expression profiling in glioblastoma and immunohistochemical evaluation of IGFBP-2 and CDC20. Virchows Arch. 2008, 453:599-609.
221. Mondal G., Sengupta S., Panda C.K., Gollin S.M., Saunders W.S., Roychoudhury S. Overexpression of Cdc20 leads to impairment of the spindle assembly checkpoint and aneuploidization in oral cancer. Carcinogenesis 2007, 28:81-92.
222. Jiang J., Jedinak A., Sliva D. Ganodermanontriol (GDNT) exerts its effect on growth and invasiveness of breast cancer cells through the down-regulation of CDC20 and uPA. Biochem. Biophys. Res. Commun. 2011, 415:325-329.
223. Manchado E., Guillamot M., de Carcer G., Eguren M., Trickey M., Garcia-Higuera I., Moreno S., Yamano H., Canamero M., Malumbres M. Targeting mitotic exit leads to tumor regression in vivo: modulation by Cdk1, Mastl, and the PP2A/B55alpha, delta phosphatase. Cancer Cell 2010, 18:641-654.
224. Fujita T., Liu W., Doihara H., Wan Y. Regulation of Skp2-p27 axis by the Cdh1/anaphase-promoting complex pathway in colorectal tumorigenesis. Am. J. Pathol. 2008, 173:217-228.
225. Fujita T., Liu W., Doihara H., Date H., Wan Y. Dissection of the APCCdh1-Skp2 cascade in breast cancer. Clin. Cancer Res. 2008, 14:1966-1975.
226. Garcia-Higuera I., Manchado E., Dubus P., Canamero M., Mendez J., Moreno S., Malumbres M. Genomic stability and tumour suppression by the APC/C cofactor Cdh1. Nat. Cell Biol. 2008, 10:802-811.
227. 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., Jackson P.K. Oncogenic regulators and substrates of the anaphase promoting complex/cyclosome are frequently overexpressed in malignant tumors. Am. J. Pathol. 2007, 170:1793-1805.
228. Li M., York J.P., Zhang P. Loss of Cdc20 causes a securin-dependent metaphase arrest in two-cell mouse embryos. Mol. Cell. Biol. 2007, 27:3481-3488.
229. Jin F., Hamada M., Malureanu L., Jeganathan K.B., Zhou W., Morbeck D.E., van Deursen J.M. Cdc20 is critical for meiosis I and fertility of female mice. PLoS Genet. 2010, 6.
230. Eguren M., Porlan E., Manchado E., Garcia-Higuera I., Canamero M., Farinas I., Malumbres M. The APC/C cofactor Cdh1 prevents replicative stress and p53-dependent cell death in neural progenitors. Nat. Commun. 2013, 4:2880.
231. Delgado-Esteban M., Garcia-Higuera I., Maestre C., Moreno S., Almeida A. APC/C-Cdh1 coordinates neurogenesis and cortical size during development. Nat. Commun. 2013, 4:2879.
232. Wang Z., Wan L., Zhong J., Inuzuka H., Liu P., Sarkar F.H., Wei W. Cdc20: a potential novel therapeutic target for cancer treatment. Curr. Pharm. Des. 2013, 19:3210-3214.
233. Yin S., Liu J.H., Ai J.S., Xiong B., Wang Q., Hou Y., Chen D.Y., Sun Q.Y. Cdc20 is required for the anaphase onset of the first meiosis but not the second meiosis in mouse oocytes. Cell Cycle 2007, 6:2990-2992.
234. Engelbert D., Schnerch D., Baumgarten A., Wasch R. The ubiquitin ligase APC(Cdh1) is required to maintain genome integrity in primary human cells. Oncogene 2008, 27:907-917.
235. Carter S.L., Eklund A.C., Kohane I.S., Harris L.N., Szallasi Z. A signature of chromosomal instability inferred from gene expression profiles predicts clinical outcome in multiple human cancers. Nat. Genet. 2006, 38:1043-1048.
236. Schvartzman J.M., Sotillo R., Benezra R. Mitotic chromosomal instability and cancer: mouse modelling of the human disease. Nat. Rev. Cancer 2010, 10:102-115.
237. Holland A.J., Cleveland D.W. Boveri revisited: chromosomal instability, aneuploidy and tumorigenesis. Nat. Rev. Mol. Cell Biol. 2009, 10:478-487.
238. 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 2000, 101:635-645.
239. Michel L.S., Liberal V., Chatterjee A., Kirchwegger R., Pasche B., Gerald W., Dobles M., Sorger P.K., Murty V.V., Benezra R. MAD2 haplo-insufficiency causes premature anaphase and chromosome instability in mammalian cells. Nature 2001, 409:355-359.
240. Chi Y.H., Ward J.M., Cheng L.I., Yasunaga J., Jeang K.T. Spindle assembly checkpoint and p53 deficiencies cooperate for tumorigenesis in mice. Int. J. Cancer 2009, 124:1483-1489.
241. Sotillo R., Hernando E., Diaz-Rodriguez E., Teruya-Feldstein J., Cordon-Cardo C., Lowe S.W., Benezra R. Mad2 overexpression promotes aneuploidy and tumorigenesis in mice. Cancer Cell 2007, 11:9-23.
242. Sotillo R., Schvartzman J.M., Socci N.D., Benezra R. Mad2-induced chromosome instability leads to lung tumour relapse after oncogene withdrawal. Nature 2010, 464:436-440.
243. Wang Q., Liu T., Fang Y., Xie S., Huang X., Mahmood R., Ramaswamy G., Sakamoto K.M., Darzynkiewicz Z., Xu M., Dai W. BUBR1 deficiency results in abnormal megakaryopoiesis. Blood 2004, 103:1278-1285.
244. Dai W., Wang Q., Liu T., Swamy M., Fang Y., Xie S., Mahmood R., Yang Y.M., Xu M., Rao C.V. Slippage of mitotic arrest and enhanced tumor development in mice with BubR1 haploinsufficiency. Cancer Res. 2004, 64:440-445.
245. Baker D.J., Jeganathan K.B., Cameron J.D., Thompson M., Juneja S., Kopecka A., Kumar R., Jenkins R.B., de Groen P.C., Roche P., van Deursen J.M. BubR1 insufficiency causes early onset of aging-associated phenotypes and infertility in mice. Nat. Genet. 2004, 36:744-749.
246. Hartman T.K., Wengenack T.M., Poduslo J.F., van Deursen J.M. Mutant mice with small amounts of BubR1 display accelerated age-related gliosis. Neurobiol. Aging 2007, 28:921-927.
247. Matsumoto T., Baker D.J., d'Uscio L.V., Mozammel G., Katusic Z.S., van Deursen J.M. Aging-associated vascular phenotype in mutant mice with low levels of BubR1. Stroke 2007, 38:1050-1056.
248. Rao C.V., Yang Y.M., Swamy M.V., Liu T., Fang Y., Mahmood R., Jhanwar-Uniyal M., Dai W. Colonic tumorigenesis in BubR1+/-ApcMin/+ compound mutant mice is linked to premature separation of sister chromatids and enhanced genomic instability. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:4365-4370.
249. Baker D.J., Perez-Terzic C., Jin F., Pitel K.S., Niederlander N.J., Jeganathan K., Yamada S., Reyes S., Rowe L., Hiddinga H.J., Eberhardt N.L., Terzic A., van Deursen J.M. Opposing roles for p16Ink4a and p19Arf in senescence and ageing caused by BubR1 insufficiency. Nat. Cell Biol. 2008, 10:825-836.
250. Baker D.J., Dawlaty M.M., Wijshake T., Jeganathan K.B., Malureanu L., van Ree J.H., Crespo-Diaz R., Reyes S., Seaburg L., Shapiro V., Behfar A., Terzic A., van de Sluis B., van Deursen J.M. Increased expression of BubR1 protects against aneuploidy and cancer and extends healthy lifespan. Nat. Cell Biol. 2013, 15:96-102.
251. Kalitsis P., Earle E., Fowler K.J., Choo K.H. Bub3 gene disruption in mice reveals essential mitotic spindle checkpoint function during early embryogenesis. Genes Dev. 2000, 14:2277-2282.
252. Babu J.R., Jeganathan K.B., Baker D.J., Wu X., Kang-Decker N., van Deursen J.M. Rae1 is an essential mitotic checkpoint regulator that cooperates with Bub3 to prevent chromosome missegregation. J. Cell Biol. 2003, 160:341-353.
253. Kalitsis P., Fowler K.J., Griffiths B., Earle E., Chow C.W., Jamsen K., Choo K.H. Increased chromosome instability but not cancer predisposition in haploinsufficient Bub3 mice. Genes Chromosomes Cancer 2005, 44:29-36.
254. Baker D.J., Jeganathan K.B., Malureanu L., Perez-Terzic C., Terzic A., van Deursen J.M. Early aging-associated phenotypes in Bub3/Rae1 haploinsufficient mice. J. Cell Biol. 2006, 172:529-540.
255. Lee H., Lee D.J., Oh S.P., Park H.D., Nam H.H., Kim J.M., Lim D.S. Mouse emi1 has an essential function in mitotic progression during early embryogenesis. Mol. Cell. Biol. 2006, 26:5373-5381.
256. Pinsky B.A., Biggins S. The spindle checkpoint: tension versus attachment. Trends Cell Biol. 2005, 15:486-493.
257. Krishnan R., Goodman B., Jin D.Y., Jeang K.T., Collins C., Stetten G., Spencer F. Map location and gene structure of the Homo sapiens mitotic arrest deficient 2 (MAD2L1) gene at 4q27. Genomics 1998, 49:475-478.
258. Rashid A., Wang J.S., Qian G.S., Lu B.X., Hamilton S.R., Groopman J.D. Genetic alterations in hepatocellular carcinomas: association between loss of chromosome 4q and p53 gene mutations. Br. J. Cancer 1999, 80:59-66.
259. Shivapurkar N., Sood S., Wistuba I.I., Virmani A.K., Maitra A., Milchgrub S., Minna J.D., Gazdar A.F. Multiple regions of chromosome 4 demonstrating allelic losses in breast carcinomas. Cancer Res. 1999, 59:3576-3580.
260. Alizadeh A.A., Eisen M.B., Davis R.E., Ma C., Lossos I.S., Rosenwald A., Boldrick J.C., Sabet H., Tran T., Yu X., Powell J.I., Yang L., Marti G.E., Moore T., Hudson J., Lu L., Lewis D.B., Tibshirani R., Sherlock G., Chan W.C., Greiner T.C., Weisenburger D.D., Armitage J.O., Warnke R., Levy R., Wilson W., Grever M.R., Byrd J.C., Botstein D., Brown P.O., Staudt L.M. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 2000, 403:503-511.
261. Garber M.E., Troyanskaya O.G., Schluens K., Petersen S., Thaesler Z., Pacyna-Gengelbach M., van de Rijn M., Rosen G.D., Perou C.M., Whyte R.I., Altman R.B., Brown P.O., Botstein D., Petersen I. Diversity of gene expression in adenocarcinoma of the lung. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:13784-13789.
262. Heighway J., Knapp T., Boyce L., Brennand S., Field J.K., Betticher D.C., Ratschiller D., Gugger M., Donovan M., Lasek A., Rickert P. Expression profiling of primary non-small cell lung cancer for target identification. Oncogene 2002, 21:7749-7763.
263. Kato T., Daigo Y., Aragaki M., Ishikawa K., Sato M., Kondo S., Kaji M. Overexpression of MAD2 predicts clinical outcome in primary lung cancer patients. Lung Cancer 2011, 74:124-131.
264. Chen X., Cheung S.T., So S., Fan S.T., Barry C., Higgins J., Lai K.M., Ji J., Dudoit S., Ng I.O., Van De Rijn M., Botstein D., Brown P.O. Gene expression patterns in human liver cancers. Mol. Biol. Cell 2002, 13:1929-1939.
265. Zhang S.H., Xu A.M., Chen X.F., Li D.H., Sun M.P., Wang Y.J. Clinicopathologic significance of mitotic arrest defective protein 2 overexpression in hepatocellular carcinoma. Hum. Pathol. 2008, 39:1827-1834.
266. Rimkus C., Friederichs J., Rosenberg R., Holzmann B., Siewert J.R., Janssen K.P. Expression of the mitotic checkpoint gene MAD2L2 has prognostic significance in colon cancer. Int. J. Cancer 2007, 120:207-211.
267. Hisaoka M., Matsuyama A., Hashimoto H. Aberrant MAD2 expression in soft-tissue sarcoma. Pathol. Int. 2008, 58:329-333.
268. Wang L., Yin F., Du Y., Du W., Chen B., Zhang Y., Wu K., Ding J., Liu J., Fan D. MAD2 as a key component of mitotic checkpoint: a probable prognostic factor for gastric cancer. Am. J. Clin. Pathol. 2009, 131:793-801.
269. Malureanu L.A., Jeganathan K.B., Hamada M., Wasilewski L., Davenport J., van Deursen J.M. BubR1 N terminus acts as a soluble inhibitor of cyclin B degradation by APC/C(Cdc20) in interphase. Dev. Cell 2009, 16:118-131.
270. Lara-Gonzalez P., Scott M.I., Diez M., Sen O., Taylor S.S. BubR1 blocks substrate recruitment to the APC/C in a KEN-box-dependent manner. J. Cell Sci. 2011, 124:4332-4345.
271. Krishnamurthy J., Torrice C., Ramsey M.R., Kovalev G.I., Al-Regaiey K., Su L., Sharpless N.E. Ink4a/Arf expression is a biomarker of aging. J. Clin. Invest. 2004, 114:1299-1307.
272. Kim W.Y., Sharpless N.E. The regulation of INK4/ARF in cancer and aging. Cell 2006, 127:265-275.
273. Guardavaccaro D., Kudo Y., Boulaire J., Barchi M., Busino L., Donzelli M., Margottin-Goguet F., Jackson P.K., Yamasaki L., Pagano M. Control of meiotic and mitotic progression by the F box protein beta-Trcp1 in vivo. Dev. Cell 2003, 4:799-812.
274. Hansen D.V., Loktev A.V., Ban K.H., Jackson P.K. Plk1 regulates activation of the anaphase promoting complex by phosphorylating and triggering SCFbetaTrCP-dependent destruction of the APC Inhibitor Emi1. Mol. Biol. Cell 2004, 15:5623-5634.
275. 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. U. S. A. 2004, 101:7937-7942.
276. Wang Q., Moyret-Lalle C., Couzon F., Surbiguet-Clippe C., Saurin J.C., Lorca T., Navarro C., Puisieux A. Alterations of anaphase-promoting complex genes in human colon cancer cells. Oncogene 2003, 22:1486-1490.
277. Glotzer M., Murray A.W., Kirschner M.W. Cyclin is degraded by the ubiquitin pathway. Nature 1991, 349:132-138.
278. Pfleger C.M., Kirschner M.W. The KEN box: an APC recognition signal distinct from the D box targeted by Cdh1. Gene Dev. 2000, 14:655-665.
279. Castro A., Vigneron S., Bernis C., Labbe J.C., Prigent C., Lorca T. The D-Box-activating domain (DAD) is a new proteolysis signal that stimulates the silent D-Box sequence of aurora-A. EMBO Rep. 2002, 3:1209-1214.
280. Araki M., Wharton R.P., Tang Z., Yu H., Asano M. Degradation of origin recognition complex large subunit by the anaphase-promoting complex in Drosophila. EMBO J. 2003, 22:6115-6126.
281. Reis A., Levasseur M., Chang H.Y., Elliott D.J., Jones K.T. The CRY box: a second APCcdh1-dependent degron in mammalian cdc20. EMBO Rep. 2006, 7:1040-1045.
282. Castro A., Vigneron S., Bernis C., Labbe J.C., Lorca T. Xkid is degraded in a D-box, KEN-box, and A-box-independent pathway. Mol. Cell. Biol. 2003, 23:4126-4138.
283. Penas C., Ramachandran V., Ayad N.G. The APC/C ubiquitin ligase: from cell biology to tumorigenesis. Front. Oncol. 2011, 1:60.
284. Chin Y.R., Toker A. Akt isoform-specific signaling in breast cancer: uncovering an anti-migratory role for palladin. Cell Adhes. Migr. 2011, 5:211-214.
285. Zeng X., Sigoillot F., Gaur S., Choi S., Pfaff K.L., Oh D.C., Hathaway N., Dimova N., Cuny G.D., King R.W. Pharmacologic inhibition of the anaphase-promoting complex induces a spindle checkpoint-dependent mitotic arrest in the absence of spindle damage. Cancer cell 2010, 18:382-395.
286. Duda D.M., Borg L.A., Scott D.C., Hunt H.W., Hammel M., Schulman B.A. Structural insights into NEDD8 activation of cullin-RING ligases: conformational control of conjugation. Cell 2008, 134:995-1006.
287. Soucy T.A., Smith P.G., Milhollen M.A., Berger A.J., Gavin J.M., Adhikari S., Brownell J.E., Burke K.E., Cardin D.P., Critchley S., Cullis C.A., Doucette A., Garnsey J.J., Gaulin J.L., Gershman R.E., Lublinsky A.R., McDonald A., Mizutani H., Narayanan U., Olhava E.J., Peluso S., Rezaei M., Sintchak M.D., Talreja T., Thomas M.P., Traore T., Vyskocil S., Weatherhead G.S., Yu J., Zhang J., Dick L.R., Claiborne C.F., Rolfe M., Bolen J.B., Langston S.P. An inhibitor of NEDD8-activating enzyme as a new approach to treat cancer. Nature 2009, 458:732-736.
288. Wang C.X., Fisk B.C., Wadehra M., Su H., Braun J. Overexpression of murine fizzy-related (fzr) increases natural killer cell-mediated cell death and suppresses tumor growth. Blood 2000, 96:259-263.