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Science 29 March 1996:
Vol. 271. no. 5257, pp. 1861 - 1864
DOI: 10.1126/science.271.5257.1861
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Reports

Translational Control of p27Kip1 Accumulation During the Cell Cycle

Ludger Hengst and Steven I. Reed *

Cell cycle phase transitions in eukaryotic cells are driven by regulation of the activity of protein kinases known as cyclin-dependent kinases (Cdks). A broad spectrum Cdk-inhibitory activity associated with a 28-kilodalton protein (p28Ick1) was induced in cells treated with the drug lovastatin or upon density-mediated growth arrest and was periodic in the cell cycle, with peak activity in G1. The p28Ick1 protein was shown to be identical to p27Kip1, and the periodic or induced inhibitory activity resulted from a periodic accumulation of the protein. Variations in the amount of p27 protein occurred, whereas the abundance of the p27 messenger RNA remained unchanged. In every instance investigated, the posttranscriptional alteration of p27 protein levels was achieved in part by a mechanism of translational control, although in density-arrested fibroblasts and thymidine-arrested HeLa cells the half-life of the protein was also changed.

Department of Molecular Biology, MB-7, Scripps Research Institute, 10666 North Torrey Pines Road, La Jolla, CA 92037, USA.
* To whom correspondence should be addressed.


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F. J. Esteva, A. A. Sahin, G. Z. Rassidakis, L. X. H. Yuan, T. L. Smith, Y. Yang, M. Z. Gilcrease, M. Cristofanilli, R. Nahta, L. Pusztai, et al. (2003)
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X. Deng, F. Gao, and W. S. May Jr. (2003)
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p21-dependent Inhibition of Colon Cancer Cell Growth by Mevastatin Is Independent of Inhibition of G1 Cyclin-dependent Kinases.
C. Ukomadu and A. Dutta (2003)
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Estrogens Down-regulate p27Kip1 in Breast Cancer Cells through Skp2 and through Nuclear Export Mediated by the ERK Pathway.
J. S. Foster, R. I. Fernando, N. Ishida, K. I. Nakayama, and J. Wimalasena (2003)
J. Biol. Chem. 278, 41355-41366
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2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) Alters the Regulation and Posttranslational Modification of p27kip1 in Lipopolysaccharide-Activated B Cells.
R. B. Crawford, C. E. W. Sulentic, B. S. Yoo, and N. E. Kaminski (2003)
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EIF3 p170, a Mediator of Mimosine Effect on Protein Synthesis and Cell Cycle Progression.
Z. Dong and J.-T. Zhang (2003)
Mol. Biol. Cell 14, 3942-3951
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11,12-Epoxyeicosatrienoic Acid-induced Inhibition of FOXO Factors Promotes Endothelial Proliferation by Down-Regulating p27Kip1.
M. Potente, B. Fisslthaler, R. Busse, and I. Fleming (2003)
J. Biol. Chem. 278, 29619-29625
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Mechanosensitive p27Kip1 Regulation and Cell Cycle Entry in Vascular Smooth Muscle Cells.
D. G. Sedding, U. Seay, L. Fink, M. Heil, W. Kummer, H. Tillmanns, and R. C. Braun-Dullaeus (2003)
Circulation 108, 616-622
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Cell cycle-dependent translation of p27 involves a responsive element in its 5'-UTR that overlaps with a uORF.
U. Gopfert, M. Kullmann, and L. Hengst (2003)
Hum. Mol. Genet. 12, 1767-1779
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p27 Labeling Index and Proliferation in Gastrointestinal Stromal Tumors: Correlations with Clinicopathologic Factors and Recurrence.
T. Gelen, G. O. Elpek, N. H. Aksoy, M. Ogus, and N. Keles (2003)
Jpn. J. Clin. Oncol. 33, 346-352
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The Role of Cyclin-dependent Kinase Inhibitor p27Kip1 in Anti-HER2 Antibody-induced G1 Cell Cycle Arrest and Tumor Growth Inhibition.
X.-F. Le, F.-X. Claret, A. Lammayot, L. Tian, D. Deshpande, R. LaPushin, A. M. Tari, and R. C. Bast Jr. (2003)
J. Biol. Chem. 278, 23441-23450
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Regulation and role of p21 and p27 cyclin-dependent kinase inhibitors during hepatocyte differentiation and growth.
G. P. Ilyin, D. Glaise, D. Gilot, G. Baffet, and C. Guguen-Guillouzo (2003)
Am J Physiol Gastrointest Liver Physiol 285, G115-G127
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Activating Transcription Factor 4 Overexpression Inhibits Proliferation and Differentiation of Mammary Epithelium Resulting in Impaired Lactation and Accelerated Involution.
R. Bagheri-Yarmand, R. K. Vadlamudi, and R. Kumar (2003)
J. Biol. Chem. 278, 17421-17429
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Inhibition of Cdk4 Activity Enhances Translation of p27kip1 in Quiescent Rb-negative Cells.
T. Gonzalez, M. Seoane, P. Caamano, J. Vinuela, F. Dominguez, and J. Zalvide (2003)
J. Biol. Chem. 278, 12688-12695
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Regulatory Role of PI 3-Kinase on Expression of Cdk4 and p27, Nuclear Localization of Cdk4, and Phosphorylation of p27 in Corneal Endothelial Cells.
H. T. Lee and E. P. Kay (2003)
Invest. Ophthalmol. Vis. Sci. 44, 1521-1528
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MAP Kinase-dependent Degradation of p27Kip1 by Calpains in Choroidal Melanoma Cells. REQUIREMENT OF p27Kip1 NUCLEAR EXPORT.
C. Delmas, N. Aragou, S. Poussard, P. Cottin, J.-M. Darbon, and S. Manenti (2003)
J. Biol. Chem. 278, 12443-12451
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Posttranscriptional and Posttranslational Regulation of C/EBPdelta in G0 Growth-arrested Mammary Epithelial Cells.
L. R. Dearth and J. DeWille (2003)
J. Biol. Chem. 278, 11246-11255
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Treatment of Relapsing Paralysis in Experimental Encephalomyelitis by Targeting Th1 Cells through Atorvastatin.
O. Aktas, S. Waiczies, A. Smorodchenko, J. Dorr, B. Seeger, T. Prozorovski, S. Sallach, M. Endres, S. Brocke, R. Nitsch, et al. (2003)
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K. A. Serikawa, X. L. Xu, V. L. MacKay, G. L. Law, Q. Zong, L. P. Zhao, R. Bumgarner, and D. R. Morris (2003)
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   Abstract »    Full Text »    PDF »
A Member of Forkhead Transcription Factor FKHRL1 Is a Downstream Effector of STI571-induced Cell Cycle Arrest in BCR-ABL-expressing Cells.
N. Komatsu, T. Watanabe, M. Uchida, M. Mori, K. Kirito, S. Kikuchi, Q. Liu, T. Tauchi, K. Miyazawa, H. Endo, et al. (2003)
J. Biol. Chem. 278, 6411-6419
   Abstract »    Full Text »    PDF »
Genetic rescue of cell number in a mouse model of microphthalmia: interactions between Chx10 and G1-phase cell cycle regulators.
E. S. Green, J. L. Stubbs, and E. M. Levine (2003)
Development 130, 539-552
   Abstract »    Full Text »    PDF »
PAX3-FKHR Transformation Increases 26 S Proteasome-dependent Degradation of p27Kip1, a Potential Role for Elevated Skp2 Expression.
L. Zhang and C. Wang (2003)
J. Biol. Chem. 278, 27-36
   Abstract »    Full Text »    PDF »
Weekly High-Dose Calcitriol and Docetaxel in Metastatic Androgen-Independent Prostate Cancer.
T. M. Beer, K. M. Eilers, M. Garzotto, M. J. Egorin, B. A. Lowe, and W. D. Henner (2003)
J. Clin. Oncol. 21, 123-128
   Abstract »    Full Text »    PDF »
CRM1/Ran-Mediated Nuclear Export of p27Kip1 Involves a Nuclear Export Signal and Links p27 Export and Proteolysis.
M. K. Connor, R. Kotchetkov, S. Cariou, A. Resch, R. Lupetti, R. G. Beniston, F. Melchior, L. Hengst, and J. M. Slingerland (2003)
Mol. Biol. Cell 14, 201-213
   Abstract »    Full Text »
ELAV/Hu proteins inhibit p27 translation via an IRES element in the p27 5'UTR.
M. Kullmann, U. Gopfert, B. Siewe, and L. Hengst (2002)
Genes & Dev. 16, 3087-3099
   Abstract »    Full Text »    PDF »
Hydroxymethylglutaryl Coenzyme A Reductase Inhibitor Simvastatin Prevents Cardiac Hypertrophy Induced by Pressure Overload and Inhibits p21ras Activation.
C. Indolfi, E. Di Lorenzo, C. Perrino, A. M. Stingone, A. Curcio, D. Torella, A. Cittadini, L. Cardone, C. Coppola, L. Cavuto, et al. (2002)
Circulation 106, 2118-2124
   Abstract »    Full Text »    PDF »
Expression of Skp2, a p27Kip1 ubiquitin ligase, in malignant lymphoma: correlation with p27Kip1 and proliferation index.
M. S. Lim, A. Adamson, Z. Lin, B. Perez-Ordonez, R. C. K. Jordan, S. Tripp, S. L. Perkins, and K. S. J. Elenitoba-Johnson (2002)
Blood 100, 2950-2956
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Early Cycling-independent Changes to p27, Cyclin D2, and Cyclin D3 in Differentiating Mouse Embryonal Carcinoma Cells.
H. Preclikova, V. Bryja, J. Pachernik, P. Krejci, P. Dvorak, and A. Hampl (2002)
Cell Growth Differ. 13, 421-430
   Abstract »    Full Text »    PDF »
Akt-dependent Phosphorylation of p27Kip1 Promotes Binding to 14-3-3 and Cytoplasmic Localization.
N. Fujita, S. Sato, K. Katayama, and T. Tsuruo (2002)
J. Biol. Chem. 277, 28706-28713
   Abstract »    Full Text »    PDF »
Mechanisms of Mitotic Inhibition in Corneal Endothelium: Contact Inhibition and TGF-{beta}2.
N. C. Joyce, D. L. Harris, and D. M. Mello (2002)
Invest. Ophthalmol. Vis. Sci. 43, 2152-2159
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Clinical and Biological Significance of S-Phase Kinase-associated Protein 2 (Skp2) Gene Expression in Gastric Carcinoma: Modulation of Malignant Phenotype by Skp2 Overexpression, Possibly via p27 Proteolysis.
T.-a. Masuda, H. Inoue, H. Sonoda, S. Mine, Y. Yoshikawa, K. Nakayama, K.-I. Nakayama, and M. Mori (2002)
Cancer Res. 62, 3819-3825
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Rho Activity Can Alter the Translation of p27 mRNA and Is Important for RasV12-induced Transformation in a Manner Dependent on p27 Status.
A. Vidal, S. S. Millard, J. P. Miller, and A. Koff (2002)
J. Biol. Chem. 277, 16433-16440
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Altered p27Kip1 Phosphorylation, Localization, and Function in Human Epithelial Cells Resistant to Transforming Growth Factor {beta}-Mediated G1 Arrest.
S. Ciarallo, V. Subramaniam, W. Hung, J.-H. Lee, R. Kotchetkov, C. Sandhu, A. Milic, and J. M. Slingerland (2002)
Mol. Cell. Biol. 22, 2993-3002
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Scatter Factor/Hepatocyte Growth Factor Stimulation of Glioblastoma Cell Cycle Progression through G1 Is c-Myc Dependent and Independent of p27 Suppression, Cdk2 Activation, or E2F1-Dependent Transcription.
K. A. Walter, M. A. Hossain, C. Luddy, N. Goel, T. E. Reznik, and J. Laterra (2002)
Mol. Cell. Biol. 22, 2703-2715
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Heterogeneous Methylation and Deletion Patterns of the INK4a/ARF Locus Within Prostate Carcinomas.
N. Konishi, M. Nakamura, M. Kishi, M. Nishimine, E. Ishida, and K. Shimada (2002)
Am. J. Pathol. 160, 1207-1214
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Transforming growth factor beta 1 mediates cell-cycle arrest of primitive hematopoietic cells independent of p21Cip1/Waf1 or p27Kip1.
T. Cheng, H. Shen, N. Rodrigues, S. Stier, and D. T. Scadden (2001)
Blood 98, 3643-3649
   Abstract »    Full Text »    PDF »


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