The 1,2-diaminocyclohexane carrier ligand in oxaliplatin induces p53-dependent transcriptional repression of factors involved in thymidylate biosynthesis

Molecular Cancer Therapeutics

Volumn 14, Issue 10, 2015, Pages 2332-2342

  Kiyonari, Shinichi ^a,b   Iimori, Makoto ^c   Matsuoka, Kazuaki ^a,d   Watanabe, Sugiko ^a   Morikawa Ichinose, Tomomi ^e   Miura, Daisuke ^e   Niimi, Shinichiro ^a,d   Saeki, Hiroshi ^c   Tokunaga, Eriko ^c   Oki, Eiji ^c   Morita, Masaru ^c   Kadomatsu, Kenji ^b   Maehara, Yoshihiko ^a,c   Kitao, Hiroyuki ^a,c  

^a KYUSHU UNIVERSITY   (Japan)

^b NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c KYUSHU UNIVERSITY   (Japan)

^d TAIHO PHARMACEUTICAL CO LTD   (Japan)

^e KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

1,2 DIAMINOCYCLOHEXANE; ANTINEOPLASTIC AGENT; DACHPLATIN; DEOXYURIDINE TRIPHOSPHATE PYROPHOSPHATASE; FLUOROURACIL; LIGAND; MICRORNA; MICRORNA 34A; NUTLIN 3; OXALIPLATIN; PARATHION; PROTEIN P53; THYMIDINE PHOSPHATE; THYMIDINE TRIPHOSPHATE; TRANSCRIPTION FACTOR E2F1; TRANSCRIPTION FACTOR E2F3; UNCLASSIFIED DRUG; DUTP PYROPHOSPHATASE; E2F1 PROTEIN, HUMAN; E2F3 PROTEIN, HUMAN; IMIDAZOLE DERIVATIVE; INORGANIC PYROPHOSPHATASE; MIRN34 MICRORNA, HUMAN; PIPERAZINE DERIVATIVE; PLATINUM COMPLEX; SP1 PROTEIN, HUMAN; TP53 PROTEIN, HUMAN; TRANSCRIPTION FACTOR SP1;

ARTICLE; CONTROLLED STUDY; DNA ADDUCT; DOWN REGULATION; DRUG CYTOTOXICITY; DRUG POTENTIATION; GENE EXPRESSION; GENE REPRESSION; HUMAN; HUMAN CELL; NUCLEIC ACID SYNTHESIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UPREGULATION; BIOSYNTHESIS; CHEMISTRY; DNA REPLICATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC TRANSCRIPTION; GENETICS; HCT116 CELL LINE; METABOLISM; PHYSIOLOGY;

BIOSYNTHETIC PATHWAYS; DNA REPLICATION; DOWN-REGULATION; DRUG SYNERGISM; E2F1 TRANSCRIPTION FACTOR; E2F3 TRANSCRIPTION FACTOR; FLUOROURACIL; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; HCT116 CELLS; HUMANS; IMIDAZOLES; MICRORNAS; ORGANOPLATINUM COMPOUNDS; PIPERAZINES; PYROPHOSPHATASES; SP1 TRANSCRIPTION FACTOR; THYMIDINE MONOPHOSPHATE; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84946782559     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-14-0748     Document Type: Article

References (44)

1. Kelland L. The resurgence of platinum-based cancer chemotherapy. Nat Rev Cancer 2007;7:573-84.
2. Jung Y, Lippard SJ. Direct cellular responses to platinum-induced DNA damage. Chem Rev 2007;107:1387-407.
3. Voland C, Bord A, Peleraux A, Penarier G, Carriere D, Galiegue S, et al. Repression of cell-cycle-related proteins by oxaliplatin but not cisplatin in human colon cancer cells. Mol Cancer Ther 2006;5:2149-57.
4. de Gramont A, Figer A, Seymour M, Homerin M, Hmissi A, Cassidy J, et al. Leucovorin and fluorouracil with or without oxaliplatin as first-line treatment in advanced colorectal cancer. J Clin Oncol 2000;18:2938-47.
5. Pettersen HS, Visnes T, Vagbo CB, Svaasand EK, Doseth B, Slupphaug G, et al. UNG-initiated base excision repair is the major repair route for 5-fluorouracil in DNA, but 5-fluorouracil cytotoxicity depends mainly on RNA incorporation. Nucleic Acids Res 2011;39:8430-44.
6. Longley DB, Harkin DP, Johnston PG. 5-fluorouracil: mechanisms of action and clinical strategies. Nat Rev Cancer 2003;3:330-8.
7. Vertessy BG, Toth J. Keeping uracil out of DNA: physiological role, structure and catalytic mechanism of dUTPases. Acc Chem Res 2009;42:97-106.
8. Ladner RD, Lynch FJ, Groshen S, Xiong YP, Sherrod A, Caradonna SJ, et al. dUTP nucleotidohydrolase isoform expression in normal and neoplastic tissues: association with survival and response to 5-fluorouracil in colorectal cancer. Cancer Res 2000;60:3493-503.
9. Koehler SE, Ladner RD. Small interfering RNA-mediated suppression of dUTPase sensitizes cancer cell lines to thymidylate synthase inhibition. Mol Pharmacol 2004;66:620-6.
10. Takatori H, Yamashita T, Honda M, Nishino R, Arai K, Yamashita T, et al. dUTP pyrophosphatase expression correlates with a poor prognosis in hepatocellular carcinoma. Liver Int 2010;30:438-46.
11. Wilson PM, LaBonte MJ, Lenz HJ, Mack PC, Ladner RD. Inhibition of dUTPase induces synthetic lethality with thymidylate synthase-targeted therapies in non-small cell lung cancer. Mol Cancer Ther 2012;11: 616-28.
12. Alcindor T, Beauger N. Oxaliplatin: a review in the era of molecularly targeted therapy. Curr Oncol 2011;18:18-25.
13. Yeh KH, Cheng AL, Wan JP, Lin CS, Liu CC. Down-regulation of thymidylate synthase expression and its steady-state mRNA by oxaliplatin in colon cancer cells. Anticancer Drugs 2004;15:371-6.
14. Wilson PM, Fazzone W, LaBonte MJ, Lenz HJ, Ladner RD. Regulation of human dUTPase gene expression and p53-mediated transcriptional repression in response to oxaliplatin-induced DNA damage. Nucleic Acids Res 2009;37:78-95.
15. Hermeking H. The miR-34 family in cancer and apoptosis. Cell Death Differ 2010;17:193-9.
16. Tazawa H, Tsuchiya N, Izumiya M, Nakagama H. Tumor-suppressive miR-34a induces senescence-like growth arrest through modulation of the E2F pathway in human colon cancer cells. Proc Natl Acad Sci U S A 2007;104:15472-7.
17. Vassilev LT, Vu BT, Graves B, Carvajal D, Podlaski F, Filipovic Z, et al. In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 2004;303:844-8.
18. Zauli G, Voltan R, di Iasio MG, Bosco R, Melloni E, Sana ME, et al. miR-34a induces the downregulation of both E2F1 and B-Myb oncogenes in leukemic cells. Clin Cancer Res 2011;17:2712-24.
19. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 2001;411:494-8.
20. Matsuoka K, Iimori M, Niimi S, Tsukihara H, Watanabe S, Kiyonari S, et al. Trifluridine induces p53-dependent sustained G2 phase arrest with its massive misincorporation into DNA and few DNA strand breaks. Mol Cancer Ther 2015;14:1004-13.
21. Paris R, Henry RE, Stephens SJ, McBryde M, Espinosa JM. Multiple p53-independent gene silencing mechanisms define the cellular response to p53 activation. Cell Cycle 2008;7:2427-33.
22. Setoyama D, Fujimura Y, Miura D. Metabolomics reveals that carnitine palmitoyltransferase-1 is a novel target for oxidative inactivation in human cells. Genes Cells 2013;18:1107-19.
23. Kato H, Izumi Y, Hasunuma T, Matsuda F, Kondo A. Widely targeted metabolic profiling analysis of yeast central metabolites. J Biosci Bioeng 2012;113:665-73.
24. Wilson PM, Fazzone W, LaBonte MJ, Deng J, Neamati N, Ladner RD. Novel opportunities for thymidylate metabolism as a therapeutic target. Mol Cancer Ther 2008;7:3029-37.
25. Rochette PJ, Bastien N, Lavoie J, Guerin SL, Drouin R. SW480, a p53 double-mutant cell line retains proficiency for some p53 functions. J Mol Biol 2005;352:44-57.
26. He G, Kuang J, Khokhar AR, Siddik ZH. The impact of S- and G2-checkpoint response on the fidelity of G1-arrest by cisplatin and its comparison to a non-cross-resistant platinum(IV) analog. GynecolOncol 2011;122:402-9.
27. Cimprich KA, Cortez D. ATR: an essential regulator of genome integrity. Nat Rev Mol Cell Biol 2008;9:616-27.
28. Lakin ND, Jackson SP. Regulation of p53 in response to DNA damage. Oncogene 1999;18:7644-55.
29. Shangary S, Ding K, Qiu S, Nikolovska-Coleska Z, Bauer JA, Liu M, et al. Reactivation of p53 by a specific MDM2 antagonist (MI-43) leads to p21-mediated cell-cycle arrest and selective cell death in colon cancer. Mol Cancer Ther 2008;7:1533-42.
30. Johnson DG, Ohtani K, Nevins JR. Autoregulatory control of E2F1 expression in response to positive and negative regulators of cell-cycle progression. Genes Dev 1994;8:1514-25.
31. Hermeking H. p53 enters the microRNA world. Cancer Cell 2007;12: 414-8.
32. Wilson PM, Danenberg PV, Johnston PG, Lenz HJ, Ladner RD. Standing the test of time: targeting thymidylate biosynthesis in cancer therapy. Nat Rev Clin Oncol 2014;11:282-98.
33. Munch-Petersen B. Enzymatic regulation of cytosolic thymidine kinase 1 and mitochondrial thymidine kinase 2: amini review. Nucleosides Nucleotides Nucleic Acids 2010;29:363-9.
34. Lin SY, Black AR, Kostic D, Pajovic S, Hoover CN, Azizkhan JC. Cell-cycle-regulated association of E2F1 and Sp1 is related to their functional interaction. Mol Cell Biol 1996;16:1668-75.
35. McEntee G, Minguzzi S, O'Brien K, Ben Larbi N, Loscher C, O'Fagain C, et al. The former annotated human pseudogene dihydrofolate reductase-like 1 (DHFRL1) is expressed and functional. Proc Natl Acad Sci U S A 2011;108:15157-62.
36. Tommasi S, Pfeifer GP. Constitutive protection of E2F recognition sequences in the human thymidine kinase promoter during cell-cycle progression. J Biol Chem 1997;272:30483-90.
37. Dong S, Lester L, Johnson LF. Transcriptional control elements and complex initiation pattern of the TATA-less bidirectional human thymidylate synthase promoter. J Cell Biochem 2000;77:50-64.
38. Andre T, Boni C, Navarro M, Tabernero J, Hickish T, Topham C, et al. Improved overall survival with oxaliplatin, fluorouracil, and leucovorin as adjuvant treatment in stage II or III colon cancer in the MOSAIC trial. J Clin Oncol 2009;27:3109-16.
39. Yothers G, O'Connell MJ, Allegra CJ, Kuebler JP, Colangelo LH, Petrelli NJ, et al. Oxaliplatin as adjuvant therapy for colon cancer: updated results of NSABP C-07 trial, including survival and subset analyses. J Clin Oncol 2011;29:3768-74.
40. de Bruijn MT, Raats DA, Hoogwater FJ, van Houdt WJ, Cameron K, Medema JP, et al. Oncogenic KRAS sensitises colorectal tumour cells to chemotherapy by p53-dependent induction of Noxa. Br J Cancer 2010; 102:1254-64.
41. Liu HF, Hu HC, Chao JI. Oxaliplatin down-regulates survivin by p38 MAP kinase and proteasome in human colon cancer cells. Chem Biol Interact 2010;188:535-45.
42. Wilson PM, Labonte MJ, Russell J, Louie S, Ghobrial AA, Ladner RD. A novel fluorescence-based assay for the rapid detection and quantification of cellular deoxyribonucleoside triphosphates. Nucleic Acids Res 2011;39: e112.
43. Zaanan A, Cuilliere-Dartigues P, Guilloux A, Parc Y, Louvet C, de Gramont A, et al. Impact of p53 expression and microsatellite instability on stage III colon cancer disease-free survival in patients treated by 5-fluorouracil and leucovorin with or without oxaliplatin. Ann Oncol 2010;21:772-80.
44. Kim ST, Lee J, Park SH, Park JO, Lim HY, Kang WK, et al. Clinical impact of microsatellite instability in colon cancer following adjuvant FOLFOX therapy. Cancer Chemother Pharmacol 2010;66:659-67.