Ama1p-activated anaphase-promoting complex regulates the destruction of Cdc20p during meiosis II

Molecular Biology of the Cell

Volumn 22, Issue 3, 2011, Pages 315-326

  Tan, Grace S ^a,c   Magurno, Jennifer ^b   Cooper, Katrina F ^a,b  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF MEDICINE AND DENTISTRY OF NEW JERSEY   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMA 1 P ENZYME; ANAPHASE PROMOTING COMPLEX; CELL CYCLE PROTEIN 20; HYBRID PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL ACTIVITY; CELL DESTRUCTION; DOWN REGULATION; ENZYME ACTIVITY; MEIOSIS; NONHUMAN; NUCLEAR DIVISION; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN FUNCTION; REGULATORY MECHANISM; YEAST;

BINDING SITES; CELL CYCLE PROTEINS; MEIOSIS; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUBSTRATE SPECIFICITY; UBIQUITIN-PROTEIN LIGASE COMPLEXES;

SACCHAROMYCES CEREVISIAE;

EID: 79551673233     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E10-04-0360     Document Type: Article

References (80)

1. Akamatsu E, Tanaka T, Kato JY (1998). Transcription factor E2F and cyclin E-Cdk2 complex cooperate to induce chromosomal DNA replication in Xenopus oocytes. J Biol Chem 273, 16494-16500.
2. Anghileri P, Branduardi P, Sternieri F, Monti P, Visintin R, Bevilacqua A, Alberghina L, Martegani E, Baroni MD (1999). Chromosome separation and exit from mitosis in budding yeast: dependence on growth revealed by cAMP-mediated inhibition. Exp Cell Res 250, 510-523.
3. Benanti JA, Toczyski DP (2008). Cdc20, an activator at last. Mol Cell 32, 460-461.
4. Bharadwaj R, Yu H (2004). The spindle checkpoint, aneuploidy, and cancer. Oncogene 23, 2016-2027.
5. Burton JL, Solomon MJ (2001). D box and KEN box motifs in budding yeast Hsl1p are required for APC-mediated degradation and direct binding to Cdc20p and Cdh1p. Genes Dev 15, 2381-2395.
6. Burton JL, Tsakraklides V, Solomon MJ (2005). Assembly of an APC-Cdh1-substrate complex is stimulated by engagement of a destruction box. Mol Cell 18, 533-542.
7. Camasses A, Bogdanova A, Shevchenko A, Zachariae W (2003). The CCT chaperonin promotes activation of the anaphase-promoting complex through the generation of functional Cdc20. Mol Cell 12, 87-100.
8. Carlile TM, Amon A (2008). Meiosis I is established through division-specific translational control of a cyclin. Cell 133, 280-291.
9. Carroll CW, Enquist-Newman M, Morgan DO (2005). The APC subunit Doc1 promotes recognition of the substrate destruction box. Curr Biol 15, 11-18. (Pubitemid 40084696)
10. Carroll CW, Morgan DO (2002). The Doc1 subunit is a processivity factor for the anaphase-promoting complex. Nat Cell Biol 4, 880-887.
11. Castro A, Vigneron S, Bernis C, Labbe JC, Lorca T (2003). Xkid is degraded in a D-box, KEN-box, and A-box-independent pathway. Mol Cell Biol 23, 4126-4138. (Pubitemid 36666418)
12. Choi E, Dial JM, Jeong DE, Hall MC (2008). Unique D box and KEN box sequences limit ubiquitination of Acm1 and promote pseudosubstrate inhibition of the anaphase-promoting complex. J Biol Chem 283, 23701-23710.
13. Christianson TW, Sikorski RS, Dante M, Shero JH, Hieter P (1992). Multifunctional yeast high-copy-number shuttle vectors. Gene 110, 119-122.
14. Chu S, DeRisi J, Eisen M, Mulholland J, Botstein D, Brown PO, Herskowitz I (1998). The transcriptional program of sporulation in budding yeast. Science 282, 699-705.
15. Chu T, Henrion G, Haegeli V, Strickland S (2001). Cortex, a Drosophila gene required to complete oocyte meiosis, is a member of the Cdc20/fizzy protein family. Genesis 29, 141-152.
16. Coluccio A, Bogengruber E, Conrad MN, Dresser ME, Briza P, Neiman AM (2004). Morphogenetic pathway of spore wall assembly in Saccharomyces cerevisiae. Eukaryot Cell 3, 1464-1475.
17. Cooper KF, Egeland DE, Mallory MJ, Jarnik M, Strich R (2000). Ama1p is a meiosis-specific regulator of the anaphase promoting complex/cyclosome in yeast. Proc Natl Acad Sci USA 97, 14548-14553.
18. Cooper KF, Mallory MJ, Guacci V, Lowe K, Strich R (2009). Pds1p is required for meiotic recombination and prophase I progression in Saccharomyces cerevisiae. Genetics 181, 65-79.
19. Cooper KF, Mallory MJ, Smith JS, Strich R (1997). Stress and developmental regulation of the yeast C-type cyclin UME3 (SRB11 / SSN8). EMBO J 16, 4665-4675.
20. Cooper KF, Mallory MJ, Strich R (1999). Oxidative stress-induced destruction of the yeast C-type cyclin Ume3p requires the phosphatidylinositolspecifi c phospholipase C and the 26S proteasome. Mol Cell Biol 19, 3338-3348.
21. Cooper KF, Strich R (1999). Functional analysis of the yeast C-type cyclin Ume3p/Srb11p- RNA polymerase II holoenzyme interaction. Gene Exp 8, 43-57.
22. Cooper KF, Strich R (2002). Saccharomyces cerevisiae C-type cyclin Ume3p/Srb11p is required for efficient induction and execution of meiotic development. Eukaryot Cell 1, 66-74.
23. Crasta K, Lim HH, Giddings TH Jr, Winey M, Surana U (2008). Inactivation of Cdh1 by synergistic action of Cdk1 and polo kinase is necessary for proper assembly of the mitotic spindle. Nat Cell Biol 10, 665-675.
24. Dawson IA, Roth S, Artavanis-Tsakonas S (1995). The Drosophila cell cycle gene fizzy is required for normal degradation of cyclins A and B during mitosis and has homology to the CDC20 gene of Saccharomyces cerevisiae. J Cell Biol 129, 725-737.
25. Deshaies RJ (1999). SCF and Cullin/RING H2-based ubiquitin ligases. Annu Rev Cell Dev Biol 15, 435-467.
26. Dial JM, Petrotchenko EV, Borchers CH (2007). Inhibition of APCCdh1 activity by Cdh1/Acm1/Bmh1 ternary complex formation. J Biol Chem 282, 5237-5248.
27. Diamond AE, Park JS, Inoue I, Tachikawa H, Neiman AM (2009). The anaphase promoting complex targeting subunit Ama1 links meiotic exit to cytokinesis during sporulation in Saccharomyces cerevisiae. Mol Biol Cell 20, 134-145.
28. Dube P, Herzog F, Gieffers C, Sander B, Riedel D, Muller SA, Engel A, Peters JM, Stark H (2005). Localization of the coactivator Cdh1 and the cullin subunit Apc2 in a cryo-electron microscopy model of vertebrate APC/C. Mol Cell 20, 867-879.
29. Enquist-Newman M, Sullivan M, Morgan DO (2008). Modulation of the mitotic regulatory network by APC-dependent destruction of the Cdh1 inhibitor Acm1. Mol Cell 30, 437-446.
30. Eytan E, Moshe Y, Braunstein I, Hershko A (2006). Roles of the anaphase-promoting complex/cyclosome and of its activator Cdc20 in functional substrate binding. Proc Natl Acad Sci USA 103, 2081-2086.
31. Fang G, Yu H, Kirschner MW (1998a). Direct binding of CDC20 protein family members activates the anaphase-promoting complex in mitosis and G1. Molecular Cell 2, 163-171.
32. Glotzer M, Murray AW, Kirschner MW (1991). Cyclin is degraded by the ubiquitin pathway. Nature 349, 132-138.
33. Goh P, Lim HL, Surana U (2000). Cdc20 protein contains a destruction-box but, unlike Clb2, its proteolysis is not acutely dependent on the activity of the anaphase-promoting complex. Eur J Biochem 267, 434-449.
34. Hall MC, Jeong DE, Henderson JT, Choi E, Bremmer SC, Iliuk AB, Charbonneau H (2008). Cdc28 and Cdc14 control stability of the anaphase-promoting complex inhibitor Acm1. J Biol Chem 283, 10396-10407.
35. Harper JW, Burton JL, Solomon MJ (2002). The anaphase-promoting complex: it's not just for mitosis any more. Genes Dev 16, 2179-2206.
36. Hendrickson C, Meyn III M, Morabito L, Holloway S (2001). The KEN box regulates Clb2 proteolysis in G1 and at the metaphase-anaphase transition. Curr Biol 11, 1781-1787.
37. Hilioti Z, Chung YS, Mochizuki Y, Hardy CF, Cohen-Fix O (2001). The anaphase inhibitor Pds1 binds to the APC/C-associated protein Cdc20 in a destruction box-dependent manner [correction published in Curr Biol (2001). 11, 1643]. Curr Biol 11, 1347-1352.
38. Huang JN, Park I, Ellingson E, Littlepage LE, Pellman D (2001). Activity of the APCCdh1 form of the anaphase promoting complex persists until S phase and prevents premature expression of Cdc20p. J Biol Chem 154, 85-94.
39. Jaquenoud M, van Drogen F, Peter M (2002). Cell cycle-dependent nuclear export of Cdh1p may contribute to the inactivation of APC/C(Cdh1). EMBO J 21, 6515-6526.
40. Jaspersen SL, Charles JF, Morgan DO (1999). Inhibitory phosphorylation of the APC regulator Hct1 is controlled by the kinase Cdc28 and the phosphatase Cdc14. Curr Biol 9, 227-236.
41. Kimata Y, Baxter JE, Fry AM, Yamano H (2008). A role for the Fizzy/Cdc20 family of proteins in activation of the APC/C distinct from substrate recruitment. Mol Cell 32, 576-583.
42. Kraft C, Herzog F, Gieffers C, Mechtler K, Hagting A, Pines J, Peters JM (2003). Mitotic regulation of the human anaphase-promoting complex by phosphorylation. EMBO J 22, 6598-6609.
43. Kraft C, Vodermaier HC, Maurer-Stroh S, Eisenhaber F, Peters JM (2005). The WD40 propeller domain of Cdh1 functions as a destruction box receptor for APC/C substrates. Mol Cell 18, 543-553.
44. Littlepage LE, Ruderman JV (2002). Identification of a new APC/C recognition domain, the A box, which is required for the Cdh1-dependent destruction of the kinase Aurora-A during mitotic exit. Genes Dev 16, 2274-2285.
45. Longtine MS, McKenzie Ar, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR (1998). Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961.
46. Mallory MJ, Cooper KF, Strich R (2007). Meiosis-specific destruction of the Ume6p repressor by the Cdc20-directed APC/C. Mol Cell 27, 951-961.
47. Martinez JS, Jeong DE, Choi E, Billings BM, Hall MC (2006). Acm1 is a negative regulator of the CDH1-dependent anaphase-promoting complex/cyclosome in budding yeast. Mol Cell Biol 26, 9162-9176.
48. Matyskiela ME, Morgan DO (2009). Analysis of activator-binding sites on the APC/C supports a cooperative substrate-binding mechanism. Mol Cell 34, 68-80.
49. McDonald CM, Cooper KF, Winter E (2005). The Ama1-directed anaphase-promoting complex regulates the Smk1 mitogen-activated protein kinase during meiosis in yeast. Genetics 171, 901-911.
50. Meyn MA III, Melloy PG, Li J, Holloway SL (2002). The destruction box of the cyclin Clb2 binds the anaphase-promoting complex/cyclosome subunit Cdc23. Arch Biochem Biophys 407, 189-195.
51. Morris MC, Kaiser P, Rudyak S, Baskerville C, Watson MH, Reed SI (2003). Cks1-dependent proteasome recruitment and activation of CDC20 transcription in budding yeast. Nature 423, 1009-1013.
52. Oelschlaegel T, Schwickart M, Matos J, Bogdanova A, Camasses A, Havlis J, Shevchenko A, Zachariae W (2005). The yeast APC/C subunit Mnd2 prevents premature sister chromatid separation triggered by the meiosis-specific APC/C-Ama1. Cell 120, 773-788.
53. Ostapenko D, Burton JL, Wang R, Solomon MJ (2008). Pseudosubstrate inhibition of the anaphase-promoting complex by Acm1: regulation by proteolysis and Cdc28 phosphorylation. Mol Cell Biol 28, 4653-4664.
54. Passmore LA, Barford D (2005). Coactivator functions in a stoichiometric complex with anaphase-promoting complex/cyclosome to mediate substrate recognition. EMBO Rep 6, 873-878.
55. Passmore LA, McCormack EA, Au SW, Paul A, Willison KR, Harper JW, Barford D (2003). Doc1 mediates the activity of the anaphase-promoting complex by contributing to substrate recognition. EMBO J 22, 786-796.
56. Penkner AM, Prinz S, Ferscha S, Klein F (2005). Mnd2, an essential antagonist of the anaphase-promoting complex during meiotic prophase. Cell 120, 789-801.
57. Pesin JA, Orr-Weaver TL (2007). Developmental role and regulation of cortex, a meiosis-specific anaphase-promoting complex/cyclosome activator. PLoS Genet 3, e202.
58. Pfleger CM, Kirschner MW (2000). The KEN box: an APC recognition signal distinct from the D box targeted by Cdh1. Genes Dev 14, 655-665.
59. Pfleger CM, Lee E, Kirschner MW (2001a). Substrate recognition by the Cdc20 and Cdh1 components of the anaphase-promoting complex. Genes Dev 15, 2396-2407.
60. Prinz S, Hwang ES, Visintin R, Amon A (1998). The regulation of Cdc20 proteolysis reveals a role for APC components Cdc23 and Cdc27 during S phase and early mitosis. Curr Biol 8, 750-760.
61. Rabitsch KP et al. (2001). A screen for genes required for meiosis and spore formation based on whole-genome expression. Curr Biol 11, 1001-1009.
62. Robbins JA, Cross FR (2010). Regulated degradation of the APC coactivator Cdc20. Cell Div 5, 23.
63. Salah SM, Nasmyth K (2000). Destruction of the securin Pds1p occurs at the onset of anaphase during both meiotic divisions in yeast. Chromosoma 109, 27-34.
64. Schwab M, Neutzner M, Mocker D, Seufert W (2001). Yeast Hct1 recognizes the mitotic cyclin Clb2 and other substrates of the ubiquitin ligase APC. EMBO J 20, 5165-5175.
65. Schwab M, Schulze Lutum A, Seufert W (1997). Yeast Hct1 is a regulator of Clb2 cyclin protolysis. Cell 90, 683-693.
66. Searle JS, Schollaert KL, Wilkins BJ, Sanchez Y (2004). The DNA damage checkpoint and PKA pathways converge on APC substrates and Cdc20 to regulate mitotic progression. Nat Cell Biol 6, 138-145.
67. Shirayama M, Toth A, Galova M, Nasmyth K (1999). APC(Cdc20) promotes exit from mitosis by destroying the anaphase inhibitor Pds1 and cyclin Clb5. Nature 402, 203-207.
68. Shirayama M, Zachariae W, Ciosk R, Nasmyth K (1998). The Polo-like kinase Cdc5p and the WD-repeat protein Cdc20p/fizzy are regulators and substrates of the anaphase promoting complex in Saccharomyces cerevisiae. EMBO J 17, 1336-1349.
69. Sigrist SJ, Lehner CF (1997). Drosophila fizzy-related down-regulates mitotic cyclins and is required for cell proliferation arrest and entry into endocycles. Cell 90, 671-681.
70. Sorensen CS, Lukas C, Kramer ER, Peters JM, Bartek J, Lukas J (2001). A conserved cyclin-binding domain determines functional interplay between anaphase-promoting complex-Cdh1 and cyclin A-Cdk2 during cell cycle progression. Mol Cell Biol 21, 3692-3703.
71. Spingola M, Ares M Jr (2000). A yeast intronic splicing enhancer and Nam8p are required for Mer1p-activated splicing. Mol Cell 6, 329-338.
72. Strich R, Slater MR, Esposito RE (1989). Identification of negative regulatory genes that govern the expression of early meiotic genes in yeast. Proc Natl Acad Sci USA 86, 10018-10022.
73. Thornton BR, Ng TM, Matyskiela ME, Carroll CW, Morgan DO, Toczyski DP (2006). An architectural map of the anaphase-promoting complex. Genes Dev 20, 449-460.
74. Valpuesta JM, Martin-Benito J, Gomez-Puertas P, Carrascosa JL, Willison KR (2002). Structure and function of a protein folding machine: the eukaryotic cytosolic chaperonin CCT. FEBS Lett 529, 11-16. (Pubitemid 35283904)
75. Visintin R, Prinz S, Amon A (1997). CDC20 and CDH1: a family of substrate-specific activators of APC-dependent proteolysis. Science 278, 460-463.
76. Vodermaier HC, Gieffers C, Maurer-Stroh S, Eisenhaber F, Peters JM (2003). TPR subunits of the anaphase-promoting complex mediate binding to the activator protein CDH1. Curr Biol 13, 1459-1468.
77. Yamano H, Gannon J, Mahbubani H, Hunt T (2004). Cell cycle-regulated recognition of the destruction box of cyclin B by the APC/C in Xenopus egg extracts. Mol Cell 13, 137-147.
78. Yu H (2007). Cdc20: a WD40 activator for a cell cycle degradation machine. Mol Cell 27, 3-16.
79. Zachariae W, Schwab M, Nasmyth K, Seufert W (1998). Control of cyclin ubiquitination by CDK-regulated binding of Hct1 to the anaphase promoting complex. Science 282, 1721-1724.
80. Zhang Y, Lees E (2001). Identification of an overlapping binding domain on Cdc20 for Mad2 and anaphase-promoting complex: model for spindle checkpoint regulation. Mol Cell Biol 21, 5190-5199.