Home LiteratureArticle Details
PMID: 21633387 Published · epublish English Review

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

Nature reviews. Molecular cell biology ·Vol. 12 ·No. 7 ·2011-00-02 ·Pages 427-38

Pines J

Abstract

One does not often look to analytic cubism for insights into the control of the cell cycle, but Pablo Picasso beautifully encapsulated the fundamentals when he said that "every act of creation is, first of all, an act of destruction". The rapid destruction of specific cell cycle regulators at just the right moment in the cell cycle ensures that daughter cells receive an equal and identical set of chromosomes from their mother and that DNA replication always follows mitosis. Remarkably, one protein complex is responsible for this surgical precision, the APC/C (anaphase-promoting complex, also known as the cyclosome). The APC/C is tightly regulated by its co-activators and by the spindle assembly checkpoint.

MeSH Terms
Anaphase-Promoting Complex-Cyclosome Animals Cell Cycle/physiology Cell Cycle Proteins/metabolism Humans Mitosis/physiology Models, Biological Spindle Apparatus/metabolism Ubiquitin-Protein Ligase Complexes/metabolism
Chemicals
Cell Cycle Proteins Ubiquitin-Protein Ligase Complexes Anaphase-Promoting Complex-Cyclosome
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Pines Jonathon
The Gurdon Institute, Tennis Court Road, Cambridge CB2 1QN, UK. [email protected]
References (140)
140 references, click to expand
  1. Geminin, an inhibitor of DNA replication, is degraded during mitosis.
    Cell. 1998 Jun 12;93(6):1043-53 PMID: 9635433
  2. Pseudosubstrate inhibition of the anaphase-promoting complex by Acm1: regulation by proteolysis and Cdc28 phosphorylation.
    Mol Cell Biol. 2008 Aug;28(15):4653-64 PMID: 18519589
  3. Accumulation of cyclin B1 requires E2F and cyclin-A-dependent rearrangement of the anaphase-promoting complex.
    Nature. 1999 Oct 21;401(6755):815-8 PMID: 10548110
  4. A fission yeast homolog of CDC20/p55CDC/Fizzy is required for recovery from DNA damage and genetically interacts with p34cdc2.
    Mol Cell Biol. 1997 Feb;17(2):742-50 PMID: 9001228
  5. UBE2S elongates ubiquitin chains on APC/C substrates to promote mitotic exit.
    Nat Cell Biol. 2009 Nov;11(11):1363-9 PMID: 19820702
  6. Catalysis of lysine 48-specific ubiquitin chain assembly by residues in E2 and ubiquitin.
    Mol Cell. 2010 Aug 27;39(4):548-59 PMID: 20797627
  7. APC(ste9/srw1) promotes degradation of mitotic cyclins in G(1) and is inhibited by cdc2 phosphorylation.
    EMBO J. 2000 Aug 1;19(15):3945-55 PMID: 10921876
  8. APC/C Cdh1 targets aurora kinase to control reorganization of the mitotic spindle at anaphase.
    Curr Biol. 2008 Nov 11;18(21):1649-58 PMID: 18976910
  9. The Doc1 subunit is a processivity factor for the anaphase-promoting complex.
    Nat Cell Biol. 2002 Nov;4(11):880-7 PMID: 12402045
  10. Loss of the anaphase-promoting complex in quiescent cells causes unscheduled hepatocyte proliferation.
    Genes Dev. 2004 Jan 1;18(1):88-98 PMID: 14724179
  11. Phosphorylation of the cyclosome is required for its stimulation by Fizzy/cdc20.
    Biochem Biophys Res Commun. 1999 Jun 24;260(1):193-8 PMID: 10381365
  12. Spindle checkpoint regulates Cdc20p stability in Saccharomyces cerevisiae.
    Genes Dev. 2004 Jun 15;18(12):1439-51 PMID: 15198982
  13. Doc1 mediates the activity of the anaphase-promoting complex by contributing to substrate recognition.
    EMBO J. 2003 Feb 17;22(4):786-96 PMID: 12574115
  14. TPR subunits of the anaphase-promoting complex mediate binding to the activator protein CDH1.
    Curr Biol. 2003 Sep 2;13(17):1459-68 PMID: 12956947
  15. Emi2-mediated inhibition of E2-substrate ubiquitin transfer by the anaphase-promoting complex/cyclosome through a D-box-independent mechanism.
    Mol Biol Cell. 2010 Aug 1;21(15):2589-97 PMID: 20534816
  16. Cohesin cleavage by separase required for anaphase and cytokinesis in human cells.
    Science. 2001 Aug 17;293(5533):1320-3 PMID: 11509732
  17. How cyclin A destruction escapes the spindle assembly checkpoint.
    J Cell Biol. 2010 Aug 23;190(4):501-9 PMID: 20733051
  18. Terminal mitoses require negative regulation of Fzr/Cdh1 by Cyclin A, preventing premature degradation of mitotic cyclins and String/Cdc25.
    Development. 2006 Aug;133(16):3201-11 PMID: 16854973
  19. Fission yeast Ste9, a homolog of Hct1/Cdh1 and Fizzy-related, is a novel negative regulator of cell cycle progression during G1-phase.
    Mol Biol Cell. 1998 May;9(5):1065-80 PMID: 9571240
  20. Ubiquitination by the anaphase-promoting complex drives spindle checkpoint inactivation.
    Nature. 2007 Apr 19;446(7138):921-5 PMID: 17443186
  21. Loss of the mammalian APC/C activator FZR1 shortens G1 and lengthens S phase but has little effect on exit from mitosis.
    J Cell Sci. 2009 Nov 15;122(Pt 22):4208-17 PMID: 19861496
  22. The E2-C vihar is required for the correct spatiotemporal proteolysis of cyclin B and itself undergoes cyclical degradation.
    Curr Biol. 2004 Oct 5;14(19):1723-33 PMID: 15458643
  23. How APC/C-Cdc20 changes its substrate specificity in mitosis.
    Nat Cell Biol. 2011 Mar;13(3):223-33 PMID: 21336306
  24. Early mitotic degradation of the homeoprotein HOXC10 is potentially linked to cell cycle progression.
    EMBO J. 2003 Jul 15;22(14):3715-24 PMID: 12853486
  25. CDK inactivation is the only essential function of the APC/C and the mitotic exit network proteins for origin resetting during mitosis.
    Mol Cell. 2000 Jan;5(1):85-95 PMID: 10678171
  26. A role for the Fizzy/Cdc20 family of proteins in activation of the APC/C distinct from substrate recruitment.
    Mol Cell. 2008 Nov 21;32(4):576-83 PMID: 19026787
  27. Control of the SCF(Skp2-Cks1) ubiquitin ligase by the APC/C(Cdh1) ubiquitin ligase.
    Nature. 2004 Mar 11;428(6979):190-3 PMID: 15014502
  28. Getting down to the phosphorylated 'nuts and bolts' of spindle checkpoint signalling.
    Trends Biochem Sci. 2010 Jan;35(1):18-27 PMID: 19836959
  29. Ordered proteolysis in anaphase inactivates Plk1 to contribute to proper mitotic exit in human cells.
    J Cell Biol. 2004 Jan 19;164(2):233-41 PMID: 14734534
  30. Structures of APC/C(Cdh1) with substrates identify Cdh1 and Apc10 as the D-box co-receptor.
    Nature. 2011 Feb 10;470(7333):274-8 PMID: 21107322
  31. Rca1 inhibits APC-Cdh1(Fzr) and is required to prevent cyclin degradation in G2.
    Dev Cell. 2002 Jan;2(1):29-40 PMID: 11782312
  32. Emi1 stably binds and inhibits the anaphase-promoting complex/cyclosome as a pseudosubstrate inhibitor.
    Genes Dev. 2006 Sep 1;20(17):2410-20 PMID: 16921029
  33. The processivity of multiubiquitination by the APC determines the order of substrate degradation.
    Cell. 2006 Jan 13;124(1):89-103 PMID: 16413484
  34. Structural basis for the subunit assembly of the anaphase-promoting complex.
    Nature. 2011 Feb 10;470(7333):227-32 PMID: 21307936
  35. APC/C- and Mad2-mediated degradation of Cdc20 during spindle checkpoint activation.
    Cell Cycle. 2009 Jan 1;8(1):167-71 PMID: 19098431
  36. Dominant-negative cyclin-selective ubiquitin carrier protein E2-C/UbcH10 blocks cells in metaphase.
    Proc Natl Acad Sci U S A. 1997 Mar 18;94(6):2362-7 PMID: 9122200
  37. Drosophila fizzy-related down-regulates mitotic cyclins and is required for cell proliferation arrest and entry into endocycles.
    Cell. 1997 Aug 22;90(4):671-81 PMID: 9288747
  38. Mutagenic analysis of the destruction signal of mitotic cyclins and structural characterization of ubiquitinated intermediates.
    Mol Biol Cell. 1996 Sep;7(9):1343-57 PMID: 8885231
  39. Mitosis: a matter of getting rid of the right protein at the right time.
    Trends Cell Biol. 2006 Jan;16(1):55-63 PMID: 16337124
  40. Temporal and spatial control of cyclin B1 destruction in metaphase.
    Nat Cell Biol. 1999 Jun;1(2):82-7 PMID: 10559878
  41. BUBR1 deficiency results in abnormal megakaryopoiesis.
    Blood. 2004 Feb 15;103(4):1278-85 PMID: 14576056
  42. Tumor susceptibility of Rassf1a knockout mice.
    Cancer Res. 2005 Jan 1;65(1):92-8 PMID: 15665283
  43. BubR1 N terminus acts as a soluble inhibitor of cyclin B degradation by APC/C(Cdc20) in interphase.
    Dev Cell. 2009 Jan;16(1):118-31 PMID: 19154723
  44. Genomic stability and tumour suppression by the APC/C cofactor Cdh1.
    Nat Cell Biol. 2008 Jul;10(7):802-11 PMID: 18552834
  45. Analysis of activator-binding sites on the APC/C supports a cooperative substrate-binding mechanism.
    Mol Cell. 2009 Apr 10;34(1):68-80 PMID: 19362536
  46. Substrate binding on the APC/C occurs between the coactivator Cdh1 and the processivity factor Doc1.
    Nat Struct Mol Biol. 2011 Jan;18(1):6-13 PMID: 21186364
  47. Three-dimensional structure of the anaphase-promoting complex.
    Mol Cell. 2001 Apr;7(4):907-13 PMID: 11336713
  48. Unattached kinetochores catalyze production of an anaphase inhibitor that requires a Mad2 template to prime Cdc20 for BubR1 binding.
    Dev Cell. 2009 Jan;16(1):105-17 PMID: 19154722
  49. Quantitative analysis of in vitro ubiquitinated cyclin B1 reveals complex chain topology.
    Nat Cell Biol. 2006 Jul;8(7):700-10 PMID: 16799550
  50. Phosphorylation by Cdc28 activates the Cdc20-dependent activity of the anaphase-promoting complex.
    J Cell Biol. 2000 Jun 26;149(7):1377-90 PMID: 10871279
  51. APC2 Cullin protein and APC11 RING protein comprise the minimal ubiquitin ligase module of the anaphase-promoting complex.
    Mol Biol Cell. 2001 Dec;12(12):3839-51 PMID: 11739784
  52. Cdc28 activates exit from mitosis in budding yeast.
    J Cell Biol. 2000 Jun 26;149(7):1361-76 PMID: 10871278
  53. The Cdc14B-Cdh1-Plk1 axis controls the G2 DNA-damage-response checkpoint.
    Cell. 2008 Jul 25;134(2):256-67 PMID: 18662541
  54. Regulation of APC/C activators in mitosis and meiosis.
    Annu Rev Cell Dev Biol. 2008;24:475-99 PMID: 18598214
  55. Control of cyclin ubiquitination by CDK-regulated binding of Hct1 to the anaphase promoting complex.
    Science. 1998 Nov 27;282(5394):1721-4 PMID: 9831566
  56. The WD40 propeller domain of Cdh1 functions as a destruction box receptor for APC/C substrates.
    Mol Cell. 2005 May 27;18(5):543-53 PMID: 15916961
  57. Two redundant oscillatory mechanisms in the yeast cell cycle.
    Dev Cell. 2003 May;4(5):741-52 PMID: 12737808
  58. Vertebrate cells genetically deficient for Cdc14A or Cdc14B retain DNA damage checkpoint proficiency but are impaired in DNA repair.
    J Cell Biol. 2010 May 17;189(4):631-9 PMID: 20479464
  59. Closing the cell cycle circle in yeast: G2 cyclin proteolysis initiated at mitosis persists until the activation of G1 cyclins in the next cycle.
    Cell. 1994 Jul 1;77(7):1037-50 PMID: 8020094
  60. CDKs promote DNA replication origin licensing in human cells by protecting Cdc6 from APC/C-dependent proteolysis.
    Cell. 2005 Sep 23;122(6):915-26 PMID: 16153703
  61. Structural analysis of the anaphase-promoting complex reveals multiple active sites and insights into polyubiquitylation.
    Mol Cell. 2005 Dec 22;20(6):855-66 PMID: 16364911
  62. Plk1 regulates activation of the anaphase promoting complex by phosphorylating and triggering SCFbetaTrCP-dependent destruction of the APC Inhibitor Emi1.
    Mol Biol Cell. 2004 Dec;15(12):5623-34 PMID: 15469984
  63. A novel yeast screen for mitotic arrest mutants identifies DOC1, a new gene involved in cyclin proteolysis.
    Mol Biol Cell. 1997 Oct;8(10):1877-87 PMID: 9348530
  64. The APC/C inhibitor, Emi1, is essential for prevention of rereplication.
    Genes Dev. 2007 Jan 15;21(2):184-94 PMID: 17234884
  65. The unique N terminus of the UbcH10 E2 enzyme controls the threshold for APC activation and enhances checkpoint regulation of the APC.
    Mol Cell. 2008 Aug 22;31(4):544-556 PMID: 18722180
  66. Strong inducible knockdown of APC/CCdc20 does not cause mitotic arrest in human somatic cells.
    Cell Cycle. 2009 Feb 15;8(4):643-6 PMID: 19197151
  67. Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1.
    Nature. 1999 Jul 1;400(6739):37-42 PMID: 10403247
  68. Apc10 and Ste9/Srw1, two regulators of the APC-cyclosome, as well as the CDK inhibitor Rum1 are required for G1 cell-cycle arrest in fission yeast.
    EMBO J. 1998 Sep 15;17(18):5388-99 PMID: 9736616
  69. 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 Jun 24;157(7):1125-37 PMID: 12070128
  70. At the interface between signaling and executing anaphase--Cdc14 and the FEAR network.
    Genes Dev. 2004 Nov 1;18(21):2581-95 PMID: 15520278
  71. Cdc20 and Cks direct the spindle checkpoint-independent destruction of cyclin A.
    Mol Cell. 2008 May 9;30(3):290-302 PMID: 18471975
  72. Chromosome missegregation and apoptosis in mice lacking the mitotic checkpoint protein Mad2.
    Cell. 2000 Jun 9;101(6):635-45 PMID: 10892650
  73. Modulation of the mitotic regulatory network by APC-dependent destruction of the Cdh1 inhibitor Acm1.
    Mol Cell. 2008 May 23;30(4):437-46 PMID: 18498748
  74. Structure of the anaphase-promoting complex/cyclosome interacting with a mitotic checkpoint complex.
    Science. 2009 Mar 13;323(5920):1477-81 PMID: 19286556
  75. Emi1 is a mitotic regulator that interacts with Cdc20 and inhibits the anaphase promoting complex.
    Cell. 2001 Jun 1;105(5):645-55 PMID: 11389834
  76. Mitotic regulation of the human anaphase-promoting complex by phosphorylation.
    EMBO J. 2003 Dec 15;22(24):6598-609 PMID: 14657031
  77. Yeast Hct1 is a regulator of Clb2 cyclin proteolysis.
    Cell. 1997 Aug 22;90(4):683-93 PMID: 9288748
  78. A Cdc20-APC ubiquitin signaling pathway regulates presynaptic differentiation.
    Science. 2009 Oct 23;326(5952):575-8 PMID: 19900895
  79. Cyclin A is destroyed in prometaphase and can delay chromosome alignment and anaphase.
    J Cell Biol. 2001 Apr 2;153(1):121-36 PMID: 11285279
  80. Segregating sister genomes: the molecular biology of chromosome separation.
    Science. 2002 Jul 26;297(5581):559-65 PMID: 12142526
  81. Early mitotic degradation of Nek2A depends on Cdc20-independent interaction with the APC/C.
    Nat Cell Biol. 2006 Jun;8(6):607-14 PMID: 16648845
  82. Inhibitory phosphorylation of cyclin-dependent kinase 1 as a compensatory mechanism for mitosis exit.
    Mol Cell Biol. 2011 Apr;31(7):1478-91 PMID: 21262764
  83. Mechanism of ubiquitin-chain formation by the human anaphase-promoting complex.
    Cell. 2008 May 16;133(4):653-65 PMID: 18485873
  84. UbcH10 has a rate-limiting role in G1 phase but might not act in the spindle checkpoint or as part of an autonomous oscillator.
    J Cell Sci. 2008 Jul 15;121(Pt 14):2319-26 PMID: 18559889
  85. An architectural map of the anaphase-promoting complex.
    Genes Dev. 2006 Feb 15;20(4):449-60 PMID: 16481473
  86. Driving the cell cycle with a minimal CDK control network.
    Nature. 2010 Dec 23;468(7327):1074-9 PMID: 21179163
  87. The APC subunit Doc1 promotes recognition of the substrate destruction box.
    Curr Biol. 2005 Jan 11;15(1):11-8 PMID: 15649358
  88. Multimodal activation of the ubiquitin ligase SCF by Nedd8 conjugation.
    Mol Cell. 2008 Oct 10;32(1):21-31 PMID: 18851830
  89. Control of the oocyte-to-embryo transition by the ubiquitin-proteolytic system in mouse and C. elegans.
    Curr Opin Cell Biol. 2010 Dec;22(6):758-63 PMID: 20943362
  90. Structural organization of the anaphase-promoting complex bound to the mitotic activator Slp1.
    Mol Cell. 2007 Dec 14;28(5):871-85 PMID: 18082611
  91. Phosphorylation of Skp2 regulated by CDK2 and Cdc14B protects it from degradation by APC(Cdh1) in G1 phase.
    EMBO J. 2008 Feb 20;27(4):679-91 PMID: 18239684
  92. Anaphase initiation is regulated by antagonistic ubiquitination and deubiquitination activities.
    Nature. 2007 Apr 19;446(7138):876-81 PMID: 17443180
  93. The disappearance of cyclin B at the end of mitosis is regulated spatially in Drosophila cells.
    EMBO J. 1999 Apr 15;18(8):2184-95 PMID: 10205172
  94. PKA and MPF-activated polo-like kinase regulate anaphase-promoting complex activity and mitosis progression.
    Mol Cell. 1998 Feb;1(3):371-80 PMID: 9660921
  95. The APC/C maintains the spindle assembly checkpoint by targeting Cdc20 for destruction.
    Nat Cell Biol. 2008 Dec;10(12):1411-20 PMID: 18997788
  96. E2F-dependent accumulation of hEmi1 regulates S phase entry by inhibiting APC(Cdh1).
    Nat Cell Biol. 2002 May;4(5):358-66 PMID: 11988738
  97. BubR1 acetylation at prometaphase is required for modulating APC/C activity and timing of mitosis.
    EMBO J. 2009 Jul 22;28(14):2077-89 PMID: 19407811
  98. Mad3 KEN boxes mediate both Cdc20 and Mad3 turnover, and are critical for the spindle checkpoint.
    PLoS One. 2007 Apr 04;2(4):e342 PMID: 17406666
  99. Targeting mitotic exit leads to tumor regression in vivo: Modulation by Cdk1, Mastl, and the PP2A/B55α,δ phosphatase.
    Cancer Cell. 2010 Dec 14;18(6):641-54 PMID: 21156286
  100. Identification of a physiological E2 module for the human anaphase-promoting complex.
    Proc Natl Acad Sci U S A. 2009 Oct 27;106(43):18213-8 PMID: 19822757
  101. The RING-H2 finger protein APC11 and the E2 enzyme UBC4 are sufficient to ubiquitinate substrates of the anaphase-promoting complex.
    Proc Natl Acad Sci U S A. 2000 Aug 1;97(16):8973-8 PMID: 10922056
  102. Coactivator functions in a stoichiometric complex with anaphase-promoting complex/cyclosome to mediate substrate recognition.
    EMBO Rep. 2005 Sep;6(9):873-8 PMID: 16113654
  103. Acm1 is a negative regulator of the CDH1-dependent anaphase-promoting complex/cyclosome in budding yeast.
    Mol Cell Biol. 2006 Dec;26(24):9162-76 PMID: 17030612
  104. The anaphase-promoting complex/cyclosome (APC/C) is required for rereplication control in endoreplication cycles.
    Genes Dev. 2008 Jun 15;22(12):1690-703 PMID: 18559483
  105. Loss of Cdc20 causes a securin-dependent metaphase arrest in two-cell mouse embryos.
    Mol Cell Biol. 2007 May;27(9):3481-8 PMID: 17325031
  106. The anaphase promoting complex/cyclosome is recruited to centromeres by the spindle assembly checkpoint.
    Nat Cell Biol. 2004 Sep;6(9):892-8 PMID: 15322556
  107. UBE2S drives elongation of K11-linked ubiquitin chains by the anaphase-promoting complex.
    Proc Natl Acad Sci U S A. 2010 Jan 26;107(4):1355-60 PMID: 20080579
  108. 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 Apr 2;153(1):137-48 PMID: 11285280
  109. Checkpoint inhibition of the APC/C in HeLa cells is mediated by a complex of BUBR1, BUB3, CDC20, and MAD2.
    J Cell Biol. 2001 Sep 3;154(5):925-36 PMID: 11535616
  110. Mouse emi1 has an essential function in mitotic progression during early embryogenesis.
    Mol Cell Biol. 2006 Jul;26(14):5373-81 PMID: 16809773
  111. Positive feedback sharpens the anaphase switch.
    Nature. 2008 Jul 17;454(7202):353-7 PMID: 18552837
  112. Degradation of the SCF component Skp2 in cell-cycle phase G1 by the anaphase-promoting complex.
    Nature. 2004 Mar 11;428(6979):194-8 PMID: 15014503
  113. Cdh1-APC controls axonal growth and patterning in the mammalian brain.
    Science. 2004 Feb 13;303(5660):1026-30 PMID: 14716021
  114. The checkpoint delaying anaphase in response to chromosome monoorientation is mediated by an inhibitory signal produced by unattached kinetochores.
    J Cell Biol. 1995 Aug;130(4):941-8 PMID: 7642709
  115. Two ubiquitin-conjugating enzymes, UbcP1/Ubc4 and UbcP4/Ubc11, have distinct functions for ubiquitination of mitotic cyclin.
    Mol Cell Biol. 2003 May;23(10):3497-505 PMID: 12724408
  116. Inhibitory phosphorylation of the APC regulator Hct1 is controlled by the kinase Cdc28 and the phosphatase Cdc14.
    Curr Biol. 1999 Mar 11;9(5):227-36 PMID: 10074450
  117. 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. 1998 Oct 1;17(19):5670-8 PMID: 9755167
  118. The small-molecule inhibitor BI 2536 reveals novel insights into mitotic roles of polo-like kinase 1.
    Curr Biol. 2007 Feb 20;17(4):304-15 PMID: 17291761
  119. Evidence that mitotic exit is a better cancer therapeutic target than spindle assembly.
    Cancer Cell. 2009 Oct 6;16(4):347-58 PMID: 19800579
  120. Cyclin E ablation in the mouse.
    Cell. 2003 Aug 22;114(4):431-43 PMID: 12941272
  121. The Rae1-Nup98 complex prevents aneuploidy by inhibiting securin degradation.
    Nature. 2005 Dec 15;438(7070):1036-9 PMID: 16355229
  122. Activation of Cdh1-dependent APC is required for G1 cell cycle arrest and DNA damage-induced G2 checkpoint in vertebrate cells.
    EMBO J. 2001 Nov 15;20(22):6499-508 PMID: 11707420
  123. 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 May 25;101(21):7937-42 PMID: 15148369
  124. CDC20 and CDH1: a family of substrate-specific activators of APC-dependent proteolysis.
    Science. 1997 Oct 17;278(5337):460-3 PMID: 9334304
  125. Structural insights into NEDD8 activation of cullin-RING ligases: conformational control of conjugation.
    Cell. 2008 Sep 19;134(6):995-1006 PMID: 18805092
  126. Emi1 is needed to couple DNA replication with mitosis but does not regulate activation of the mitotic APC/C.
    J Cell Biol. 2007 May 7;177(3):425-37 PMID: 17485488
  127. The tumour suppressor RASSF1A regulates mitosis by inhibiting the APC-Cdc20 complex.
    Nat Cell Biol. 2004 Feb;6(2):129-37 PMID: 14743218
  128. The Mad1/Mad2 complex as a template for Mad2 activation in the spindle assembly checkpoint.
    Curr Biol. 2005 Feb 8;15(3):214-25 PMID: 15694304
  129. Mad3p, a pseudosubstrate inhibitor of APCCdc20 in the spindle assembly checkpoint.
    Genes Dev. 2007 Mar 15;21(6):655-67 PMID: 17369399
  130. APC-dependent proteolysis of the mitotic cyclin Clb2 is essential for mitotic exit.
    Nature. 2002 Aug 1;418(6897):556-62 PMID: 12152084
  131. Systematic identification of pathways that couple cell growth and division in yeast.
    Science. 2002 Jul 19;297(5580):395-400 PMID: 12089449
  132. The ubiquitin system.
    Annu Rev Biochem. 1998;67:425-79 PMID: 9759494
  133. The spindle-assembly checkpoint in space and time.
    Nat Rev Mol Cell Biol. 2007 May;8(5):379-93 PMID: 17426725
  134. The D-Box-activating domain (DAD) is a new proteolysis signal that stimulates the silent D-Box sequence of Aurora-A.
    EMBO Rep. 2002 Dec;3(12):1209-14 PMID: 12446569
  135. Activation of cyclin B1-Cdk1 synchronizes events in the nucleus and the cytoplasm at mitosis.
    J Cell Biol. 2010 Apr 19;189(2):247-59 PMID: 20404109
  136. Autonomous regulation of the anaphase-promoting complex couples mitosis to S-phase entry.
    Nature. 2004 Dec 2;432(7017):588-95 PMID: 15558010
  137. Checkpoint protein BubR1 acts synergistically with Mad2 to inhibit anaphase-promoting complex.
    Mol Biol Cell. 2002 Mar;13(3):755-66 PMID: 11907259
  138. 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 Sep 1;16(17):2274-85 PMID: 12208850
  139. Independent regulation of synaptic size and activity by the anaphase-promoting complex.
    Cell. 2004 Nov 24;119(5):707-18 PMID: 15550251
  140. Mps1 directs the assembly of Cdc20 inhibitory complexes during interphase and mitosis to control M phase timing and spindle checkpoint signaling.
    J Cell Biol. 2010 Jul 12;190(1):89-100 PMID: 20624902
Article Info
Journal
Nature reviews. Molecular cell biology
Abbr.
Nat Rev Mol Cell Biol
ISSN
1471-0080
Published
2011-00-02
Epub
2011-00-02
Pages
427-38
Language
English
Region
England
NLM ID
100962782
Subset
IM
Corrections
ErratumIn
-
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]