Insights into the cellular mechanism of the yeast ubiquitin ligase APC/C-Cdh1 from the analysis of in vivo degrons

Molecular Biology of the Cell

Volumn 26, Issue 5, 2015, Pages 843-858

  Arnold, Lea ^a   Höckner, Sebastian ^a   Seufert, Wolfgang ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANAPHASE PROMOTING COMPLEX; CELL CYCLE PROTEIN; CELL CYCLE PROTEIN 20; CELL CYCLE PROTEIN 5; PEPTIDES AND PROTEINS; PROTEIN KEN BOX; UNCLASSIFIED DRUG; UVOMORULIN; CDC20 PROTEIN, S CEREVISIAE; CDC5 PROTEIN, S CEREVISIAE; CDH1 PROTEIN, S CEREVISIAE; FIZZY RELATED PROTEIN; PROTEIN SERINE THREONINE KINASE; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CELL NUCLEUS; DEGRON; GENE STRUCTURE; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; YEAST; BINDING SITE; CHEMISTRY; ENZYMOLOGY; METABOLISM; PROTEIN DOMAIN; SACCHAROMYCES CEREVISIAE;

BINDING SITES; CDC20 PROTEINS; CDH1 PROTEINS; CELL CYCLE PROTEINS; CELL NUCLEUS; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN-SERINE-THREONINE KINASES; PROTEOLYSIS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84923826105     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E14-09-1342     Document Type: Article

References (66)

1. Almeida A (2012). Regulation of APC/C-Cdh1 and its function in neuronal survival. Mol Neurobiol 46, 547-554.
2. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (2005). Current Protocols in Molecular Biology, New York: John Wiley & Sons.
3. Barford D (2011). Structural insights into anaphase-promoting complex function and mechanism. Philos Trans R Soc Lond B Biol Sci 366, 3605-3624.
4. Barral Y, Parra M, Bidlingmaier S, Snyder M (1999). Nim1-related kinases coordinate cell cycle progression with the organization of the peripheral cytoskeleton in yeast. Genes Dev 13, 176-187.
5. Burton JL, Solomon MJ (2000). Hsl1p, a Swe1p inhibitor, is degraded via the anaphase-promoting complex. Mol Cell Biol 20, 4614-4625.
6. 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.
7. Burton JL, Xiong Y, Solomon MJ (2011). Mechanisms of pseudosubstrate inhibition of the anaphase promoting complex by Acm1. EMBO J 30, 1818-1829.
8. Bäumer M, Kunzler M, Steigemann P, Braus GH, Irniger S (2000). Yeast Ran-binding protein Yrb1p is required for efficient proteolysis of cell cycle regulatory proteins Pds1p and Sic1p. J Biol Chem 275, 38929-38937.
9. Chao WC, Kulkarni K, Zhang Z, Kong EH, Barford D (2012). Structure of the mitotic checkpoint complex. Nature 484, 208-213.
10. Charles JF, Jaspersen SL, Tinker-Kulberg RL, Hwang L, Szidon A, Morgan DO (1998). The Polo-related kinase Cdc5 activates and is destroyed by the mitotic cyclin destruction machinery in S. cerevisiae. Curr Biol 8, 497-507.
11. Clute P, Pines J (1999). Temporal and spatial control of cyclin B1 destruction in metaphase. Nat Cell Biol 1, 82-87.
12. Cohen-Fix O, Peters JM, Kirschner MW, Koshland D (1996). Anaphase initiation in Saccharomyces cerevisiae is controlled by the APC-dependent degradation of the anaphase inhibitor Pds1p. Genes Dev 10, 3081-3093.
13. Cormack BP, Bertram G, Egerton M, Gow NA, Falkow S, Brown AJ (1997). Yeast-enhanced green fluorescent protein (yEGFP): a reporter of gene expression in Candida albicans. Microbiology 143, 303-311.
14. Eguren M, Manchado E, Malumbres M (2011). Non-mitotic functions of the Anaphase-Promoting Complex. Semin Cell Dev Biol 22, 572-578.
15. Epp JA, Chant J (1997). An IQGAP-related protein controls actin-ring formation and cytokinesis in yeast. Curr Biol 7, 921-929.
16. Gadal O, Strauss D, Kessl J, Trumpower B, Tollervey D, Hurt E (2001). Nuclear export of 60s ribosomal subunits depends on Xpo1p and requires a nuclear export sequence-containing factor, Nmd3p, that associates with the large subunit protein Rpl10p. Mol Cell Biol 21, 3405-3415.
17. Geil C, Schwab M, Seufert W (2008). A nucleolus-localized activator of Cdc14 phosphatase supports rDNA segregation in yeast mitosis. Curr Biol 18, 1001-1005.
18. Gieffers C, Peters BH, Kramer ER, Dotti CG, Peters JM (1999). Expression of the CDH1-associated form of the anaphase-promoting complex in postmitotic neurons. Proc Natl Acad Sci USA 96, 11317-11322.
19. Glotzer M, Murray AW, Kirschner MW (1991). Cyclin is degraded by the ubiquitin pathway. Nature 349, 132-138.
20. Gordon DM, Roof DM (2001). Degradation of the kinesin Kip1p at anaphase onset is mediated by the anaphase-promoting complex and Cdc20p. Proc Natl Acad Sci USA 98, 12515-12520.
21. Grosskortenhaus R, Sprenger F (2002). Rca1 inhibits APC-Cdh1(Fzr) and is required to prevent cyclin degradation in G2. Dev Cell 2, 29-40.
22. He J, Chao WC, Zhang Z, Yang J, Cronin N, Barford D (2013). Insights into degron recognition by APC/C coactivators from the structure of an Acm1-Cdh1 complex. Mol Cell 50, 649-660.
23. Hildebrandt ER, Hoyt MA (2001). Cell cycle-dependent degradation of the Saccharomyces cerevisiae spindle motor Cin8p requires APC(Cdh1) and a bipartite destruction sequence. Mol Biol Cell 12, 3402-3416.
24. Hood JK, Hwang WW, Silver PA (2001). The Saccharomyces cerevisiae cyclin Clb2p is targeted to multiple subcellular locations by cis- and trans-acting determinants. J Cell Sci 114, 589-597.
25. Hu D, Liu W, Wu G, Wan Y (2011). Nuclear translocation of Skp2 facilitates its destruction in response to TGFbeta signaling. Cell Cycle 10, 285-292.
26. Huang JN, Park I, Ellingson E, Littlepage LE, Pellman D (2001). 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 154, 85-94.
27. 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.
28. 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.
29. Jörgensen PM, Brundell E, Starborg M, Hoog C (1998). A subunit of the anaphase-promoting complex is a centromere-associated protein in mammalian cells. Mol Cell Biol 18, 468-476.
30. Juang YL, Huang J, Peters JM, McLaughlin ME, Tai CY, Pellman D (1997). APC-mediated proteolysis of Ase1 and the morphogenesis of the mitotic spindle. Science 275, 1311-1314.
31. Keppler-Ross S, Douglas L, Konopka JB, Dean N (2010). Recognition of yeast by murine macrophages requires mannan but not glucan. Eukaryot Cell 9, 1776-1787.
32. Ko N, Nishihama R, Tully GH, Ostapenko D, Solomon MJ, Morgan DO, Pringle JR (2007). Identification of yeast IQGAP (Iqg1p) as an anaphase-promoting-complex substrate and its role in actomyosin-ring-independent cytokinesis. Mol Biol Cell 18, 5139-5153.
33. Kramer ER, Scheuringer N, Podtelejnikov AV, Mann M, Peters JM (2000). Mitotic regulation of the APC activator proteins CDC20 and CDH1. Mol Biol Cell 11, 1555-1569.
34. Lee KS, Park JE, Asano S, Park CJ (2005). Yeast polo-like kinases: functionally conserved multitask mitotic regulators. Oncogene 24, 217-229.
35. Melloy PG, Holloway SL (2004). Changes in the localization of the Saccharomyces cerevisiae anaphase-promoting complex upon microtubule depolymerization and spindle checkpoint activation. Genetics 167, 1079-1094.
36. Michael S, Trave G, Ramu C, Chica C, Gibson TJ (2008). Discovery of candidate KEN-box motifs using cell cycle keyword enrichment combined with native disorder prediction and motif conservation. Bioinformatics 24, 453-457.
37. Miller JJ, Summers MK, Hansen DV, Nachury MV, Lehman NL, Loktev A, Jackson PK (2006). Emi1 stably binds and inhibits the anaphase-promoting complex/cyclosome as a pseudosubstrate inhibitor. Genes Dev 20, 2410-2420.
38. Moll T, Tebb G, Surana U, Robitsch H, Nasmyth K (1991). The role of phosphorylation and the CDC28 protein kinase in cell cycle-regulated nuclear import of the S. cerevisiae transcription factor SWI5. Cell 66, 743-758.
39. Morgan DO (1999). Regulation of the APC and the exit from mitosis. Nat Cell Biol 1, E47-53.
40. Perzlmaier AF, Richter F, Seufert W (2013). Translation initiation requires cell division cycle 123 (Cdc123) to facilitate biogenesis of the eukaryotic initiation factor 2 (eIF2). J Biol Chem 288, 21537-21546.
41. Peters JM (2006). The anaphase promoting complex/cyclosome: a machine designed to destroy. Nat Rev Mol Cell Biol 7, 644-656.
42. 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.
43. Pfleger CM, Lee E, Kirschner MW (2001). Substrate recognition by the Cdc20 and Cdh1 components of the anaphase-promoting complex. Genes Dev 15, 2396-2407.
44. Primorac I, Musacchio A (2013). Panta rhei: the APC/C at steady state. J Cell Biol 201, 177-189.
45. 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.
46. Robbins JA, Cross FR (2010). Regulated degradation of the APC coactivator Cdc20. Cell Div 5, 23.
47. Rudner AD, Murray AW (2000). Phosphorylation by Cdc28 activates the Cdc20-dependent activity of the anaphase-promoting complex. J Cell Biol 149, 1377-1390.
48. Schwab M, Lutum AS, Seufert W (1997). Yeast Hct1 is a regulator of Clb2 cyclin proteolysis. Cell 90, 683-693.
49. 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.
50. Shaner NC, Campbell RE, Steinbach PA, Giepmans BN, Palmer AE, Tsien RY (2004). Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22, 1567-1572.
51. Shannon KB (2012). IQGAP family members in yeast, Dictyostelium, and mammalian cells. Int J Cell Biol 2012, 894817.
52. Sheff MA, Thorn KS (2004). Optimized cassettes for fluorescent protein tagging in Saccharomyces cerevisiae. Yeast 21, 661-670.
53. 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.
54. 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.
55. Sikorski RS, Hieter P (1989). A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27.
56. Tian W, Li B, Warrington R, Tomchick DR, Yu H, Luo X (2012). Structural analysis of human Cdc20 supports multisite degron recognition by APC/C. Proc Natl Acad Sci USA 109, 18419-18424.
57. Topper LM, Campbell MS, Tugendreich S, Daum JR, Burke DJ, Hieter P, Gorbsky GJ (2002). The dephosphorylated form of the anaphase-promoting complex protein Cdc27/Apc3 concentrates on kinetochores and chromosome arms in mitosis. Cell Cycle 1, 282-292.
58. Visintin R, Craig K, Hwang ES, Prinz S, Tyers M, Amon A (1998). The phosphatase Cdc14 triggers mitotic exit by reversal of Cdk-dependent phosphorylation. Mol Cell 2, 709-718.
59. Visintin R, Prinz S, Amon A (1997). CDC20 and CDH1: a family of substrate-specific activators of APC-dependent proteolysis. Science 278, 460-463.
60. Waizenegger IC, Hauf S, Meinke A, Peters JM (2000). Two distinct pathways remove mammalian cohesin from chromosome arms in prophase and from centromeres in anaphase. Cell 103, 399-410.
61. Wäsch R, Cross FR (2002). APC-dependent proteolysis of the mitotic cyclin Clb2 is essential for mitotic exit. Nature 418, 556-562.
62. Winey M, Bloom K (2012). Mitotic spindle form and function. Genetics 190, 1197-1224.
63. Yoshida S, Asakawa K, Toh-e A (2002). Mitotic exit network controls the localization of Cdc14 to the spindle pole body in Saccharomyces cerevisiae. Curr Biol 12, 944-950.
64. 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.
65. Zachariae W, Shin TH, Galova M, Obermaier B, Nasmyth K (1996). Identification of subunits of the anaphase-promoting complex of Saccharomyces cerevisiae. Science 274, 1201-1204.
66. Zhou Y, Ching YP, Chun AC, Jin DY (2003). Nuclear localization of the cell cycle regulator CDH1 and its regulation by phosphorylation. J Biol Chem 278, 12530-12536.