p53 Restoration in Induction and Maintenance of Senescence: Differential Effects in Premalignant and Malignant Tumor Cells

REFERENCES

• Muñoz-Espín D, Serrano M. 2014. Cellular senescence: from physiology to pathology. Nat Rev Mol Cell Biol 15:482–496. http://dx.doi.org/10.1038/nrm3823.
   PubMed Web of Science ®Google Scholar
• Collado M, Gil J, Efeyan A, Guerra C, Schuhmacher AJ, Barradas M, Benguría A, Zaballos A, Flores JM, Barbacid M, Beach D, Serrano M. 2005. Tumour biology: senescence in premalignant tumours. Nature 436:642. http://dx.doi.org/10.1038/436642a.
   PubMed Web of Science ®Google Scholar
• Pérez-Mancera PA, Young AR, Narita M. 2014. Inside and out: the activities of senescence in cancer. Nat Rev Cancer 14:547–558. http://dx.doi.org/10.1038/nrc3773.
   PubMed Web of Science ®Google Scholar
• Saab R. 2011. Senescence and pre-malignancy: how do tumors progress? Semin Cancer Biol 21:385–391. http://dx.doi.org/10.1016/j.semcancer.2011.09.013.
   PubMedGoogle Scholar
• Rufini A, Tucci P, Celardo I, Melino G. 2013. Senescence and aging: the critical roles of p53. Oncogene 32:5129–5143. http://dx.doi.org/10.1038/onc.2012.640.
   PubMed Web of Science ®Google Scholar
• Salama R, Sadaie M, Hoare M, Narita M. 2014. Cellular senescence and its effector programs. Genes Dev 28:99–114. http://dx.doi.org/10.1101/gad.235184.113.
   PubMed Web of Science ®Google Scholar
• Beauséjour CM, Krtolica A, Galimi F, Narita M, Lowe SW, Yaswen P, Campisi J. 2003. Reversal of human cellular senescence: roles of the p53 and p16 pathways. EMBO J 22:4212–4222. http://dx.doi.org/10.1093/emboj/cdg417.
   PubMed Web of Science ®Google Scholar
• Ma D, Zhou P, Harbour JW. 2003. Distinct mechanisms for regulating the tumor suppressor and antiapoptotic functions of Rb. J Biol Chem 278:19358–19366. http://dx.doi.org/10.1074/jbc.M301761200.
   PubMedGoogle Scholar
• Dirac AM, Bernards R. 2003. Reversal of senescence in mouse fibroblasts through lentiviral suppression of p53. J Biol Chem 278:11731–11734. http://dx.doi.org/10.1074/jbc.C300023200.
   PubMed Web of Science ®Google Scholar
• Christophorou MA, Martin-Zanca D, Soucek L, Lawlor ER, Brown-Swigart L, Verschuren EW, Evan GI. 2005. Temporal dissection of p53 function in vitro and in vivo. Nat Genet 37:718–726. http://dx.doi.org/10.1038/ng1572.
   PubMed Web of Science ®Google Scholar
• Jeanblanc M, Ragu S, Gey C, Contrepois K, Courbeyrette R, Thuret JY, Mann C. 2012. Parallel pathways in RAF-induced senescence and conditions for its reversion. Oncogene 31:3072–3085. http://dx.doi.org/10.1038/onc.2011.481.
   PubMed Web of Science ®Google Scholar
• Skapek SX, Lin SC, Jablonski MM, McKeller RN, Tan M, Hu N, Lee EY. 2001. Persistent expression of cyclin D1 disrupts normal photoreceptor differentiation and retina development. Oncogene 20:6742–6751. http://dx.doi.org/10.1038/sj.onc.1204876.
   PubMedGoogle Scholar
• Christophorou MA, Ringshausen I, Finch AJ, Swigart LB, Evan GI. 2006. The pathological response to DNA damage does not contribute to p53-mediated tumour suppression. Nature 443:214–217. http://dx.doi.org/10.1038/nature05077.
   PubMed Web of Science ®Google Scholar
• Martins CP, Brown-Swigart L, Evan GI. 2006. Modeling the therapeutic efficacy of p53 restoration in tumors. Cell 127:1323–1334. http://dx.doi.org/10.1016/j.cell.2006.12.007.
   PubMed Web of Science ®Google Scholar
• Junttila MR, Karnezis AN, Garcia D, Madriles F, Kortlever RM, Rostker F, Brown Swigart L, Pham DM, Seo Y, Evan GI, Martins CP. 2010. Selective activation of p53-mediated tumour suppression in high-grade tumours. Nature 468:567–571. http://dx.doi.org/10.1038/nature09526.
   PubMedGoogle Scholar
• Zalzali H, Harajly M, Abdul-Latif L, El-Chaar N, Dbaibo G, Skapek SX, Saab R. 2012. Temporally distinct roles for tumor suppressor pathways in cell cycle arrest and cellular senescence in Cyclin D1-driven tumor. Mol Cancer 11:28. http://dx.doi.org/10.1186/1476-4598-11-28.
   PubMedGoogle Scholar
• Esteller M, Tortola S, Toyota M, Capella G, Peinado MA, Baylin SB, Herman JG. 2000. Hypermethylation-associated inactivation of p14(ARF) is independent of p16(INK4a) methylation and p53 mutational status. Cancer Res 60:129–133.
   PubMed Web of Science ®Google Scholar
• Saab R, Rodriguez-Galindo C, Matmati K, Rehg JE, Baumer SH, Khoury JD, Billups C, Neale G, Helton KJ, Skapek SX. 2009. p18Ink4c and p53 Act as tumor suppressors in cyclin D1-driven primitive neuroectodermal tumor. Cancer Res 69:440–448. http://dx.doi.org/10.1158/0008-5472.CAN-08-1892.
   PubMedGoogle Scholar
• Itahana K, Campisi J, Dimri GP. 2007. Methods to detect biomarkers of cellular senescence: the senescence-associated beta-galactosidase assay. Methods Mol Biol 371:21–31. http://dx.doi.org/10.1007/978-1-59745-361-5_3.
   PubMedGoogle Scholar
• Adams PD. 2007. Remodeling of chromatin structure in senescent cells and its potential impact on tumor suppression and aging. Gene 397:84–93. http://dx.doi.org/10.1016/j.gene.2007.04.020.
   PubMed Web of Science ®Google Scholar
• Collado M, Serrano M. 2006. The power and the promise of oncogene-induced senescence markers. Nat Rev Cancer 6:472–476. http://dx.doi.org/10.1038/nrc1884.
   PubMed Web of Science ®Google Scholar
• Qian Y, Zhang J, Yan B, Chen X. 2008. DEC1, a basic helix-loop-helix transcription factor and a novel target gene of the p53 family, mediates p53-dependent premature senescence. J Biol Chem 283:2896–2905. http://dx.doi.org/10.1074/jbc.M708624200.
   PubMedGoogle Scholar
• Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW. 1997. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88:593–602. http://dx.doi.org/10.1016/S0092-8674(00)81902-9.
   PubMed Web of Science ®Google Scholar
• Saab R. 2010. Cellular senescence: many roads, one final destination. ScientificWorldJournal 10:727–741. http://dx.doi.org/10.1100/tsw.2010.68.
   PubMedGoogle Scholar
• Ozenne P, Eymin B, Brambilla E, Gazzeri S. 2010. The ARF tumor suppressor: structure, functions and status in cancer. Int J Cancer 127:2239–2247. http://dx.doi.org/10.1002/ijc.25511.
   PubMed Web of Science ®Google Scholar
• Larsson LG. 2011. Oncogene- and tumor suppressor gene-mediated suppression of cellular senescence. Semin Cancer Biol 21:367–376. http://dx.doi.org/10.1016/j.semcancer.2011.10.005.
   PubMedGoogle Scholar
• Feldser DM, Kostova KK, Winslow MM, Taylor SE, Cashman C, Whittaker CA, Sanchez-Rivera FJ, Resnick R, Bronson R, Hemann MT, Jacks T. 2010. Stage-specific sensitivity to p53 restoration during lung cancer progression. Nature 468:572–575. http://dx.doi.org/10.1038/nature09535.
   PubMedGoogle Scholar
• Levine AJ. 1997. p53, the cellular gatekeeper for growth and division. Cell 88:323–331. http://dx.doi.org/10.1016/S0092-8674(00)81871-1.
   PubMed Web of Science ®Google Scholar
• Wu L, Levine AJ. 1997. 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 3:441–451.
   PubMed Web of Science ®Google Scholar
• Pomerantz J, Schreiber-Agus N, Liégeois NJ, Silverman A, Alland L, Chin L, Potes J, Chen K, Orlow I, Lee HW, Cordon-Cardo C, DePinho RA. 1998. The Ink4a tumor suppressor gene product, p19Arf, interacts with MDM2 and neutralizes MDM2's inhibition of p53. Cell 92:713–723. http://dx.doi.org/10.1016/S0092-8674(00)81400-2.
   PubMed Web of Science ®Google Scholar
• Chen J, Wu X, Lin J, Levine AJ. 1996. mdm-2 inhibits the G1 arrest and apoptosis functions of the p53 tumor suppressor protein. Mol Cell Biol 16:2445–2452. http://dx.doi.org/10.1128/MCB.16.5.2445.
   PubMed Web of Science ®Google Scholar
• Finlay CA. 1993. The mdm-2 oncogene can overcome wild-type p53 suppression of transformed cell growth. Mol Cell Biol 13:301–306. http://dx.doi.org/10.1128/MCB.13.1.301.
   PubMed Web of Science ®Google Scholar
• Momand J, Zambetti GP, Olson DC, George D, Levine AJ. 1992. The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell 69:1237–1245. http://dx.doi.org/10.1016/0092-8674(92)90644-R.
   PubMed Web of Science ®Google Scholar
• Haupt Y, Maya R, Kazaz A, Oren M. 1997. Mdm2 promotes the rapid degradation of p53. Nature 387:296–299. http://dx.doi.org/10.1038/387296a0.
   PubMed Web of Science ®Google Scholar
• Kubbutat MH, Jones SN, Vousden KH. 1997. Regulation of p53 stability by Mdm2. Nature 387:299–303. http://dx.doi.org/10.1038/387299a0.
   PubMed Web of Science ®Google Scholar
• Ramos YF, Stad R, Attema J, Peltenburg LT, van der Eb AJ, Jochemsen AG. 2001. Aberrant expression of HDMX proteins in tumor cells correlates with wild-type p53. Cancer Res 61:1839–1842.
   PubMed Web of Science ®Google Scholar
• Lianes P, Orlow I, Zhang ZF, Oliva MR, Sarkis AS, Reuter VE, Cordon-Cardo C. 1994. Altered patterns of MDM2 and TP53 expression in human bladder cancer. J Natl Cancer Inst 86:1325–1330. http://dx.doi.org/10.1093/jnci/86.17.1325.
   PubMed Web of Science ®Google Scholar
• Gorgoulis VG, Zoumpourlis V, Rassidakis GZ, Karameris A, Rassidakis AN, Spandidos DA, Kittas C. 1996. A molecular and immunohistochemical study of the MDM2 protein isoforms and p53 gene product in bronchogenic carcinoma. J Pathol 180:129–137.
   PubMed Web of Science ®Google Scholar
• Leach FS, Tokino T, Meltzer P, Burrell M, Oliner JD, Smith S, Hill DE, Sidransky D, Kinzler KW, Vogelstein B. 1993. p53 mutation and MDM2 amplification in human soft tissue sarcomas. Cancer Res 53:2231–2234.
   PubMed Web of Science ®Google Scholar
• Vassilev LT. 2004. Small-molecule antagonists of p53-MDM2 binding: research tools and potential therapeutics. Cell Cycle 3:419–421.
   PubMed Web of Science ®Google Scholar
• Choe YJ, Lee SY, Ko KW, Shin SJ, Kim HS. 2014. Nutlin-3 induces HO-1 expression by activating JNK in a transcription-independent manner of p53. Int J Oncol 44:761–768.
   PubMed Web of Science ®Google Scholar
• Baek KH, Bhang D, Zaslavsky A, Wang LC, Vachani A, Kim CF, Albelda SM, Evan GI, Ryeom S. 2013. Thrombospondin-1 mediates oncogenic Ras-induced senescence in premalignant lung tumors. J Clin Investig 123:4375–4389. http://dx.doi.org/10.1172/JCI67465.
   PubMed Web of Science ®Google Scholar
• Lee SY, Shin SJ, Kim HS. 2013. ERK1/2 activation mediated by the nutlin-3-induced mitochondrial translocation of p53. Int J Oncol 42:1027–1035.
   PubMed Web of Science ®Google Scholar
• Bragado P, Armesilla A, Silva A, Porras A. 2007. Apoptosis by cisplatin requires p53 mediated p38alpha MAPK activation through ROS generation. Apoptosis 12:1733–1742. http://dx.doi.org/10.1007/s10495-007-0082-8.
   PubMed Web of Science ®Google Scholar
• Eischen CM, Lozano G. 2014. The Mdm network and its regulation of p53 activities: a rheostat of cancer risk. Hum Mutat 35:728–737. http://dx.doi.org/10.1002/humu.22524.
   PubMed Web of Science ®Google Scholar
• Wade M, Li YC, Wahl GM. 2013. MDM2, MDMX and p53 in oncogenesis and cancer therapy. Nat Rev Cancer 13:83–96. http://dx.doi.org/10.1038/nrc3430.
   PubMed Web of Science ®Google Scholar
• Esteller M. 2002. CpG island hypermethylation and tumor suppressor genes: a booming present, a brighter future. Oncogene 21:5427–5440. http://dx.doi.org/10.1038/sj.onc.1205600.
   PubMed Web of Science ®Google Scholar
• Xue W, Zender L, Miething C, Dickins RA, Hernando E, Krizhanovsky V, Cordon-Cardo C, Lowe SW. 2007. Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature 445:656–660. http://dx.doi.org/10.1038/nature05529.
   PubMed Web of Science ®Google Scholar
• Ventura A, Kirsch DG, McLaughlin ME, Tuveson DA, Grimm J, Lintault L, Newman J, Reczek EE, Weissleder R, Jacks T. 2007. Restoration of p53 function leads to tumour regression in vivo. Nature 445:661–665. http://dx.doi.org/10.1038/nature05541.
   PubMed Web of Science ®Google Scholar
• Shchors K, Persson AI, Rostker F, Tihan T, Lyubynska N, Li N, Swigart LB, Berger MS, Hanahan D, Weiss WA, Evan GI. 2013. Using a preclinical mouse model of high-grade astrocytoma to optimize p53 restoration therapy. Proc Natl Acad Sci U S A 110:E1480–E1489. http://dx.doi.org/10.1073/pnas.1219142110.
   PubMedGoogle Scholar
• Riley MF, Lozano G. 2012. The many faces of MDM2 binding partners. Genes Cancer 3:226–239. http://dx.doi.org/10.1177/1947601912455322.
   PubMedGoogle Scholar
• Manfredi JJ. 2010. The Mdm2-p53 relationship evolves: Mdm2 swings both ways as an oncogene and a tumor suppressor. Genes Dev 24:1580–1589. http://dx.doi.org/10.1101/gad.1941710.
   PubMed Web of Science ®Google Scholar
• Ganguli G, Wasylyk B. 2003. p53-independent functions of MDM2. Mol Cancer Res 1:1027–1035.
   PubMed Web of Science ®Google Scholar
• Jackson JG, Pant V, Li Q, Chang LL, Quintás-Cardama A, Garza D, Tavana O, Yang P, Manshouri T, Li Y, El-Naggar AK, Lozano G. 2012. p53-mediated senescence impairs the apoptotic response to chemotherapy and clinical outcome in breast cancer. Cancer Cell 21:793–806. http://dx.doi.org/10.1016/j.ccr.2012.04.027.
   PubMed Web of Science ®Google Scholar
• Hallett RM, Huang C, Motazedian A, Auf der Mauer S, Pond GR, Hassell JA, Nordon RE, Draper JS. 2015. Treatment-induced cell cycle kinetics dictate tumor response to chemotherapy. Oncotarget 6:7040–7052. http://dx.doi.org/10.18632/oncotarget.3140.
   PubMedGoogle Scholar
• Sarkisian CJ, Keister BA, Stairs DB, Boxer RB, Moody SE, Chodosh LA. 2007. Dose-dependent oncogene-induced senescence in vivo and its evasion during mammary tumorigenesis. Nat Cell Biol 9:493–505. http://dx.doi.org/10.1038/ncb1567.
   PubMed Web of Science ®Google Scholar
• Juntilla MM, Patil VD, Calamito M, Joshi RP, Birnbaum MJ, Koretzky GA. 2010. AKT1 and AKT2 maintain hematopoietic stem cell function by regulating reactive oxygen species. Blood 115:4030–4038. http://dx.doi.org/10.1182/blood-2009-09-241000.
   PubMed Web of Science ®Google Scholar
• Gire V, Wynford-Thomas D. 1998. Reinitiation of DNA synthesis and cell division in senescent human fibroblasts by microinjection of anti-p53 antibodies. Mol Cell Biol 18:1611–1621. http://dx.doi.org/10.1128/MCB.18.3.1611.
   PubMedGoogle Scholar
• Li M, Lockwood W, Zielenska M, Northcott P, Ra YS, Bouffet E, Yoshimoto M, Rutka JT, Yan H, Taylor MD, Eberhart C, Hawkins CE, Lam W, Squire JA, Huang A. 2012. Multiple CDK/CYCLIND genes are amplified in medulloblastoma and supratentorial primitive neuroectodermal brain tumor. Cancer Genet 205:220–231. http://dx.doi.org/10.1016/j.cancergen.2012.03.002.
   PubMedGoogle Scholar
• Becker LE, Hinton D. 1983. Primitive neuroectodermal tumors of the central nervous system. Hum Pathol 14:538–550. http://dx.doi.org/10.1016/S0046-8177(83)80006-9.
   PubMedGoogle Scholar
• Li MH, Bouffet E, Hawkins CE, Squire JA, Huang A. 2005. Molecular genetics of supratentorial primitive neuroectodermal tumors and pineoblastoma. Neurosurg Focus 19:E3.
   PubMedGoogle Scholar
• Johnston DL, Keene DL, Lafay-Cousin L, Steinbok P, Sung L, Carret AS, Crooks B, Strother D, Wilson B, Odame I, Eisenstat DD, Mpofu C, Zelcer S, Huang A, Bouffet E. 2008. Supratentorial primitive neuroectodermal tumors: a Canadian pediatric brain tumor consortium report. J Neurooncol 86:101–108. http://dx.doi.org/10.1007/s11060-007-9440-1.
   PubMedGoogle Scholar
• Jakacki RI. 2005. Treatment strategies for high-risk medulloblastoma and supratentorial primitive neuroectodermal tumors. Review of the literature. J Neurosurg 102:44–52.
   PubMedGoogle Scholar
• Larson JD, Largaespada DA. 2012. Review: in vivo models for defining molecular subtypes of the primitive neuroectodermal tumor genome: current challenges and solutions. In Vivo 26:487–500.
   PubMedGoogle Scholar
• Kraus JA, Felsberg J, Tonn JC, Reifenberger G, Pietsch T. 2002. Molecular genetic analysis of the TP53, PTEN, CDKN2A, EGFR, CDK4 and MDM2 tumour-associated genes in supratentorial primitive neuroectodermal tumours and glioblastomas of childhood. Neuropathol Appl Neurobiol 28:325–333. http://dx.doi.org/10.1046/j.1365-2990.2002.00413.x.
   PubMedGoogle Scholar
• Zak K, Pecak A, Rys B, Wladyka B, Dömling A, Weber L, Holak TA, Dubin G. 2013. Mdm2 and MdmX inhibitors for the treatment of cancer: a patent review (2011-present). Expert Opin Ther Pat 23:425–448. http://dx.doi.org/10.1517/13543776.2013.765405.
   PubMed Web of Science ®Google Scholar
• Nag S, Zhang X, Srivenugopal KS, Wang MH, Wang W, Zhang R. 2014. Targeting MDM2-p53 interaction for cancer therapy: are we there yet? Curr Med Chem 21:553–574. http://dx.doi.org/10.2174/09298673113206660325.
   PubMed Web of Science ®Google Scholar
• Van Maerken T, Rihani A, Van Goethem A, De Paepe A, Speleman F, Vandesompele J. 2014. Pharmacologic activation of wild-type p53 by nutlin therapy in childhood cancer. Cancer Lett 344:157–165. http://dx.doi.org/10.1016/j.canlet.2013.11.002.
   PubMed Web of Science ®Google Scholar
• Zawacka-Pankau J, Selivanova G. 2015. Pharmacological reactivation of p53 as a strategy to treat cancer. J Intern Med 277:248–259. http://dx.doi.org/10.1111/joim.12336.
   PubMed Web of Science ®Google Scholar
• Duffy MJ, Synnott NC, McGowan PM, Crown J, O'Connor D, Gallagher WM. 2014. p53 as a target for the treatment of cancer. Cancer Treat Rev 40:1153–1160. http://dx.doi.org/10.1016/j.ctrv.2014.10.004.
   PubMed Web of Science ®Google Scholar
• Khoo KH, Hoe KK, Verma CS, Lane DP. 2014. Drugging the p53 pathway: understanding the route to clinical efficacy. Nat Rev Drug Discov 13:217–236. http://dx.doi.org/10.1038/nrd4236.
   PubMed Web of Science ®Google Scholar
• Brown CJ, Lain S, Verma CS, Fersht AR, Lane DP. 2009. Awakening guardian angels: drugging the p53 pathway. Nat Rev Cancer 9:862–873. http://dx.doi.org/10.1038/nrc2763.
   PubMed Web of Science ®Google Scholar
• Cheok CF, Verma CS, Baselga J, Lane DP. 2011. Translating p53 into the clinic. Nat Rev Clin Oncol 8:25–37. http://dx.doi.org/10.1038/nrclinonc.2010.174.
   PubMed Web of Science ®Google Scholar