Cdk1 phosphorylation sites on Cdc27 are required for correct chromosomal localisation and APC/C function in syncytial Drosophila embryos

Journal of Cell Science

Volumn 120, Issue 12, 2007, Pages 1990-1997

  Huang, Jun Yong ^a   Morley, Gary ^a   Li, Deyu ^a   Whitaker, Michael ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

APC C; Cdc27; Cdk1; Drosophila; Metaphase; Mitosis; Phosphorylation

Indexed keywords

ALANINE; ANAPHASE PROMOTING COMPLEX; CELL CYCLE PROTEIN; CELL CYCLE PROTEIN 27; CYCLIN A; CYCLIN B; CYCLIN DEPENDENT KINASE 1; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; MUTANT PROTEIN; PROLINE; SECURIN; UNCLASSIFIED DRUG;

ANAPHASE; ANIMAL EMBRYO; ANIMAL TISSUE; ARTICLE; CELL CYCLE REGULATION; CHROMOSOMAL LOCALIZATION; CHROMOSOME; CONSENSUS SEQUENCE; CONTROLLED STUDY; DROSOPHILA; EMBRYO; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE CONSTRUCT; GENE MUTATION; IN VIVO STUDY; LARVA; METAPHASE; MITOSIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CDC2 PROTEIN KINASE; CELL CYCLE PROTEINS; CHROMOSOMES; COLCHICINE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GIANT CELLS; MITOSIS; MITOTIC SPINDLE APPARATUS; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; RECOMBINANT FUSION PROTEINS; TUBULIN MODULATORS; UBIQUITIN-PROTEIN LIGASE COMPLEXES;

EID: 34347356586     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.006833     Document Type: Article

References (48)

1. Acquaviva, C., Herzog, E, Kraft, C. and Pines, J. (2004). The anaphase promoting complex/cyclosome is recruited to centromeres by the spindle assembly checkpoint. Nat. Cell Biol. 6, 892-898.
2. Balicki, D., Putnam, C. D., Scaria, F. V. and Bender, E. (2002). Structure and function correlation in histone H2A peptide-mediated gene transfer. Proc. Natl. Acad. Sci. USA 99, 7467-7471.
3. Baumer, M., Braus, G. H. and Irniger, S. (2000). Two different modes of cyclin c1b2 proteolysis during mitosis in Saccharomyces cerevisiae. FEBS Lett. 468, 142-148.
4. Campbell, S. D., Sprenger, F., Edgar, B. A. and O'Farrell, P. H. (1995). Drosophila Wee1 kinase rescues fission yeast from mitotic catastrophe and phosphorylates Drosophila Cdc2 in vitro. Mol. Biol. Cell 6, 1333-1347.
5. Charles, I K, 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. Clute, P. and Pines, J. (1999). Temporal and spatial control of cyclin B1 destruction in metaphase. Nat. Cell Biol. 1, 82-87.
7. Deak, F., Donaldson, M. and Glover, A M. (2003). Mutal ons in makos, a Drosophila gene encoding the Cdc27 subunit of the anaphase promoting complex, enhance centrosomal defects in polo and are suppressed by mutations in twins/aar, which encodes a regulatory subunit of PP2A. J. Cell Sci. 116, 4147-4158.
8. Felix, M. A., Labbe, J. C., Doree, M., Hunt, T. and Karsenti, E. (1990). Triggering of cyclin degradation in interphase extracts of amphibian eggs by cdc2 kinase. Nature 346, 379-382.
9. Glover, D. M., Hagan, I. M. and Tavares, A. A. (1998). Polo-like kinases: a team that plays throughout mitosis. Genes Dev. 12, 3777-3787.
10. Golan, A., Yudkovsky, Y. and Hershko, A. (2002). The cyclin-ubiquitin ligase activity of cyclosome/APC is jointly activated by protein kinases Cdkl-cyclin B and Plk. J. Biol. Chem. 277, 15552-15557.
11. Hardwick, K. G., Weiss, E., Luca, E C., Winey, M. and Murray, A. W. (1996). Activation of the budding yeast spindle assembly checkpoint without mitotic spindle disruption. Science 273, 953-956.
12. Huang, J. and Raff, J. W. (1999). The disappearance of cyclin B at the end of mitosis is regulated spatially in Drosophila cells. EMBO J. 18, 2184-2195.
13. Huang, J. Y. and Raff, J. W. (2002). The dynamic localisation of the Drosophila APC/C: evidence for the existence of multiple complexes that perform distinct functions and are differentially localised. J. Cell Sci. 115, 2847-2856.
14. 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.
15. Jorgensen P. M., Brundell, E., Starborg, M. and Hong, C. (1998). A subunit of the anaphase-promoting complex is a centromere-associated protein in mammalian cells. Mol. Cell. Biol. 18, 468-476.
16. King, R. W., Peters, J. M., Tugendreich, S., Roffe, 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.
17. Kramer, E. R., Gieffers, C., Holzl, G., Hengstschlager, M. and Peters, J. M. (1998). Activation of the human anaphase-promoting complex by proteins of the CDC20/Fizzy family. Curr. Biol. 8, 1207-1210.
18. Lamb, J. R., Michaud, W. A., Sikorski, R. S. and Hieter, P. A. (1994). Cdc16p, Cdc23p and Cdc27p form a complex essential for mitosis. EMBO J. 13, 4321-4328.
19. Lew, J., Beaudette, K., Litwin, C. M. and Wang, J. H. (1992). Purification and characterization of a novel proline-directed protein kinase from bovine brain. J. Biol. Chem. 267, 13383-13390.
20. Lim, H. H., Goh, P. Y. and Surana, U. (1998). Cdc20 is essential for the cyclosome-mediated proteolysis of both PdsI and Clb2 during M phase in budding yeast. Curr. Biol. 8, 231-234.
21. May, K. M., Reynolds, N., Cullen, C. K, Yanagida, M. and Ohkura, H. (2002). Polo boxes and Cut23 (Apc8) mediate an interaction between polo kinase and the anaphase-promoting complex for fission yeast mitosis. J. Cell Biol. 156, 23-28.
22. Michaelis, C., Ciosk, R. and Nasmyth, K. (1997). Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell 91, 35-45.
23. Mirabito, P. M. and Morris, N. R. (1993). BIMA, a TPR-containing protein required for mitosis, localizes to the spindle pole body in Aspergillus nidulans. J. Cell Biol. 120, 959-968.
24. Niggg E. A. (1991). The substrates of the cdc2 kinase. Semin. Cell Biol. 2, 261-270.
25. Pahlavan, G., Polanski, Z., Kalab, P., Golsteyn, R., Nigg, E. A. and Maro, B. (2000). Characterization of polo-like kinase I during meiotic maturation of the mouse oocyte. Dev. Biol. 220, 392-400.
26. Parry, H., McDougall, A. and Whitaker, M. (2005). Microdomains bounded by endoplasmic reticulum segregate cell cycle calcium transients in syncytial Drosophila embryos. J. Cell Biol. 171, 47-59.
27. Patra, D. and Dunphy, W. G. (1998). Xe-p9, a Xenopus Sucl/Cks protein, is essential for the Cdc2-dependent pbosphorylation of the anaphase- promoting complex at mitosis. Genes Dev. 12, 2549-2559.
28. Peters, J. M., King, R. W., Hong, C. and Kirschner, M. W. (1996). Identification of BIME as a subunit of the anaphase-promoting complex. Science 274, 1199-1201.
29. Raff, J. W., Jeffers, K. and Huang, J. Y. (2002). The roles of Fzy/Cdc20 and Fzr/Cdh1 in regulating the destruction of cyclin B in space and time. J. Cell Biol. 157, 1139-1149.
30. Robertson, H. M., Preston, C. R., Phillis, R. W., Johnson-Schlitz, D. M., Benz, W. K. and Engels, W. R. (1988). A stable genomic source of P element transposase in Drosophila melanogaster. Genetics 118, 461-470.
31. Rudner, A. D. and Murray, A. W. (2000). Phosphorylation by Cdc28 activates the Cdc20-dependent activity of the anaphase-promoLing complex. J. Cell Biol. 149, 1377-1390.
32. Rudner, A. D., Hardwick, K. G. and Murray, A. W. (2000). Cdc28 activates exit from mitosis in budding yeast. J. Cell Biol. 149, 1361-1376.
33. Schuldt, A. J., Adams, J. H., Davidson, C. M., Micklem, D. R., Haseloff, J., St Johnston, D. and Brand, A. H. (1998). Miranda mediates asymmetric protein and RNA localization in the developing nervous system. Genes Dev. 12, 1847-1857.
34. Shah, O. J., Ghosh, S. and Hunter, T. (2003). Mitotic regulation of ribosomal S6 kinase 1 involves Ser/Thr, Pro phosphorylation ofconsensus and non-consensus sites by Cdc2. J. Biol. Chem. 278, 16433-16442.
35. Shetty, K. T., Link, W. T. and Pant, H. C. (1993). cdc2-like kinase from rat spinal cord specifically phosphorylates KSPXK motifs in neurofilament proteins: isolation and characterization. Proc. Natl. Acad Sci. USA 90, 6844-6848.
36. Shirayama, M., Toth, A., Galova, M. and Nasmyth, K. (1999). APC(Cdc2O) promotes exit from mitosis by destroying the anaphase inhibitor Pds1 and cyclin Clb5. Nature 402, 203-207.
37. Shteinberg, M., Protopopov, Y., Listovsky, T., Brandeis, M. and Hershko, A. (1999). Phosphorylation of the cyclosome is required for its stimulation by Fizzy/cdc20. Biochem. Biophys. Res. Commun. 260, 193-198.
38. Sikorski, R. S., Boguski, M. S., Goebl, M. and Hieter, P. (1990). A repeating amino acid motif in CDC23 defines a family of proteins and a new relationship among genes required for mitosis and RNA synthesis. Cell 60, 307-317.
39. Songyang, Z., Blechner, S., Hoagland, N., Hoekstra, M. E, Piwnica-Worms, H. and Cantley, L. C. (1994). Use of an oriented peptide library to determine the optimal substrates of protein kinases. Curr. Biol. 4, 973-982.
40. Sudakin, V., Ganoth, D., Dahan, A., Heller, H., Hershko, J., Luca, E 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.
41. Sudakin, V., Chan, G. K. and Yen, T. J. (2001). Checkpoint inhibition of the APC/C in HeLa cells is mediated by a complex of BUBR1, BUB3, CDC20, and MAD2. J. Cell Biol. 154, 925-936.
42. Topper, L. M., Campbell, M. S., Tugendreich, S., Daum, J. R., Burke, D. J., Hieter, P. and Gorbsky, G. J. (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.
43. Tugendreich, S., Tomkiel, J., Earnshaw, W. and Hieter, F. (1995). CDC27Hs colocalizes with CDC16Hs to the centrosome and mitotic spindle and is essential for the metaphase to anaphase transition. Cell 81, 261-268.
44. van Vugt, M. A., Smits, V. A., Klompmaker, R. and Medema, R. H. (2001). Inhibition of Polo-like kinase- I by DNA damage occurs in an ATM- or ATR-dependent fashion. J. Biol. Chem. 276, 41656-41660.
45. Visintin, R., Prinz, S. and Amon, A. (1997). CDC20 and CDH1: a family of substrate-specific activators of APC-dependent proteolysis. Science 278, 460-463.
46. Weinert, T. (1997). A DNA damage checkpoint meets the cell cycle engine. Science 277, 1450-1451.
47. Yamada, H., Kumada, K. and Yanagida, M. (1997). Distinct subunit functions and cell cycle regulated phosphorylation of 20S APC/cyclosome required for anaphase in fission yeast. J Cell Sci. 110, 1793-1804.
48. Yeong, R M., Lim, H. H., Padmashree, C. G. and Surana, U. (2000). Exit from mitosis in budding yeast: biphasic inactivation of the Cdc28-C1b2 mitotic kinase and the role of Cdc20. Mol. Cell 5, 501-511.