Activation and activities of the p53 tumour suppressor protein

Abstract

The p53 tumour suppressor protein inhibits malignant progression by mediating cell cycle arrest, apoptosis or repair following cellular stress. One of the major regulators of p53 function is the MDM2 protein, and multiple forms of cellular stress activate p53 by inhibiting the MDM2-mediated degradation of p53. Mutations in p53, or disruption of the pathways that allow activation of p53, seem to be a general feature of all cancers. Here we review recent advances in our understanding of the pathways that regulate p53 and the pathways that are induced by p53, as well as their implications for cancer therapy.

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    Not checked
94. 94.

    Komarov P. G., Komarova E. A., Kondratov R. V., Christov-Tselkov K., Coon J. S., Chernov M. V., Gudkov A. V. A chemical inhibitor of p53 that protects mice from the side effects of cancer therapy. Science. 1999;285(5434):1733-1737.

    Not in our library10.1126/science.285.5434.1733

95. 95.

    Koumenis C., Alarcon R., Hammond E., Sutphin P., Hoffman W., Murphy M., Derr J., Taya Y., Lowe S. W., Kastan M. Regulation of p53 by hypoxia: dissociation of transcriptional repression and apoptosis from p53-dependent transactivation. Mol Cell Biol. 2001;21(4):1297-1310.

    Not in our library10.1128/mcb.21.4.1297-1310.2001

96. 96.

    Kubbutat M. H., Jones S. N., Vousden K. H. Regulation of p53 stability by Mdm2. Nature. 1997;387(6630):299-303.

    Not in our library10.1038/387299a0

97. 97.

    Kubbutat M. H., Ludwig R. L., Levine A. J., Vousden K. H. Analysis of the degradation function of Mdm2. Cell Growth Differ. 1999;10(2):87-92.

    Not in our library

98. 98.

    Kubbutat M. H., Vousden K. H. Proteolytic cleavage of human p53 by calpain: a potential regulator of protein stability. Mol Cell Biol. 1997;17(1):460-468.

    Not in our library10.1128/mcb.17.1.460

99. 99.

    Lakin N. D., Jackson S. P. Regulation of p53 in response to DNA damage. Oncogene. 1999;18(53):7644-7655.

    Not in our library10.1038/sj.onc.1203015

100. 100.

     Laín S., Midgley C., Sparks A., Lane E. B., Lane D. P. An inhibitor of nuclear export activates the p53 response and induces the localization of HDM2 and p53 to U1A-positive nuclear bodies associated with the PODs. Exp Cell Res. 1999;248(2):457-472.

     Not in our library10.1006/excr.1999.4433

101. 101.

     Li P. F., Dietz R., von Harsdorf R. p53 regulates mitochondrial membrane potential through reactive oxygen species and induces cytochrome c-independent apoptosis blocked by Bcl-2. EMBO J. 1999;18(21):6027-6036.

     Not in our library10.1093/emboj/18.21.6027

102. 102.

     Lin Y., Benchimol S. Cytokines inhibit p53-mediated apoptosis but not p53-mediated G1 arrest. Mol Cell Biol. 1995;15(11):6045-6054.

     Not in our library10.1128/mcb.15.11.6045

103. 103.

     Lin Y., Ma W., Benchimol S. Pidd, a new death-domain-containing protein, is induced by p53 and promotes apoptosis. Nat Genet. 2000;26(1):122-127.

     Not in our library10.1038/79102

104. 104.

     Liu L., Scolnick D. M., Trievel R. C., Zhang H. B., Marmorstein R., Halazonetis T. D., Berger S. L. p53 sites acetylated in vitro by PCAF and p300 are acetylated in vivo in response to DNA damage. Mol Cell Biol. 1999;19(2):1202-1209.

     Not in our library10.1128/mcb.19.2.1202

105. 105.

     Ljungman M. Dial 9-1-1 for p53: mechanisms of p53 activation by cellular stress. Neoplasia. 2000;2(3):208-225.

     Not in our library10.1038/sj.neo.7900073

106. 106.

     Lohrum M. A., Ashcroft M., Kubbutat M. H., Vousden K. H. Identification of a cryptic nucleolar-localization signal in MDM2. Nat Cell Biol. 2000;2(3):179-181.

     Not in our library10.1038/35004057

107. 107.

     Lohrum M., Scheidtmann K. H. Differential effects of phosphorylation of rat p53 on transactivation of promoters derived from different p53 responsive genes. Oncogene. 1996;13(12):2527-2539.

     Not in our library

108. 108.

     Loughran O., La Thangue N. B. Apoptotic and growth-promoting activity of E2F modulated by MDM2. Mol Cell Biol. 2000;20(6):2186-2197.

     Not in our library10.1128/mcb.20.6.2186-2197.2000

109. 109.

     Lu W., Pochampally R., Chen L., Traidej M., Wang Y., Chen J. Nuclear exclusion of p53 in a subset of tumors requires MDM2 function. Oncogene. 2000;19(2):232-240.

     Not in our library10.1038/sj.onc.1203262

110. 110.

     Lundberg A. S., Hahn W. C., Gupta P., Weinberg R. A. Genes involved in senescence and immortalization. Curr Opin Cell Biol. 2000;12(6):705-709.

     Not in our library10.1016/s0955-0674(00)00155-1

111. 111.

     Lundgren K., Montes de Oca Luna R., McNeill Y. B., Emerick E. P., Spencer B., Barfield C. R., Lozano G., Rosenberg M. P., Finlay C. A. Targeted expression of MDM2 uncouples S phase from mitosis and inhibits mammary gland development independent of p53. Genes Dev. 1997;11(6):714-725.

     Not in our library10.1101/gad.11.6.714

112. 112.

     Luo J., Su F., Chen D., Shiloh A., Gu W. Deacetylation of p53 modulates its effect on cell growth and apoptosis. Nature. 2000;408(6810):377-381.

     Not in our library10.1038/35042612

113. 113.

     Ma Y., Yuan R., Meng Q., Goldberg I. D., Rosen E. M., Fan S. P53-independent down-regulation of Mdm2 in human cancer cells treated with adriamycin. Mol Cell Biol Res Commun. 2000;3(2):122-128.

     Not in our library10.1006/mcbr.2000.0201

114. 114.

     Maestro R., Dei Tos A. P., Hamamori Y., Krasnokutsky S., Sartorelli V., Kedes L., Doglioni C., Beach D. H., Hannon G. J. Twist is a potential oncogene that inhibits apoptosis. Genes Dev. 1999;13(17):2207-2217.

     Not in our library10.1101/gad.13.17.2207

115. 115.

     Maheswaran S., Englert C., Bennett P., Heinrich G., Haber D. A. The WT1 gene product stabilizes p53 and inhibits p53-mediated apoptosis. Genes Dev. 1995;9(17):2143-2156.

     Not in our library10.1101/gad.9.17.2143

116. 116.

     Malkin D., Li F. P., Strong L. C., Fraumeni J. F., Nelson C. E., Kim D. H., Kassel J., Gryka M. A., Bischoff F. Z., Tainsky M. A. Germ line p53 mutations in a familial syndrome of breast cancer, sarcomas, and other neoplasms. Science. 1990;250(4985):1233-1238.

     Not in our library10.1126/science.1978757

117. 117.

     Marchenko N. D., Zaika A., Moll U. M. Death signal-induced localization of p53 protein to mitochondria. A potential role in apoptotic signaling. J Biol Chem. 2000;275(21):16202-16212.

     Not in our library10.1074/jbc.275.21.16202

118. 118.

     Marechal V., Elenbaas B., Piette J., Nicolas J. C., Levine A. J. The ribosomal L5 protein is associated with mdm-2 and mdm-2-p53 complexes. Mol Cell Biol. 1994;14(11):7414-7420.

     Not in our library10.1128/mcb.14.11.7414-7420.1994

119. 119.

     Marin M. C., Jost C. A., Irwin M. S., DeCaprio J. A., Caput D., Kaelin W. G. Viral oncoproteins discriminate between p53 and the p53 homolog p73. Mol Cell Biol. 1998;18(11):6316-6324.

     Not in our library10.1128/mcb.18.11.6316

120. 120.

     Maya R., Oren M. Unmasking of phosphorylation-sensitive epitopes on p53 and Mdm2 by a simple Western-phosphatase procedure. Oncogene. 2000;19(28):3213-3215.

     Not in our library10.1038/sj.onc.1203658

121. 121.

     Mayo L. D., Turchi J. J., Berberich S. J. Mdm-2 phosphorylation by DNA-dependent protein kinase prevents interaction with p53. Cancer Res. 1997;57(22):5013-5016.

     Not in our library

122. 122.

     McCormick F. Interactions between adenovirus proteins and the p53 pathway: the development of ONYX-015. Semin Cancer Biol. 2000;10(6):453-459.

     Not in our library10.1006/scbi.2000.0336

123. 123.

     McKay B. C., Ljungman M., Rainbow A. J. Potential roles for p53 in nucleotide excision repair. Carcinogenesis. 1999;20(8):1389-1396.

     Not in our library10.1093/carcin/20.8.1389

124. 124.

     Meek D. W. Mechanisms of switching on p53: a role for covalent modification? Oncogene. 1999;18(53):7666-7675.

     Not in our library10.1038/sj.onc.1202951

125. 125.

     Meyn M. S. Ataxia-telangiectasia, cancer and the pathobiology of the ATM gene. Clin Genet. 1999;55(5):289-304.

     Not in our library10.1034/j.1399-0004.1999.550501.x

126. 126.

     Midgley C. A., Desterro J. M., Saville M. K., Howard S., Sparks A., Hay R. T., Lane D. P. An N-terminal p14ARF peptide blocks Mdm2-dependent ubiquitination in vitro and can activate p53 in vivo. Oncogene. 2000;19(19):2312-2323.

     Not in our library10.1038/sj.onc.1203593

127. 127.

     Miyashita T., Reed J. C. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell. 1995;80(2):293-299.

     Not in our library10.1016/0092-8674(95)90412-3

128. 128.

     Momand J., Zambetti G. P., Olson D. C., George D., Levine A. J. The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell. 1992;69(7):1237-1245.

     Not in our library10.1016/0092-8674(92)90644-r

129. 129.

     Montes de Oca Luna R., Wagner D. S., Lozano G. Rescue of early embryonic lethality in mdm2-deficient mice by deletion of p53. Nature. 1995;378(6553):203-206.

     Not in our library10.1038/378203a0

130. 130.

     Muller S., Berger M., Lehembre F., Seeler J. S., Haupt Y., Dejean A. c-Jun and p53 activity is modulated by SUMO-1 modification. J Biol Chem. 2000;275(18):13321-13329.

     Not in our library10.1074/jbc.275.18.13321

131. 131.

     Muslin A. J., Xing H. 14-3-3 proteins: regulation of subcellular localization by molecular interference. Cell Signal. 2000;12(11-12):703-709.

     Not in our library10.1016/s0898-6568(00)00131-5

132. 132.

     Nakano K., Bálint E., Ashcroft M., Vousden K. H. A ribonucleotide reductase gene is a transcriptional target of p53 and p73. Oncogene. 2000;19(37):4283-4289.

     Not in our library10.1038/sj.onc.1203774

133. 133.

     Nakano K., Vousden K. H. PUMA, a novel proapoptotic gene, is induced by p53. Mol Cell. 2001;7(3):683-694.

     Not in our library10.1016/s1097-2765(01)00214-3

134. 134.

     Nishimori H., Shiratsuchi T., Urano T., Kimura Y., Kiyono K., Tatsumi K., Yoshida S., Ono M., Kuwano M., Nakamura Y. A novel brain-specific p53-target gene, BAI1, containing thrombospondin type 1 repeats inhibits experimental angiogenesis. Oncogene. 1997;15(18):2145-2150.

     Not in our library10.1038/sj.onc.1201542

135. 135.

     O'Connor D. J., Lu X. Stress signals induce transcriptionally inactive E2F-1 independently of p53 and Rb. Oncogene. 2000;19(20):2369-2376.

     Not in our library10.1038/sj.onc.1203540

136. 136.

     Oda E., Ohki R., Murasawa H., Nemoto J., Shibue T., Yamashita T., Tokino T., Taniguchi T., Tanaka N. Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. Science. 2000;288(5468):1053-1058.

     Not in our library10.1126/science.288.5468.1053

137. 137.

     Oda K., Arakawa H., Tanaka T., Matsuda K., Tanikawa C., Mori T., Nishimori H., Tamai K., Tokino T., Nakamura Y. p53AIP1, a potential mediator of p53-dependent apoptosis, and its regulation by Ser-46-phosphorylated p53. Cell. 2000;102(6):849-862.

     Not in our library10.1016/s0092-8674(00)00073-8

138. 138.

     Offer H., Zurer I., Banfalvi G., Reha'k M., Falcovitz A., Milyavsky M., Goldfinger N., Rotter V. p53 modulates base excision repair activity in a cell cycle-specific manner after genotoxic stress. Cancer Res. 2001;61(1):88-96.

     Not in our library

139. 139.

     Ohki R., Nemoto J., Murasawa H., Oda E., Inazawa J., Tanaka N., Taniguchi T. Reprimo, a new candidate mediator of the p53-mediated cell cycle arrest at the G2 phase. J Biol Chem. 2000;275(30):22627-22630.

     Not in our library10.1074/jbc.c000235200

140. 140.

     Oliner J. D., Kinzler K. W., Meltzer P. S., George D. L., Vogelstein B. Amplification of a gene encoding a p53-associated protein in human sarcomas. Nature. 1992;358(6381):80-83.

     Not in our library10.1038/358080a0

141. 141.

     Ongkeko W. M., Wang X. Q., Siu W. Y., Lau A. W., Yamashita K., Harris A. L., Cox L. S., Poon R. Y. MDM2 and MDMX bind and stabilize the p53-related protein p73. Curr Biol. 9(15);829-832.

     Not in our library10.1016/s0960-9822(99)80367-4

142. 142.

     Owen-Schaub L. B., Zhang W., Cusack J. C., Angelo L. S., Santee S. M., Fujiwara T., Roth J. A., Deisseroth A. B., Zhang W. W., Kruzel E. Wild-type human p53 and a temperature-sensitive mutant induce Fas/APO-1 expression. Mol Cell Biol. 1995;15(6):3032-3040.

     Not in our library10.1128/mcb.15.6.3032

143. 143.

     Pariat M., Carillo S., Molinari M., Salvat C., Debüssche L., Bracco L., Milner J., Piechaczyk M. Proteolysis by calpains: a possible contribution to degradation of p53. Mol Cell Biol. 1997;17(5):2806-2815.

     Not in our library10.1128/mcb.17.5.2806

144. 144.

     Pearson M., Carbone R., Sebastiani C., Cioce M., Fagioli M., Saito S., Higashimoto Y., Appella E., Minucci S., Pandolfi P. P. PML regulates p53 acetylation and premature senescence induced by oncogenic Ras. Nature. 2000;406(6792):207-210.

     Not in our library10.1038/35018127

145. 145.

     Perry M. E., Mendrysa S. M., Saucedo L. J., Tannous P., Holubar M. p76(MDM2) inhibits the ability of p90(MDM2) to destabilize p53. J Biol Chem. 2000;275(8):5733-5738.

     Not in our library10.1074/jbc.275.8.5733

146. 146.

     Phillips A. C., Ernst M. K., Bates S., Rice N. R., Vousden K. H. E2F-1 potentiates cell death by blocking antiapoptotic signaling pathways. Mol Cell. 1999;4(5):771-781.

     Not in our library10.1016/s1097-2765(00)80387-1

147. 147.

     Pietenpol J. A., Tokino T., Thiagalingam S., el-Deiry W. S., Kinzler K. W., Vogelstein B. Sequence-specific transcriptional activation is essential for growth suppression by p53. Proc Natl Acad Sci U S A. 1994;91(6):1998-2002.

     Not in our library10.1073/pnas.91.6.1998

148. 148.

     Polyak K., Xia Y., Zweier J. L., Kinzler K. W., Vogelstein B. A model for p53-induced apoptosis. Nature. 1997;389(6648):300-305.

     Not in our library10.1038/38525

149. 149.

     Pomerantz J., Schreiber-Agus N., Liégeois N. J., Silverman A., Alland L., Chin L., Potes J., Chen K., Orlow I., Lee H. W. The Ink4a tumor suppressor gene product, p19Arf, interacts with MDM2 and neutralizes MDM2's inhibition of p53. Cell. 1998;92(6):713-723.

     Not in our library10.1016/s0092-8674(00)81400-2

150. 150.

     Prisco M., Hongo A., Rizzo M. G., Sacchi A., Baserga R. The insulin-like growth factor I receptor as a physiologically relevant target of p53 in apoptosis caused by interleukin-3 withdrawal. Mol Cell Biol. 1997;17(3):1084-1092.

     Not in our library10.1128/mcb.17.3.1084

151. 151.

     Radfar A., Unnikrishnan I., Lee H. W., DePinho R. A., Rosenberg N. p19(Arf) induces p53-dependent apoptosis during abelson virus-mediated pre-B cell transformation. Proc Natl Acad Sci U S A. 1998;95(22):13194-13199.

     Not in our library10.1073/pnas.95.22.13194

152. 152.

     Rampino N., Yamamoto H., Ionov Y., Li Y., Sawai H., Reed J. C., Perucho M. Somatic frameshift mutations in the BAX gene in colon cancers of the microsatellite mutator phenotype. Science. 1997;275(5302):967-969.

     Not in our library10.1126/science.275.5302.967

153. 153.

     Riemenschneider M. J., Büschges R., Wolter M., Reifenberger J., Boström J., Kraus J. A., Schlegel U., Reifenberger G. Amplification and overexpression of the MDM4 (MDMX) gene from 1q32 in a subset of malignant gliomas without TP53 mutation or MDM2 amplification. Cancer Res. 1999;59(24):6091-6096.

     Not in our library

154. 154.

     Rodriguez M. S., Desterro J. M., Lain S., Midgley C. A., Lane D. P., Hay R. T. SUMO-1 modification activates the transcriptional response of p53. EMBO J. 1999;18(22):6455-6461.

     Not in our library10.1093/emboj/18.22.6455

155. 155.

     Roth J. A., Swisher S. G., Meyn R. E. p53 tumor suppressor gene therapy for cancer. Oncology (Williston Park). 1999;13(10 Suppl 5):148-154.

     Not in our library

156. 156.

     Ryan K. M., Ernst M. K., Rice N. R., Vousden K. H. Role of NF-kappaB in p53-mediated programmed cell death. Nature. 2000;404(6780):892-897.

     Not in our library10.1038/35009130

157. 157.

     Ryan K. M., Vousden K. H. Characterization of structural p53 mutants which show selective defects in apoptosis but not cell cycle arrest. Mol Cell Biol. 1998;18(7):3692-3698.

     Not in our library10.1128/mcb.18.7.3692

158. 158.

     Sakaguchi K., Herrera J. E., Saito S., Miki T., Bustin M., Vassilev A., Anderson C. W., Appella E. DNA damage activates p53 through a phosphorylation-acetylation cascade. Genes Dev. 1998;12(18):2831-2841.

     Not in our library10.1101/gad.12.18.2831

159. 159.

     Sakaguchi K., Saito S., Higashimoto Y., Roy S., Anderson C. W., Appella E. Damage-mediated phosphorylation of human p53 threonine 18 through a cascade mediated by a casein 1-like kinase. Effect on Mdm2 binding. J Biol Chem. 2000;275(13):9278-9283.

     Not in our library10.1074/jbc.275.13.9278

160. 160.

     Sakaguchi K., Sakamoto H., Lewis M. S., Anderson C. W., Erickson J. W., Appella E., Xie D. Phosphorylation of serine 392 stabilizes the tetramer formation of tumor suppressor protein p53. Biochemistry. 1997;36(33):10117-10124.

     Not in our library10.1021/bi970759w

161. 161.

     Scheffner M., Huibregtse J. M., Vierstra R. D., Howley P. M. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell. 1993;75(3):495-505.

     Not in our library10.1016/0092-8674(93)90384-3

162. 162.

     Selivanova G., Iotsova V., Okan I., Fritsche M., Ström M., Groner B., Grafström R. C., Wiman K. G. Restoration of the growth suppression function of mutant p53 by a synthetic peptide derived from the p53 C-terminal domain. Nat Med. 1997;3(6):632-638.

     Not in our library10.1038/nm0697-632

163. 163.

     Sengupta S., Vonesch J. L., Waltzinger C., Zheng H., Wasylyk B. Negative cross-talk between p53 and the glucocorticoid receptor and its role in neuroblastoma cells. EMBO J. 2000;19(22):6051-6064.

     Not in our library10.1093/emboj/19.22.6051

164. 164.

     Sharp D. A., Kratowicz S. A., Sank M. J., George D. L. Stabilization of the MDM2 oncoprotein by interaction with the structurally related MDMX protein. J Biol Chem. 1999;274(53):38189-38196.

     Not in our library10.1074/jbc.274.53.38189

165. 165.

     Shaw P., Freeman J., Bovey R., Iggo R. Regulation of specific DNA binding by p53: evidence for a role for O-glycosylation and charged residues at the carboxy-terminus. Oncogene. 1996;12(4):921-930.

     Not in our library

166. 166.

     Sherr C. J., Weber J. D. The ARF/p53 pathway. Curr Opin Genet Dev. 2000;10(1):94-99.

     Not in our library10.1016/s0959-437x(99)00038-6

167. 167.

     Shieh S. Y., Ahn J., Tamai K., Taya Y., Prives C. The human homologs of checkpoint kinases Chk1 and Cds1 (Chk2) phosphorylate p53 at multiple DNA damage-inducible sites. Genes Dev. 2000;14(3):289-300.

     Not in our library

168. 168.

     Shieh S. Y., Ikeda M., Taya Y., Prives C. DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2. Cell. 1997;91(3):325-334.

     Not in our library10.1016/s0092-8674(00)80416-x

169. 169.

     Shvarts A., Steegenga W. T., Riteco N., van Laar T., Dekker P., Bazuine M., van Ham R. C., van der Houven van Oordt W., Hateboer G., van der Eb A. J. MDMX: a novel p53-binding protein with some functional properties of MDM2. EMBO J. 1996;15(19):5349-5357.

     Not in our library

170. 170.

     Sigalas I., Calvert A. H., Anderson J. J., Neal D. E., Lunec J. Alternatively spliced mdm2 transcripts with loss of p53 binding domain sequences: transforming ability and frequent detection in human cancer. Nat Med. 1996;2(8):912-917.

     Not in our library10.1038/nm0896-912

171. 171.

     Sionov R. V., Moallem E., Berger M., Kazaz A., Gerlitz O., Ben-Neriah Y., Oren M., Haupt Y. c-Abl neutralizes the inhibitory effect of Mdm2 on p53. J Biol Chem. 1999;274(13):8371-8374.

     Not in our library10.1074/jbc.274.13.8371

172. 172.

     Smith M. L., Chen I. T., Zhan Q., Bae I., Chen C. Y., Gilmer T. M., Kastan M. B., O'Connor P. M., Fornace A. J. Interaction of the p53-regulated protein Gadd45 with proliferating cell nuclear antigen. Science. 1994;266(5189):1376-1380.

     Not in our library10.1126/science.7973727

173. 173.

     Smith M. L., Ford J. M., Hollander M. C., Bortnick R. A., Amundson S. A., Seo Y. R., Deng C. X., Hanawalt P. C., Fornace A. J. p53-mediated DNA repair responses to UV radiation: studies of mouse cells lacking p53, p21, and/or gadd45 genes. Mol Cell Biol. 2000;20(10):3705-3714.

     Not in our library10.1128/mcb.20.10.3705-3714.2000

174. 174.

     Soengas M. S., Alarcón R. M., Yoshida H., Giaccia A. J., Hakem R., Mak T. W., Lowe S. W. Apaf-1 and caspase-9 in p53-dependent apoptosis and tumor inhibition. Science. 1999;284(5411):156-159.

     Not in our library10.1126/science.284.5411.156

175. 175.

     Soengas M. S., Capodieci P., Polsky D., Mora J., Esteller M., Opitz-Araya X., McCombie R., Herman J. G., Gerald W. L., Lazebnik Y. A. Inactivation of the apoptosis effector Apaf-1 in malignant melanoma. Nature. 2001;409(6817):207-211.

     Not in our library10.1038/35051606

176. 176.

     Srivastava S., Zou Z. Q., Pirollo K., Blattner W., Chang E. H. Germ-line transmission of a mutated p53 gene in a cancer-prone family with Li-Fraumeni syndrome. Nature. 1990;348(6303):747-749.

     Not in our library10.1038/348747a0

177. 177.

     Stommel J. M., Marchenko N. D., Jimenez G. S., Moll U. M., Hope T. J., Wahl G. M. A leucine-rich nuclear export signal in the p53 tetramerization domain: regulation of subcellular localization and p53 activity by NES masking. EMBO J. 1999;18(6):1660-1672.

     Not in our library10.1093/emboj/18.6.1660

178. 178.

     Stott F. J., Bates S., James M. C., McConnell B. B., Starborg M., Brookes S., Palmero I., Ryan K., Hara E., Vousden K. H. The alternative product from the human CDKN2A locus, p14(ARF), participates in a regulatory feedback loop with p53 and MDM2. EMBO J. 1998;17(17):5001-5014.

     Not in our library10.1093/emboj/17.17.5001

179. 179.

     Takekawa M., Adachi M., Nakahata A., Nakayama I., Itoh F., Tsukuda H., Taya Y., Imai K. p53-inducible wip1 phosphatase mediates a negative feedback regulation of p38 MAPK-p53 signaling in response to UV radiation. EMBO J. 2000;19(23):6517-6526.

     Not in our library10.1093/emboj/19.23.6517

180. 180.

     Takimoto R., El-Deiry W. S. Wild-type p53 transactivates the KILLER/DR5 gene through an intronic sequence-specific DNA-binding site. Oncogene. 2000;19(14):1735-1743.

     Not in our library10.1038/sj.onc.1203489

181. 181.

     Tanaka H., Arakawa H., Yamaguchi T., Shiraishi K., Fukuda S., Matsui K., Takei Y., Nakamura Y. A ribonucleotide reductase gene involved in a p53-dependent cell-cycle checkpoint for DNA damage. Nature. 2000;404(6773):42-49.

     Not in our library10.1038/35003506

182. 182.

     Tanimura S., Ohtsuka S., Mitsui K., Shirouzu K., Yoshimura A., Ohtsubo M. MDM2 interacts with MDMX through their RING finger domains. FEBS Lett. 1999;447(1):5-9.

     Not in our library10.1016/s0014-5793(99)00254-9

183. 183.
     Nucleocytoplasmic shuttling of oncoprotein Hdm2 is required for Hdm2-mediated degradation of p53 · 1999

     Not checked
184. 184.

     Thornborrow E. C., Manfredi J. J. One mechanism for cell type-specific regulation of the bax promoter by the tumor suppressor p53 is dictated by the p53 response element. J Biol Chem. 1999;274(47):33747-33756.

     Not in our library10.1074/jbc.274.47.33747

185. 185.

     Unger T., Juven-Gershon T., Moallem E., Berger M., Vogt Sionov R., Lozano G., Oren M., Haupt Y. Critical role for Ser20 of human p53 in the negative regulation of p53 by Mdm2. EMBO J. 1999;18(7):1805-1814.

     Not in our library10.1093/emboj/18.7.1805

186. 186.

     Van Antwerp D. J., Martin S. J., Kafri T., Green D. R., Verma I. M. Suppression of TNF-alpha-induced apoptosis by NF-kappaB. Science. 1996;274(5288):787-789.

     Not in our library10.1126/science.274.5288.787

187. 187.

     Vaziri H., West M. D., Allsopp R. C., Davison T. S., Wu Y. S., Arrowsmith C. H., Poirier G. G., Benchimol S. ATM-dependent telomere loss in aging human diploid fibroblasts and DNA damage lead to the post-translational activation of p53 protein involving poly(ADP-ribose) polymerase. EMBO J. 1997;16(19):6018-6033.

     Not in our library10.1093/emboj/16.19.6018

188. 188.

     Vogelstein B., Lane D., Levine A. J. Surfing the p53 network. Nature. 2000;408(6810):307-310.

     Not in our library10.1038/35042675

189. 189.

     Vousden K. H. p53: death star. Cell. 2000;103(5):691-694.

     Not in our library10.1016/s0092-8674(00)00171-9

190. 190.

     Wadgaonkar R., Collins T. Murine double minute (MDM2) blocks p53-coactivator interaction, a new mechanism for inhibition of p53-dependent gene expression. J Biol Chem. 1999;274(20):13760-13767.

     Not in our library10.1074/jbc.274.20.13760

191. 191.

     Waldman T., Kinzler K. W., Vogelstein B. p21 is necessary for the p53-mediated G1 arrest in human cancer cells. Cancer Res. 1995;55(22):5187-5190.

     Not in our library

192. 192.

     Waldman T., Lengauer C., Kinzler K. W., Vogelstein B. Uncoupling of S phase and mitosis induced by anticancer agents in cells lacking p21. Nature. 1996;381(6584):713-716.

     Not in our library10.1038/381713a0

193. 193.

     Wang X. W., Zhan Q., Coursen J. D., Khan M. A., Kontny H. U., Yu L., Hollander M. C., O'Connor P. M., Fornace A. J., Harris C. C. GADD45 induction of a G2/M cell cycle checkpoint. Proc Natl Acad Sci U S A. 1999;96(7):3706-3711.

     Not in our library10.1073/pnas.96.7.3706

194. 194.

     Wang X., Ohnishi K., Takahashi A., Ohnishi T. Poly(ADP-ribosyl)ation is required for p53-dependent signal transduction induced by radiation. Oncogene. 1998;17(22):2819-2825.

     Not in our library10.1038/sj.onc.1202216

195. 195.

     Wani M. A., Zhu Q. Z., El-Mahdy M., Wani A. A. Influence of p53 tumor suppressor protein on bias of DNA repair and apoptotic response in human cells. Carcinogenesis. 1999;20(5):765-772.

     Not in our library10.1093/carcin/20.5.765

196. 196.

     Waterman M. J., Stavridi E. S., Waterman J. L., Halazonetis T. D. ATM-dependent activation of p53 involves dephosphorylation and association with 14-3-3 proteins. Nat Genet. 1998;19(2):175-178.

     Not in our library10.1038/542

197. 197.

     Weber J. D., Kuo M. L., Bothner B., DiGiammarino E. L., Kriwacki R. W., Roussel M. F., Sherr C. J. Cooperative signals governing ARF-mdm2 interaction and nucleolar localization of the complex. Mol Cell Biol. 2000;20(7):2517-2528.

     Not in our library10.1128/mcb.20.7.2517-2528.2000

198. 198.

     Weber J. D., Taylor L. J., Roussel M. F., Sherr C. J., Bar-Sagi D. Nucleolar Arf sequesters Mdm2 and activates p53. Nat Cell Biol. 1999;1(1):20-26.

     Not in our library10.1038/8991

199. 199.

     Wu G. S., Burns T. F., McDonald E. R., Jiang W., Meng R., Krantz I. D., Kao G., Gan D. D., Zhou J. Y., Muschel R. KILLER/DR5 is a DNA damage-inducible p53-regulated death receptor gene. Nat Genet. 1997;17(2):141-143.

     Not in our library10.1038/ng1097-141

200. 200.

     Wu H., Lozano G. NF-kappa B activation of p53. A potential mechanism for suppressing cell growth in response to stress. J Biol Chem. 1994;269(31):20067-20074.

     Not in our library

201. 201.

     Wu L., Levine A. J. Differential regulation of the p21/WAF-1 and mdm2 genes after high-dose UV irradiation: p53-dependent and p53-independent regulation of the mdm2 gene. Mol Med. 1997;3(7):441-451.

     Not in our library

202. 202.

     Wu X., Bayle J. H., Olson D., Levine A. J. The p53-mdm-2 autoregulatory feedback loop. Genes Dev. 1993;7(7A):1126-1132.

     Not in our library10.1101/gad.7.7a.1126

203. 203.

     Yam C. H., Siu W. Y., Arooz T., Chiu C. H., Lau A., Wang X. Q., Poon R. Y. MDM2 and MDMX inhibit the transcriptional activity of ectopically expressed SMAD proteins. Cancer Res. 1999;59(20):5075-5078.

     Not in our library

204. 204.

     Yu Z. K., Geyer R. K., Maki C. G. MDM2-dependent ubiquitination of nuclear and cytoplasmic P53. Oncogene. 2000;19(51):5892-5897.

     Not in our library10.1038/sj.onc.1203980

205. 205.

     Zaika A., Marchenko N., Moll U. M. Cytoplasmically "sequestered" wild type p53 protein is resistant to Mdm2-mediated degradation. J Biol Chem. 1999;274(39):27474-27480.

     Not in our library10.1074/jbc.274.39.27474

206. 206.

     Zeimet A. G., Riha K., Berger J., Widschwendter M., Hermann M., Daxenbichler G., Marth C. New insights into p53 regulation and gene therapy for cancer. Biochem Pharmacol. 2000;60(8):1153-1163.

     Not in our library10.1016/s0006-2952(00)00442-1

207. 207.

     Zeng X., Chen L., Jost C. A., Maya R., Keller D., Wang X., Kaelin W. G., Oren M., Chen J., Lu H. MDM2 suppresses p73 function without promoting p73 degradation. Mol Cell Biol. 1999;19(5):3257-3266.

     Not in our library10.1128/mcb.19.5.3257

208. 208.

     Zeng X., Keller D., Wu L., Lu H. UV but not gamma irradiation accelerates p53-induced apoptosis of teratocarcinoma cells by repressing MDM2 transcription. Cancer Res. 2000;60(21):6184-6188.

     Not in our library

209. 209.

     Zhang W., Lu Q., Xie Z. J., Mellgren R. L. Inhibition of the growth of WI-38 fibroblasts by benzyloxycarbonyl-Leu-Leu-Tyr diazomethyl ketone: evidence that cleavage of p53 by a calpain-like protease is necessary for G1 to S-phase transition. Oncogene. 1997;14(3):255-263.

     Not in our library10.1038/sj.onc.1200841

210. 210.

     Zhang Y., Xiong Y., Yarbrough W. G. ARF promotes MDM2 degradation and stabilizes p53: ARF-INK4a locus deletion impairs both the Rb and p53 tumor suppression pathways. Cell. 1998;92(6):725-734.

     Not in our library10.1016/s0092-8674(00)81401-4

211. 211.

     Zhou J., Ahn J., Wilson S. H., Prives C. A role for p53 in base excision repair. EMBO J. 2001;20(4):914-923.

     Not in our library10.1093/emboj/20.4.914

212. 212.

     el-Deiry W. S., Tokino T., Velculescu V. E., Levy D. B., Parsons R., Trent J. M., Lin D., Mercer W. E., Kinzler K. W., Vogelstein B. WAF1, a potential mediator of p53 tumor suppression. Cell. 1993;75(4):817-825.

     Not in our library10.1016/0092-8674(93)90500-p

Cited by papers we hold 2

• Tumor Suppressor p53 Alters Host Cell Metabolism to Limit Chlamydia trachomatis Infection · 2014
  Not checked
• P53 abnormalities and outcomes in colorectal cancer: a systematic review · 2005
  No notice

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