Overproduction of Human Myt1 Kinase Induces a G₂ Cell Cycle Delay by Interfering with the Intracellular Trafficking of Cdc2-Cyclin B1 Complexes

REFERENCES

• Adams, P. D., W. R. Sellers, S. K. Sharma, A. D. Wu, C. M. Nalin, and J. Kaelin 1996. Identification of a cyclin-cdk2 recognition motif present in substrates and p21-like cyclin-dependent kinase inhibitors. Mol. Cell. Biol. 16:6623–6633.
   PubMed Web of Science ®Google Scholar
• Atherton-Fessler, S., G. Hannig, and J. Piwnica-Worms 1993. Reversible tyrosine phosphorylation and cell cycle control. Semin. Cell Biol. 4:433–442.
   PubMedGoogle Scholar
• Atherton-Fessler, S., F. Liu, B. Gabrielli, M. S. Lee, C.-Y. Peng, and J. Piwnica-Worms 1994. Cell cycle regulation of the p34cdc2 inhibitory kinases. Mol. Biol. Cell 5:989–1001.
   PubMed Web of Science ®Google Scholar
• Atherton-Fessler, S., L. L. Parker, R. L. Geahlen, and J. Piwnica-Worms 1993. Mechanism of p34cdc2 regulation. Mol. Cell. Biol. 13:1675–1685.
   PubMed Web of Science ®Google Scholar
• Bailly, E., J. Pines, T. Hunter, and J. Bornens 1992. Cytoplasmic accumulation of cyclin B1 in human cells: association with a detergent-resistent compartment and with the centrosome. J. Cell Sci. 101:529–545.
   PubMed Web of Science ®Google Scholar
• Baldin, V., and J. Ducommun 1995. Subcellular localisation of human wee1 kinase is regulated during the cell cycle. J. Cell Sci. 108:2425–2432.
   PubMed Web of Science ®Google Scholar
• Becker, T. C., R. J. Noel, W. S. Coats, A. M. Gomez-Foix, T. Alam, R. D. Gerard, C. B. Newgard 1994. Use of recombinant adenovirus for metabolic engineering of mammalian cells, p. 161–189. In M. G. Roth (ed.), Methods in cell biology. Academic Press, Inc., New York, N.Y.
   Google Scholar
• Blasina, A., E. S. Paegle, and J. McGowan 1997. The role of inhibitory phosphorylation of Cdc2 following DNA replication block and radiation-induced damage in human cells. Mol. Biol. Cell 8:1013–1023.
   PubMedGoogle Scholar
• Booher, R. N., P. S. Holman, and J. Fattaey 1997. Human Myt1 is a cell cycle regulated kinase that inhibits Cdc2 but not Cdk2 activity. J. Biol. Chem. 272:22300–22306.
   PubMed Web of Science ®Google Scholar
• Chen, J., P. Saha, S. Kornbluth, B. D. Dynlacht, and J. Dutta 1996. Cyclin-binding motifs are essential for the function of p21Cip1. Mol. Cell. Biol. 16:4673–4682.
   PubMed Web of Science ®Google Scholar
• Cliby, W. A., C. J. Roberts, K. A. Cimprich, C. M. Stringer, J. R. Lamb, S. L. Schreiber, and J. Friend 1998. Overexpression of a kinase-inactive ATR protein causes sensitivity to DNA-damaging agents and defects in cell cycle checkpoints. EMBO J. 17:159–169.
   PubMed Web of Science ®Google Scholar
• Draetta, G., and J. Beach 1988. Activation of cdc2 protein kinase during mitosis in human cells: cell cycle-dependent phosphorylation and subunit rearrangement. Cell 54:17–26.
   PubMed Web of Science ®Google Scholar
• Draetta, G., H. Piwnica-Worms, D. Morrison, B. Druker, T. Roberts, and J. Beach 1988. Human cdc2 protein kinase is a major cell-cycle regulated tyrosine kinase substrate. Nature 336:738–744.
   PubMed Web of Science ®Google Scholar
• Dunphy, W. G., and J. Kumagai 1991. The cdc25 protein contains an intrinsic phosphatase activity. Cell 67:189–196.
   PubMed Web of Science ®Google Scholar
• Featherstone, C., and J. Russell 1991. Fission yeast p107wee1 mitotic inhibitor is a tyrosine/serine kinase. Nature 349:808–811.
   PubMed Web of Science ®Google Scholar
• Gallant, P., and J. Nigg 1992. Cyclin B2 undergoes cell cycle-dependent nuclear translocation and, when expressed as a non-destructible mutant, causes mitotic arrest in HeLa cells. J. Cell Biol. 117:213–224.
   PubMedGoogle Scholar
• Gautier, J., M. J. Solomon, R. N. Booher, J. F. Bazan, and J. Kirschner 1991. cdc25 is a specific tyrosine phosphatase that directly activates p34cdc2. Cell 67:197–211.
   PubMed Web of Science ®Google Scholar
• Gould, K. L., S. Moreno, D. J. Owen, S. Sazer, and J. Nurse 1991. Phosphorylation at Thr 167 is required for Schizosaccharomyces pombe p34cdc2 function. EMBO J. 10:3297–3309.
   PubMed Web of Science ®Google Scholar
• Gould, K. L., and J. Nurse 1989. Tyrosine phosphorylation of the fission yeast cdc2+ protein kinase regulates entry into mitosis. Nature 342:39–45.
   PubMed Web of Science ®Google Scholar
• Gulbis, J. M., Z. Kelman, J. Hurwitz, M. O’Donnell, and J. Kuriyan 1996. Structure of the C-terminal region of p21WAF1/CIP1 complexed with human PCNA. Cell 87:297–306.
   PubMed Web of Science ®Google Scholar
• Hagting, A., C. Karlsson, P. Clute, M. Jackman, and J. Pines 1998. MPF localization is controlled by nuclear export. EMBO J. 17:4127–4138.
   PubMed Web of Science ®Google Scholar
• He, T.-C., S. Zhou, L. T. DaCosta, J. Yu, K. W. Kinzler, and J. Vogelstein 1998. A simplified system for generating recombinant adenoviruses. Proc. Natl. Acad. Sci. USA 95:2509–2514.
   PubMed Web of Science ®Google Scholar
• Heald, R., M. McLoughlin, and J. McKeon 1993. Human Wee1 maintains mitotic timing by protecting the nucleus from cytoplasmically activated Cdc2 kinase. Cell 74:463–474.
   PubMed Web of Science ®Google Scholar
• Hoffmann, I., P. R. Clarke, M. J. Marcote, E. Karsenti, and J. Draetta 1993. Phosphorylation and activation of human cdc25-C by cdc2-cyclin B and its involvement in the self-amplification of MPF at mitosis. EMBO J. 12:53–63.
   PubMed Web of Science ®Google Scholar
• Honda, R., Y. Ohba, and J. Yasuda 1992. The cell cycle regulator, human p50wee1, is a tyrosine kinase and not a serine/tyrosine kinase. Biochem. Biophys. Res. Commun. 186:1333–1338.
   PubMedGoogle Scholar
• Igarashi, M., A. Nagata, S. Jinno, K. Suto, and J. Okayama 1991. Wee1+-like gene in human cells. Nature 353:80–83.
   PubMedGoogle Scholar
• Izumi, T., D. H. Walker, and J. Maller 1992. Periodic changes in phosphorylation of the Xenopus cdc25 phosphatase regulate its activity. Mol. Biol. Cell 3:927–939.
   PubMed Web of Science ®Google Scholar
• Jin, P., Y. Gu, and J. Morgan 1996. Role of inhibitory Cdc2 phosphorylation in radiation-induced G2 arrest in human cells. J. Cell Biol. 134:963–970.
   PubMedGoogle Scholar
• Jin, P., S. Hardy, and J. Morgan 1998. Nuclear localization of cyclin B1 controls mitotic entry after DNA damage. J. Cell Biol. 141:875–885.
   PubMed Web of Science ®Google Scholar
• Kornbluth, S., B. Sebastian, T. Hunter, and J. Newport 1994. Membrane localization of the kinase which phosphorylates p34cdc2 on threonine 14. Mol. Biol. Cell 5:273–282.
   PubMedGoogle Scholar
• Krek, W., and J. Nigg 1991. Differential phosphorylation of vertebrate p34cdc2 kinase at the G1/S and G2/M transitions of the cell cycle: identification of major phosphorylation sites. EMBO J. 10:305–316.
   PubMed Web of Science ®Google Scholar
• Krek, W., and J. Nigg 1991. Mutations of p34cdc2 phosphorylation sites induce premature mitotic events in HeLa cells: evidence for a double block to p34cdc2 kinase activation in vertebrates. EMBO J. 10:3331–3341.
   PubMedGoogle Scholar
• Kudo, N., S. Khochbin, K. Nishi, K. Kitano, M. Yanagida, M. Yoshida, and J. Horinouchi 1997. Molecular cloning and cell cycle-dependent expression of mammalian CRM1, a protein involved in nuclear export of proteins. J. Biol. Chem. 272:29742–29751.
   PubMed Web of Science ®Google Scholar
• Kumagai, A., and J. Dunphy 1992. Regulation of the cdc25 protein during the cell cycle in Xenopus extracts. Cell 70:139–151.
   PubMed Web of Science ®Google Scholar
• Kumagai, A., and J. Dunphy 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.
   PubMed Web of Science ®Google Scholar
• Lee, M. S., T. Enoch, and J. Piwnica-Worms 1994. Mik1+ encodes a tyrosine kinase that phosphorylates p34cdc2 on tyrosine 15. J. Biol. Chem. 269:30530–30537.
   PubMed Web of Science ®Google Scholar
• Lee, M. S., S. Ogg, M. Xu, L. L. Parker, D. J. Donoghue, J. L. Maller, and J. Piwnica-Worms 1992. cdc25+ encodes a protein phosphatase that dephosphorylates p34cdc2. Mol. Biol. Cell 3:73–84.
   PubMed Web of Science ®Google Scholar
• Lee, T. H., and J. Kirschner 1996. An inhibitor of p34cdc2/cyclin B that regulates the G2/M transition in Xenopus extracts. Proc. Natl. Acad. Sci. USA 93:352–356.
   PubMedGoogle Scholar
• Li, J., A. N. Meyer, and J. Donoghue 1995. Requirement for phosphorylation of cyclin B1 for Xenopus oocyte maturation. Mol. Biol. Cell 6:1111–1124.
   PubMedGoogle Scholar
• Liu, F., J. J. Stanton, Z. Wu, and J. Piwnica-Worms 1997. The human Myt1 kinase preferentially phosphorylates Cdc2 on threonine 14 and localizes to the endoplasmic reticulum and Golgi complex. Mol. Cell. Biol. 17:571–583.
   PubMed Web of Science ®Google Scholar
• Lundgren, K., N. Walworth, R. Booher, M. Dembski, M. Kirschner, and J. Beach 1991. mik1 and wee1 cooperate in the inhibitory tyrosine phosphorylation of cdc2. Cell 64:1111–1122.
   PubMed Web of Science ®Google Scholar
• McGowan, C. H., and J. Russell 1993. Human Wee1 kinase inhibits cell division by phosphorylating p34cdc2 exclusively on Tyr 15. EMBO J. 12:75–85.
   PubMed Web of Science ®Google Scholar
• McGowan, C. H., and J. Russell 1995. Cell cycle regulation of human WEE1. EMBO J. 14:2166–2175.
   PubMed Web of Science ®Google Scholar
• Morgan, D. O. 1997. Cyclin dependent kinases: engines, clocks, and microprocessors. Annu. Rev. Cell Deve. Biol. 13:261–291.
   PubMed Web of Science ®Google Scholar
• Morla, A. O., G. Draetta, D. Beach, and J. Wang 1989. Reversible tyrosine phosphorylation of cdc2: dephosphorylation accompanies activation during entry into mitosis. Cell 58:193–203.
   PubMed Web of Science ®Google Scholar
• Mueller, P. R., T. R. Coleman, A. Kumagai, and J. Dunphy 1995. Myt1: a membrane-associated inhibitory kinase that phosphorylates Cdc2 on both threonine-14 and tyrosine-15. Science 270:86–90.
   PubMed Web of Science ®Google Scholar
• Nishi, K., M. Yoshida, D. Fujiwara, M. Nishikawa, S. Horinouchi, and J. Beppu 1994. Leptomycin B targets a regulatory cascade or crm1, a fission yeast nuclear protein, involved in control of higher order chromosome structure and gene expression. J. Biol. Chem. 9:6320–6324.
   Google Scholar
• Norbury, C., J. Blow, and J. Nurse 1991. Regulatory phosphorylation of the p34cdc2 protein kinase in vertebrates. EMBO J. 10:3321–3329.
   PubMed Web of Science ®Google Scholar
• Ookata, K., S.-I. Hisanaga, T. Okano, K. Tachibana, and J. Kishimoto 1992. Relocation and distinct subcellular localization of p34cdc2-cyclin B complex at meiosis reinitiation in starfish oocytes. EMBO J. 11:1763–1772.
   PubMed Web of Science ®Google Scholar
• Palmer, A., A. Gavin, and J. Nebreda 1998. A link between MAP kinase and p34cdc2/cyclin B during oocyte maturation: p90rsk phosphorylates and inactivates the p34cdc2 inhibitory kinase Myt1. EMBO J. 17:5037–5047.
   PubMed Web of Science ®Google Scholar
• Parker, L. L., S. Atherton-Fessler, M. S. Lee, S. Ogg, F. L. Falk, K. I. Swenson, and J. Piwnica-Worms 1991. Cyclin promotes the tyrosine phosphorylation of p34cdc2 in a wee1+ dependent manner. EMBO J. 10:1255–1263.
   PubMed Web of Science ®Google Scholar
• Parker, L. L., S. Atherton-Fessler, and J. Piwnica-Worms 1992. p107wee1 is a dual specificity kinase that phosphorylates p34cdc2 on tyrosine 15. Proc. Natl. Acad. Sci. USA 89:2917–2921.
   PubMed Web of Science ®Google Scholar
• Parker, L. L., and J. Piwnica-Worms 1992. Inactivation of the p34cdc2-cyclin B complex by the human wee1 tyrosine kinase. Science 257:1955–1957.
   PubMed Web of Science ®Google Scholar
• Parker, L. L., P. J. Sylvestre, M. J. Byrnes III, F. Liu, and J. Piwnica-Worms 1995. Identification of a 95-kDa WEE1-like tyrosine kinase in HeLa cells. Proc. Natl. Acad. Sci. USA 92:9638–9642.
   PubMedGoogle Scholar
• Pines, J., and J. Hunter 1991. Human cyclin A and B1 are differentially located in the cell and undergo cell cycle-dependent nuclear transport. J. Cell Biol. 115:1–17.
   PubMed Web of Science ®Google Scholar
• Pines, J., and J. Hunter 1994. The differential localization of human cyclin A and B is due to a cytoplasmic retention signal in cyclin B. EMBO J. 13:3772–3781.
   PubMed Web of Science ®Google Scholar
• Russell, P., and J. Nurse 1987. Negative regulation of mitosis by wee1+, a gene encoding a protein kinase homolog. Cell 49:559–567.
   PubMed Web of Science ®Google Scholar
• Russo, A. A., P. D. Jeffrey, A. K. Patten, J. Massague, and J. Pavletich 1996. Crystal structure of the p27kip1 cyclin dependent kinase inhibitor bound to the cyclin A-cdk2 complex. Nature 382:325–331.
   PubMed Web of Science ®Google Scholar
• Saha, P., Q. Eichbaum, E. D. Silberman, B. J. Mayer, and J. Dutta 1997. p21CIP1 and Cdc25A: competition between an inhibitor and an activator of cyclin-dependent kinases. Mol. Cell. Biol. 17:4338–4345.
   PubMedGoogle Scholar
• Schulman, B. A., D. L. Lindstrom, and J. Harlow 1998. Substrate recruitment to cyclin-dependent kinase 2 by a multipurpose docking site on cyclin A. Proc. Natl. Acad. Sci. USA 95:10453–10458.
   PubMed Web of Science ®Google Scholar
• Sebastian, B., A. Kakizuka, and J. Hunter 1993. Cdc25M2 activation of cyclin-dependent kinases by dephosphorylation of threonine-14 and tyrosine-15. Proc. Natl. Acad. Sci. USA 90:3521–3524.
   PubMed Web of Science ®Google Scholar
• Solomon, M. J., T. Lee, and J. Kirschner 1992. Role of phosphorylation in p34cdc2 activation: identification of an activating kinase. Mol. Biol. Cell 3:13–27.
   PubMed Web of Science ®Google Scholar
• Strausfeld, U., J. C. Labbe, D. Fesquet, J. C. Cavadore, A. Picard, K. Sadhu, P. Russell, and J. Doree 1991. Dephosphorylation and activation of a p34cdc2/cyclin B complex in vitro by human cdc25 protein. Nature 351:242–245.
   PubMed Web of Science ®Google Scholar
• Toyoshima, F., T. Moriguchi, A. Wada, M. Fukuda, and J. Nishida 1998. Nuclear export of cyclin B1 and its possible role in the DNA damage-induced G2 checkpoint. EMBO J. 17:2728–2735.
   PubMed Web of Science ®Google Scholar
• Watanabe, N., M. Broome, and J. Hunter 1995. Regulation of the human WEE1Hu CDK tyrosine 15-kinase during the cell cycle. EMBO J. 14:1878–1891.
   PubMed Web of Science ®Google Scholar
• Yang, J., E. S. G. Bardes, J. D. Moore, J. Brennan, M. A. Powers, and J. Kornbluth 1998. Control of cyclin B1 localization through regulated binding of the nuclear export factor CRM1. Genes Dev. 12:2131–2143.
   PubMed Web of Science ®Google Scholar