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The cyclosome, a large complex containing cyclin-selective ubiquitin ligase activity, targets cyclins for destruction at the end of mitosis

V Sudakin, D Ganoth, A Dahan, H Heller, J Hershko, FC Luca, JV Ruderman and A Hershko

Unit of Biochemistry, B. Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa.

The ubiquitin-mediated degradation of mitotic cyclins is required for cells to exit from mitosis. Previous work with cell-free systems has revealed four components required for cyclin-ubiquitin ligation and proteolysis: a nonspecific ubiquitin-activating enzyme E1, a soluble fraction containing a ubiquitin carrier protein activity called E2-C, a crude particulate fraction containing a ubiquitin ligase (E3) activity that is activated during M-phase, and a constitutively active 26S proteasome that degrades ubiquitinated proteins. Here, we identify a novel approximately 1500-kDa complex, termed the cyclosome, which contains a cyclin-selective ubiquitin ligase activity, E3-C. E3-C is present but inactive during interphase; it can be activated in vitro by the addition of cdc2, enabling the transfer of ubiquitin from E2-C to cyclin. The kinetics of E3-C activation suggest the existence of one or more intermediates between cdc2 and E3-C. Cyclosome-associated E3-C acts on both cyclin A and B, and requires the presence of wild-type N- terminal destruction box motifs in each cyclin. Ubiquitinated cyclins are then rapidly recognized and degraded by the proteasome. These results identify the cyclosome-associated E3-C as the component of the cyclin destruction machinery whose activity is ultimately regulated by cdc2 and, as such, the element directly responsible for setting mitotic cyclin levels during early embryonic cell cycles.

Volume 6, Issue 2, pp. 185-197, 02/01/1995
Copyright © 1995 by The American Society for Cell Biology




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Biol. Reprod.Home page
T. Azuma, S. Ikeda, T. Kondo, H. Imai, and M. Yamada
Ethylenediamine-N,N,N',N'-Tetraacetic Acid Induces Parthenogenetic Activation of Porcine Oocytes at the Germinal Vesicle Stage, Leading to Formation of Blastocysts
Biol Reprod, February 1, 2001; 64(2): 647 - 653.
[Abstract] [Full Text]


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J. Cell Sci.Home page
J. Hood, W. Hwang, and P. Silver
The Saccharomyces cerevisiae cyclin Clb2p is targeted to multiple subcellular locations by cis- and trans-acting determinants
J. Cell Sci., January 2, 2001; 114(3): 589 - 597.
[Abstract] [PDF]


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Genes Dev.Home page
A. Nishiyama, K. Tachibana, Y. Igarashi, H. Yasuda, N. Tanahashi, K. Tanaka, K. Ohsumi, and T. Kishimoto
A nonproteolytic function of the proteasome is required for the dissociation of Cdc2 and cyclin B at the end of M phase
Genes & Dev., September 15, 2000; 14(18): 2344 - 2357.
[Abstract] [Full Text]


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JCBHome page
D. Perez-Mongiovi, C. Beckhelling, P. Chang, C. C. Ford, and E. Houliston
Nuclei and Microtubule Asters Stimulate Maturation/M Phase Promoting Factor (Mpf) Activation in Xenopus Eggs and Egg Cytoplasmic Extracts
J. Cell Biol., September 4, 2000; 150(5): 963 - 974.
[Abstract] [Full Text] [PDF]


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Clin. Cancer Res.Home page
A. Frankel, S. Man, P. Elliott, J. Adams, and R. S. Kerbel
Lack of Multicellular Drug Resistance Observed in Human Ovarian and Prostate Carcinoma Treated with the Proteasome Inhibitor PS-341
Clin. Cancer Res., September 1, 2000; 6(9): 3719 - 3728.
[Abstract] [Full Text]


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Mol. Biol. CellHome page
A. Yamanaka, S. Hatakeyama, K.-i. Kominami, M. Kitagawa, M. Matsumoto, and K.-i. Nakayama
Cell Cycle-Dependent Expression of Mammalian E2-C Regulated by the Anaphase-Promoting Complex/Cyclosome
Mol. Biol. Cell, August 1, 2000; 11(8): 2821 - 2831.
[Abstract] [Full Text]


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Mol. Cell. Biol.Home page
J. L. Burton and M. J. Solomon
Hsl1p, a Swe1p Inhibitor, Is Degraded via the Anaphase-Promoting Complex
Mol. Cell. Biol., July 1, 2000; 20(13): 4614 - 4625.
[Abstract] [Full Text] [PDF]


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Mol. Biol. CellHome page
J. D. Leverson, C. A.P. Joazeiro, A. M. Page, H.-k. Huang, P. Hieter, and T. Hunter
The APC11 RING-H2 Finger Mediates E2-Dependent Ubiquitination
Mol. Biol. Cell, July 1, 2000; 11(7): 2315 - 2325.
[Abstract] [Full Text]


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JCBHome page
A. D. Rudner, K. G. Hardwick, and A. W. Murray
Cdc28 Activates Exit from Mitosis in Budding Yeast
J. Cell Biol., June 26, 2000; 149(7): 1361 - 1376.
[Abstract] [Full Text] [PDF]


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JCBHome page
A. D. Rudner and A. W. Murray
Phosphorylation by Cdc28 Activates the Cdc20-Dependent Activity of the Anaphase-Promoting Complex
J. Cell Biol., June 26, 2000; 149(7): 1377 - 1390.
[Abstract] [Full Text] [PDF]


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Mol. Biol. CellHome page
E. R. Kramer, N. Scheuringer, A. V. Podtelejnikov, M. Mann, and J.-M. Peters
Mitotic Regulation of the APC Activator Proteins CDC20 and CDH1
Mol. Biol. Cell, May 1, 2000; 11(5): 1555 - 1569.
[Abstract] [Full Text]


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Mol. Biol. CellHome page
A. Meimoun, T. Holtzman, Z. Weissman, H. J. McBride, D. J. Stillman, G. R. Fink, and D. Kornitzer
Degradation of the Transcription Factor Gcn4 Requires the Kinase Pho85 and the SCFCDC4 Ubiquitin-Ligase Complex
Mol. Biol. Cell, March 1, 2000; 11(3): 915 - 927.
[Abstract] [Full Text]


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J. Cell Sci.Home page
H. Yamada, S Matsumoto, and T Matsumoto
High dosage expression of a zinc finger protein, Grt1, suppresses a mutant of fission yeast slp1(+), a homolog of CDC20/p55CDC/Fizzy
J. Cell Sci., January 11, 2000; 113(22): 3989 - 3999.
[Abstract] [PDF]


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Mol. Biol. CellHome page
K. C. Chen, A. Csikasz-Nagy, B. Gyorffy, J. Val, B. Novak, and J. J. Tyson
Kinetic Analysis of a Molecular Model of the Budding Yeast Cell Cycle
Mol. Biol. Cell, January 1, 2000; 11(1): 369 - 391.
[Abstract] [Full Text]


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Mol. Biol. CellHome page
H. Bastians, L. M. Topper, G. L. Gorbsky, and J. V. Ruderman
Cell Cycle-regulated Proteolysis of Mitotic Target Proteins
Mol. Biol. Cell, November 1, 1999; 10(11): 3927 - 3941.
[Abstract] [Full Text]


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J. Biol. Chem.Home page
T. P. Moynihan, H. C. Ardley, U. Nuber, S. A. Rose, P. F. Jones, A. F. Markham, M. Scheffner, and P. A. Robinson
The Ubiquitin-conjugating Enzymes UbcH7 and UbcH8 Interact with RING Finger/IBR Motif-containing Domains of HHARI and H7-AP1
J. Biol. Chem., October 22, 1999; 274(43): 30963 - 30968.
[Abstract] [Full Text] [PDF]


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Mol. Cell. Biol.Home page
E. Bailly and S. I. Reed
Functional Characterization of Rpn3 Uncovers a Distinct 19S Proteasomal Subunit Requirement for Ubiquitin-Dependent Proteolysis of Cell Cycle Regulatory Proteins in Budding Yeast
Mol. Cell. Biol., October 1, 1999; 19(10): 6872 - 6890.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
C. Gieffers, B. H. Peters, E. R. Kramer, C. G. Dotti, and J.-M. Peters
Expression of the CDH1-associated form of the anaphase-promoting complex in postmitotic neurons
PNAS, September 28, 1999; 96(20): 11317 - 11322.
[Abstract] [Full Text] [PDF]


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JCBHome page
G.K.T. Chan, S.A. Jablonski, V. Sudakin, J.C. Hittle, and T.J. Yen
Human Bubr1 Is a Mitotic Checkpoint Kinase That Monitors Cenp-E Functions at Kinetochores and Binds the Cyclosome/APC
J. Cell Biol., September 6, 1999; 146(5): 941 - 954.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
R. A. Hastings, I. Eyheralde, S. P. Dawson, G. Walker, S. E. Reynolds, M. A. Billett, and R. J. Mayer
A 220-kDa Activator Complex of the 26 S Proteasome in Insects and Humans. A ROLE IN TYPE II PROGRAMMED INSECT MUSCLE CELL DEATH AND CROSS-ACTIVATION OF PROTEASOMES FROM DIFFERENT SPECIES
J. Biol. Chem., September 3, 1999; 274(36): 25691 - 25700.
[Abstract] [Full Text] [PDF]


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JCBHome page
S. Kotani, H. Tanaka, H. Yasuda, and K. Todokoro
Regulation of APC Activity by Phosphorylation and Regulatory Factors
J. Cell Biol., August 23, 1999; 146(4): 791 - 800.
[Abstract] [Full Text] [PDF]


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Genes Dev.Home page
W. Zachariae and K. Nasmyth
Whose end is destruction: cell division and the anaphase-promoting complex
Genes & Dev., August 15, 1999; 13(16): 2039 - 2058.
[Full Text]


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Mol. Cell. Biol.Home page
P.-Y. Goh and U. Surana
Cdc4, a Protein Required for the Onset of S Phase, Serves an Essential Function during G2/M Transition in Saccharomyces cerevisiae
Mol. Cell. Biol., August 1, 1999; 19(8): 5512 - 5522.
[Abstract] [Full Text] [PDF]


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Genes Dev.Home page
R. L. Tinker-Kulberg and D. O. Morgan
Pds1 and Esp1 control both anaphase and mitotic exit in normal cells and after DNA damage
Genes & Dev., August 1, 1999; 13(15): 1936 - 1949.
[Abstract] [Full Text]


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Genes Dev.Home page
O. Cohen-Fix and D. Koshland
Pds1p of budding yeast has dual roles: inhibition of anaphase initiation and regulation of mitotic exit
Genes & Dev., August 1, 1999; 13(15): 1950 - 1959.
[Abstract] [Full Text]


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Mol. Biol. CellHome page
R.-H. Chen, D. M. Brady, D. Smith, A. W. Murray, and K. G. Hardwick
The Spindle Checkpoint of Budding Yeast Depends on a Tight Complex between the Mad1 and Mad2 Proteins
Mol. Biol. Cell, August 1, 1999; 10(8): 2607 - 2618.
[Abstract] [Full Text]


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Genes Dev.Home page
G. Goshima, S. Saitoh, and M. Yanagida
Proper metaphase spindle length is determined by centromere proteins Mis12 and Mis6 required for faithful chromosome segregation
Genes & Dev., July 1, 1999; 13(13): 1664 - 1677.
[Abstract] [Full Text]


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Proc. Natl. Acad. Sci. USAHome page
D. C. Farruggio, F. M. Townsley, and J. V. Ruderman
Cdc20 associates with the kinase aurora2/Aik
PNAS, June 22, 1999; 96(13): 7306 - 7311.
[Abstract] [Full Text] [PDF]


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Mol. Cell. Biol.Home page
L. Cheng, T. Collyer, and C. F. J. Hardy
Cell Cycle Regulation of DNA Replication Initiator Factor Dbf4p
Mol. Cell. Biol., June 1, 1999; 19(6): 4270 - 4278.
[Abstract] [Full Text] [PDF]


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GeneticsHome page
K. G. Hardwick, R. Li, C. Mistrot, R.-H. Chen, P. Dann, A. Rudner, and A. W. Murray
Lesions in Many Different Spindle Components Activate the Spindle Checkpoint in the Budding Yeast Saccharomyces cerevisiae
Genetics, June 1, 1999; 152(2): 509 - 518.
[Abstract] [Full Text]


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JCBHome page
R. Fraschini, E. Formenti, G. Lucchini, and S. Piatti
Budding Yeast Bub2 Is Localized at Spindle Pole Bodies and Activates the Mitotic Checkpoint via a Different Pathway from Mad2
J. Cell Biol., May 31, 1999; 145(5): 979 - 991.
[Abstract] [Full Text] [PDF]




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