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Science 302 (5652): 1972-1975

Copyright © 2003 by the American Association for the Advancement of Science

Mono- Versus Polyubiquitination: Differential Control of p53 Fate by Mdm2

Muyang Li, Christopher L. Brooks, Foon Wu-Baer, Delin Chen, Richard Baer, Wei Gu*

Abstract: Although Mdm2-mediated ubiquitination is essential for both degradation and nuclear export of p53, the molecular basis for the differential effects of Mdm2 remains unknown. Here we show that low levels of Mdm2 activity induce monoubiquitination and nuclear export of p53, whereas high levels promote p53's polyubiquitination and nuclear degradation. A p53-ubiquitin fusion protein that mimics monoubiquitinated p53 was found to accumulate in the cytoplasm in an Mdm2-independent manner, indicating that monoubiquitination is critical for p53 trafficking. These results clarify the nature of ubiquitination-mediated p53 regulation and suggest that distinct mechanisms regulate p53 function in accordance with the levels of Mdm2 activity.

Institute for Cancer Genetics and Department of Pathology, College of Physicians & Surgeons, Columbia University, 1150 St. Nicholas Avenue, New York, NY 10032, USA.

* To whom correspondence should be addressed. E-mail: wg8{at}

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B. Guan, P. Pungaliya, X. Li, C. Uquillas, L. N. Mutton, E. H. Rubin, and C. J. Bieberich (2008)
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Z. Matijasevic, H. A. Steinman, K. Hoover, and S. N. Jones (2008)
Mol. Cell. Biol. 28, 1265-1273
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S. M. Planchon, K. A. Waite, and C. Eng (2008)
J. Cell Sci. 121, 249-253
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Regulation of p53 tetramerization and nuclear export by ARC.
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Site-specific ubiquitination exposes a linear motif to promote interferon-{alpha} receptor endocytosis.
K.G. S. Kumar, H. Barriere, C. J. Carbone, J. Liu, G. Swaminathan, P. Xu, Y. Li, D. P. Baker, J. Peng, G. L. Lukacs, et al. (2007)
J. Cell Biol. 179, 935-950
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A High-Throughput Screen Measuring Ubiquitination of p53 by Human mdm2.
M. F. Murray, A. J. Jurewicz, J. D. Martin, T. F. Ho, Hong Zhang, K. O. Johanson, R. B. Kirkpatrick, Jianhong Ma, L. A. Lor, S. H. Thrall, et al. (2007)
J Biomol Screen 12, 1050-1058
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NM23-H1 Tumor Suppressor and Its Interacting Partner STRAP Activate p53 Function.
H. Jung, H.-A. Seong, and H. Ha (2007)
J. Biol. Chem. 282, 35293-35307
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Stabilization of p53 in Human Cytomegalovirus-initiated Cells Is Associated with Sequestration of HDM2 and Decreased p53 Ubiquitination.
Z. Chen, E. Knutson, S. Wang, L. A. Martinez, and T. Albrecht (2007)
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Regulation of p53 Nuclear Export through Sequential Changes in Conformation and Ubiquitination.
L. Nie, M. Sasaki, and C. G. Maki (2007)
J. Biol. Chem. 282, 14616-14625
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MDM2 Binding Induces a Conformational Change in p53 That Is Opposed by Heat-shock Protein 90 and Precedes p53 Proteasomal Degradation.
M. Sasaki, L. Nie, and C. G. Maki (2007)
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Ubiquitin and Ubiquitin-Like Proteins in Protein Regulation.
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Circ. Res. 100, 1276-1291
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beta-Arrestin and Mdm2 Mediate IGF-1 Receptor-stimulated ERK Activation and Cell Cycle Progression.
L. Girnita, S. K. Shenoy, B. Sehat, R. Vasilcanu, D. Vasilcanu, A. Girnita, R. J. Lefkowitz, and O. Larsson (2007)
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Mitogen-Activated Protein Kinase Kinase Inhibition Enhances Nuclear Proapoptotic Function of p53 in Acute Myelogenous Leukemia Cells.
K. Kojima, M. Konopleva, I. J. Samudio, V. Ruvolo, and M. Andreeff (2007)
Cancer Res. 67, 3210-3219
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The p53 Isoform {Delta}p53 Lacks Intrinsic Transcriptional Activity and Reveals the Critical Role of Nuclear Import in Dominant-Negative Activity.
W. M. Chan and R. Y.C. Poon (2007)
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Monoubiquitylation promotes mitochondrial p53 translocation.
N. D. Marchenko, S. Wolff, S. Erster, K. Becker, and U. M. Moll (2007)
EMBO J. 26, 923-934
   Abstract »    Full Text »    PDF »
CIN85, a Cbl-interacting protein, is a component of AMAP1-mediated breast cancer invasion machinery.
J.-M. Nam, Y. Onodera, Y. Mazaki, H. Miyoshi, S. Hashimoto, and H. Sabe (2007)
EMBO J. 26, 647-656
   Abstract »    Full Text »    PDF »
Cancer-Associated Mutations in the MDM2 Zinc Finger Domain Disrupt Ribosomal Protein Interaction and Attenuate MDM2-Induced p53 Degradation.
M. S. Lindstrom, A. Jin, C. Deisenroth, G. White Wolf, and Y. Zhang (2007)
Mol. Cell. Biol. 27, 1056-1068
   Abstract »    Full Text »    PDF »
FBXO11 Promotes the Neddylation of p53 and Inhibits Its Transcriptional Activity.
W. M. Abida, A. Nikolaev, W. Zhao, W. Zhang, and W. Gu (2007)
J. Biol. Chem. 282, 1797-1804
   Abstract »    Full Text »    PDF »
Outcomes of p53 activation - spoilt for choice.
K. H. Vousden (2006)
J. Cell Sci. 119, 5015-5020
   Abstract »    Full Text »    PDF »
Regulation of p53 Localization and Activity by Ubc13.
A. Laine, I. Topisirovic, D. Zhai, J. C. Reed, K. L. B. Borden, and Z. Ronai (2006)
Mol. Cell. Biol. 26, 8901-8913
   Abstract »    Full Text »    PDF »
MDM2 Is Required for Suppression of Apoptosis by Activated Akt1 in Salivary Acinar Cells.
K. H. Limesand, K. L. Schwertfeger, and S. M. Anderson (2006)
Mol. Cell. Biol. 26, 8840-8856
   Abstract »    Full Text »    PDF »
p53-Independent Induction of Rat Hepatic Mdm2 following Administration of Phenobarbital and Pregnenolone 16{alpha}-Carbonitrile.
D. M. Nelson, V. Bhaskaran, W. R. Foster, and L. D. Lehman-McKeeman (2006)
Toxicol. Sci. 94, 272-280
   Abstract »    Full Text »    PDF »
Posttranslational Modification and Cell Type-Specific Degradation of Varicella-Zoster Virus ORF29p.
C. L. Stallings and S. J. Silverstein (2006)
J. Virol. 80, 10836-10846
   Abstract »    Full Text »    PDF »

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