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Science 289 (5477): 304-306

Copyright © 2000 by the American Association for the Advancement of Science

An Anti-Apoptotic Role for the p53 Family Member, p73, During Developmental Neuron Death

Christine D. Pozniak, 1 Stevo Radinovic, 2 Annie Yang, 3 Frank McKeon, 3 David R. Kaplan, 12 Freda D. Miller 1*

p53 plays an essential pro-apoptotic role, a function thought to be shared with its family members p73 and p63. Here, we show that p73 is primarily present in developing neurons as a truncated isoform whose levels are dramatically decreased when sympathetic neurons apoptose after nerve growth factor (NGF) withdrawal. Increased expression of truncated p73 rescues these neurons from apoptosis induced by NGF withdrawal or p53 overexpression. In p73-/- mice, all isoforms of p73 are deleted and the apoptosis of developing sympathetic neurons is greatly enhanced. Thus, truncated p73 is an essential anti-apoptotic protein in neurons, serving to counteract the pro-apoptotic function of p53.

1 Center for Neuronal Survival,
2 Brain Tumor Research Center, Montreal Neurological Institute, McGill University, Montreal, Canada H3A 2B4.
3 Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA.
*   To whom correspondence should be addressed. E-mail: mdfm{at}

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   Abstract »    Full Text »    PDF »
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Development 133, 4783-4792
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Mdm2-mediated NEDD8 Modification of TAp73 Regulates Its Transactivation Function.
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J. Biol. Chem. 281, 34096-34103
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Wnt Activation and Alternative Promoter Repression of LEF1 in Colon Cancer.
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Mol. Cell. Biol. 26, 5284-5299
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Recombinant Adenoviral Vectors Can Induce Expression of p73 via the E4-orf6/7 Protein.
G. S. Shapiro, C. Van Peursem, D. A. Ornelles, J. Schaack, and J. DeGregori (2006)
J. Virol. 80, 5349-5360
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MEK1 inhibition sensitizes primary acute myelogenous leukemia to arsenic trioxide-induced apoptosis.
P. Lunghi, A. Costanzo, L. Salvatore, N. Noguera, L. Mazzera, A. Tabilio, F. Lo-Coco, M. Levrero, and A. Bonati (2006)
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{Delta}TAp73 Upregulation Correlates With Poor Prognosis in Human Tumors: Putative In Vivo Network Involving p73 Isoforms, p53, and E2F-1.
G. Dominguez, J. M. Garcia, C. Pena, J. Silva, V. Garcia, L. Martinez, C. Maximiano, M. E. Gomez, J. A. Rivera, C. Garcia-Andrade, et al. (2006)
J. Clin. Oncol. 24, 805-815
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The p53-homologue p63 may promote thyroid cancer progression.
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Endocr. Relat. Cancer 12, 953-971
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Family Members p53 and p73 Act Together in Chromatin Modification and Direct Repression of {alpha}-Fetoprotein Transcription.
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J. Biol. Chem. 280, 39152-39160
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p73 Interacts with Human Immunodeficiency Virus Type 1 Tat in Astrocytic Cells and Prevents Its Acetylation on Lysine 28.
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Mol. Cell. Biol. 25, 8126-8138
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p53: link to the past, bridge to the future.
A. A. Mills (2005)
Genes & Dev. 19, 2091-2099
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A Role of p73 in Mitotic Exit.
P. Merlo, M. Fulco, A. Costanzo, R. Mangiacasale, S. Strano, G. Blandino, Y. Taya, P. Lavia, and M. Levrero (2005)
J. Biol. Chem. 280, 30354-30360
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Transactivation-dependent and -independent Regulation of p73 Stability.
I. Dulloo and K. Sabapathy (2005)
J. Biol. Chem. 280, 28203-28214
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TNF-{alpha}-mediated apoptosis in vascular smooth muscle cells requires p73.
V. Tang, A. Dhirapong, A. P. Yabes, and R. H. Weiss (2005)
Am J Physiol Cell Physiol 289, C199-C206
   Abstract »    Full Text »    PDF »
Spatiotemporal Switch from {Delta}Np73 to TAp73 Isoforms during Nephrogenesis: IMPACT ON DIFFERENTIATION GENE EXPRESSION.
Z. Saifudeen, V. Diavolitsis, J. Stefkova, S. Dipp, H. Fan, and S. S. El-Dahr (2005)
J. Biol. Chem. 280, 23094-23102
   Abstract »    Full Text »    PDF »
Identification of Protein Kinase A Catalytic Subunit {beta} as a Novel Binding Partner of p73 and Regulation of p73 Function.
T. Hanamoto, T. Ozaki, K. Furuya, M. Hosoda, S. Hayashi, M. Nakanishi, H. Yamamoto, H. Kikuchi, S. Todo, and A. Nakagawara (2005)
J. Biol. Chem. 280, 16665-16675
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Differential Regulation of MDR1 Transcription by the p53 Family Members: ROLE OF THE DNA BINDING DOMAIN.
R. A. Johnson, E. M. Shepard, and K. W. Scotto (2005)
J. Biol. Chem. 280, 13213-13219
   Abstract »    Full Text »    PDF »
Ectopic Expression of p73{alpha}, but Not p73{beta}, Suppresses Myogenic Differentiation.
C.-Y. Li, J. Zhu, and J. Y. J. Wang (2005)
J. Biol. Chem. 280, 2159-2164
   Abstract »    Full Text »    PDF »
Developmental Roles of p73 in Cajal-Retzius Cells and Cortical Patterning.
G. Meyer, A. C. Socorro, C. G. P. Garcia, L. M. Millan, N. Walker, and D. Caput (2004)
J. Neurosci. 24, 9878-9887
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The Invulnerability of Adult Neurons: A Critical Role for p73.
G. S. Walsh, N. Orike, D. R. Kaplan, and F. D. Miller (2004)
J. Neurosci. 24, 9638-9647
   Abstract »    Full Text »    PDF »
c-Jun Regulates the Stability and Activity of the p53 Homologue, p73.
W. H. Toh, M. M. Siddique, L. Boominathan, K. W. Lin, and K. Sabapathy (2004)
J. Biol. Chem. 279, 44713-44722
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Expression of {Delta}Np73 Predicts Poor Prognosis in Lung Cancer.
H. Uramoto, K. Sugio, T. Oyama, S. Nakata, K. Ono, M. Morita, K. Funa, and K. Yasumoto (2004)
Clin. Cancer Res. 10, 6905-6911
   Abstract »    Full Text »    PDF »
Evidence That {Delta}Np73 Promotes Neuronal Survival by p53-Dependent and p53-Independent Mechanisms.
A. F. Lee, D. K. Ho, P. Zanassi, G. S. Walsh, D. R. Kaplan, and F. D. Miller (2004)
J. Neurosci. 24, 9174-9184
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Neuronal Survival and p73/p63/p53: A Family Affair.
W. B. Jacobs, G. S. Walsh, and F. D. Miller (2004)
Neuroscientist 10, 443-455
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Treatment with arsenic trioxide (ATO) and MEK1 inhibitor activates the p73-p53AIP1 apoptotic pathway in leukemia cells.
P. Lunghi, A. Costanzo, M. Levrero, and A. Bonati (2004)
Blood 104, 519-525
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p63 and p73: Roles in Development and Tumor Formation.
U. M. Moll and N. Slade (2004)
Mol. Cancer Res. 2, 371-386
   Abstract »    Full Text »    PDF »
Tumor Necrosis Factor Alpha-Induced Apoptosis Requires p73 and c-ABL Activation Downstream of RB Degradation.
B. N. Chau, T.-T. Chen, Y. Y. Wan, J. DeGregori, and J. Y. J. Wang (2004)
Mol. Cell. Biol. 24, 4438-4447
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p73{alpha} is a candidate effector in the p53 independent apoptosis pathway of cisplatin damaged primary murine colonocytes.
A Oniscu, N Sphyris, R G Morris, S Bader, and D J Harrison (2004)
J. Clin. Pathol. 57, 492-498
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p73 and Reelin in Cajal-Retzius Cells of the Developing Human Hippocampal Formation.
H. Abraham, C. G. Perez-Garcia, and G. Meyer (2004)
Cereb Cortex 14, 484-495
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Regulation of the MiTF/TFE bHLH-LZ transcription factors through restricted spatial expression and alternative splicing of functional domains.
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Nucleic Acids Res. 32, 2315-2322
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How Many Mutant p53 Molecules Are Needed To Inactivate a Tetramer?.
W. M. Chan, W. Y. Siu, A. Lau, and R. Y. C. Poon (2004)
Mol. Cell. Biol. 24, 3536-3551
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Nerve Growth Factor Withdrawal-mediated Apoptosis in Naive and Differentiated PC12 Cells through p53/Caspase-3-dependent and -independent Pathways.
H. Vaghefi, A. L. Hughes, and K. E. Neet (2004)
J. Biol. Chem. 279, 15604-15614
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N. Billon, A. Terrinoni, C. Jolicoeur, A. McCarthy, W. D. Richardson, G. Melino, and M. Raff (2004)
Development 131, 1211-1220
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{Delta}Np73{beta} Is Active in Transactivation and Growth Suppression.
G. Liu, S. Nozell, H. Xiao, and X. Chen (2004)
Mol. Cell. Biol. 24, 487-501
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Differential response of p53 target genes to p73 overexpression in SH-SY5Y neuroblastoma cell line.
D. Goldschneider, E. Blanc, G. Raguenez, M. Barrois, A. Legrand, G. Le Roux, H. Haddada, J. Benard, and S. Douc-Rasy (2004)
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SHP-1 negatively regulates neuronal survival by functioning as a TrkA phosphatase.
H. N. Marsh, C. I. Dubreuil, C. Quevedo, A. Lee, M. Majdan, G. S. Walsh, S. Hausdorff, F. A. Said, O. Zoueva, M. Kozlowski, et al. (2003)
J. Cell Biol. 163, 999-1010
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p73 Is Regulated by Phosphorylation at the G2/M Transition.
M. Fulco, A. Costanzo, P. Merlo, R. Mangiacasale, S. Strano, G. Blandino, C. Balsano, P. Lavia, and M. Levrero (2003)
J. Biol. Chem. 278, 49196-49202
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The Role of p63 and p73 in Tumor Formation and Progression: Coming of Age Toward Clinical Usefulness: Commentary re: F. Koga et al., Impaired p63 Expression Associates with Poor Prognosis and Uroplakin III Expression in Invasive Urothelial Carcinoma of the Bladder. Clin. Cancer Res., 9: 5501-5507, 2003, and P. Puig et al., p73 Expression in Human Normal and Tumor Tissues: Loss of p73{alpha} Expression Is Associated with Tumor Progression in Bladder Cancer. Clin. Cancer Res., 9: 5642-5651, 2003..
U. M. Moll (2003)
Clin. Cancer Res. 9, 5437-5441
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c-Abl Tyrosine Kinase Selectively Regulates p73 Nuclear Matrix Association.
M. Ben-Yehoyada, I. Ben-Dor, and Y. Shaul (2003)
J. Biol. Chem. 278, 34475-34482
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{Delta}Np73 Facilitates Cell Immortalization and Cooperates with Oncogenic Ras in Cellular Transformation In Vivo.
O. Petrenko, A. Zaika, and U. M. Moll (2003)
Mol. Cell. Biol. 23, 5540-5555
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Cyclin-dependent Kinases Phosphorylate p73 at Threonine 86 in a Cell Cycle-dependent Manner and Negatively Regulate p73.
C. Gaiddon, M. Lokshin, I. Gross, D. Levasseur, Y. Taya, J.-P. Loeffler, and C. Prives (2003)
J. Biol. Chem. 278, 27421-27431
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Exclusion of c-Abl from the Nucleus Restrains the p73 Tumor Suppression Function.
V. Vella, J. Zhu, F. Frasca, C.-Y. Li, P. Vigneri, R. Vigneri, and J. Y. J. Wang (2003)
J. Biol. Chem. 278, 25151-25157
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c-Abl Stabilizes p73 by a Phosphorylation-augmented Interaction.
K. K. C. Tsai and Z.-M. Yuan (2003)
Cancer Res. 63, 3418-3424
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Novel Cell-specific and Dominant Negative Anti-apoptotic Roles of p73 in Transformed Leukemia Cells.
W. J. Freebern, J. L. Smith, S. S. Chaudhry, C. M. Haggerty, and K. Gardner (2003)
J. Biol. Chem. 278, 2249-2255
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Overexpression of p73 causes apoptosis in vascular smooth muscle cells.
B. B. Davis, Y. Dong, and R. H. Weiss (2003)
Am J Physiol Cell Physiol 284, C16-C23
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A C-Terminal Inhibitory Domain Controls the Activity of p63 by an Intramolecular Mechanism.
Z. Serber, H. C. Lai, A. Yang, H. D. Ou, M. S. Sigal, A. E. Kelly, B. D. Darimont, P. H. G. Duijf, H. van Bokhoven, F. McKeon, et al. (2002)
Mol. Cell. Biol. 22, 8601-8611
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p73 Is Required for Survival and Maintenance of CNS Neurons.
C. D. Pozniak, F. Barnabe-Heider, V. V. Rymar, A. F. Lee, A. F. Sadikot, and F. D. Miller (2002)
J. Neurosci. 22, 9800-9809
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Identification of Direct p73 Target Genes Combining DNA Microarray and Chromatin Immunoprecipitation Analyses.
G. Fontemaggi, I. Kela, N. Amariglio, G. Rechavi, J. Krishnamurthy, S. Strano, A. Sacchi, D. Givol, and G. Blandino (2002)
J. Biol. Chem. 277, 43359-43368
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p73 Independent of c-Myc Represses Transcription of Platelet-derived Growth Factor {beta}-Receptor through Interaction with NF-Y.
A. Hackzell, H. Uramoto, H. Izumi, K. Kohno, and K. Funa (2002)
J. Biol. Chem. 277, 39769-39776
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{Delta}Np73, A Dominant-Negative Inhibitor of Wild-type p53 and TAp73, Is Up-regulated in Human Tumors.
A. I. Zaika, N. Slade, S. H. Erster, C. Sansome, T. W. Joseph, M. Pearl, E. Chalas, and U. M. Moll (2002)
J. Exp. Med. 196, 765-780
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Human Cytomegalovirus Induces Drug Resistance and Alteration of Programmed Cell Death by Accumulation of {Delta}N-p73{alpha}.
S. Allart, H. Martin, C. Detraves, J. Terrasson, D. Caput, and C. Davrinche (2002)
J. Biol. Chem. 277, 29063-29068
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c-jun is essential for sympathetic neuronal death induced by NGF withdrawal but not by p75 activation.
M. Palmada, S. Kanwal, N.J. Rutkoski, C. Gustafson-Brown, R.S. Johnson, R. Wisdom, and B.D. Carter (2002)
J. Cell Biol. 158, 453-461
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Transactivation-deficient {Delta}TA-p73 Acts as an Oncogene.
T. Stiewe, S. Zimmermann, A. Frilling, H. Esche, and B. M. Putzer (2002)
Cancer Res. 62, 3598-3602
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Expression of p73 and Reelin in the Developing Human Cortex.
G. Meyer, C. G. Perez-Garcia, H. Abraham, and D. Caput (2002)
J. Neurosci. 22, 4973-4986
   Abstract »    Full Text »    PDF »
A Role for p53 in Maintaining and Establishing the Quiescence Growth Arrest in Human Cells.
K. Itahana, G. P. Dimri, E. Hara, Y. Itahana, Y. Zou, P.-Y. Desprez, and J. Campisi (2002)
J. Biol. Chem. 277, 18206-18214
   Abstract »    Full Text »    PDF »
Physical Interaction of p73 with c-Myc and MM1, a c-Myc-binding Protein, and Modulation of the p73 Function.
K.-i. Watanabe, T. Ozaki, T. Nakagawa, K. Miyazaki, M. Takahashi, M. Hosoda, S. Hayashi, S. Todo, and A. Nakagawara (2002)
J. Biol. Chem. 277, 15113-15123
   Abstract »    Full Text »    PDF »
Autoinhibitory Regulation of p73 by {Delta}Np73 To Modulate Cell Survival and Death through a p73-Specific Target Element within the {Delta}Np73 Promoter.
T. Nakagawa, M. Takahashi, T. Ozaki, K.-i. Watanabe, S. Todo, H. Mizuguchi, T. Hayakawa, and A. Nakagawara (2002)
Mol. Cell. Biol. 22, 2575-2585
   Abstract »    Full Text »    PDF »
Transactivation-deficient Delta TA-p73 Inhibits p53 by Direct Competition for DNA Binding. IMPLICATIONS FOR TUMORIGENESIS.
T. Stiewe, C. C. Theseling, and B. M. Putzer (2002)
J. Biol. Chem. 277, 14177-14185
   Abstract »    Full Text »    PDF »
Possible Oncogenic Potential of {Delta}Np73: A Newly Identified Isoform of Human p73.
O. Ishimoto, C. Kawahara, K. Enjo, M. Obinata, T. Nukiwa, and S. Ikawa (2002)
Cancer Res. 62, 636-641
   Abstract »    Full Text »    PDF »
N-myc Promotes Survival and Induces S-Phase Entry of Postmitotic Sympathetic Neurons.
K. Wartiovaara, F. Barnabe-Heider, F. D. Miller, and D. R. Kaplan (2002)
J. Neurosci. 22, 815-824
   Abstract »    Full Text »    PDF »
The Transcriptional Repressor ZEB Regulates p73 Expression at the Crossroad between Proliferation and Differentiation.
G. Fontemaggi, A. Gurtner, S. Strano, Y. Higashi, A. Sacchi, G. Piaggio, and G. Blandino (2001)
Mol. Cell. Biol. 21, 8461-8470
   Abstract »    Full Text »    PDF »
Cyclin-Dependent Kinases and P53 Pathways Are Activated Independently and Mediate Bax Activation in Neurons after DNA Damage.
E. J. Morris, E. Keramaris, H. J. Rideout, R. S. Slack, N. J. Dyson, L. Stefanis, and D. S. Park (2001)
J. Neurosci. 21, 5017-5026
   Abstract »    Full Text »    PDF »

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