1,631
Views
48
CrossRef citations to date
0
Altmetric
Report

CDK4 inhibition restores G₁-S arrest in MYCN-amplified neuroblastoma cells in the context of doxorubicin-induced DNA damage

, , , , , , , , & show all
Pages 1091-1104 | Received 23 Nov 2012, Accepted 23 Feb 2013, Published online: 05 Mar 2013

References

  • D’Angio GJ, Evans AE, Koop CE. Special pattern of widespread neuroblastoma with a favourable prognosis. Lancet 1971; 1:1046 - 9; http://dx.doi.org/10.1016/S0140-6736(71)91606-0; PMID: 4102970
  • Haas D, Ablin AR, Miller C, Zoger S, Matthay KK. Complete pathologic maturation and regression of stage IVS neuroblastoma without treatment. Cancer 1988; 62:818 - 25; http://dx.doi.org/10.1002/1097-0142(19880815)62:4<818::AID-CNCR2820620430>3.0.CO;2-K; PMID: 3293764
  • Evans AE, Gerson J, Schnaufer L. Spontaneous regression of neuroblastoma. Natl Cancer Inst Monogr 1976; 44:49 - 54; PMID: 1030781
  • De Bernardi B, Nicolas B, Boni L, Indolfi P, Carli M, Cordero Di Montezemolo L, et al, Italian Co-Operative Group for Neuroblastoma. Disseminated neuroblastoma in children older than one year at diagnosis: comparable results with three consecutive high-dose protocols adopted by the Italian Co-Operative Group for Neuroblastoma. J Clin Oncol 2003; 21:1592 - 601; http://dx.doi.org/10.1200/JCO.2003.05.191; PMID: 12697885
  • Matthay KK, Villablanca JG, Seeger RC, Stram DO, Harris RE, Ramsay NK, et al, Children’s Cancer Group. Treatment of high-risk neuroblastoma with intensive chemotherapy, radiotherapy, autologous bone marrow transplantation, and 13-cis-retinoic acid. N Engl J Med 1999; 341:1165 - 73; http://dx.doi.org/10.1056/NEJM199910143411601; PMID: 10519894
  • Zage PE, Kletzel M, Murray K, Marcus R, Castleberry R, Zhang Y, et al, Children’s Oncology Group. Outcomes of the POG 9340/9341/9342 trials for children with high-risk neuroblastoma: a report from the Children’s Oncology Group. Pediatr Blood Cancer 2008; 51:747 - 53; http://dx.doi.org/10.1002/pbc.21713; PMID: 18704922
  • Seeger RC, Brodeur GM, Sather H, Dalton A, Siegel SE, Wong KY, et al. Association of multiple copies of the N-myc oncogene with rapid progression of neuroblastomas. N Engl J Med 1985; 313:1111 - 6; http://dx.doi.org/10.1056/NEJM198510313131802; PMID: 4047115
  • Brodeur GM, Seeger RC, Schwab M, Varmus HE, Bishop JM. Amplification of N-myc in untreated human neuroblastomas correlates with advanced disease stage. Science 1984; 224:1121 - 4; http://dx.doi.org/10.1126/science.6719137; PMID: 6719137
  • Fulda S, Lutz W, Schwab M, Debatin KM. MycN sensitizes neuroblastoma cells for drug-induced apoptosis. Oncogene 1999; 18:1479 - 86; http://dx.doi.org/10.1038/sj.onc.1202435; PMID: 10050884
  • Lutz W, Fulda S, Jeremias I, Debatin KM, Schwab M. MycN and IFNgamma cooperate in apoptosis of human neuroblastoma cells. Oncogene 1998; 17:339 - 46; http://dx.doi.org/10.1038/sj.onc.1200201; PMID: 9690515
  • Paffhausen T, Schwab M, Westermann F. Targeted MYCN expression affects cytotoxic potential of chemotherapeutic drugs in neuroblastoma cells. Cancer Lett 2007; 250:17 - 24; http://dx.doi.org/10.1016/j.canlet.2006.09.010; PMID: 17141950
  • Bell E, Premkumar R, Carr J, Lu X, Lovat PE, Kees UR, et al. The role of MYCN in the failure of MYCN amplified neuroblastoma cell lines to G1 arrest after DNA damage. Cell Cycle 2006; 5:2639 - 47; http://dx.doi.org/10.4161/cc.5.22.3443; PMID: 17172827
  • Chen L, Iraci N, Gherardi S, Gamble LD, Wood KM, Perini G, et al. p53 is a direct transcriptional target of MYCN in neuroblastoma. Cancer Res 2010; 70:1377 - 88; http://dx.doi.org/10.1158/0008-5472.CAN-09-2598; PMID: 20145147
  • Knudsen KE, Booth D, Naderi S, Sever-Chroneos Z, Fribourg AF, Hunton IC, et al. RB-dependent S-phase response to DNA damage. Mol Cell Biol 2000; 20:7751 - 63; http://dx.doi.org/10.1128/MCB.20.20.7751-7763.2000; PMID: 11003670
  • Mayhew CN, Perkin LM, Zhang X, Sage J, Jacks T, Knudsen ES. Discrete signaling pathways participate in RB-dependent responses to chemotherapeutic agents. Oncogene 2004; 23:4107 - 20; http://dx.doi.org/10.1038/sj.onc.1207503; PMID: 15064736
  • Harrington EA, Bruce JL, Harlow E, Dyson N. pRB plays an essential role in cell cycle arrest induced by DNA damage. Proc Natl Acad Sci USA 1998; 95:11945 - 50; http://dx.doi.org/10.1073/pnas.95.20.11945; PMID: 9751770
  • Brugarolas J, Moberg K, Boyd SD, Taya Y, Jacks T, Lees JA. Inhibition of cyclin-dependent kinase 2 by p21 is necessary for retinoblastoma protein-mediated G1 arrest after gamma-irradiation. Proc Natl Acad Sci USA 1999; 96:1002 - 7; http://dx.doi.org/10.1073/pnas.96.3.1002; PMID: 9927683
  • Lowe SW, Bodis S, McClatchey A, Remington L, Ruley HE, Fisher DE, et al. p53 status and the efficacy of cancer therapy in vivo. Science 1994; 266:807 - 10; http://dx.doi.org/10.1126/science.7973635; PMID: 7973635
  • Carr-Wilkinson J, O’Toole K, Wood KM, Challen CC, Baker AG, Board JR, et al. High Frequency of p53/MDM2/p14ARF Pathway Abnormalities in Relapsed Neuroblastoma. Clin Cancer Res 2010; 16:1108 - 18; http://dx.doi.org/10.1158/1078-0432.CCR-09-1865; PMID: 20145180
  • Bell E, Chen L, Liu T, Marshall GM, Lunec J, Tweddle DA. MYCN oncoprotein targets and their therapeutic potential. Cancer Lett 2010; 293:144 - 57; http://dx.doi.org/10.1016/j.canlet.2010.01.015; PMID: 20153925
  • Tweddle DA, Pearson AD, Haber M, Norris MD, Xue C, Flemming C, et al. The p53 pathway and its inactivation in neuroblastoma. Cancer Lett 2003; 197:93 - 8; http://dx.doi.org/10.1016/S0304-3835(03)00088-0; PMID: 12880966
  • Carr-Wilkinson J, Griffiths R, Elston R, Gamble LD, Goranov B, Redfern CP, et al. Outcome of the p53-mediated DNA damage response in neuroblastoma is determined by morphological subtype and MYCN expression. Cell Cycle 2011; 10:3778 - 87; http://dx.doi.org/10.4161/cc.10.21.17973; PMID: 22052359
  • Eckerle I, Muth D, Batzler J, Henrich KO, Lutz W, Fischer M, et al. Regulation of BIRC5 and its isoform BIRC5-2B in neuroblastoma. Cancer Lett 2009; 285:99 - 107; http://dx.doi.org/10.1016/j.canlet.2009.05.007; PMID: 19497660
  • Westermann F, Muth D, Benner A, Bauer T, Henrich KO, Oberthuer A, et al. Distinct transcriptional MYCN/c-MYC activities are associated with spontaneous regression or malignant progression in neuroblastomas. Genome Biol 2008; 9:R150; http://dx.doi.org/10.1186/gb-2008-9-10-r150; PMID: 18851746
  • Slack A, Chen Z, Tonelli R, Pule M, Hunt L, Pession A, et al. The p53 regulatory gene MDM2 is a direct transcriptional target of MYCN in neuroblastoma. Proc Natl Acad Sci USA 2005; 102:731 - 6; http://dx.doi.org/10.1073/pnas.0405495102; PMID: 15644444
  • He J, Gu L, Zhang H, Zhou M. Crosstalk between MYCN and MDM2-p53 signal pathways regulates tumor cell growth and apoptosis in neuroblastoma. Cell Cycle 2011; 10:2994 - 3002; http://dx.doi.org/10.4161/cc.10.17.17118; PMID: 21862876
  • McKenzie PP, Guichard SM, Middlemas DS, Ashmun RA, Danks MK, Harris LC. Wild-type p53 can induce p21 and apoptosis in neuroblastoma cells but the DNA damage-induced G1 checkpoint function is attenuated. Clin Cancer Res 1999; 5:4199 - 207; PMID: 10632361
  • McKenzie PP, Danks MK, Kriwacki RW, Harris LC. P21Waf1/Cip1 dysfunction in neuroblastoma: a novel mechanism of attenuating G0-G1 cell cycle arrest. Cancer Res 2003; 63:3840 - 4; PMID: 12839982
  • Tweddle DA, Malcolm AJ, Cole M, Pearson AD, Lunec J. p53 cellular localization and function in neuroblastoma: evidence for defective G(1) arrest despite WAF1 induction in MYCN-amplified cells. Am J Pathol 2001; 158:2067 - 77; http://dx.doi.org/10.1016/S0002-9440(10)64678-0; PMID: 11395384
  • Keshelava N, Seeger RC, Groshen S, Reynolds CP. Drug resistance patterns of human neuroblastoma cell lines derived from patients at different phases of therapy. Cancer Res 1998; 58:5396 - 405; PMID: 9850071
  • Gewirtz DA. A critical evaluation of the mechanisms of action proposed for the antitumor effects of the anthracycline antibiotics adriamycin and daunorubicin. Biochem Pharmacol 1999; 57:727 - 41; http://dx.doi.org/10.1016/S0006-2952(98)00307-4; PMID: 10075079
  • Rouaud P, Fiancette R, Vincent-Fabert C, Magnone V, Cogné M, Dubus P, et al. Mantle cell lymphoma-like lymphomas in c-myc-3’RR/p53+/- mice and c-myc-3’RR/Cdk4R24C mice: differential oncogenic mechanisms but similar cellular origin. Oncotarget 2012; 3:586 - 93; PMID: 22592113
  • Muth D, Ghazaryan S, Eckerle I, Beckett E, Pöhler C, Batzler J, et al. Transcriptional repression of SKP2 is impaired in MYCN-amplified neuroblastoma. Cancer Res 2010; 70:3791 - 802; http://dx.doi.org/10.1158/0008-5472.CAN-09-1245; PMID: 20424123
  • Lutz W, Stöhr M, Schürmann J, Wenzel A, Löhr A, Schwab M. Conditional expression of N-myc in human neuroblastoma cells increases expression of alpha-prothymosin and ornithine decarboxylase and accelerates progression into S-phase early after mitogenic stimulation of quiescent cells. Oncogene 1996; 13:803 - 12; PMID: 8761302
  • Agami R, Bernards R. Distinct initiation and maintenance mechanisms cooperate to induce G1 cell cycle arrest in response to DNA damage. Cell 2000; 102:55 - 66; http://dx.doi.org/10.1016/S0092-8674(00)00010-6; PMID: 10929713
  • Burgess A, Wigan M, Giles N, Depinto W, Gillespie P, Stevens F, et al. Inhibition of S/G2 phase CDK4 reduces mitotic fidelity. J Biol Chem 2006; 281:9987 - 95; http://dx.doi.org/10.1074/jbc.M512714200; PMID: 16476733
  • Wohlbold L, Merrick KA, De S, Amat R, Kim JH, Larochelle S, et al. Chemical genetics reveals a specific requirement for Cdk2 activity in the DNA damage response and identifies Nbs1 as a Cdk2 substrate in human cells. PLoS Genet 2012; 8:e1002935; http://dx.doi.org/10.1371/journal.pgen.1002935; PMID: 22927831
  • Molenaar JJ, Ebus ME, Geerts D, Koster J, Lamers F, Valentijn LJ, et al. Inactivation of CDK2 is synthetically lethal to MYCN over-expressing cancer cells. Proc Natl Acad Sci USA 2009; 106:12968 - 73; http://dx.doi.org/10.1073/pnas.0901418106; PMID: 19525400
  • Kitagawa M, Higashi H, Jung HK, Suzuki-Takahashi I, Ikeda M, Tamai K, et al. The consensus motif for phosphorylation by cyclin D1-Cdk4 is different from that for phosphorylation by cyclin A/E-Cdk2. EMBO J 1996; 15:7060 - 9; PMID: 9003781
  • Serrano M, Hannon GJ, Beach D. A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4. Nature 1993; 366:704 - 7; http://dx.doi.org/10.1038/366704a0; PMID: 8259215
  • Chan FK, Zhang J, Cheng L, Shapiro DN, Winoto A. Identification of human and mouse p19, a novel CDK4 and CDK6 inhibitor with homology to p16ink4. Mol Cell Biol 1995; 15:2682 - 8; PMID: 7739548
  • Guan KL, Jenkins CW, Li Y, O’Keefe CL, Noh S, Wu X, et al. Isolation and characterization of p19INK4d, a p16-related inhibitor specific to CDK6 and CDK4. Mol Biol Cell 1996; 7:57 - 70; PMID: 8741839
  • Gogolin S, Dreidax D, Becker G, Ehemann V, Schwab M, Westermann F. MYCN/MYC-mediated drug resistance mechanisms in neuroblastoma. Int J Clin Pharmacol Ther 2010; 48:489 - 91; PMID: 20557856
  • Johnson SM, Torrice CD, Bell JF, Monahan KB, Jiang Q, Wang Y, et al. Mitigation of hematologic radiation toxicity in mice through pharmacological quiescence induced by CDK4/6 inhibition. J Clin Invest 2010; 120:2528 - 36; http://dx.doi.org/10.1172/JCI41402; PMID: 20577054
  • Baughn LB, Di Liberto M, Wu K, Toogood PL, Louie T, Gottschalk R, et al. A novel orally active small molecule potently induces G1 arrest in primary myeloma cells and prevents tumor growth by specific inhibition of cyclin-dependent kinase 4/6. Cancer Res 2006; 66:7661 - 7; http://dx.doi.org/10.1158/0008-5472.CAN-06-1098; PMID: 16885367
  • Finn RS, Dering J, Conklin D, Kalous O, Cohen DJ, Desai AJ, et al. PD 0332991, a selective cyclin D kinase 4/6 inhibitor, preferentially inhibits proliferation of luminal estrogen receptor-positive human breast cancer cell lines in vitro. Breast Cancer Res 2009; 11:R77; http://dx.doi.org/10.1186/bcr2419; PMID: 19874578
  • Konecny GE, Winterhoff B, Kolarova T, Qi J, Manivong K, Dering J, et al. Expression of p16 and retinoblastoma determines response to CDK4/6 inhibition in ovarian cancer. Clin Cancer Res 2011; 17:1591 - 602; http://dx.doi.org/10.1158/1078-0432.CCR-10-2307; PMID: 21278246
  • Marzec M, Kasprzycka M, Lai R, Gladden AB, Wlodarski P, Tomczak E, et al. Mantle cell lymphoma cells express predominantly cyclin D1a isoform and are highly sensitive to selective inhibition of CDK4 kinase activity. Blood 2006; 108:1744 - 50; http://dx.doi.org/10.1182/blood-2006-04-016634; PMID: 16690963
  • Wang L, Wang J, Blaser BW, Duchemin AM, Kusewitt DF, Liu T, et al. Pharmacologic inhibition of CDK4/6: mechanistic evidence for selective activity or acquired resistance in acute myeloid leukemia. Blood 2007; 110:2075 - 83; http://dx.doi.org/10.1182/blood-2007-02-071266; PMID: 17537993
  • Fry DW, Harvey PJ, Keller PR, Elliott WL, Meade M, Trachet E, et al. Specific inhibition of cyclin-dependent kinase 4/6 by PD 0332991 and associated antitumor activity in human tumor xenografts. Mol Cancer Ther 2004; 3:1427 - 38; PMID: 15542782
  • Michaud K, Solomon DA, Oermann E, Kim JS, Zhong WZ, Prados MD, et al. Pharmacologic inhibition of cyclin-dependent kinases 4 and 6 arrests the growth of glioblastoma multiforme intracranial xenografts. Cancer Res 2010; 70:3228 - 38; http://dx.doi.org/10.1158/0008-5472.CAN-09-4559; PMID: 20354191
  • Flaherty KT, Lorusso PM, Demichele A, Abramson VG, Courtney R, Randolph SS, et al. Phase I, dose-escalation trial of the oral cyclin-dependent kinase 4/6 inhibitor PD 0332991, administered using a 21-day schedule in patients with advanced cancer. Clin Cancer Res 2012; 18:568 - 76; http://dx.doi.org/10.1158/1078-0432.CCR-11-0509; PMID: 22090362
  • Leonard JP, LaCasce AS, Smith MR, Noy A, Chirieac LR, Rodig SJ, et al. Selective CDK4/6 inhibition with tumor responses by PD0332991 in patients with mantle cell lymphoma. Blood 2012; 119:4597 - 607; http://dx.doi.org/10.1182/blood-2011-10-388298; PMID: 22383795
  • Schwartz GK, LoRusso PM, Dickson MA, Randolph SS, Shaik MN, Wilner KD, et al. Phase I study of PD 0332991, a cyclin-dependent kinase inhibitor, administered in 3-week cycles (Schedule 2/1). Br J Cancer 2011; 104:1862 - 8; http://dx.doi.org/10.1038/bjc.2011.177; PMID: 21610706
  • www.clinicaltrials.gov/ct2/results?/term=PD-0332991.
  • Roberts PJ, Bisi JE, Strum JC, Combest AJ, Darr DB, Usary JE, et al. Multiple roles of cyclin-dependent kinase 4/6 inhibitors in cancer therapy. J Natl Cancer Inst 2012; 104:476 - 87; http://dx.doi.org/10.1093/jnci/djs002; PMID: 22302033
  • Sottile F, Gnemmi I, Cantilena S, D’Acunto WC, Sala A. A chemical screen identifies the chemotherapeutic drug topotecan as a specific inhibitor of the B-MYB/MYCN axis in neuroblastoma. Oncotarget 2012; 3:535 - 45; PMID: 22619121
  • Horvilleur E, Bauer M, Goldschneider D, Mergui X, de la Motte A, Bénard J, et al. p73alpha isoforms drive opposite transcriptional and post-transcriptional regulation of MYCN expression in neuroblastoma cells. Nucleic Acids Res 2008; 36:4222 - 32; http://dx.doi.org/10.1093/nar/gkn394; PMID: 18583365
  • Dunn T, Praissman L, Hagag N, Viola MV. ERG gene is translocated in an Ewing’s sarcoma cell line. Cancer Genet Cytogenet 1994; 76:19 - 22; http://dx.doi.org/10.1016/0165-4608(94)90063-9; PMID: 8076344
  • Henrich KO, Bauer T, Schulte J, Ehemann V, Deubzer H, Gogolin S, et al. CAMTA1, a 1p36 tumor suppressor candidate, inhibits growth and activates differentiation programs in neuroblastoma cells. Cancer Res 2011; 71:3142 - 51; http://dx.doi.org/10.1158/0008-5472.CAN-10-3014; PMID: 21385898
  • Afanasyeva EA, Mestdagh P, Kumps C, Vandesompele J, Ehemann V, Theissen J, et al. MicroRNA miR-885-5p targets CDK2 and MCM5, activates p53 and inhibits proliferation and survival. Cell Death Differ 2011; 18:974 - 84; http://dx.doi.org/10.1038/cdd.2010.164; PMID: 21233845
  • Ehemann V, Hashemi B, Lange A, Otto HF. Flow cytometric DNA analysis and chromosomal aberrations in malignant glioblastomas. Cancer Lett 1999; 138:101 - 6; http://dx.doi.org/10.1016/S0304-3835(98)00383-8; PMID: 10378780
  • Brueckner LM, Sagulenko E, Hess EM, Zheglo D, Blumrich A, Schwab M, et al. Genomic rearrangements at the FRA2H common fragile site frequently involve non-homologous recombination events across LTR and L1(LINE) repeats. Hum Genet 2012; 131:1345 - 59; http://dx.doi.org/10.1007/s00439-012-1165-3; PMID: 22476624

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.