Normal Cell Cycle and Checkpoint Responses in Mice and Cells Lacking Cdc25B and Cdc25C Protein Phosphatases

REFERENCES

• Abrieu, A., T. Brassac, S. Galas, D. Fisher, J. C. Labbe, and M. Doree. 1998. The Polo-like kinase Plx1 is a component of the MPF amplification loop at the G2/M-phase transition of the cell cycle in Xenopus eggs. J. Cell Sci. 111:1751–1757.
   PubMed Web of Science ®Google Scholar
• Atherton-Fessler, S., F. Liu, B. Gabrielli, M. S. Lee, C.-Y. Peng, and H. Piwnica-Worms. 1994. Cell cycle regulation of the p34cdc2 inhibitory kinases. Mol. Biol. Cell 5:989–1001.
   PubMed Web of Science ®Google Scholar
• Barlow, C., K. D. Brown, C. X. Deng, D. A. Tagle, and A. Wynshaw-Boris. 1997. Atm selectively regulates distinct p53-dependent cell-cycle checkpoint and apoptotic pathways. Nat. Genet. 17:453–456.
   PubMed Web of Science ®Google Scholar
• Bernardi, R., D. A. Lieberman, and B. Hoffman. 2000. Cdc25A stability is controlled by the ubiquitin-proteasome pathway during cell cycle progression and terminal differentiation. Oncogene 19:2447–2454.
   PubMedGoogle Scholar
• Blomberg, I., and I. Hoffman. 1999. Ectopic expression of Cdc25A accelerates the G1/S transition and leads to premature activation of cyclin E- and cyclin A-dependent kinases. Mol. Cell. Biol. 19:6183–6194.
   PubMed Web of Science ®Google Scholar
• Busino, L., M. Donzelli, M. Chiesa, D. Guardavaccaro, D. Ganoth, N. V. Dorrello, A. Hershko, M. Pagano, and G. F. Draetta. 2003. Degradation of Cdc25A by beta-TrCP during S phase and in response to DNA damage. Nature 426:87–91.
   PubMed Web of Science ®Google Scholar
• Chen, M.-S., J. Hurov, L. S. White, T. Woodford-Thomas, and H. Piwnica-Worms. 2001. Absence of apparent phenotype in mice lacking Cdc25C protein phosphatase. Mol. Cell. Biol. 21:3853–3861.
   PubMed Web of Science ®Google Scholar
• Chen, M.-S., C. E. Ryan, and H. Piwnica-Worms. 2003. Chk1 kinase negatively regulates mitotic function of Cdc25A phosphatase through 14-3-3 binding. Mol. Cell. Biol. 23:7488–7497.
   PubMed Web of Science ®Google Scholar
• Conklin, D. S., K. Galaktionov, and D. Beach. 1995. 14-3-3 proteins associate with cdc25 phosphatases. Proc. Natl. Acad. Sci. USA 92:7892–7896.
   PubMed Web of Science ®Google Scholar
• Dalal, S. N., C. M. Schweitzer, J. Gan, and J. Decaprio. 1999. Cytoplasmic localization of human Cdc25C during interphase requires an intact 14-3-3 binding site. Mol. Cell. Biol. 19:4465–4479.
   PubMed Web of Science ®Google Scholar
• Davezac, N., V. Baldin, B. Gabrielli, A. Forrest, N. Theis-Febvre, M. Yashida, and B. Ducommun. 2000. Regulation of CDC25B phosphatases' subcellular localization. Oncogene 19:2179–2185.
   PubMedGoogle Scholar
• Donzelli, M., M. Squatrito, D. Ganoth, A. Hershko, M. Pagano, and G. F. Draetta. 2002. Dual mode of degradation of Cdc25 A phosphatase. EMBO J. 21:4875–4884.
   PubMed Web of Science ®Google Scholar
• Ducommun, B., G. Draetta, P. Young, and D. Beach. 1990. Fission yeast cdc25 is a cell cycle regulated protein. Biochem. Biophys. Res. Commun. 167:301–309.
   PubMed Web of Science ®Google Scholar
• Dunphy, W. G., and A. Kumagai. 1991. The cdc25 protein contains an intrinsic phosphatase activity. Cell 67:189–196.
   PubMed Web of Science ®Google Scholar
• Falck, J., N. Mailand, R. G. Syljuasen, J. Bartek, and J. Lukas. 2001. The ATM-Chk2-Cdc25A checkpoint pathway guards against radioresistant DNA synthesis. Nature 410:842–847.
   PubMed Web of Science ®Google Scholar
• Falck, J., J. H. Petrini, B. R. Williams, J. Lukas, and J. Bartek. 2002. The DNA damage-dependent intra-S phase checkpoint is regulated by parallel pathways. Nat. Genet. 30:290–294.
   PubMed Web of Science ®Google Scholar
• Gabrielli, B. G., J. M. Clark, A. K. McCormack, and K. A. Ellem. 1997. Hyperphosphorylation of the N-terminal domain of Cdc25 regulates activity toward cyclin B1/Cdc2 but not cyclin A/Cdk2. J. Biol. Chem. 272:28607–28614.
   PubMedGoogle Scholar
• Gabrielli, B. G., C. P. C. De Souza, I. D. Tonks, J. M. Clark, and N. K. Hayward. 1996. Cytoplasmic accumulation of cdc25B phosphatase in mitosis triggers centrosomal microtubule nucleation in HeLa cells. J. Cell Sci. 109:1081–1093.
   PubMed Web of Science ®Google Scholar
• Galaktionov, K., and D. Beach. 1991. Specific activation of cdc25 tyrosine phosphatases by B-type cyclins: evidence for multiple roles of mitotic cyclins. Cell 67:1181–1194.
   PubMed Web of Science ®Google Scholar
• Gautier, J., M. J. Solomon, R. N. Booher, J. F. Bazan, and M. W. Kirschner. 1991. cdc25 is a specific tyrosine phosphatase that directly activates p34cdc2. Cell 67:197–211.
   PubMed Web of Science ®Google Scholar
• Goloudina, A., H. Yamaguchi, D. B. Chervyakova, E. Appella, A. J. Fornace, and D. V. Bulavin. 2003. Regulation of human Cdc25A stability by serine 75 phosphorylation is not sufficient to activate a S-phase checkpoint. Cell Cycle 2:473–478.
   PubMedGoogle Scholar
• Graves, P. R., C. M. Lovly, G. L. Uy, and H. Piwnica-Worms. 2001. Localization of human Cdc25C is regulated both by nuclear export and 14-3-3 binding. Oncogene 20:1839–1851.
   PubMedGoogle Scholar
• Graves, P. R., L. Yu, J. K. Schwarz, J. Gales, E. A. Sausville, P. M. O'Connor, and H. Piwnica-Worms. 2000. The Chk1 protein kinase and the Cdc25C regulatory pathway are targets of the anticancer agent UCN-01. J. Biol. Chem. 275:5600–5605.
   PubMed Web of Science ®Google Scholar
• Hassepass, I., R. Voit, and I. Hoffmann. 2003. Phosphorylation at serine-75 is required for UV-mediated degradation of human Cdc25A phosphatase at the S-phase checkpoint. J. Biol. Chem. 278:29824–29829.
   PubMedGoogle Scholar
• Hoffmann, I., P. R. Clarke, M. J. Marcote, E. Karsenti, and G. 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
• Hoffmann, I., G. Draetta, and E. Karsenti. 1994. Activation of the phosphatase activity of human cdc25A by a cdk2-cyclin E dependent phosphorylation at the G1/S transition. EMBO J. 13:4302–4310.
   PubMed Web of Science ®Google Scholar
• Honda, R., Y. Ohba, A. Nagata, H. Okayama, and H. Yasuda. 1993. Dephosphorylation of human p34cdc2 kinase on both Thr-14 and Tyr-15 by human cdc25B phosphatase. FEBS Lett. 318:331–334.
   PubMedGoogle Scholar
• Izumi, T., and J. L. Maller. 1993. Elimination of cdc2 phosphorylation sites in the cdc25 phosphatase blocks initiation of M-phase. Mol. Biol. Cell 4:1337–1350.
   PubMed Web of Science ®Google Scholar
• Izumi, T., D. H. Walker, and J. M. 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, J., T. Shirogane, L. Xu, G. Nalepa, J. Qin, S. J. Elledge, and J. W. Harper. 2003. SCFbeta-TRCP links Chk1 signaling to degradation of the Cdc25A protein phosphatase. Genes Dev. 17:3062–3074.
   PubMed Web of Science ®Google Scholar
• Jinno, S., K. Suto, A. Nagata, M. Igarashi, Y. Kanaoka, H. Nojima, and H. Okayama. 1994. Cdc25A is a novel phosphatase functioning early in the cell cycle. EMBO J. 13:1549–1556.
   PubMed Web of Science ®Google Scholar
• Kakizuka, A., B. Sebastian, U. Borgmeyer, I. Hermans-Borgmeyer, J. Bolado, T. Hunter, M. F. Hoekstra, and R. M. Evans. 1992. A mouse cdc25 homolog is differentially and developmentally expressed. Genes Dev. 6:578–590.
   PubMedGoogle Scholar
• Kim, S. H., L. Chuan, and J. L. Maller. 1999. A maternal form of the phosphatase Cdc25A regulates early embryonic cell cycles in Xenopus laevis. Dev. Biol. 212:381–391.
   PubMed Web of Science ®Google Scholar
• Kuang, J., C. L. Ashorn, M. Gonzalez-Kuyvenhoven, and J. E. Penkala. 1994. cdc25 is one of the MPM-2 antigens involved in the activation of maturation-promoting factor. Mol. Biol. Cell 5:135–145.
   PubMedGoogle Scholar
• Kumagai, A., and W. G. Dunphy. 1996. Purification and molecular cloning of Plx1, a cdc25-regulatory kinase from Xenopus egg extracts. Science 273:1377–1380.
   PubMed Web of Science ®Google Scholar
• Kumagai, A., and W. G. 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., Z. Guo, K. Emami, S. X. Wang, and W. G. Dunphy. 1998. The Xenopus Chk1 protein kinase mediates a caffeine-sensitive pathway of checkpoint control in cell-free extracts. J. Cell Biol. 142:1559–1569.
   PubMed Web of Science ®Google Scholar
• Lammer, C., S. Wagerer, R. Saffrich, D. Mertens, W. Ansorge, and I. Hoffmann. 1998. The cdc25B phosphatase is essential for the G2/M phase transition in human cells. J. Cell Sci. 111:2445–2453.
   PubMed Web of Science ®Google Scholar
• Lee, M. S., S. Ogg, M. Xu, L. L. Parker, D. J. Donoghue, J. L. Maller, and H. Piwnica-Worms. 1992. cdc25+ encodes a protein phosphatase that dephosphorylates p34cdc2. Mol. Biol. Cell 3:73–84.
   PubMed Web of Science ®Google Scholar
• Lincoln, A. J., D. Wickramasinghe, P. Stein, R. M. Schultz, M. E. Palko, A. P. De Miguel, L. Tessarollo, and P. J. Donovan. 2002. Cdc25b phosphatase is required for resumption of meiosis during oocyte maturation. Nat. Genet. 30:446–449.
   PubMed Web of Science ®Google Scholar
• Mailand, N., J. Falck, C. Lukas, R. G. Syljuasen, M. Welcker, J. Bartek, and J. Lukas. 2000. Rapid destruction of human Cdc25A in response to DNA damage. Science 288:1425–1429.
   PubMed Web of Science ®Google Scholar
• Mailand, N., A. V. Podtelejnikov, A. Groth, M. Mann, J. Bartek, and J. Lukas. 2002. Regulation of G2/M events by Cdc25A through phosphorylation-dependent modulation of its stability. EMBO J. 21:5911–5920.
   PubMed Web of Science ®Google Scholar
• Millar, J. B. A., J. Blevitt, L. Gerace, K. Sadhu, C. Featherstone, and P. Russell. 1991. p55cdc25 is a nuclear protein required for the initiation of mitosis in human cells. Proc. Natl. Acad. Sci. USA 88:10500–10504.
   PubMed Web of Science ®Google Scholar
• Molinari, M., C. Mercurio, J. Dominguez, F. Goubin, and G. F. Draetta. 2000. Human Cdc25A inactivation in response to S phase inhibition and its role in preventing premature mitosis. EMBO Rep. 1:71–79.
   PubMed Web of Science ®Google Scholar
• Nagata, A., M. Igarashi, S. Jinno, K. Suto, and H. Okayama. 1991. An additional homolog of the fission yeast cdc25+ gene occurs in humans and is highly expressed in some cancer cells. New Biol. 3:959–968.
   PubMedGoogle Scholar
• Nargi, J. L., and T. A. Woodford-Thomas. 1994. Cloning and characterization of a cdc25 phosphatase from mouse lymphocytes. Immunogenetics 39:99–108.
   PubMedGoogle Scholar
• Nishijima, H., H. Nishitani, T. Seki, and T. Nishimoto. 1997. A dual-specificity phosphatase Cdc25B is an unstable protein and triggers p34(cdc2)/cyclin B activation in hamster BHK21 cells arrested with hydroxyurea. J. Cell Biol. 138:1105–1116.
   PubMedGoogle Scholar
• Parker, L. L., S. Atherton-Fessler, M. S. Lee, S. Ogg, F. L. Falk, K. I. Swenson, and H. 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
• Peng, C.-Y., P. R. Graves, R. S. Thoma, Z. Wu, A. Shaw, and H. Piwnica-Worms. 1997. Mitotic- and G2-checkpoint control: regulation of 14-3-3 protein binding by phosphorylation of Cdc25C on serine 216. Science 277:1501–1505.
   PubMed Web of Science ®Google Scholar
• Qian, Y. W., E. Erikson, F. E. Taieb, and J. L. Maller. 2001. The polo-like kinase Plx1 is required for activation of the phosphatase Cdc25C and cyclin B-Cdc2 in Xenopus oocytes. Mol. Biol. Cell 12:1791–1799.
   PubMed Web of Science ®Google Scholar
• Russell, P., and P. Nurse. 1986. cdc25+ functions as an inducer in the mitotic control of fission yeast. Cell 45:145–153.
   PubMed Web of Science ®Google Scholar
• Sadhu, K., S. I. Reed, H. Richardson, and P. Russell. 1990. Human homolog of fission yeast cdc25 mitotic inducer is predominantly expressed in G2. Proc. Natl. Acad. Sci. USA 87:5139–5143.
   PubMed Web of Science ®Google Scholar
• Sage, J., A. L. Miller, P. A. Perez-Mancera, J. M. Wysocki, and T. Jacks. 2003. Acute mutation of retinoblastoma gene function is sufficient for cell cycle re-entry. Nature 424:223–228.
   PubMed Web of Science ®Google Scholar
• Sebastian, B., A. Kakizuka, and T. 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
• Sexl, V., J. Diehl, C. Sherr, R. Ashmun, D. Beach, and M. F. Roussel. 1999. A rate limiting function of Cdc25A for S phase entry inversely correlates with tyrosine dephosphorylation of Cdk2. Oncogene 18:573–582.
   PubMed Web of Science ®Google Scholar
• Solomon, M. J., T. Lee, and M. W. 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
• Sorensen, C. S., R. G. Syluasen, J. Falck, T. Schroeder, L. Ronnstrand, K. K. Khanna, B.-B. Zhou, J. Bartek, and J. Lukas. 2003. Chk1 regulates the S phase checkpoint by coupling the physiological turnover and ionizing radiation-induced accelerated proteolysis of Cdc25A. Cancer Cell 3:247–258.
   PubMed Web of Science ®Google Scholar
• Strausfeld, U., J. C. Labbe, D. Fesquet, J. C. Cavadore, A. Picard, K. Sadhu, P. Russell, and M. 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
• Vigo, E., H. Muller, E. Properini, G. Hatevoer, P. Cartwright, M. C. Moroni, and K. Helin. 1999. CDC25A phosphatase is a target of E2F and is required for efficient E2F-induced S phase. Mol. Cell. Biol. 19:6379–6395.
   PubMed Web of Science ®Google Scholar
• Villa-Moruzzi, E. 1993. Activation of the cdc25C phosphatase in mitotic HeLa cells. Biochem. Biophys. Res. Commun. 196:1248–1254.
   PubMedGoogle Scholar
• Wickramasinghe, D., S. Becker, M. K. Ernst, J. L. Resnick, J. M. Centanni, L. Tessarollo, L. B. Grabel, and P. J. Donovan. 1995. Two CDC25 homologues are differentially expressed during mouse development. Development 121:2047–2056.
   PubMed Web of Science ®Google Scholar
• Wu, S., and D. J. Wolgemuth. 1995. The distinct and developmentally regulated patterns of expression of members of the mouse Cdc25 gene family suggest differential functions during gametogenesis. Dev. Biol. 170:195–206.
   PubMed Web of Science ®Google Scholar
• Xiao, Z., Z. Chen, A. H. Gunasekera, T. J. Sowin, S. H. Rosenberg, S. Fesik, and H. Zhang. 2003. Chk1 mediates S and G2 arrests through Cdc25A degradation in response to DNA-damaging agents. J. Biol. Chem. 278:21767–21773.
   PubMed Web of Science ®Google Scholar
• Xu, B., S.-T. Kim, and M. B. Kastan. 2001. Involvement of Brcai in S-phase and G2-phase checkpoints after ionizing radiation. Mol. Cell. Biol. 21:3445–3450.
   PubMed Web of Science ®Google Scholar
• Xu, B., S.-T. Kim, D.-S. Lim, and M. B. Kastan. 2002. Two molecularly distinct G2/M checkpoints are induced by ionizing radiation. Mol. Cell. Biol. 22:1049–1059.
   PubMed Web of Science ®Google Scholar
• Zhao, H., J. L. Watkins, and H. Piwnica-Worms. 2002. Disruption of the checkpoint kinase 1/cell division cycle 25A pathway abrogates ionizing radiation-induced S and G2 checkpoints. Proc. Natl. Acad. Sci. USA 99:14795–14800.
   PubMed Web of Science ®Google Scholar