Increasing cisplatin sensitivity by scheduledependent inhibition of AKT and Chk1

Cancer Biology and Therapy

Volumn 15, Issue 12, 2014, Pages 1600-1612

  Duan, Lei ^a   Perez, Ricardo E ^a   Hansen, Michael ^a   Gitelis, Steven ^a   Maki, Carl G ^a  

^a RUSH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

AKT; Apoptosis; Chk1; Cisplatin; Osteosarcoma; P53

Indexed keywords

8 [4 (1 AMINOCYCLOBUTYL)PHENYL] 9 PHENYL 1,2,4 TRIAZOLO[3,4 F][1,6]NAPHTHYRIDIN 3(2H) ONE; CHECKPOINT KINASE 1; CISPLATIN; PROTEIN KINASE B; PROTEIN P27; PROTEIN P53; RABUSERTIB; ANTINEOPLASTIC AGENT; CYCLIN DEPENDENT KINASE INHIBITOR 1B; FUSED HETEROCYCLIC RINGS; PROTEIN KINASE; PROTEIN KINASE INHIBITOR; SMALL INTERFERING RNA;

APOPTOSIS; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CANCER SURVIVAL; CELL SURVIVAL; CHEMOSENSITIVITY; CONTROLLED STUDY; DRUG EFFICACY; DRUG SENSITIVITY; ENZYME ACTIVATION; ENZYME INHIBITION; G1 PHASE CELL CYCLE CHECKPOINT; MONOTHERAPY; NOXA GENE; OSTEOSARCOMA CELL LINE; PROTEIN EXPRESSION; PUMA GENE; TUMOR GENE; WILD TYPE; ANTAGONISTS AND INHIBITORS; CELL CYCLE CHECKPOINT; DNA DAMAGE; DRUG EFFECTS; DRUG RESISTANCE; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; HUMAN; METABOLISM; PHOSPHORYLATION; RNA INTERFERENCE; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; CISPLATIN; CYCLIN-DEPENDENT KINASE INHIBITOR P27; DNA DAMAGE; DRUG RESISTANCE, NEOPLASM; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HETEROCYCLIC COMPOUNDS, 3-RING; HUMANS; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTEIN KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RNA INTERFERENCE; RNA, SMALL INTERFERING; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84920110056     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/15384047.2014.961876     Document Type: Article

References (56)

1. Eastman A. Cell cycle checkpoints and their impact on anticancer therapeutic strategies. J Cell Biochem 2004; 91:223-31; PMID:14743382; http://dx.doi.org/ 10.1002/jcb.10699
2. Mitchison TJ. The proliferation rate paradox in antimitotic chemotherapy. Mol Biol Cell 2012; 23:1-6; PMID:22210845; http://dx.doi.org/10.1091/mbc.E10-04-0335
3. Lu C, Fu W, Zhao D, Mattson MP. The DNA damaging agent etoposide activates a cell survival pathway involving alpha-amino-3-hydroxy-5-methylisoxazole-4-propionate receptors and mitogen-activated protein kinases in hippocampal neurons. J Neurosci Res 2002; 70:671-9; PMID:12424735; http://dx.doi.org/ 10.1002/jnr.10413
4. Wang X, McCullough KD, Franke TF, Holbrook NJ. Epidermal growth factor receptor-dependent Akt activation by oxidative stress enhances cell survival. J Biol Chem 2000; 275:14624-31; PMID:10799549; http:// dx.doi.org/10.1074/jbc.275.19.14624
5. Li HF, Kim JS, Waldman T. Radiation-induced Akt activation modulates radioresistance in human glioblastoma cells. Radiation Oncol 2009; 4:43; http://dx.doi. org/10.1186/1748-717X-4-43
6. Smith J, Tho LM, Xu N, Gillespie DA. The ATMChk2 and ATR-Chk1 pathways in DNA damage signaling and cancer. Adv Can Res 2010; 108:73-112; PMID:21034966; http://dx.doi.org/10.1016/B978-0-12-380888-2.00003-0
7. el-DeiryWS, Tokino T, Velculescu VE, Levy DB, Parsons R, Trent JM, Lin D, Mercer WE, Kinzler KW, Vogelstein B. WAF1, a potential mediator of p53 tumor suppression. Cell 1993; 75:817-25; PMID:8242752; http://dx.doi.org/ 10.1016/0092-8674(93)90500-P
8. Xiong Y, Hannon GJ, Zhang H, Casso D, Kobayashi R, Beach D. p21 is a universal inhibitor of cyclin kinases. Nature 1993; 366:701-4; PMID:8259214; http:// dx.doi.org/10.1038/366701a0
9. Carvajal LA, Manfredi JJ. Another fork in the road-life or death decisions by the tumour suppressor p53. EMBO Rep 2013; 14:414-21; PMID:23588418; http://dx.doi.org/10.1038/embor.2013.25
10. Oda K, Arakawa H, Tanaka T, Matsuda K, Tanikawa C, Mori T, Nishimori H, Tamai K, Tokino T, Nakamura Y, et al. p53AIP1, a potential mediator of p53-dependent apoptosis, and its regulation by Ser-46-phosphorylated p53. Cell 2000; 102:849-62; PMID:11030628; http://dx.doi.org/10.1016/S0092-8674(00)00073-8
11. Zachos G, Rainey MD, Gillespie DA. Chk1-dependent S-M checkpoint delay in vertebrate cells is linked to maintenance of viable replication structures. Mol Cell Biol 2005; 25:563-74; PMID:15632059; http://dx.doi. org/10.1128/MCB.25.2.563-574.2005
12. Feijoo C, Hall-Jackson C, Wu R, Jenkins D, Leitch J, Gilbert DM, Smythe C. Activation of mammalian Chk1 during DNA replication arrest: a role for Chk1 in the intra-S phase checkpoint monitoring replication origin firing. J Cell Biol 2001; 154:913-23; PMID:11535615; http://dx. doi.org/10.1083/jcb.200104099
13. Chen T, Stephens PA, Middleton FK, Curtin NJ. Targeting the S and G2 checkpoint to treat cancer. Drug Discov Today 2012; 17:194-202; PMID:22192883; http://dx.doi.org/10.1016/j.drudis.2011.12.009
14. Taylor WR, Stark GR. Regulation of the G2/M transition by p53. Oncogene 2001; 20:1803-15; PMID:11313928; http://dx.doi.org/10.1038/sj.onc.1204252
15. Norbury C, Blow J, Nurse P. Regulatory phosphorylation of the p34cdc2 protein kinase in vertebrates. EMBO J 1991; 10:3321-9; PMID:1655417
16. Iliakis G, Wang Y, Guan J, Wang H. DNA damage checkpoint control in cells exposed to ionizing radiation. Oncogene 2003; 22:5834-47; PMID:12947390; http://dx.doi.org/10.1038/sj.onc.1206682
17. Kawabe T. G2 checkpoint abrogators as anticancer drugs. Mol Can Ther 2004; 3:513-9; PMID:15078995
18. Bunz F, Dutriaux A, Lengauer C, Waldman T, Zhou S, Brown JP, Sedivy JM, Kinzler KW, Vogelstein B. Requirement for p53 and p21 to sustainG2 arrest afterDNA damage. Science 1998; 282:1497-501; PMID:9822382; http:// dx.doi.org/10.1126/science.282.5393.1497
19. Hermeking H, Lengauer C, Polyak K, He TC, Zhang L, Thiagalingam S, Kinzler KW, Vogelstein B. 14-3-3 sigma is a p53-regulated inhibitor of G2/M progression. Mol Cell 1997; 1:3-11; PMID:9659898; http:// dx.doi.org/10.1016/S1097-2765(00)80002-7
20. 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 Can Ther 2008; 7:252-62; http://dx. doi.org/10.1158/1535-7163.MCT-07-2066
21. Thompson R, Eastman A. The cancer therapeutic potential of Chk1 inhibitors: how mechanistic studies impact on clinical trial design. Br J Clin Pharmacol 2013; 76:358-69; PMID:23593991; http://dx.doi.org/ 10.1111/bcp.12139
22. Origanti S, Cai SR, Munir AZ, White LS, Piwnica-Worms H. Synthetic lethality of Chk1 inhibition combined with p53 and/or p21 loss during a DNA damage response in normal and tumor cells. Oncogene 2013; 32:577-88; PMID:22430210; http://dx.doi.org/ 10.1038/onc.2012.84
23. Bhaskar PT, Hay N. The two TORCs and Akt. Dev Cell 2007; 12:487-502; PMID:17419990; http://dx. doi.org/10.1016/j.devcel.2007.03.020
24. Zhang X, Tang N, Hadden TJ, Rishi AK. Akt, FoxO and regulation of apoptosis. Biochim Biophys Acta 2011; 1813:1978-86; PMID:21440011; http://dx.doi. org/10.1016/j.bbamcr.2011.03.010
25. Datta SR, Dudek H, Tao X, Masters S, Fu H, Gotoh Y, Greenberg ME. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 1997; 91:231-41; PMID: 9346240; http://dx.doi.org/10.1016/S0092-8674 (00)80405-5
26. Ogawara Y, Kishishita S, Obata T, Isazawa Y, Suzuki T, Tanaka K, Masuyama N, Gotoh Y. Akt enhances Mdm2-mediated ubiquitination and degradation of p53. J Biol Chem 2002; 277:21843-50; PMID:11923280; http://dx. doi.org/10.1074/jbc.M109745200
27. Mayo LD, Donner DB. A phosphatidylinositol 3-kinase/Akt pathway promotes translocation of Mdm2 from the cytoplasm to the nucleus. Proc Natl Acad Sci USA 2001; 98:11598-603; PMID:11504915; http:// dx.doi.org/10.1073/pnas.181181198
28. Stronach EA, Chen M, Maginn EN, Agarwal R, Mills GB, Wasan H, Gabra H. DNA-PK mediates AKT activation and apoptosis inhibition in clinically acquired platinum resistance. Neoplasia 2011; 13:1069-80; PMID:22131882
29. Rodemann HP, Dittmann K, Toulany M. Radiationinduced EGFR-signaling and control of DNA-damage repair. Int J Rad Oncol 2007; 83:781-91; PMID:18058366
30. Cosaceanu D, Budiu RA, Carapancea M, Castro J, Lewensohn R, Dricu A. Ionizing radiation activates IGF-1R triggering a cytoprotective signaling by interfering with Ku-DNA binding and by modulating Ku86 expression via a p38 kinase-dependent mechanism. Oncogene 2007; 26:2423-34; PMID:17043647; http://dx.doi.org/10.1038/sj.onc.1210037
31. Valerie K, Yacoub A, Hagan MP, Curiel DT, Fisher PB, Grant S, Dent P. Radiation-induced cell signaling: inside-out and outside-in. Mol Can Ther 2007; 6:789-801; http://dx.doi.org/10.1158/1535-7163.MCT-06-0596
32. Hirai H, Sootome H, Nakatsuru Y, Miyama K, Taguchi S, Tsujioka K, Ueno Y, Hatch H, Majumder PK, Pan BS, et al. MK-2206, an allosteric Akt inhibitor, enhances antitumor efficacy by standard chemotherapeutic agents or molecular targeted drugs in vitro and in vivo. Mol Can Ther 2010; 9:1956-67; http://dx.doi. org/10.1158/1535-7163.MCT-09-1012
33. Tonic I, Yu WN, Park Y, Chen CC, Hay N. Akt activation emulates Chk1 inhibition and Bcl2 overexpression and abrogates G2 cell cycle checkpoint by inhibiting BRCA1 foci. J Biol Chem 2010; 285:23790-8; PMID:20495005; http://dx.doi.org/ 10.1074/jbc.M110.104372
34. Shtivelman E, Sussman J, Stokoe D. A role for PI 3-kinase and PKB activity in the G2/M phase of the cell cycle. Curr Biol 2002; 12:919-24; PMID:12062056; http://dx.doi.org/10.1016/S0960-9822(02)00843-6
35. Liang J, Zubovitz J, Petrocelli T, Kotchetkov R, Connor MK, Han K, Lee JH, Ciarallo S, Catzavelos C, Beniston R, et al. PKB/Akt phosphorylates p27, impairs nuclear import of p27 and opposes p27-mediated G1 arrest. Nature Med 2002; 8:1153-60; PMID:12244302; http://dx.doi.org/10.1038/nm761
36. Rassidakis GZ, Feretzaki M, Atwell C, Grammatikakis I, Lin Q, Lai R, Claret FX, Medeiros LJ, Amin HM. Inhibition of Akt increases p27Kip1 levels and induces cell cycle arrest in anaplastic large cell lymphoma. Blood 2005; 105:827-9; PMID:15374880; http://dx. doi.org/10.1182/blood-2004-06-2125
37. O'Day K, Gorlick R. Novel therapeutic agents for osteosarcoma. Expert Rev Anticancer Ther 2009; 9:511-23; PMID:19374604; http://dx.doi.org/10.1586/ era.09.7
38. Kim JS, Lee C, Bonifant CL, Ressom H, Waldman T. Activation of p53-dependent growth suppression in human cells by mutations in PTEN or PIK3CA. Mol Cell Biol 2007; 27:662-77; PMID:17060456; http:// dx.doi.org/10.1128/MCB.00537-06
39. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM. Phosphorylation and regulation of AKT/PKB by the rictor-mTOR complex. Science 2005: 307:1098-1101; PMID:15718470; http://dx.doi. org/10.1126/science.1106148
40. Alessi DR, Andjelkovic M, Caudwell B, Cron P, Morrice N, Cohen P, Hemmings BA. Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J 1996; 15:6541-51; PMID:8978681
41. Capasso H, Palermo C, Wan S, Rao H, John UP, O'Connell MJ, Walworth NC. Phosphorylation activates Chk1 and is required for checkpoint-mediated cell cycle arrest. J Cell Sci 2002; 115:4555-64; PMID:12415000; http://dx.doi.org/10.1242/jcs.00133
42. Okita N, Minato S, Ohmi E, Tanuma S, Higami Y. DNA damage-induced CHK1 autophosphorylation at Ser296 is regulated by an intramolecular mechanism. FEBS Lett 2012; 586:3974-9; PMID:23068608; http://dx.doi.org/10.1016/j.febslet.2012.09.048
43. Shibue T, Suzuki S, Okamoto H, Yoshida H, Ohba Y, Takaoka A, Taniguchi T. Differential contribution of Puma and Noxa in dual regulation of p53-mediated apoptotic pathways. EMBO J 2006; 25:4952-62; PMID:17024184; http://dx.doi.org/ 10.1038/sj.emboj.7601359
44. Shibue T, Taniguchi T. BH3-only proteins: integrated control point of apoptosis. Int J Cancer 2006; 119:2036-43; PMID:16572413; http://dx.doi.org/ 10.1002/ijc.21751
45. Galluzzi L, Senovilla L, Vitale I, Michels J, Martins I, Kepp O, Castedo M, Kroemer G. Molecular mechanisms of cisplatin resistance. Oncogene 2012; 31:1869-83; PMID:21892204; http://dx.doi.org/10.1038/ onc.2011.384
46. KatouY, KanohY,BandoM,NoguchiH,TanakaH,Ashikari T, Sugimoto K, Shirahige K. S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex. Nature 2003; 424:1078-83; PMID:12944972; http://dx.doi.org/10.1038/nature01900
47. Kelsey I, Manning BD. mTORC1 status dictates tumor response to targeted therapeutics. Sci Signaling 2013; 6: pe31; http://dx.doi.org/10.1126/scisignal.2004632
48. Lee CH, Inoki K, Karbowniczek M, Petroulakis E, Sonenberg N, Henske EP, Guan KL. Constitutive mTOR activation in TSC mutants sensitizes cells to energy starvation and genomic damage via p53. EMBO J 2007; 26:4812-23; PMID:17962806; http://dx.doi. org/10.1038/sj.emboj.7601900
49. Alimonti A, Nardella C, Chen Z, Clohessy JG, Carracedo A, Trotman LC, Cheng K, Varmeh S, Kozma SC, Thomas G, et al. A novel type of cellular senescence that can be enhanced in mouse models and human tumor xenografts to suppress prostate tumorigenesis. J Clin Invest 2010; 120:681-93; PMID:20197621; http://dx.doi.org/10.1172/JCI40535
50. Charvet C,WisslerM, Brauns-Schubert P,Wang SJ, Tang Y, Sigloch FC, Mellert H, Brandenburg M, Lindner SE, Breit B, et al. Phosphorylation of Tip60 by GSK-3 determines the induction of PUMA and apoptosis by p53. Mol Cell 2011; 42:584-96;PMID:21658600; http://dx.doi.org/ 10.1016/j.molcel.2011.03.033
51. Evans DL, Dive C. Effects of cisplatin on the induction of apoptosis in proliferating hepatoma cells and nonproliferating immature thymocytes. Cancer Res 1993; 53:2133-9; PMID:8481916
52. Fan S, Chang JK, Smith ML, Duba D, Fornace AJ Jr, O'Connor PM. Cells lacking CIP1/WAF1 genes exhibit preferential sensitivity to cisplatin and nitrogen mustard. Oncogene 1997; 14:2127-36; PMID:9174048; http://dx. doi.org/10.1038/sj.onc.1201052
53. Fan S, Smith ML, Rivet DJ 2nd, Duba D, Zhan Q, Kohn KW, Fornace AJ Jr, O'Connor PM. Disruption of p53 function sensitizes breast cancer MCF-7 cells to cisplatin and pentoxifylline. Cancer Res 1995; 55:1649-54; PMID:7712469
54. Xu N, Lao Y, Zhang Y, Gillespie DA. Akt: a doubleedged sword in cell proliferation and genome stability. J. Oncol. 2012: 2012:951724; PMID:22481935; http://dx.doi.org/10.1155/2012/951724
55. Parcellier A, Tintignac LA, Zhuravleva E, Hemmings BA. PKB and the mitochondria: AKTing on apoptosis. Cell Signaling 2008: 20:21-30; PMID:17716864; http://dx.doi.org/10.1016/j.cellsig.2007.07.010
56. Ali AY, Farrand L, Kim JY, Byun S, Suh JY, Lee HJ, Tsang BK. Molecular determinants of ovarian cancer chemoresistance: new insights into an old conundrum. Annals New York Acad. Sci. 2012: 1271:58-67; PMID:23050965; http://dx.doi.org/10.1111/j.1749-6632.2012.06734.x