Differential regulation of p21^waf1 protein half-life by DNA damage and Nutlin-3 in p53 wild-type tumors and its therapeutic implications

References

• Massagué J. G1 cell-cycle control and cancer. Nature 2004; 432:298 - 306; http://dx.doi.org/10.1038/nature03094; PMID: 15549091
   PubMed Web of Science ®Google Scholar
• Al-Ejeh F, Kumar R, Wiegmans A, Lakhani SR, Brown MP, Khanna KK. Harnessing the complexity of DNA-damage response pathways to improve cancer treatment outcomes. Oncogene 2010; 29:6085 - 98; http://dx.doi.org/10.1038/onc.2010.407; PMID: 20818418
   PubMed Web of Science ®Google Scholar
• Kastan MB, Bartek J. Cell-cycle checkpoints and cancer. Nature 2004; 432:316 - 23; http://dx.doi.org/10.1038/nature03097; PMID: 15549093
   PubMed Web of Science ®Google Scholar
• Rudolph J. Inhibiting transient protein-protein interactions: lessons from the Cdc25 protein tyrosine phosphatases. Nat Rev Cancer 2007; 7:202 - 11; http://dx.doi.org/10.1038/nrc2087; PMID: 17287826
   PubMed Web of Science ®Google Scholar
• Aylon Y, Oren M. New plays in the p53 theater. Curr Opin Genet Dev 2011; 21:86 - 92; http://dx.doi.org/10.1016/j.gde.2010.10.002; PMID: 21317061
   PubMed Web of Science ®Google Scholar
• Bucher N, Britten CD. G2 checkpoint abrogation and checkpoint kinase-1 targeting in the treatment of cancer. Br J Cancer 2008; 98:523 - 8; http://dx.doi.org/10.1038/sj.bjc.6604208; PMID: 18231106
   PubMed Web of Science ®Google Scholar
• Kuntz K, O’Connell MJ. The G(2) DNA damage checkpoint: could this ancient regulator be the Achilles heel of cancer?. Cancer Biol Ther 2009; 8:1433 - 9; http://dx.doi.org/10.4161/cbt.8.15.9081; PMID: 19574738
   PubMed Web of Science ®Google Scholar
• Tse AN, Carvajal R, Schwartz GK. Targeting checkpoint kinase 1 in cancer therapeutics. Clin Cancer Res 2007; 13:1955 - 60; http://dx.doi.org/10.1158/1078-0432.CCR-06-2793; PMID: 17404075
   PubMed Web of Science ®Google Scholar
• Eastman A, Kohn EA, Brown MK, Rathman J, Livingstone M, Blank DH, et al. A novel indolocarbazole, ICP-1, abrogates DNA damage-induced cell cycle arrest and enhances cytotoxicity: similarities and differences to the cell cycle checkpoint abrogator UCN-01. Mol Cancer Ther 2002; 1:1067 - 78; PMID: 12481430
   PubMed Web of Science ®Google Scholar
• Kohn EA, Ruth ND, Brown MK, Livingstone M, Eastman A. Abrogation of the S phase DNA damage checkpoint results in S phase progression or premature mitosis depending on the concentration of 7-hydroxystaurosporine and the kinetics of Cdc25C activation. J Biol Chem 2002; 277:26553 - 64; http://dx.doi.org/10.1074/jbc.M202040200; PMID: 11953432
   PubMed Web of Science ®Google Scholar
• Chang L-J, Eastman A. Decreased translation of p21waf1 mRNA causes attenuated p53 signaling in some p53 wild-type tumors. Cell Cycle 2012; 11:1818 - 26; http://dx.doi.org/10.4161/cc20208; PMID: 22510560
   PubMed Web of Science ®Google Scholar
• Levesque AA, Fanous AA, Poh A, Eastman A. Defective p53 signaling in p53 wild-type tumors attenuates p21waf1 induction and cyclin B repression rendering them sensitive to Chk1 inhibitors that abrogate DNA damage-induced S and G2 arrest. Mol Cancer Ther 2008; 7:252 - 62; http://dx.doi.org/10.1158/1535-7163.MCT-07-2066; PMID: 18281511
   PubMed Web of Science ®Google Scholar
• Eastman A. The importance of p53 signaling in the response of cells to checkpoint inhibitors. In: Siddik ZH (ed). Checkpoint Controls and Targets in Cancer Therapy. Humana Press, 2010 pp. 189-98.
   Google Scholar
• Oliver TG, Meylan E, Chang GP, Xue W, Burke JR, Humpton TJ, et al. Caspase-2-mediated cleavage of Mdm2 creates a p53-induced positive feedback loop. Mol Cell 2011; 43:57 - 71; http://dx.doi.org/10.1016/j.molcel.2011.06.012; PMID: 21726810
   PubMed Web of Science ®Google Scholar
• Pochampally R, Fodera B, Chen L, Lu W, Chen J. Activation of an MDM2-specific caspase by p53 in the absence of apoptosis. J Biol Chem 1999; 274:15271 - 7; http://dx.doi.org/10.1074/jbc.274.21.15271; PMID: 10329737
   PubMed Web of Science ®Google Scholar
• Pochampally R, Fodera B, Chen L, Shao W, Levine EA, Chen J. A 60 kd MDM2 isoform is produced by caspase cleavage in non-apoptotic tumor cells. Oncogene 1998; 17:2629 - 36; http://dx.doi.org/10.1038/sj.onc.1202206; PMID: 9840926
   PubMed Web of Science ®Google Scholar
• Chen L, Marechal V, Moreau J, Levine AJ, Chen J. Proteolytic cleavage of the mdm2 oncoprotein during apoptosis. J Biol Chem 1997; 272:22966 - 73; http://dx.doi.org/10.1074/jbc.272.36.22966; PMID: 9278461
   PubMed Web of Science ®Google Scholar
• Bartel F, Harris LC, Würl P, Taubert H. MDM2 and its splice variant messenger RNAs: expression in tumors and down-regulation using antisense oligonucleotides. Mol Cancer Res 2004; 2:29 - 35; PMID: 14757843
   PubMed Web of Science ®Google Scholar
• Bartel F, Taubert H, Harris LC. Alternative and aberrant splicing of MDM2 mRNA in human cancer. Cancer Cell 2002; 2:9 - 15; http://dx.doi.org/10.1016/S1535-6108(02)00091-0; PMID: 12150820
   PubMed Web of Science ®Google Scholar
• Gottifredi V, Karni-Schmidt O, Shieh SS, Prives C. p53 down-regulates CHK1 through p21 and the retinoblastoma protein. Mol Cell Biol 2001; 21:1066 - 76; http://dx.doi.org/10.1128/MCB.21.4.1066-1076.2001; PMID: 11158294
   PubMed Web of Science ®Google Scholar
• Zhao H, Watkins JL, Piwnica-Worms H. Disruption of the checkpoint kinase 1/cell division cycle 25A pathway abrogates ionizing radiation-induced S and G2 checkpoints. Proc Natl Acad Sci USA 2002; 99:14795 - 800; http://dx.doi.org/10.1073/pnas.182557299; PMID: 12399544
   PubMed Web of Science ®Google Scholar
• Jin Y, Lee H, Zeng SX, Dai MS, Lu H. MDM2 promotes p21waf1/cip1 proteasomal turnover independently of ubiquitylation. EMBO J 2003; 22:6365 - 77; http://dx.doi.org/10.1093/emboj/cdg600; PMID: 14633995
   PubMed Web of Science ®Google Scholar
• Xu H, Zhang Z, Li M, Zhang R. MDM2 promotes proteasomal degradation of p21Waf1 via a conformation change. J Biol Chem 2010; 285:18407 - 14; http://dx.doi.org/10.1074/jbc.M109.059568; PMID: 20308078
   PubMed Web of Science ®Google Scholar
• Zhang Z, Wang H, Li M, Agrawal S, Chen X, Zhang R. MDM2 is a negative regulator of p21WAF1/CIP1, independent of p53. J Biol Chem 2004; 279:16000 - 6; http://dx.doi.org/10.1074/jbc.M312264200; PMID: 14761977
   PubMed Web of Science ®Google Scholar
• Coleman ML, Marshall CJ, Olson MF. Ras promotes p21(Waf1/Cip1) protein stability via a cyclin D1-imposed block in proteasome-mediated degradation. EMBO J 2003; 22:2036 - 46; http://dx.doi.org/10.1093/emboj/cdg189; PMID: 12727871
   PubMed Web of Science ®Google Scholar
• Jin Y, Zeng SX, Sun XX, Lee H, Blattner C, Xiao Z, et al. MDMX promotes proteasomal turnover of p21 at G1 and early S phases independently of, but in cooperation with, MDM2. Mol Cell Biol 2008; 28:1218 - 29; http://dx.doi.org/10.1128/MCB.01198-07; PMID: 18086887
   PubMed Web of Science ®Google Scholar
• Xu S, Feng Z, Zhang M, Wu Y, Sang Y, Xu H, et al. hSSB1 binds and protects p21 from ubiquitin-mediated degradation and positively correlates with p21 in human hepatocellular carcinomas. Oncogene 2011; 30:2219 - 29; http://dx.doi.org/10.1038/onc.2010.596; PMID: 21242961
   PubMed Web of Science ®Google Scholar
• Montano R, Chung I, Garner KM, Parry D, Eastman A. Preclinical development of the novel Chk1 inhibitor SCH900776 in combination with DNA-damaging agents and antimetabolites. Mol Cancer Ther 2012; 11:427 - 38; http://dx.doi.org/10.1158/1535-7163.MCT-11-0406; PMID: 22203733
   PubMed Web of Science ®Google Scholar
• Zhou BB, Bartek J. Targeting the checkpoint kinases: chemosensitization versus chemoprotection. Nat Rev Cancer 2004; 4:216 - 25; http://dx.doi.org/10.1038/nrc1296; PMID: 14993903
   PubMed Web of Science ®Google Scholar
• Shangary S, Wang S. Small-molecule inhibitors of the MDM2-p53 protein-protein interaction to reactivate p53 function: a novel approach for cancer therapy. Annu Rev Pharmacol Toxicol 2009; 49:223 - 41; http://dx.doi.org/10.1146/annurev.pharmtox.48.113006.094723; PMID: 18834305
   PubMed Web of Science ®Google Scholar
• Tovar C, Rosinski J, Filipovic Z, Higgins B, Kolinsky K, Hilton H, et al. Small-molecule MDM2 antagonists reveal aberrant p53 signaling in cancer: implications for therapy. Proc Natl Acad Sci USA 2006; 103:1888 - 93; http://dx.doi.org/10.1073/pnas.0507493103; PMID: 16443686
   PubMed Web of Science ®Google Scholar
• Lee H, Zeng SX, Lu H. UV Induces p21 rapid turnover independently of ubiquitin and Skp2. J Biol Chem 2006; 281:26876 - 83; http://dx.doi.org/10.1074/jbc.M605366200; PMID: 16803887
   PubMed Web of Science ®Google Scholar
• Stuart SA, Wang JY. Ionizing radiation induces ATM-independent degradation of p21Cip1 in transformed cells. J Biol Chem 2009; 284:15061 - 70; http://dx.doi.org/10.1074/jbc.M808810200; PMID: 19332548
   PubMed Web of Science ®Google Scholar
• Menendez JA, Mehmi I, Lupu R. Heregulin-triggered Her-2/neu signaling enhances nuclear accumulation of p21WAF1/CIP1 and protects breast cancer cells from cisplatin-induced genotoxic damage. Int J Oncol 2005; 26:649 - 59; PMID: 15703820
   PubMed Web of Science ®Google Scholar
• Nam M, Lee WH, Bae EJ, Kim SG. Compound C inhibits clonal expansion of preadipocytes by increasing p21 level irrespectively of AMPK inhibition. Arch Biochem Biophys 2008; 479:74 - 81; http://dx.doi.org/10.1016/j.abb.2008.07.029; PMID: 18721791
   PubMed Web of Science ®Google Scholar
• Gaedicke S, Firat-Geier E, Constantiniu O, Lucchiari-Hartz M, Freudenberg M, Galanos C, et al. Antitumor effect of the human immunodeficiency virus protease inhibitor ritonavir: induction of tumor-cell apoptosis associated with perturbation of proteasomal proteolysis. Cancer Res 2002; 62:6901 - 8; PMID: 12460905
   PubMed Web of Science ®Google Scholar
• Luo XJ, Li W, Yang LF, Yu XF, Xiao LB, Tang M, et al. DAPK1 mediates the G1 phase arrest in human nasopharyngeal carcinoma cells induced by grifolin, a potential antitumor natural product. Eur J Pharmacol 2011; 670:427 - 34; http://dx.doi.org/10.1016/j.ejphar.2011.08.026; PMID: 21914449
   PubMed Web of Science ®Google Scholar
• Riley T, Sontag E, Chen P, Levine A. Transcriptional control of human p53-regulated genes. Nat Rev Mol Cell Biol 2008; 9:402 - 12; http://dx.doi.org/10.1038/nrm2395; PMID: 18431400
   PubMed Web of Science ®Google Scholar
• Ashcroft M, Taya Y, Vousden KH. Stress signals utilize multiple pathways to stabilize p53. Mol Cell Biol 2000; 20:3224 - 33; http://dx.doi.org/10.1128/MCB.20.9.3224-3233.2000; PMID: 10757806
   PubMed Web of Science ®Google Scholar
• Vermeulen K, Van Bockstaele DR, Berneman ZN. The cell cycle: a review of regulation, deregulation and therapeutic targets in cancer. Cell Prolif 2003; 36:131 - 49; http://dx.doi.org/10.1046/j.1365-2184.2003.00266.x; PMID: 12814430
   PubMed Web of Science ®Google Scholar
• Valentine JM, Kumar S, Moumen A. A p53-independent role for the MDM2 antagonist Nutlin-3 in DNA damage response initiation. BMC Cancer 2011; 11:79; http://dx.doi.org/10.1186/1471-2407-11-79; PMID: 21338495
   PubMed Web of Science ®Google Scholar
• Thompson T, Tovar C, Yang H, Carvajal D, Vu BT, Xu Q, et al. Phosphorylation of p53 on key serines is dispensable for transcriptional activation and apoptosis. J Biol Chem 2004; 279:53015 - 22; http://dx.doi.org/10.1074/jbc.M410233200; PMID: 15471885
   PubMed Web of Science ®Google Scholar
• Verma R, Rigatti MJ, Belinsky GS, Godman CA, Giardina C. DNA damage response to the Mdm2 inhibitor nutlin-3. Biochem Pharmacol 2010; 79:565 - 74; http://dx.doi.org/10.1016/j.bcp.2009.09.020; PMID: 19788889
   PubMed Web of Science ®Google Scholar
• Shangary S, Qin D, McEachern D, Liu M, Miller RS, Qiu S, et al. Temporal activation of p53 by a specific MDM2 inhibitor is selectively toxic to tumors and leads to complete tumor growth inhibition. Proc Natl Acad Sci USA 2008; 105:3933 - 8; http://dx.doi.org/10.1073/pnas.0708917105; PMID: 18316739
   PubMed Web of Science ®Google Scholar
• Bachman KE, Blair BG, Brenner K, Bardelli A, Arena S, Zhou S, et al. p21(WAF1/CIP1) mediates the growth response to TGF-beta in human epithelial cells. Cancer Biol Ther 2004; 3:221 - 5; http://dx.doi.org/10.4161/cbt.3.2.666; PMID: 14726675
   PubMed Web of Science ®Google Scholar
• Waldman T, Kinzler KW, Vogelstein B. p21 is necessary for the p53-mediated G1 arrest in human cancer cells. Cancer Res 1995; 55:5187 - 90; PMID: 7585571
   PubMed Web of Science ®Google Scholar
• Demarcq C, Bunch RT, Creswell D, Eastman A. The role of cell cycle progression in cisplatin-induced apoptosis in Chinese hamster ovary cells. Cell Growth Differ 1994; 5:983 - 93; PMID: 7819136
   PubMedGoogle Scholar
• Rago R, Mitchen J, Wilding G. DNA fluorometric assay in 96-well tissue culture plates using Hoechst 33258 after cell lysis by freezing in distilled water. Anal Biochem 1990; 191:31 - 4; http://dx.doi.org/10.1016/0003-2697(90)90382-J; PMID: 1706565
   PubMed Web of Science ®Google Scholar
• Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001; 29:e45; http://dx.doi.org/10.1093/nar/29.9.e45; PMID: 11328886
   PubMed Web of Science ®Google Scholar