A Bub2p-dependent spindle checkpoint pathway regulates the Dbf2p kinase in budding yeast

EMBO Journal

Volumn 18, Issue 9, 1999, Pages 2424-2434

  Fesquet, Didier ^a,b   Fitzpatrick, Patrick J ^a   Johnson, Anthony L ^a   Kramer, Kate M ^a   Toyn, Jeremy H ^a,c   Johnston, Leland H ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b Centre National de la Recherche Scientifique   (France)

^c DUPONT COMPANY   (United States)

Author keywords

Bub2p; Cell cycle; Dbf2p kinase; Saccharomyces cerevisiae; Spindle checkpoint

Indexed keywords

CYCLINE; DNA; PROTEIN KINASE;

ANAPHASE; ARTICLE; CELL CYCLE; CENTROMERE; ENZYME ACTIVITY; FUNGAL GENETICS; GENE AMPLIFICATION; GENE MUTATION; METAPHASE; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; YEAST CELL;

ANAPHASE; CALCIUM-BINDING PROTEINS; CARRIER PROTEINS; CELL CYCLE PROTEINS; CELL DIVISION; ENZYME ACTIVATION; EPISTASIS, GENETIC; FUNGAL PROTEINS; METAPHASE; MITOTIC SPINDLE APPARATUS; MODELS, BIOLOGICAL; NUCLEAR PROTEINS; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES; SCHIZOSACCHAROMYCES POMBE;

EID: 0033522390     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.9.2424     Document Type: Article

References (54)

1. Balasubramanian, M.K., McCollum, D., Chang, L., Wong, K.C., Naqvi, N.I., He, X., Sazer, S. and Gould, K.L. (1998) Isolation and characterization of new fission yeast cytokinesis mutants. Genetics, 149, 1265-1275.
2. Berben, G., Dumont, J., Gilliquet, V., Bolle, P.A. and Hilger, F. (1991) The YDp plasmids: a uniform set of vectors bearing versatile gene disruption cassettes for Saccharomyces cerevisiae. Yeast, 5, 475-477.
3. Cahill, D.P., Lengauer, C., Yu, J., Riggins, G.J., Willson, J.K., Markowitz, S.D., Kinzler, K.W. and Vogelstein, B. (1998) Mutations of mitotic checkpoint genes in human cancers. Nature, 392, 300-303.
4. 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.
5. Chen, R.H., Waters, J.C., Salmon, E.D. and Murray, A.W. (1996) Association of spindle assembly checkpoint component XMAD2 with unattached kinetochores. Science, 274, 242-246.
6. Chen, R.H., Shevchenko, A., Mann, M. and Murray, A.W. (1998) Spindle checkpoint protein xmad1 recruits xmad2 to unattached kinetochores. J. Cell Biol., 143, 283-295.
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. Descombes, P. and Nigg, E.A. (1998) The polo-like kinase Plx1 is required for M phase exit and destruction of mitotic regulators in Xenopus egg extracts. EMBO J., 17, 1328-1335.
9. Deshaies, R.J. (1997) Phosphorylation and proteolysis: partners in the regulation of cell division in budding yeast. Curr. Opin. Genet. Dev., 7, 7-16.
10. 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 Dev., 12, 1871-1883.
11. cdc2 kinase activity and regulation of septum formation: a link between mitosis and cytokinesis? EMBO J., 12, 2697-2704.
12. Farr, K.A. and Hoyt, M.A. (1998) Bub1p kinase activates the Saccharomyces cerevisiae spindle assembly checkpoint. Mol. Cell. Biol., 18, 2738-2747.
13. Fitzpatrick, P.J., Toyn, J.H., Millar, J.B.A. and Johnston, L.H. (1998) DNA replication is completed in Saccharomyces cerevisiae cells that lack functional Cdc14, a dual-specificity protein phosphatase. Mol. Gen. Genet., 258, 437-441.
14. Funabiki, H., Yamano, H., Kumada, K., Nagao, K., Hunt, T. and Yanagida, M. (1996) Cut2 proteolysis required for sister-chromatid separation in fission yeast. Nature, 381, 438-441.
15. Furge, K.A., Wong, K., Armstrong, J., Balasubramanian, M. and Albright, C.F. (1998) Byr4 and Cdc16 form a two-component GTPase-activating protein for the Spg1 GTPase that controls septation in fission yeast. Curr. Biol., 8, 947-954.
16. Ghiara, J.B., Richardson, H.E., Sugimoto, K., Henze, M., Lew, D.J., Wittenberg, C. and Reed, S.I. (1991) A cyclin B homolog in S.cerevisiae: chronic activation of the Cdc28 protein kinase by cyclin prevents exit from mitosis. Cell, 65, 163-174.
17. Gould, K.L. and Simanis, V. (1997) The control of septum formation in fission yeast. Genes Dev., 11, 2939-2951.
18. Hardwick, K.G. (1998) The spindle checkpoint. Trends Genet., 14, 1-4.
19. Hardwick, K.G. and Murray, A.W. (1995) Mad1p, a phosphoprotein component of the spindle assembly checkpoint in budding yeast. J. Cell Biol., 131, 709-720.
20. Hardwick, K.G., Weiss, E., Luca, F.C., Winey, M. and Murray, A.W. (1996) Activation of the budding yeast spindle assembly checkpoint without mitotic spindle disruption. Science, 273, 953-956.
21. 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.
22. Hoyt, M.A., Totis, L. and Roberts, B.T. (1991) S.cerevisiae genes required for cell cycle arrest in response to loss of microtubule function. Cell, 66, 507-517.
23. Hwang, L.H., Lau, L.F., 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 [published erratum appears in Science 1998, 280, 1331]. Science, 279, 1041-1044.
24. Jaspersen, S.L., Charles, J.F., Tinker-Kulberg, R.L. and Morgan, D.O. (1998) A late mitotic regulatory network controlling cyclin destruction in Saccharomyces cerevisiae. Mol. Biol. Cell, 9, 2803-2817.
25. Johnston, L.H., Eberly, S.L., Chapman, J.W., Araki, H. and Sugino, A. (1990) The product of the Saccharomyces cerevisiae cell cycle gene DBF2 has homology with protein kinases and is periodically expressed in the cell cycle. Mol. Cell. Biol., 10, 1358-1366.
26. 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.
27. 1 cell cycle mutant gene dbf4 encodes a protein kinase and is identified as CDC5. Mol. Cell. Biol., 13, 4445-4457.
28. Komarnitsky, S.I., Chiang, Y.C., Luca, F.C., Chen, J., Toyn, J.H., Winey, M., Johnston, L.H. and Denis, C.L. (1998) DBF2 protein kinase binds to and acts through the cell cycle-regulated MOB1 protein. Mol. Cell. Biol., 18, 2100-2107.
29. 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.
30. Kramer, K.M., Fesquet, D., Johnson, A.L. and Johnston, L.H. (1998) Budding yeast RSI1/APC2, a novel gene necessary for initiation of anaphase, encodes an APC subunit. EMBO J., 17, 498-506.
31. Li, R. and Murray, A.W. (1991) Feedback control of mitosis in budding yeast. Cell, 66, 519-531.
32. 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.
33. Lorca, T., Castro, A., Martinez, A.M., Vigneron, S., Morin, N., Sigrist, S., Lehner, C., Doree, M. and Labbe, J.C. (1998) Fizzy is required for activation of the APC/cyclosome in Xenopus egg extracts. EMBO J., 17, 3565-3575.
34. Luca, F.C. and Winey, M. (1998) MOB1, an essential yeast gene required for completion of mitosis and maintenance of ploidy. Mol. Biol. Cell, 9, 29-46.
35. Nasmyth, K. (1996) At the heart of the budding yeast cell cycle. Trends Genet., 12, 405-412.
36. Page, A.M. and Hieter, P. (1997) The anaphase promoting complex. Cancer Surv., 29, 133-150.
37. Parkes, V. and Johnston, L.H. (1992) SPO12 and SIT4 suppress mutations in DBF2, which encodes a cell cycle protein kinase that is periodically expressed. Nucleic Acids Res., 20, 5617-5623.
38. Roberts, B.T., Farr, K.A. and Hoyt, M.A. (1994) The Saccharomyces cerevisiae checkpoint gene BUB1 encodes a novel protein kinase. Mol. Cell. Biol., 14, 8282-8291.
39. Rudner, A.D. and Murray, A.W. (1996) The spindle assembly checkpoint. Curr. Opin. Cell Biol., 8, 773-780.
40. Schwab, M., Lutum, A.S. and Seufert, W. (1997) Yeast Hct1 is a regulator of Clb2 cyclin proteolysis. Cell. 90, 683-693.
41. 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 substrates of the anaphase promoting complex in Saccharomyces cerevisiae. EMBO J., 17, 1336-1349.
42. 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.
43. Tavormina, P.A. and Burke, D.J. (1998) Cell cycle arrest in cdc20 mutants of Saccharomyces cerevisiae is independent of Ndc10p and kinetochore function but requires a subset of spindle checkpoint genes. Genetics, 148, 1701-1713.
44. Taylor, S.S., Ha, E. and McKeon, F. (1998) The human homologue of Bub3 is required for kinetochore localization of Bub1 and a Mad3/ Bub1-related protein kinase. J. Cell Biol., 142, 1-11.
45. Toyn, J.H. and Johnston, L.H. (1993) Spo12 is a limiting factor that interacts with the cell cycle protein kinases Dbf2 and Dbf20, which are involved in mitotic chromatid disjunction. Genetics, 135, 963-971.
46. Toyn, J.H. and Johnston, L.H. (1994) The Dbf2 and Dbf20 protein kinases of budding yeast are activated after the metaphase to anaphase cell cycle transition. EMBO J., 13, 1103-1113.
47. Toyn, J.H., Araki, H., Sugino, A. and Johnston, L.H. (1991) The cell-cycle-regulated budding yeast gene DBF2, encoding a putative protein kinase, has a homologue that is not under cell-cycle control. Gene, 104, 63-70.
48. 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.
49. Wang, Y. and Burke, D.J. (1995) Checkpoint genes required to delay cell division in response to nocodazole respond to impaired kinetochore function in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol., 15, 6838-6844.
50. Winey, M. (1996) Keeping the centrosome cycle on track. Genome stability. Curr. Biol., 8, 962-964.
51. Yamamoto, A., Guacci, V. and Koshland, D. (1996a) Pds1p is required for faithful execution of anaphase in the yeast, Saccharomyces cerevisiae. J. Cell Biol., 133, 85-97.
52. Yamamoto, A., Guacci, V. and Koshland, D. (1996b) 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.
53. Zachariae, W., Shin, T.H., Galova, M., Obermaier, B. and Nasmyth, K. (1996) Identification of subunits of the anaphase-promoting complex of Saccharomyces cerevisiae. Science, 274, 1201-1204.
54. 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.