The synergistic effects of DNA-damaging drugs cisplatin and etoposide with a histone deacetylase inhibitor valproate in high-risk neuroblastoma cells

International Journal of Oncology

Volumn 47, Issue 1, 2015, Pages 343-352

  Groh, Tomas ^a   Hrabeta, Jan ^a   Khalil, Mohammed Ashraf ^a   Doktorova, Helena ^a   Eckschlager, Tomas ^a   Stiborova, Marie ^a  

^a CHARLES UNIVERSITY   (Czech Republic)

Author keywords

Acetylation of hi stones; Apoptosis; Cisplatin; Etoposide; Neuroblastoma; Valproate

Indexed keywords

CASPASE 3; CELL DNA; CISPLATIN; ETOPOSIDE; HISTONE H2AX; HISTONE H3; HISTONE H4; TRICHOSTATIN A; VALPROIC ACID; VALPROMIDE; VINCRISTINE; CASP3 PROTEIN, HUMAN; DNA; HISTONE; HISTONE DEACETYLASE INHIBITOR;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL VIABILITY; CLINICAL EVALUATION; CONTROLLED STUDY; CYTOTOXICITY; DNA DAMAGE; DRUG EFFICACY; DRUG EXPOSURE; DRUG POTENTIATION; HISTONE ACETYLATION; HUMAN; HUMAN CELL; NEUROBLASTOMA; NEUROBLASTOMA CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SENSITIZATION; ACETYLATION; CELL PROLIFERATION; DRUG EFFECTS; GENETICS; METABOLISM; TUMOR CELL LINE;

ACETYLATION; APOPTOSIS; CASPASE 3; CELL LINE, TUMOR; CELL PROLIFERATION; CISPLATIN; DNA DAMAGE; DNA, NEOPLASM; DRUG SYNERGISM; ETOPOSIDE; HISTONE DEACETYLASE INHIBITORS; HISTONES; HUMANS; NEUROBLASTOMA; VALPROIC ACID;

EID: 84931071502     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2015.2996     Document Type: Article

References (56)

1. Brodeur GM: Neuroblastoma: Biological insights into a clinical enigma. Nat Rev Cancer 3: 203-216, 2003.
2. Schwab M, Westermann F, Hero B and Berthold F: Neuroblastoma: Biology and molecular and chromosomal pathology. Lancet Oncol 4: 472-480, 2003.
3. Maris JM, Hogarty MD, Bagatell R and Cohn SL: Neuroblastoma. Lancet 369: 2106-2120, 2007
4. Furchert SE, Lanvers-Kaminsky C, JuUrgens H., Jung M, Loidl A and Frühwald MC: Inhibitors of histone deacetylases as potential therapeutic tools for high-risk embryonal tumors of the nervous system of childhood. Int J Cancer 120: 1787-1794, 2007
5. Decock A, Ongenaert M, Vandesompele J and Speleman F: Neuroblastoma epigenetics: From candidate gene approaches to genome-wide screenings. Epigenetics 6: 962-970, 2011.
6. Santini V, Gozzini A and Ferrari G: Histone deacetylase inhibitors: Molecular and biological activity as a premise to clinical application. Curr Drug Metab 8: 383-393, 2007
7. Portela A and Esteller M: Epigenetic modifications and human disease. Nat Biotechnol 28: 1057-1068, 2010.
8. Kouzarides T: Chromatin modifications and their function. Cell 128: 693-705, 2007
9. Glozak MA, Sengupta N, Zhang X and Seto E: Acetylation and deacetylation of non-histone proteins. Gene 363: 15-23, 2005
10. Stiborová M, Eckschlager T, Poljaková J, Hraběta J, Adam V, Kizek R and Frei E: The synergistic effects of DNA-targeted chemotherapeutics and histone deacetylase inhibitors as therapeutic strategies for cancer treatment. Curr Med Chem 19: 4218-4238, 2012.
11. Atmaca A, Al-Batran SE, Maurer A., Neumann A, Heinzel T, Hentsch B., Schwarz SE, Hövelmann S, Göttlicher M, Knuth A, et al.: Valproic acid (VPA) in patients with refractory advanced cancer: a dose escalating phase I clinical trial. Br J Cancer 97 177-182, 2007
12. Munster P, Marchion D, Bicaku E., Lacevic M, Kim J, Centeno B., Daud A, Neuger A, Minton S and Sullivan D: Clinical and biological effects of valproic acid as a histone deacetylase inhibitor on tumor and surrogate tissues: Phase I/II trial of valproic acid and epirubicin/FEC. Clin Cancer Res 15: 2488-2496, 2009
13. Rocca A, Minucci S, Tosti G., Croci D, Contegno F, Ballarini M., Nolè F, Munzone E, Salmaggi A, Goldhirsch A, et al.: A phase I-II study of the histone deacetylase inhibitor valproic acid plus chemoimmunotherapy in patients with advanced melanoma. Br J Cancer 100: 28-36, 2009
14. Vandermeers F, Hubert P, Delvenne P., Mascaux C, Grigoriu B, Burny A., Scherpereel A and Willems L Valproate, in combination with pemetrexed and cisplatin, provides additional efficacy to the treatment of malignant mesothelioma. Clin Cancer Res 15: 2818-2828, 2009
15. Kim MS, Blake M, Baek J.H., Kohlhagen G., Pommier Y and Carrier F Inhibition of histone deacetylase increases cytotoxicity to anticancer drugs targeting DNA. Cancer Res 63: 7291-7300, 2003.
16. Munshi A, Kurland JF, Nishikawa T, Tanaka T., Hobbs ML, Tucker SL, Ismail S, Stevens C and Meyn RE: Histone deacetylase inhibitors radiosensitize human melanoma cells by suppressing DNA repair activity. Clin Cancer Res 11: 4912-4922, 2005
17. Das CM, Zage PE, Taylor P, Aguilera D., Wolff JE, Lee D and Gopalakrishnan V: Chromatin remodelling at the topoisomerase II-beta promoter is associated with enhanced sensitivity to etoposide in human neuroblastoma cell lines. Eur J Cancer 46: 2771-2780, 2010.
18. Poljakova J, Hrebackova J, Dvorakova M., Moserova M, Eckschlager T, Hrabeta J., Göttlicherova M, Kopejtkova B, Frei E, Kizek R, et al.: Anticancer agent ellipticine combined with histone deacetylase inhibitors, valproic acid and trichostatin A, is an effective DNA damage strategy in human neuroblastoma. Neuro Endocrinol Lett 32 (Suppl 1): 101-116, 2011.
19. Cipro Š, Hřebacková J, Hraběta J, Poljaková J and Eckschlager T: Valproic acid overcomes hypoxia-induced resistance to apoptosis. Oncol Rep 27: 1219-1226, 2012.
20. Groh T, Hrabeta J, Poljakova J., Eckschlager T and Stiborova M: Impact of histone deacetylase inhibitor valproic acid on the anticancer effect of etoposide on neuroblastoma cells. Neuro Endocrinol Lett 33 (Suppl 3): S16-S24, 2012.
21. Wang G, Edwards H, Caldwell J.T., Buck SA, Qing WY, Taub JW, Ge Y and Wang Z: Panobinostat synergistically enhances the cytotoxic effects of cisplatin, doxorubicin or etoposide on high-risk neuroblastoma cells. PLoS One 8: e76662, 2013.
22. Hrabeta J, Stiborova M, Adam V., Kizek R and Eckschlager T: Histone deacetylase inhibitors in cancer therapy. A review. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 158: 161-169, 2014.
23. Kartalou M and Essigmann JM: Mechanisms of resistance to cisplatin. Mutat Res 478: 23-43, 2001.
24. Miyajima A, Nakashima J, Yoshioka K., Tachibana M, Tazaki H and Murai M: Role of reactive oxygen species in cis-dichlorodi-ammineplatinum-induced cytotoxicity on bladder cancer cells. Br J Cancer 76: 206-210, 1997
25. Huang H-L, Fang L-W, Lu S-P, Chou C-K, Luh T-Y and Lai M-Z: DNA-damaging reagents induce apoptosis through reactive oxygen species-dependent Fas aggregation. Oncogene 22: 8168-8177, 2003.
26. Wozniak AJ and Ross WE: DNA damage as a basis lor 4-demethy-lepipodophyllotoxin-9-(4, 6-0-ethylidene-beta-D-glucopyranoside) (etoposide) cytotoxicity. Cancer Res 43: 120-124, 1983.
27. Hande KR: Etoposide: Four decades of development of a topoi-somerase II inhibitor. Eur J Cancer 34: 1514-1521, 1998
28. Baldwin EL and Osheroff N: Etoposide, topoisomerase II and cancer. Curr Med Chem Anticancer Agents 5: 363-372, 2005
29. New M, Olzscha H and La Thangue NB: HDAC inhibitor-based therapies: Can we interpret the code? Mol Oncol 6: 637-656, 2012.
30. Yoshida M, Kijima M, Akita M and Beppu T: Potent and specific inhibition of mammalian histone deacetylase both in vivo and in vitro by trichostatin A. J Biol Chem 265: 17174-17179, 1990.
31. Yoon CY, Park MJ, Lee J.S., Lee SC, Oh JJ, Park H, Chung C.W., Abdullajanov MM, Jeong SJ, Hong SK, et al.: The histone deacetylase inhibitor trichostatin A synergistically resensitizes a cisplatin resistant human bladder cancer cell line. J Urol 185: 1102-1111, 2011.
32. Meng J, Zhang H-H, Zhou C-X, Li C, Zhang F and Mei Q-B: The histone deacetylase inhibitor trichostatin A induces cell cycle arrest and apoptosis in colorectal cancer cells via p53-dependent and -independent pathways. Oncol Rep 28: 384-388, 2012.
33. Poljaková J, Eckschlager T, Hraběta J, Hrebacková J, Smutný S, Frei E, Martínek V, Kizek R and Stiborová M: The mechanism of cytotoxicity and DNA adduct formation by the anticancer drug ellipticine in human neuroblastoma cells. Biochem Pharmacol 77: 1466-1479, 2009
34. Poljaková J, Groh T, Gudino ZO, Hraběta J, Bořek-Dohalská L, Kizek R, Doktorová H, Eckschlager T and Stiborová M: Hypoxia-mediated histone acetylation and expression of N-myc transcription lactor dictate aggressiveness of neuroblastoma cells. Oncol Rep 31: 1928-1934, 2014
35. Shechter D, Dormann HL, Allis CD and Hake SB: Extraction, purification and analysis of histones. Nat Protoc 2: 1445-1457, 2007
36. Lowry OH, Rosebrough NJ, Farr AL and Randall RJ: Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275, 1951.
37. Ke N, Wang X, Xu X and Abassi YA: The xCELLigence system for real-time and label-free monitoring of cell viability. Methods Mol Biol 740: 33-43, 2011.
38. Earnshaw WC, Martins LM and Kaulmann SH: Mammalian caspases: Structure, activation, substrates, and lunctions during apoptosis. Annu Rev Biochem 68: 383-424, 1999
39. Porter AG and Jänicke RU: Emerging roles of caspase-3 in apoptosis. Cell Death Differ 6: 99-104, 1999
40. Slee EA, Adrain C and Martin SJ: Executioner caspase-3, -6, and -7 perform distinct, non-redundant roles during the demolition phase of apoptosis. J Biol Chem 276: 7320-7326, 2001.
41. Atienza JM, Yu N, Kirstein S.L., Xi B., Wang X, Xu X and Abassi YA: Dynamic and label-lree cell-based assays using the real-time cell electronic sensing system. Assay Drug Dev Technol 4: 597-607, 2006.
42. Chou TC and Talalay P: Quantitative analysis of dose-effect relationships: The combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 22: 27-55, 1984
43. Chou T-C: Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 58: 621-681, 2006.
44. Luchenko VL, Salcido CD, Zhang Y, Agama K., Komlodi-Pasztor E, Murphy RF, Giaccone G, Pommier Y., Bates SE and Varticovski L Schedule-dependent synergy of histone deacetylase inhibitors with DNA damaging agents in small cell lung cancer. Cell Cycle 10: 3119-3128, 2011.
45. Jordan MA and Wilson L: Microtubules as a target for anticancer drugs. Nat Rev Cancer 4: 253-265, 2004
46. Tu Y, Cheng S, Zhang S., Sun H and Xu Z: Vincristine induces cell cycle arrest and apoptosis in SH-SY5Y human neuroblastoma cells. Int J Mol Med 31: 113-119, 2013.
47. Phiel CJ, Zhang F, Huang E.Y., Guenther MG, Lazar MA and Klein PS: Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J Biol Chem 276: 36734-36741, 2001.
48. Sokolov MV, Dickey JS, Bonner WM and Sedelnikova OA: gamma-H2AX in bystander cells: Not just a radiation-triggered event, a cellular response to stress mediated by intercellular communication. Cell Cycle 6: 2210-2212, 2007
49. Bonner WM, Redon CE, Dickey J.S., Nakamura AJ, Sedelnikova OA, Solier S and Pommier Y GammaH2AX and cancer. Nat Rev Cancer 8: 957-967, 2008.
50. Nakamura AJ, Rao VA, Pommier Y and Bonner WM: The complexity of phosphorylated H2AX foci formation and DNA repair assembly at DNA double-strand breaks. Cell Cycle 9: 389-397, 2010.
51. Yuan J, Adamski R and Chen J: Focus on histone variant H2AX: To be or not to be. FEB S Lett 584: 3717-3724, 2010.
52. dos Santos MP, Schwartsmann G, Roesler R., Brunetto AL and Abujamra AL: Sodium butyrate enhances the cytotoxic effect of antineoplastic drugs in human lymphoblastic T-cells. Leuk Res 33: 218-221, 2009
53. Kurz EU, Wilson SE, Leader K.B., Sampey BP, Allan WP, Yalowich JC and Kroll DJ: The histone deacetylase inhibitor sodium butyrate induces DNA topoisomerase II alpha expression and confers hypersensitivity to etoposide in human leukemic cell lines. Mol Cancer Ther 1: 121-131, 2001.
54. Bruzzese F, Rocco M, Castelli S., Di Gennaro E, Desideri A and Budillon A: Synergistic antitumor effect between vorinostat and topotecan in small cell lung cancer cells is mediated by generation of reactive oxygen species and DNA damage-induced apoptosis. Mol Cancer Ther 8: 3075-3087, 2009
55. Itoh T, Terazawa R, Kojima K., Nakane K, Deguchi T, Ando M., Tsukamasa Y, Ito M and Nozawa Y Cisplatin induces production of reactive oxygen species via NADPH oxidase activation in human prostate cancer cells. Free Radic Res 45: 1033-1039, 2011.
56. Yu C, Friday BB, Lai J.P., McCollum A., Atadja P, Roberts LR and Adjei AA: Abrogation of MAPK and Akt signaling by AEE788 synergistically potentiates histone deacetylase inhibitor-induced apoptosis through reactive oxygen species generation. Clin Cancer Res 13: 1140-1148, 2007