Ama1p-activated Anaphase-promoting Complex Regulates the Destruction of Cdc20p During Meiosis II

Overview

Journal Mol Biol Cell

Specialties Cell Biology
Molecular Biology

Date 2010 Dec 2

PMID 21118994

Citations 17

Authors

Grace S Tan

Jennifer Magurno

Katrina F Cooper

Affiliations

Soon will be listed here.

Abstract

The execution of meiotic divisions in Saccharomyces cerevisiae is regulated by anaphase-promoting complex/cyclosome (APC/C)-mediated protein degradation. During meiosis, the APC/C is activated by association with Cdc20p or the meiosis-specific activator Ama1p. We present evidence that, as cells exit from meiosis II, APC/C(Ama1) mediates Cdc20p destruction. APC/C(Ama1) recognizes two degrons on Cdc20p, the destruction box and destruction degron, with either domain being sufficient to mediate Cdc20p destruction. Cdc20p does not need to associate with the APC/C to bind Ama1p or be destroyed. Coimmunoprecipitation analyses showed that the diverged amino-terminal region of Ama1p recognizes both Cdc20p and Clb1p, a previously identified substrate of APC/C(Ama1). Domain swap experiments revealed that the C-terminal WD region of Cdh1p, when fused to the N-terminal region of Ama1p, could direct most of Ama1p functions, although at a reduced level. In addition, this fusion protein cannot complement the spore wall defect in ama1Δ strains, indicating that substrate specificity is also derived from the WD repeat domain. These findings provide a mechanism to temporally down-regulate APC/C(Cdc20) activity as the cells complete meiosis II and form spores.

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References

Burton J, Tsakraklides V, Solomon M . Assembly of an APC-Cdh1-substrate complex is stimulated by engagement of a destruction box. Mol Cell. 2005; 18(5):533-42. DOI: 10.1016/j.molcel.2005.04.022. View

Benanti J, Toczyski D . Cdc20, an activator at last. Mol Cell. 2008; 32(4):460-1. PMC: 2880502. DOI: 10.1016/j.molcel.2008.11.006. View

Pfleger C, Lee E, Kirschner M . Substrate recognition by the Cdc20 and Cdh1 components of the anaphase-promoting complex. Genes Dev. 2001; 15(18):2396-407. PMC: 312782. DOI: 10.1101/gad.918201. View

Hendrickson C, Meyn 3rd M, Morabito L, Holloway S . The KEN box regulates Clb2 proteolysis in G1 and at the metaphase-to-anaphase transition. Curr Biol. 2001; 11(22):1781-7. DOI: 10.1016/s0960-9822(01)00564-4. View

Thornton B, Ng T, Matyskiela M, Carroll C, Morgan D, Toczyski D . An architectural map of the anaphase-promoting complex. Genes Dev. 2006; 20(4):449-60. PMC: 1369047. DOI: 10.1101/gad.1396906. View

Hilioti Z, Chung Y, Mochizuki Y, Hardy C . The anaphase inhibitor Pds1 binds to the APC/C-associated protein Cdc20 in a destruction box-dependent manner. Curr Biol. 2001; 11(17):1347-52. DOI: 10.1016/s0960-9822(01)00399-2. View

Visintin R, Prinz S, Amon A . CDC20 and CDH1: a family of substrate-specific activators of APC-dependent proteolysis. Science. 1997; 278(5337):460-3. DOI: 10.1126/science.278.5337.460. View

Littlepage L, Ruderman J . 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(17):2274-85. PMC: 186670. DOI: 10.1101/gad.1007302. View

Castro A, Vigneron S, Bernis C, Labbe J, Lorca T . Xkid is degraded in a D-box, KEN-box, and A-box-independent pathway. Mol Cell Biol. 2003; 23(12):4126-38. PMC: 156142. DOI: 10.1128/MCB.23.12.4126-4138.2003. View

10.

Carroll C, Morgan D . The Doc1 subunit is a processivity factor for the anaphase-promoting complex. Nat Cell Biol. 2002; 4(11):880-7. DOI: 10.1038/ncb871. View

11.

Anghileri P, Branduardi P, Sternieri F, Monti P, Visintin R, Bevilacqua A . Chromosome separation and exit from mitosis in budding yeast: dependence on growth revealed by cAMP-mediated inhibition. Exp Cell Res. 1999; 250(2):510-23. DOI: 10.1006/excr.1999.4531. View

12.

Shirayama M, Toth A, Galova M, Nasmyth K . APC(Cdc20) promotes exit from mitosis by destroying the anaphase inhibitor Pds1 and cyclin Clb5. Nature. 2000; 402(6758):203-7. DOI: 10.1038/46080. View

13.

Passmore L, McCormack E, Au S, Paul A, Willison K, Harper J . Doc1 mediates the activity of the anaphase-promoting complex by contributing to substrate recognition. EMBO J. 2003; 22(4):786-96. PMC: 145444. DOI: 10.1093/emboj/cdg084. View

14.

Morris M, Kaiser P, Rudyak S, Baskerville C, Watson M, Reed S . Cks1-dependent proteasome recruitment and activation of CDC20 transcription in budding yeast. Nature. 2003; 423(6943):1009-13. DOI: 10.1038/nature01720. View

15.

Vodermaier H, Gieffers C, Maurer-Stroh S, Eisenhaber F, Peters J . TPR subunits of the anaphase-promoting complex mediate binding to the activator protein CDH1. Curr Biol. 2003; 13(17):1459-68. DOI: 10.1016/s0960-9822(03)00581-5. View

16.

McDonald C, Cooper K, Winter E . The Ama1-directed anaphase-promoting complex regulates the Smk1 mitogen-activated protein kinase during meiosis in yeast. Genetics. 2005; 171(3):901-11. PMC: 1456836. DOI: 10.1534/genetics.105.045567. View

17.

Robbins J, Cross F . Regulated degradation of the APC coactivator Cdc20. Cell Div. 2010; 5:23. PMC: 2949745. DOI: 10.1186/1747-1028-5-23. View

18.

Chu T, Henrion G, Haegeli V, Strickland S . Cortex, a Drosophila gene required to complete oocyte meiosis, is a member of the Cdc20/fizzy protein family. Genesis. 2001; 29(3):141-52. DOI: 10.1002/gene.1017. View

19.

Rabitsch K, Toth A, Galova M, Schleiffer A, Schaffner G, Aigner E . A screen for genes required for meiosis and spore formation based on whole-genome expression. Curr Biol. 2001; 11(13):1001-9. DOI: 10.1016/s0960-9822(01)00274-3. View

20.

Cooper K, Mallory M, Smith J, Strich R . Stress and developmental regulation of the yeast C-type cyclin Ume3p (Srb11p/Ssn8p). EMBO J. 1997; 16(15):4665-75. PMC: 1170093. DOI: 10.1093/emboj/16.15.4665. View