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 Journal

Volumn 17, Issue 19, 1998, Pages 5670-5678

  Yamano, Hiroyuki ^a   Tsurumi, Chizuko ^a   Gannon, Julian ^a   Hunt, Tim ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

APC cyclosome; Cell cycle; Cyclin; Destruction box; Proteolysis

Indexed keywords

CYCLIN B; LYSINE; RECEPTOR PROTEIN;

ANAPHASE; ARTICLE; ASSAY; CELL CYCLE; CONTROLLED STUDY; METAPHASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; SCHIZOSACCHAROMYCES POMBE; SITE DIRECTED MUTAGENESIS;

AMINO ACID SEQUENCE; ANAPHASE; CONSERVED SEQUENCE; CYCLIN B; LIGASES; LYSINE; SCHIZOSACCHAROMYCES; SEQUENCE DELETION; SUBSTRATE SPECIFICITY; UBIQUITIN-PROTEIN LIGASE COMPLEXES; UBIQUITIN-PROTEIN LIGASES; UBIQUITINS;

SCHIZOSACCHAROMYCES POMBE;

EID: 0032189040     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.19.5670     Document Type: Article

References (80)

1. 1 cyclins in the next cycle. Cell, 77, 1037-1050.
2. rum1 CDK inhibitor. EMBO J., 17, 482-497.
3. Bogyo, M., McMaster, J.S., Gaczynska, M., Tortorella, D., Goldberg, A.L. and Ploegh, H. (1997) Covalent modification of the active site threonine of proteasomal beta subunits and the Esherichia coli homolog HsIV by a new class of inhibitors. Proc. Natl Acad. Sci. USA, 94, 6629-6634.
4. Brandeis, M. and Hunt, T. (1996) The proteolysis of mitotic cyclins in mammalian cells persists from the end of mitosis until the onset of S phase. EMBO J., 15, 5280-5289.
5. Charles, J.F., Jaspersen, S.L., Tinker-Kulberg, R.L., Hwang, L., Szidon, A. and Morgan, D.O. (1998) The polo-related kinase cdc5 activates and is destroyed by the mitotic cyclin destruction machinery in S. cerevisiae. Curr. Biol., 8, 497-507.
6. Ciechanover, A. (1994) The ubiquitin-proteasome proteolytic pathway. Cell, 79, 13-21.
7. Cohen-Fix, O., Peters, J.M., Kirschner, M.W. and 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.
8. Craig, D., Howell, M.T. Gibbs, C.L., Hunt, T. and Jackson, R.J. (1992) Plasmid cDNA-directed protein synthesis in a coupled eukaryotic in vitro transcription-translation system. Nucleic Acids Res., 20, 4987-4995.
9. 1 cyclin Cln2p by a Cdc34p-dependent pathway. EMBO J., 14, 303-312.
10. Drury, L.S., Perkins, G. and Diffley, J.F. (1997) The Cdc4/34/53 pathway targets Cdc6p for proteolysis in budding yeast. EMBO J., 16, 5966-5976.
11. Elledge, S.J. and Harper, J.W. (1998) The role of protein stability in the cell cycle and cancer. Biochim. Biophys. Acta, 1377, M61-M70.
12. Fang, G., Yu, H. and Kirschner, M.W. (1998) The checkpoint protein MAD2 and the mitotic regulator CDC20 form a ternary complex with the anaphase-promoting complex to control anaphase initiation. Genes Cells, 12, 1871-1883.
13. Félix, M.-A., Labbé, J.-C., Dorée, M., Hunt, T. and Karsenti, E. (1990) Triggering of cyclin degradation in interphase extracts of amphibian eggs by cdc2 kinase. Nature, 346, 379-382.
14. Funabiki, H., Yamano, H., Kumada, K., Nagao, K., Hunt, T. and Yanagida, M. (1996) Cut2 proteolysis required for sister-chromalid seperation in fission yeast. Nature, 381, 438-141.
15. 2/metaphase. Nature, 366, 358-361.
16. Glas, R., Bogyo, M., McMaster, J.S., Gaczynska, M. and Ploegh, H.L. (1998) A proteolytic system that compensates for loss of proteasome function. Nature, 392, 618-622.
17. Glotzer, M., Murray, A.W. and Kirschner, M.W. (1991) Cyclin is degraded by the ubiquitin pathway. Nature, 349, 132-138.
18. Gordon, C., McGurk, G., Dillon, P., Rosen, C. and Hastie, N.D. (1993) Defective mitosis due to a mutation in the gene for a fission yeast 26S protease subunit. Nature, 366, 355-357.
19. Grieco, D., Porcellini, A., Avvedimento, E.V. and Gottesman, M.E. (1996) Requirement for cAMP-PKA pathway activation by M phase-promoting factor in the transition from mitosis to interphase. Science, 271, 1718-1723.
20. Harlow, E. and Lane, D. (1988). Antibodies: a Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
21. Hatakeyama, S., Jensen, J.P. and Weissman, A.M. (1997) Subcellular localization and ubiquitin-conjugating enzyme (E2) interactions of mammalian HECT family ubiquitin protein ligases. J. Biol. Chem., 272, 15085-15092.
22. Henchoz, S., Chi, Y., Catarin, B., Herskowitz, I., Deshaies, R.J. and Peter, M. (1997) Phosphorylation- and ubiquitin-dependent degradation of the cyclin-dependent kinase inhibitor Far1p in budding yeast. Genes Dev., 11, 3046-3060.
23. Hershko, A. (1997) Roles of ubiquitin-mediated proteolysis in cell cycle control. Curr. Opin. Cell Biol., 9, 788-799.
24. Hershko, A., Heller, H., Elias, S. and Ciechanover, A. (1983) Components of ubiquitin-protein ligase system. Resolution, affinity purification and role in protein breakdown. J. Biol. Chem., 258, 8206-8214.
25. Hirano, T., Funahashi, S., Uemura, T. and Yanagida, M. (1986) Isolation and characterization of Schizosaccharomyces pombe cut mutants that block nuclear division but not cytokinesis. EMBO J., 5, 2973-2979.
26. Hirano, T., Hiraoka, Y. and Yanagida, M. (1988) A temperature-sensitive mutation of the Schizosaccharomyces pombe gene nuc2+ that encodes a nuclear scaffold-like protein blocks spindle elongation in mitotic anaphase. J. Cell Biol., 106, 1171-1183.
27. Hochstrasser, M. (1996) Ubiquitin-dependent protein degradation. Annu. Rev. Genet., 30, 405-439.
28. Hoffmann, A. and Roeder, R.G. (1991) Purification of his-tagged proteins in non-denaturing conditions suggests a convenient method for protein interaction studies. Nucleic Acids Res., 19, 6337-6338.
29. Holloway, S.L., Glotzer, M. King, R.W. and Murray, A.W. (1993) Anaphase is initiated by proteolysis rather than by the inactivation of maturation-promoting factor. Cell, 73, 1393-1402.
30. Horton, R.M. and Pease, L.R. (1991) Recombination and mutagenesis of DNA sequences using PCR. In McPherson, M.J. (ed.). Directed Mutagenesis. IRL Press at OUP, Oxford, UK, pp. 217-247.
31. Huibregtse, J.M., Scheffner, M., Beaudenon, S. and Howley, P.M. (1995) A family of proteins structurally and functionally related to the E6-AP ubiquitin-protein ligase. Proc. Natl Acad. Sci. USA, 92, 2563-2567.
32. Hwang, L.H., Lau, L.K. Smith, D.L., Mistrot, C.A., Hardwick, K.G., Hwang, E.S., Amon, A. and Murray, A.W. (1998) Budding yeast Cdc20: a target of the spindle checkpoint. Science, 279, 1041-1044.
33. Irniger, S., Piatti, S., Michaelis, C. and Nasmyth, K. (1995) Genes involved in sister chromatid separation are needed for B-type cyclin proteolysis in budding yeast. Cell, 81, 269-278.
34. cdc18 by CDK phosphorylation. Genes Dev., 11, 2767-2779.
35. Juang, Y.L., Huang, J., Peters, J.M., McLaughlin, M.E., Tai, C.Y. and Pellman, D. (1997) APC-mediated proteolysis of Ase1 and the morphogenesis of the mitotic spindle. Science, 275, 1311-1314.
36. Kim, S.H., Lin, D.P. Matsumoto, S., Kitazono, A. and Matsumoto, T. (1998) Fission yeast Slp1: an effector of the Mad2-dependent spindle checkpoint. Science, 279, 1045-1047.
37. King, R.W., Peters, J.M., Tugendreich, S., Rolfe, M., Hieter, P. and Kirschner, M.W. (1995) A 20S complex containing CDC27 and CDC16 catalyzes the mitosis-specific conjugation of ubiquitin to cyclin B. Cell, 81, 279-288.
38. King, R.W., Deshaies, R.J., Peters, J.M. and Kirschner, M.W. (1996a) How proteolysis drives the cell cycle. Science, 274, 1652-1659.
39. King, R.W., Glotzer, M. and Kirschner, M.W. (1996b) Mutagenic analysis of the destruction signal of mitotic cyclins and structural characterization of ubiquitinated intermediates. Mol. Biol. Cell, 7, 1343-1357.
40. 1-phase. Mol. Biol. Cell. 9, 1065-1080.
41. Klotzbücher, A., Stewart, E., Harrison, D. and Hunt, T. (1996) The 'destruction box' of cyclin A allows B-type cyclins to be ubiquitinated, but not efficiently destroyed. EMBO J., 15, 3053-3064.
42. Knoblich, J.A., Sauer, K., Jones,L., Richardson, H., Saint, R. and Lehner, C.F. (1994) Cyclin E controls S phase progression and its down-regulation during Drosophila embryogenesis is required for the arrest of cell proliferation. Cell, 77, 107-120.
43. cdc2 with half-times of 4 and 15 h, respectively, regardless of the phase of the cell cycle. J. Biol. Chem., 269, 29153-29160.
44. Kominami, K. and Toda, T. (1997) Fission yeast WD-repeat protein pop1 regulates genome ploidy through ubiquitin-proteasome-mediated degration of the CDK inhibitor Rum1 and the S-phase initiator Cdc18. Genes Dev., 11, 1548-1560.
45. Kotani, S., Tugendreich, S., Fujii, M., Jorgensen, P.-M., Watanabe, N., Hoog, C., Hieter, P. and Todokoro, K. (1998) PKA and MPF-activated polo-like kinase regulate anaphase-promoting complex activity and mitosis progression. Mol. Cell., 1, 371-380.
46. Lahav-Baratz, S., Sudakin, V., Ruderman, J.V. and Hershko, A. (1995) Reversible phoshorylation controls the activity of cyclosome-associated cyclin-ubiquitin ligase. Proc. Natl Acad. Sci. USA, 92, 9303-9307.
47. 1 cyclin Cln2 induced by CDK-dependant phosphorylation. Science, 271, 1597-1601.
48. Lim, H.H., Goh, P.Y. and Surana, U. (1998) Cdc20 is essential for the cyclosome-mediated proteolysis of both Pds1 and Clb2 during M phase in budding yeast. Curr. Biol., 8, 231-234.
49. Lorca, T., Devault, A., Colas, P., Vanloon, A., Fesquet, D., Lazaro, J.B. and Dorée, M. (1992) Cyclin A cys41 does not undergo cell cycle-dependent degradation in Xenopus extracts. FEBS Lett., 306, 90-93.
50. cdc2. Mol. Cell. Biol., 17, 742-750.
51. Moreno, S., Klar, A. and Nurse, P. (1991) Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol., 194, 795-823.
52. Murray, A.W., Solomon, M.J. and Kirschner, M.W. (1989) The role of cyclin synthesis and degradation in the control of maturation promoting factor activity. Nature, 339, 280-286.
53. Okazaki, K., Okazaki, N., Kume, K., Jinno, S., Tanaka, K. and Okayama, H. (1990) High-frequency transformation method and library transducing vectors for cloning mammalian cDNAs by trans-complementation of Schizosaccharomyces pombe. Nucleic Acids Res., 18, 6485-6489.
54. Patton, E.E., Willems, A.R., Sa, D., Kuras, L., Thomas, D., Craig, K.L. and Tyers, M. (1998a) Cdc53 is a scaffold protein for multiple Cdc4/Skp1/ F-box protein complexes that regulate cell division and methionine biosynthesis in yeast. Genes Dev., 12, 692-705.
55. Patton, E.E., Willems, A.R. and Tyers, M. (1998b) Combinatorial control in ubiquitin-dependent proteolysis: don't Skp the F-box hypothesis. Trends Genet., 14, 235-243.
56. Peters, J.M., King, R.W., Hoog, C. and Kirschner, M.W. (1996) Indentification of BIME as a subunit of the anaphase-promoting complex. Science, 274, 1199-1201.
57. cdc2. EMBO J., 12, 3123-3132.
58. Rimmington, G., Dalby, B. and Glover, D.M. (1994) Expression of N-terminally truncated cyclin B in the Drosophila larval brain leads to mitotic delay at late anaphase. J. Cell. Sci., 107, 2729-2738.
59. Samejima, I. and Yanagida, M. (1994) Bypassing anaphase by fission yeast cut9 mutation: requirement of cut9+ to initiate anaphase. J. Cell Biol., 127, 1655-1670.
60. Schwab, M., Lutum, A.S. and Seufert, W. (1997) Yeast Hct1 is a regulator of Clb2 cyclin proteolysis. Cell, 90, 683-693.
61. Shirayama, M., Zachariae, W., Ciosk, R. and Nasmyth, K. (1998) The Polo-like kinase Cdc5p and the WD-repeat protein Cdc20p/fizzy are regulators and substrated of the anaphase promoting complex in Saccharomyces cerevisiae. EMBO J., 17, 1336-1349.
62. Sigrist, S.J. and Lehner, C.F. (1997) Drosophila fizzy-related down-regulates mitotic cyclins and is required for cell proliferation arrest and entry into endocycles. Cell, 90, 671-681.
63. Sigrist, S., Jacobs, H., Stratmann, R. and Lehner, C.F. (1995) Exit from mitosis is regulated by Drosophila fizzy and the sequential destruction of cyclins A, B and B3. EMBO J., 14, 4827-4838.
64. Skowyra, D., Craig, K.L., Tyers, M., Elledge, S.J. and Harper, J.W. (1997) F-box proteins are receptors that recruit phosphorylated substrated to the SCF ubiquitin-ligase complex. Cell, 91, 209-219.
65. cdc2. EMBO J., 13, 584-594.
66. Stone, E.M., Yamano, H., Kinoshita, N. and Yanagida, M. (1993) Mitotic regulation of protein phosphatases by the fission yeast sds22 protein. Curr. Biol., 3, 13-26.
67. Sudakin, V., Ganoth, D., Dahan, A., Heller, H., Hershko, J., Luca, F.C., Ruderman, J.V. and Hershko, A. (1995) The cyclosome, a large complex containing cyclin-selective ubiquitin ligase activity targets cyclins for destruction at the end of mitosis. Mol. Biol. Cell, 6, 185-197.
68. Surana, U., Amon, A., Dowzer, C., McGrew, J., Byers, B. and Nasmyth, K. (1993) Destruction of the CDC28/CLB mitotic kinase is not required for the metaphase to anaphase transition in budding yeast. EMBO J., 12, 1969-1978.
69. Tugendreich, S., Tomkiel, J., Earnshaw, W. and Hieter, P. (1995) CDC27Hs colocalizes with CDC16Hs to the centrosome and mitotic spindle and is essential for the metaphase to anaphase transition. Cell, 81, 61-268.
70. Varshavsky, A. (1997) The ubiquitin system. Trends Biochem. Sci., 22, 383-387.
71. Verma, R., Feldman, R.M. and Deshaies, R.J. (1997) SIC1 is ubiquitinated in vitro by a pathway that requires CDC4, CDC34 and cyclin/CDK activities. Mol. Biol. Cell, 8, 1427-1437.
72. Visintin, R., Prinz, S. and Amon, A. (1997) CD20 and CDK1: a family of substrate-specific activators of APC-dependent proteolysis. Science, 278, 460-463.
73. 1 cyclins for degradation by the ubiquitin proteolytic pathway. Cell, 86, 453-463.
74. Yamaguchi, S., Murakami, H. and Okayama, H. (1997) A WD repeat protein controls the cell cycle and differentiation by negatively regulating Cdc2/B-type cyclin complexes. Mol. Biol. Cell, 8, 2475-2486.
75. Yamamoto, A., Guacci, V. and Koshland, D. (1996) Pds1p, an inhibitor of anaphase in budding yeast, plays a critical role in the APC and checkpoint pathway(s). J. Cell Biol., 133, 99-110.
76. Yamano, H., Gannon, J. and Hunt, T. (1996) The role of proteolysis in cell cycle progression in Schizosaccharomyces pombe. EMBO J., 15, 5268-5279.
77. Yamashita, Y.M., Nakaseko, Y., Samejima, I., Kumada, K., Yamada, H., Michaelson, D. and Yanagida, M. (1996) 20S cyclosome complex formation and proteolytic activity inhibited by the cAMP/PKA pathway. Nature, 384, 276-279.
78. Yu, H., Peters, J.M., King, R.W., Page, A.M., Hieter, P. and Kirschner, M.W. (1998) Identification of a cullin homology region in a subunit of the anaphase-promoting complex. Science, 279, 1219-1222.
79. Zachariae, W., Shin, T.H., Galova, M., Obermaier, B. and Nasmyth, K. (1996) Idenfication of subunits of the anaphase-promoting complex of Saccharomyces cerevisiae. Science, 274, 1201-1204.
80. Zachariae, W., Shevchenko, A., Andrews, P.D., Ciosk, R., Galova, M., Stark, M.J., Mann, M. and Nasmyth, K. (1998) Mass spectrometric analysis of the anaphase-promoting complex from yeast: identification of a subunit related to cullins. Science, 279, 1216-1219.