Two S-phase checkpoint systems, one involving the function of both BIME and Tyr15 phosphorylation of p34(cdc2), inhibit NIMA and prevent premature mitosis

EMBO Journal

Volumn 15, Issue 14, 1996, Pages 3599-3610

  Ye, Xiang S ^a   Fincher, Russell R ^a   Tang, Alice ^a   O'Donnell, Kerry ^b   Osmani, Stephen A ^a  

^a WEIS CENTER FOR RESEARCH   (United States)

^b NATIONAL CENTER FOR AGRICULTURAL UTILIZATION RESEARCH   (United States)

Author keywords

Aspergillus; BIME; NIMA; S phase checkpoints; Tyrl5 phosphorylation of p34(cdc2)

Indexed keywords

CYCLIN DEPENDENT KINASE; DNA; HYDROXYUREA;

ARTICLE; ASPERGILLUS; CELL CYCLE S PHASE; CONTROLLED STUDY; DNA REPLICATION; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; MITOSIS; NONHUMAN; PRIORITY JOURNAL;

ASPERGILLUS;

EID: 0030008450     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1996.tb00729.x     Document Type: Article

References (65)

1. Al-Khodairy, F. and Carr, A.M. (1992) DNA repair mutants defining G2 checkpoint pathways in Schizosaccharomyces pombe. EMBO J., 11, 1343-1350.
2. Allen, J., Zhou, Z., Siede, W., Friedberg, E. and Elledge, S. (1994) The SAD1/RAD53 protein kinase controls multiple checkpoints and DNA damage-induced transcription in yeast. Genes Dev., 8, 2416-2428.
3. cdc28 tyrosine phosphorylation is not required for entry into mitosis in S.cerevisiae. Nature, 355, 368-371.
4. Bergen, L.G. and Morris, N.R. (1983) Kinetics of the nuclear division cycle of Aspergillus nidulans. J. Bacteriol., 156, 155-160.
5. Bergen, L.G., Upshall, A. and Morris, N.R. (1984) S-phase, G2, and nuclear division mutants of Aspergillus nidulans. J. Bacteriol., 159, 114-119.
6. Booher, R.N., Alfa, C.E., Hyams, J.S. and Beach, D.H. (1989) The fission yeast cdc2/cdc13/suc1 protein kinase: regulation of catalytic activity and nuclear localization. Cell, 58, 485-497.
7. cdc2 mitotic kinase. Cell, 83, 1001-1009.
8. Doonan, J.H., MacKintosh, C., Osmani, S., Cohen, P., Bai, G., Lee, E.Y.C. and Morris, N.R. (1991) A cDNA encoding rabbit muscle protein phosphatase 1 a complements the Aspergillus cell cycle mutation. bimG11. J. Biol. Chem., 266, 18889-18894.
9. Draetta, G. (1990) Cell cycle control in eukaryotes: molecular mechanisms of cdc2 activation. Trends Biochem. Sci., 15, 378-383.
10. Dunphy, W.G. (1994) The decision to enter mitosis. Trends Cell Biol., 4, 202-207.
11. Edgar, B. and O'Farrell, P. (1990) The three postblastoderm cell cycles of Drosophila embryogenesis are regulated in G2 by string. Cell, 62, 469-480.
12. Enoch, T. and Nurse, P. (1990) Mutation of fission yeast cell cycle control genes abolishes dependence of mitosis on DNA replication. Cell, 60, 665-673.
13. Enoch, T., Carr, A.M. and Nurse, P. (1992) Fission yeast genes involved in coupling mitosis to completion of DNA replication. Genes Dev., 6, 2035-2046.
14. Evans, T.E., Rosenthal, J., Youngbloom, K. and Hunt, T. (1983) Cyclin: a protein specified by maternal mRNA in sea urchin eggs that is destroyed at each cleavage division. Cell, 33, 389-396.
15. Fesquet, D., Labbe, J.C., Derancourt, J., Capony, S.G., Girard, F., Lorca, T., Shuttleworth, J., Doree, M. and Cavadore, J.C. (1993) The MO15 gene encodes the catalytic subunit of a protein kinase that activates cdc2 and other cyclin-dependent kinases (CDK) through phosphorylation of Thr161 and its homologues. EMBO J., 12, 3111-3121.
16. Fry, A.M., Schultz, S.J., Bartek, J. and Nigg, E.A. (1995) Substrate specificity and cell cycle regulation of the Nek2 protein kinase, a potential human homolog of the mitotic regulator NIMA of Aspergillus nidulans. J. Biol. Chem., 270, 12899-12905.
17. Gale, J.M. and Parsons, M. (1993) A Trypanosoma brucei gene family encoding protein kinases with catalytic domains structurally related to Nek1 and NIMA. Mol. Biochem. Parasitol., 59, 111-122.
18. Gould, K.L. and Nurse, P. (1989) Tyrosine phosphorylation of the fission yeast cdc2+ protein kinase regulates entry into mitosis. Nature, 342, 39-45.
19. Haese, G.J.D., Walworth, N., Carr, A.M. and Gould, K.L. (1995) The Wee1 protein kinase regulates T14 phosphorylation of fission yeast Cdc2. Mol. Biol. Cell, 6, 371-385.
20. Harlow, E. and Lane, D. (1988) Antibodies: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
21. Hartwell, L.H. and Weinert, T.A. (1989) Checkpoints: controls that ensure the order of cell cycle events. Science, 246, 629-634.
22. Heald, R., McLoughlin, M. and McKeon, F. (1993) Human Wee1 maintains mitotic timing by protecting the nucleus from cytoplasmically activated Cdc2 kinase. Cell, 74, 463-474.
23. James, S.W., Mirabito, P.M., Scacheri, P.C. and Morris, N.R. (1995) The Aspergillus nidulans bimE (blocked-in-mitosis) gene encodes multiple cell cycle functions involved in mitotic checkpoint control and mitosis. J. Cell Sci., 108, 3485-3499.
24. Jones, D.G.L. and Rosamond, J. (1990) Isolation of a novel protein kinase-encoding gene from yeast by oligodeoxynucleotide probing. Gene, 90, 87-92.
25. cdc2 kinase activation in vertebrates. EMBO J., 10, 3331-3341.
26. Kumagai, A. and Dunphy, W.G. (1995) Control of the Cdc2/cyclin B complex in Xenopus egg extracts arrested at a G2/M checkpoint with DNA synthesis inhibitors. Mol. Biol. Cell, 6, 199-213.
27. cdc2/cyclinB that regulates the G2/M transition in Xenopus extracts. Proc. Natl Acad. Sci. USA, 93, 352-356.
28. Letwin, K., Mizzen, L., Motro, B., Ben-David, Y., Bernstein, A. and Pawson, T. (1992) A mammalian dual specificity protein kinase. Nek1, is related to the NIMA cell cycle regulator and highly expressed in meiotic germ cells. EMBO J., 11, 3521-3531.
29. Levedakou, E.N. et al. (1994) Two novel human serine/threonine kinases with homologies to the cell cycle regulating Xenopus MO15, and NIMA kinases: cloning and characterization of their expression pattern. Oncogene, 8, 1977-1988.
30. Lu, K.P. and Hunter, T. (1995a) Evidence for a NIMA-like mitotic pathway in vertebrate cells. Cell, 81, 413-424.
31. Lu, K.P. and Hunter, T. (1995b) The NIMA kinase: a mitotic regulator in Aspergillus nidulans and vertebrate cells. In Meijer, L., Guidet, S. and Tung, H.Y.L. (eds). Progress in Cell Cycle Research, Vol 1. Plenum Press, New York, pp. 187-205.
32. Lu, K.P. and Means, A.R. (1994) Expression of the noncatalytic domain of the NIMA kinase causes a G2 arrest in Aspergillus nidulans. EMBO J., 13, 2103-2113.
33. Lu, K.P., Osmani, S.A. and Means, A.R. (1993) Properties and regulation of the cell cycle-specific NIMA protein kinase of Aspergillus nidulans. J. Biol. Chem., 268, 8769-8776.
34. Lundgren, K., Walworth, N., Booher, R., Dembski, M., Kirschner, M. and Beach, D. (1991) mik1 and wee1 cooperate in the inhibitory tyrosine phosphorylation of cdc2. Cell, 64, 1111-1122.
35. Morris, N.R. (1976) Mitotic mutants of Aspergillus nidulans. Genet. Res. Camb., 26, 237-254.
36. Mueller, P.R., Coleman, T.R., Kumagai, A. and Dunphy, W.G. (1995) Myt1: a membrane-associated inhibitory kinase that phosphorylates Cdc2 on both threonine-14 and tyrosine-15. Science, 270, 86-90.
37. Murray, A.W. (1992) Creative clocks: cell cycle checkpoints and feedback controls. Nature, 359, 599-604.
38. Murray, A.W. (1995) The genetics of cell cycle checkpoints. Curr. Opin. Genet. Dev., 5, 5-11.
39. Navas, T., Zhou, Z. and Elledge, S. (1995) DNA polymerase ε links the DNA replication machinery to the S phase checkpoint. Cell, 80, 29-39.
40. Nurse, P. (1990) Universal control mechanism regulating onset of M-phase. Nature, 344, 503-508.
41. Oakley, B.R. and Morris, N.R. (1983) A mutation in Aspergillus nidulans that blocks the transition from interphase to prophase. J. Cell Biol., 96, 1155-1158.
42. Oakley, B.R. and Osmani, S.A. (1993) Cell-cycle analysis using the filamentous fungus Aspergillus nidulans. In Fantes, P. and Brooks, R. (eds). The Cell Cycle: A Practical Approach. IRL Press at Oxford University Press, pp. 127-142.
43. O'Connell, M.J., Norbury, C. and Nurse, P. (1994) Premature chromatin condensation upon accumulation of NIMA. EMBO J., 13, 4926-4937.
44. cdc2 cell cycle-regulated protein kinases is required to initiate mitosis in A.nidulans. Cell, 67, 283-291.
45. Osmani, A.H., O'Donnell, K., Pu, R.T. and Osmani, S.A. (1991b) Activation of the NIMA protein kinase plays a unique role during mitosis that cannot be bypassed by absence of the himE checkpoint. EMBO J., 10, 2669-2679.
46. cdc2) is required at G1 and G2 in Aspergillus nidulans. J. Cell Sci., 107, 1519-1528.
47. Osmani, S.A., May, G.S. and Morris, N.R. (1987) Regulation of the mRNA levels of nimA, a gene required for the G2-M transition in Aspergillus nidulans. J. Cell Biol., 104, 1495-1504.
48. Osmani, S.A., Engle, D.B., Doonan, J.H. and Morris, N.R. (1988a) Spindle formation and chromatin condensation in cells blocked at interphase by mutation of a negative cell cycle control gene. Cell, 52, 241-251.
49. Osmani, S.A., Pu, R.T. and Morris, N.R. (1988b) Mitotic induction and maintenance by overexpression of a G2-specific gene that encodes a potential protein kinase. Cell, 53, 237-244.
50. Paulovich, A. and Hartwell, L. (1995) A checkpoint regulates the rate of progression through S phase in S.cerevisiae in response to DNA damage. Cell, 82, 841-847.
51. cdc2. EMBO J., 12, 3123-3132.
52. Pu, R.T. and Osmani, S.A. (1995) Mitotic destruction of the cell cycle regulated NIMA protein kinase of Aspergillus nidulans is required for mitotic exit. EMBO J., 14, 995-1003.
53. Pu, R.T., Xu, G., Wu, L., Vierula, J., O'Donnell, K., Ye, S.X. and Osmani, S.A. (1995) Isolation of a functional homolog of the cell cycle specific NIMA protein kinase and functional analysis of conserved residues. J. Biol. Chem., 271, 18110-18116.
54. Russell, P. and Nurse, P. (1986) cdc25 functions as an inducer in the mitotic control of fission yeast. Cell, 45, 145-153.
55. Sambrook, S., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
56. Schultz, S.J. and Nigg, E.A. (1993) Identification of 21 novel human protein kinases, including 3 members of a family related to the cell cycle regulator nimA of Aspergillus nidulans. Cell Growth Differ., 4, 821-830.
57. Schultz, S.J., Fry, A.M., Sutterlin, C., Ried, T. and Nigg, E.A. (1994) Cell cycle-dependent expression of Nek2, a novel human protein kinase related to the NIMA mitotic regulator of Aspergillus nidulans. Cell Growth Differ., 5, 1-11.
58. MO15. EMBO J., 12, 3133-3142.
59. cdc28. Nature, 355, 365-367.
60. Starborg, M., Brundell, E., Gell, K. and Hoog, C. (1994) A novel murine gene encoding a 216-kDa protein is related to a mitotic checkpoint regulator previously identified in Aspergillus nidulans. J. Biol. Chem., 269, 24133-24137.
61. cdc28 histone H1 kinase activity is unable to promote entry into mitosis in checkpoint-arrested cells of the yeast Saccharomyces cerevisiae. Mol. Cell Biol., 13, 3744-3755.
62. Waring, R.B., May, G.S. and Morris, N.R. (1989) Characterization of an inducible expression system in Aspergillus nidulans using alcA and tubulin-coding genes. Gene, 79, 119-130.
63. Weinert, T.A. and Hartwell, L.H. (1988) The RAD9 gene controls the cell cycle response to DNA damage in Saccharomyces cerevisiae. Science, 241, 317-322.
64. Weinert, T., Kiser, G. and Hartwell, L. (1994) Mitotic checkpoint genes in budding yeast and the dependence of mitosis on DNA replication and repair. Genes Dev., 8, 652-665.
65. cdc2/cyclin B: coordination of two mitosis promoting kinases. EMBO J., 14, 986-994.