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Science 5 September 1997:
Vol. 277. no. 5331, pp. 1501 - 1505
DOI: 10.1126/science.277.5331.1501
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Reports

Mitotic and G2 Checkpoint Control: Regulation of 14-3-3 Protein Binding by Phosphorylation of Cdc25C on Serine-216

Cheng-Yuan Peng, Paul R. Graves, Richard S. Thoma, Zhiqi Wu, Andrey S. Shaw, Helen Piwnica-Worms *

Human Cdc25C is a dual-specificity protein phosphatase that controls entry into mitosis by dephosphorylating the protein kinase Cdc2. Throughout interphase, but not in mitosis, Cdc25C was phosphorylated on serine-216 and bound to members of the highly conserved and ubiquitously expressed family of 14-3-3 proteins. A mutation preventing phosphorylation of serine-216 abrogated 14-3-3 binding. Conditional overexpression of this mutant perturbed mitotic timing and allowed cells to escape the G2 checkpoint arrest induced by either unreplicated DNA or radiation-induced damage. Chk1, a fission yeast kinase involved in the DNA damage checkpoint response, phosphorylated Cdc25C in vitro on serine-216. These results indicate that serine-216 phosphorylation and 14-3-3 binding negatively regulate Cdc25C and identify Cdc25C as a potential target of checkpoint control in human cells.

C.-Y. Peng, Department of Cell Biology and Physiology, Washington University School of Medicine, 660 South Euclid Avenue, St. Louis, MO 63110, USA, and Committee on Virology, Harvard Medical School, 200 Longwood Avenue, Boston, MA 02115, USA.
P. R. Graves, Department of Cell Biology and Physiology, Washington University School of Medicine, 660 South Euclid Avenue, St. Louis, MO 63110, USA.
R. S. Thoma, Z. Wu, H. Piwnica-Worms, Department of Cell Biology and Physiology, Washington University School of Medicine, 660 South Euclid Avenue, St. Louis, MO 63110, USA, and Howard Hughes Medical Institute, Washington University School of Medicine, 660 South Euclid Avenue, St. Louis, MO 63110, USA.
A. S. Shaw, Department of Pathology, Washington University School of Medicine, 660 South Euclid Avenue, St. Louis, MO 63110, USA.
*   To whom correspondence should be addressed. E-mail: hpiwnica{at}cellbio.wustl.edu

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Sulforaphane-induced G2/M Phase Cell Cycle Arrest Involves Checkpoint Kinase 2-mediated Phosphorylation of Cell Division Cycle 25C.
S. V. Singh, A. Herman-Antosiewicz, A. V. Singh, K. L. Lew, S. K. Srivastava, R. Kamath, K. D. Brown, L. Zhang, and R. Baskaran (2004)
J. Biol. Chem. 279, 25813-25822
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DNA damage responses triggered by a highly cytotoxic monofunctional DNA alkylator, hedamycin, a pluramycin antitumor antibiotic.
L. C. Tu, T. Melendy, and T. A. Beerman (2004)
Mol. Cancer Ther. 3, 577-586
   Abstract »    Full Text »    PDF »
Unlocking the code of 14-3-3.
M. K. Dougherty and D. K. Morrison (2004)
J. Cell Sci. 117, 1875-1884
   Abstract »    Full Text »    PDF »
G2 checkpoint abrogators as anticancer drugs.
T. Kawabe (2004)
Mol. Cancer Ther. 3, 513-519
   Abstract »    Full Text »    PDF »
Isoform-specific differences in rapid nucleocytoplasmic shuttling cause distinct subcellular distributions of 14-3-3{sigma} and 14-3-3{zeta}.
M. J. van Hemert, M. Niemantsverdriet, T. Schmidt, C. Backendorf, and H. P. Spaink (2004)
J. Cell Sci. 117, 1411-1420
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Differential Mode of Regulation of the Checkpoint Kinases CHK1 and CHK2 by Their Regulatory Domains.
C.-P. Ng, H. C. Lee, C. W. Ho, T. Arooz, W. Y. Siu, A. Lau, and R. Y. C. Poon (2004)
J. Biol. Chem. 279, 8808-8819
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Recovery from DNA Damage-induced G2 Arrest Requires Actin-binding Protein Filamin-A/Actin-binding Protein 280.
X. Meng, Y. Yuan, A. Maestas, and Z. Shen (2004)
J. Biol. Chem. 279, 6098-6105
   Abstract »    Full Text »    PDF »
Dysregulation of the Polo-Like Kinase Pathway in CD4+ T Cells Is Characteristic of Pathogenic Simian Immunodeficiency Virus Infection.
P. Bostik, G. L. Dodd, F. Villinger, A. E. Mayne, and A. A. Ansari (2004)
J. Virol. 78, 1464-1472
   Abstract »    Full Text »    PDF »
Hyperoxia activates the ATR-Chk1 pathway and phosphorylates p53 at multiple sites.
K. C. Das and R. Dashnamoorthy (2004)
Am J Physiol Lung Cell Mol Physiol 286, L87-L97
   Abstract »    Full Text »    PDF »
Wee1-dependent mechanisms required for coordination of cell growth and cell division.
D. R. Kellogg (2003)
J. Cell Sci. 116, 4883-4890
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SCF{beta}-TRCP links Chk1 signaling to degradation of the Cdc25A protein phosphatase.
J. Jin, T. Shirogane, L. Xu, G. Nalepa, J. Qin, S. J. Elledge, and J. W. Harper (2003)
Genes & Dev. 17, 3062-3074
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Functions of Saccharomyces cerevisiae 14-3-3 Proteins in Response to DNA Damage and to DNA Replication Stress.
F. Lottersberger, F. Rubert, V. Baldo, G. Lucchini, and M. P. Longhese (2003)
Genetics 165, 1717-1732
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Chk1 Kinase Negatively Regulates Mitotic Function of Cdc25A Phosphatase through 14-3-3 Binding.
M.-S. Chen, C. E. Ryan, and H. Piwnica-Worms (2003)
Mol. Cell. Biol. 23, 7488-7497
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DNA Damage-induced G2/M Checkpoint in SV40 Large T Antigen-immortalized Embryonic Fibroblast Cells Requires SHP-2 Tyrosine Phosphatase.
L. Yuan, W.-M. Yu, and C.-K. Qu (2003)
J. Biol. Chem. 278, 42812-42820
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Regulation of Cdc2/Cyclin B Activation in Xenopus Egg Extracts via Inhibitory Phosphorylation of Cdc25C Phosphatase by Ca2+/Calmodium-dependent Kinase II.
J. R. A. Hutchins, D. Dikovskaya, and P. R. Clarke (2003)
Mol. Biol. Cell 14, 4003-4014
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Regulation of Molecular Chaperone Gene Transcription Involves the Serine Phosphorylation, 14-3-3{varepsilon} Binding, and Cytoplasmic Sequestration of Heat Shock Factor 1.
X. Wang, N. Grammatikakis, A. Siganou, and S. K. Calderwood (2003)
Mol. Cell. Biol. 23, 6013-6026
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Regulation of Cdc25A Half-life in Interphase by Cyclin-dependent Kinase 2 Activity.
A. P. Ducruet and J. S. Lazo (2003)
J. Biol. Chem. 278, 31838-31842
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Phosphorylation at Serine 75 Is Required for UV-mediated Degradation of Human Cdc25A Phosphatase at the S-phase Checkpoint.
I. Hassepass, R. Voit, and I. Hoffmann (2003)
J. Biol. Chem. 278, 29824-29829
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Regulatory Interactions between the Checkpoint Kinase Chk1 and the Proteins of the DNA-dependent Protein Kinase Complex.
D. M. Goudelock, K. Jiang, E. Pereira, B. Russell, and Y. Sanchez (2003)
J. Biol. Chem. 278, 29940-29947
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14-3-3 Acts as an Intramolecular Bridge to Regulate cdc25B Localization and Activity.
N. Giles, A. Forrest, and B. Gabrielli (2003)
J. Biol. Chem. 278, 28580-28587
   Abstract »    Full Text »    PDF »


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