Valproic acid, a histone deacetylase inhibitor, enhances radiosensitivity in esophageal squamous cell carcinoma

International Journal of Oncology

Volumn 40, Issue 6, 2012, Pages 2140-2146

  Shoji, Masatoshi ^a   Ninomiya, Itasu ^a   Makino, Isamu ^a   Kinoshita, Jun ^a   Nakamura, Keishi ^a   Oyama, Katsunobu ^a   Nakagawara, Hisatoshi ^a   Fujita, Hideto ^a   Tajima, Hidehiro ^a   Takamura, Hiroyuki ^a   Kitagawa, Hirohisa ^a   Fushida, Sachio ^a   Harada, Shinichi ^a   Fujimura, Takashi ^a   Ohta, Tetsuo ^a  

^a KANAZAWA UNIVERSITY   (Japan)

Author keywords

Double strand break; Esophageal cancer; Histone deacetylase inhibitor; Rad51; Radiosensitization; Valproic acid

Indexed keywords

HISTONE H2AX; HISTONE H3; HISTONE H4; NUCLEIC ACID BINDING PROTEIN; RAD51 PROTEIN; RADIOSENSITIZING AGENT; VALPROIC ACID;

APOPTOSIS; ARTICLE; CANCER CELL; CANCER RADIOTHERAPY; CELL SURVIVAL; CELL VIABILITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOTOXICITY; DOSE RESPONSE; DOUBLE STRANDED DNA BREAK; DOWN REGULATION; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; HISTONE ACETYLATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RADIOSENSITIZATION; WESTERN BLOTTING;

APOPTOSIS; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CELL SURVIVAL; DNA BREAKS, DOUBLE-STRANDED; ESOPHAGEAL NEOPLASMS; GENE EXPRESSION; HISTONE DEACETYLASE INHIBITORS; HUMANS; INHIBITORY CONCENTRATION 50; RAD51 RECOMBINASE; RADIATION TOLERANCE; RADIATION-SENSITIZING AGENTS; VALPROIC ACID;

EID: 84861775963     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2012.1416     Document Type: Article

References (50)

1. Jemal A, Siegel R, Xu J and Ward E: Cancer statistics, 2010. CA Cancer J Clin 60: 277-300, 2010.
2. Herskovic A, Martz K, al-Sarraf M, et al: Combined chemotherapy and radiotherapy compared with radiotherapy alone in patients with cancer of the esophagus. N Engl J Med 326: 1593-1598, 1992.
3. al-Sarraf M, Martz K, Herskovic A, et al: Progress report of combined chemoradiotherapy versus radiotherapy alone in patients with esophageal cancer: an intergroup study. J Clin Oncol 15: 277-284, 1997. (Pubitemid 27020584)
4. Ohtsu A, Boku N, Muro K, et al: Definitive chemoradiotherapy for T4 and/or M1 lymph node squamous cell carcinoma of the esophagus. J Clin Oncol 17: 2915-2921, 1999. (Pubitemid 29415253)
5. Ishida K, Ando N, Yamamoto S, Ide H and Shinoda M: Phase II study of cisplatin and 5-fluorouracil with concurrent radiotherapy in advanced squamous cell carcinoma of the esophagus: a Japan Esophageal Oncology Group (JEOG)/Japan Clinical Oncology Group trial (JCOG9516). Jpn J Clin Oncol 34: 615-619, 2004. (Pubitemid 40662717)
6. Scanlon KJ, Newman EM, Lu Y and Priest DG: Biochemical basis for cisplatin and 5-fluorouracil synergism in human ovarian carcinoma cells. Proc Natl Acad Sci USA 83: 8923-8925, 1986. (Pubitemid 17223512)
7. Douple EB and Richmond RC: A review of interactions between platinum coordination complexes and ionizing radiation: implication for cancer therapy. In: Cisplatin: Current Status and New Developments. Prestayko AW, Crooke ST and Karter SK (eds). Academic, Orlando, FL, pp125-147, 1980.
8. Tepper J, Krasna MJ, Niedzwiecki D, et al: Phase III trial of trimodality therapy with cisplatin, fluorouracil, radiotherapy, and surgery compared with surgery alone for esophageal cancer: CALGB 9781. J Clin Oncol 26: 1086-1092, 2008.
9. Abou-Jawde RM, Mekhail T, Adelstein DJ, et al: Impact of induction concurrent chemoradiotherapy on pulmonary function and postoperative acute respiratory complications in esophageal cancer. Chest 128: 250-255, 2005. (Pubitemid 40994481)
10. Morota M, Gomi K, Kozuka T, et al: Late toxicity after definitive concurrent chemoradiotherapy for thoracic esophageal carcinoma. Int J Radiat Oncol Biol Phys 75: 122-128, 2009.
11. D'Journo XB, Michelet P, Dahan L, et al: Indications and outcome of salvage surgery for oesophageal cancer. Eur J Cardiothorac Surg 33: 1117-1123, 2008.
12. Grunstein M: Histone acetylation in chromatin structure and transcription. Nature 389: 349-352, 1997.
13. Wu J and Grunstein M: 25 years after the nucleosome model: chromatin modifications. Trends Biochem Sci 25: 619-623, 2000.
14. Ropero S and Esteller M: The role of histone deacetylases (HDACs) in human cancer. Mol Oncol 1: 19-25, 2007. (Pubitemid 46776612)
15. Lane AA and Chabner BA: Histone deacetylase inhibitors in cancer therapy. J Clin Oncol 27: 5459-5468, 2009.
16. Marks PA: Histone deacetylase inhibitors: a chemical genetics approach to understanding cellular functions. Biochim Biophys Acta 1799: 717-725, 2010.
17. Toh Y, Yamamoto M, Endo K, et al: Histone H4 acetylation and histone deacetylase 1 expression in esophageal squamous cell carcinoma. Oncol Rep 10: 333-338, 2003.
18. Zhang B, Wang Y and Pang X: Enhanced radiosensitivity of EC109 cells by inhibition of HDAC1 expression. Med Oncol 2010.
19. Mann BS, Johnson JR, He K, et al: Vorinostat for treatment of cutaneous manifestations of advanced primary cutaneous T-cell lymphoma. Clin Cancer Res 13: 2318-2322, 2007. (Pubitemid 46698579)
20. Camphausen K, Cerna D, Scott T, et al: Enhancement of in vitro and in vivo tumor cell radiosensitivity by valproic acid. Int J Cancer 114: 380-386, 2005. (Pubitemid 40279957)
21. Chen X, Wong P, Radany E and Wong JY: HDAC inhibitor, valproic acid, induces p53-dependent radiosensitization of colon cancer cells. Cancer Biother Radiopharm 24: 689-699, 2009.
22. Chinnaiyan P, Cerna D, Burgan WE, et al: Postradiation sensitization of the histone deacetylase inhibitor valproic acid. Clin Cancer Res 14: 5410-5415, 2008.
23. Harikrishnan KN, Karagiannis TC, Chow MZ and El-Osta A: Effect of valproic acid on radiation-induced DNA damage in euchromatic and heterochromatic compartments. Cell Cycle 7: 468-476, 2008. (Pubitemid 351366475)
24. Karagiannis TC, Kn H and El-Osta A: The epigenetic modifier, valproic acid, enhances radiation sensitivity. Epigenetics 1: 131-137, 2006.
25. Kawano T, Akiyama M, Agawa-Ohta M, et al: Histone deacetylase inhibitors valproic acid and depsipeptide sensitize retinoblastoma cells to radiotherapy by increasing H2AX phosphorylation and p53 acetylation-phosphorylation. Int J Oncol 37: 787-795, 2010.
26. Rezacova M, Zaskodova D, Vavrova J, Vokurkova D and Tichy A: Antileukemic activity of the combination of ionizing radiation with valproic acid in promyelocytic leukemia cells HL-60. Neoplasma 55: 519-525, 2008.
27. Zaskodova D, Rezacova M, Vavrova J, Vokurkova D and Tichy A: Effect of valproic acid, a histone deacetylase inhibitor, on cell death and molecular changes caused by low-dose irradiation. Ann NY Acad Sci 1091: 385-398, 2006. (Pubitemid 47092252)
28. Candelaria M, Cetina L, Perez-Cardenas E, et al: Epigenetic therapy and cisplatin chemoradiation in FIGO stage IIIB cervical cancer. Eur J Gynaecol Oncol 31: 386-391, 2010.
29. Ree AH, Dueland S, Folkvord S, et al: Vorinostat, a histone deacetylase inhibitor, combined with pelvic palliative radiotherapy for gastrointestinal carcinoma: the Pelvic Radiation and Vorinostat (PRAVO) phase 1 study. Lancet Oncol 11: 459-464, 2010.
30. Su JM, Li XN, Thompson P, et al: Phase 1 study of valproic acid in pediatric patients with refractory solid or CNS tumors: a children's oncology group report. Clin Cancer Res 17: 589-597, 2011.
31. Wolff JE, Kramm C, Kortmann RD, et al: Valproic acid was well tolerated in heavily pretreated pediatric patients with high-grade glioma. J Neurooncol 90: 309-314, 2008.
32. Duenas-Gonzalez A, Candelaria M, Perez-Plascencia C, Perez-Cardenas E, de la Cruz-Hernandez E and Herrera LA: Valproic acid as epigenetic cancer drug: preclinical, clinical and transcriptional effects on solid tumors. Cancer Treat Rev 34: 206-222, 2008.
33. Adimoolam S, Sirisawad M, Chen J, Thiemann P, Ford JM and Buggy JJ: HDAC inhibitor PCI-24781 decreases RAD51 expression and inhibits homologous recombination. Proc Natl Acad Sci USA 104: 19482-19487, 2007.
34. Blattmann C, Oertel S, Ehemann V, et al: Enhancement of radiation response in osteosarcoma and rhabdomyosarcoma cell lines by histone deacetylase inhibition. Int J Radiat Oncol Biol Phys 78: 237-245, 2010.
35. Chinnaiyan P, Vallabhaneni G, Armstrong E, Huang SM and Harari PM: Modulation of radiation response by histone deacetylase inhibition. Int J Radiat Oncol Biol Phys 62: 223-229, 2005. (Pubitemid 40591946)
36. Goh M, Chen F, Paulsen MT, Yeager AM, Dyer ES and Ljungman M: Phenylbutyrate attenuates the expression of Bcl-X(L), DNA-PK, caveolin-1, and VEGF in prostate cancer cells. Neoplasia 3: 331-338, 2001. (Pubitemid 32801883)
37. Kuribayashi T, Ohara M, Sora S and Kubota N: Scriptaid, a novel histone deacetylase inhibitor, enhances the response of human tumor cells to radiation. Int J Mol Med 25: 25-29, 2010.
38. Munshi A, Kurland JF, Nishikawa T, et al: Histone deacetylase inhibitors radiosensitize human melanoma cells by suppressing DNA repair activity. Clin Cancer Res 11: 4912-4922, 2005. (Pubitemid 41557212)
39. Munshi A, Tanaka T, Hobbs ML, Tucker SL, Richon VM and Meyn RE: Vorinostat, a histone deacetylase inhibitor, enhances the response of human tumor cells to ionizing radiation through prolongation of gamma-H2AX foci. Mol Cancer Ther 5: 1967-1974, 2006. (Pubitemid 44336568)
40. Zhang F, Zhang T, Teng ZH, Zhang R, Wang JB and Mei QB: Sensitization to gamma-irradiation-induced cell cycle arrest and apoptosis by the histone deacetylase inhibitor trichostatin A in non-small cell lung cancer (NSCLC) cells. Cancer Biol Ther 8: 823-831, 2009.
41. Pajonk F, Vlashi E and McBride WH: Radiation resistance of cancer stem cells: the 4 R's of radiobiology revisited. Stem Cells 28: 639-648, 2010.
42. Petitjean A, Mathe E, Kato S, et al: Impact of mutant p53 functional properties on TP53 mutation patterns and tumor phenotype: lessons from recent developments in the IARC TP53 database. Hum Mutat 28: 622-629, 2007. (Pubitemid 46744292)
43. Shimada H, Matsushita K and Tagawa M: Recent advances in esophageal cancer gene therapy. Ann Thorac Cardiovasc Surg 14: 3-8, 2008.
44. Chen X, Wong J, Wong P and Radany EH: Low-dose valproic acid enhances radiosensitivity of prostate cancer through acetylated p53-dependent modulation of mitochondrial membrane potential and apoptosis. Mol Cancer Res 9: 448-461, 2011.
45. Lopez CA, Feng FY, Herman JM, Nyati MK, Lawrence TS and Ljungman M: Phenylbutyrate sensitizes human glioblastoma cells lacking wild-type p53 function to ionizing radiation. Int J Radiat Oncol Biol Phys 69: 214-220, 2007. (Pubitemid 47247526)
46. Kim IA, Kim IH, Kim HJ, Chie EK and Kim JS: HDAC inhibitor-mediated radiosensitization in human carcinoma cells: a general phenomenon? J Radiat Res (Tokyo) 51: 257-263, 2010.
47. Flatmark K, Nome RV, Folkvord S, et al: Radiosensitization of colorectal carcinoma cell lines by histone deacetylase inhibition. Radiat Oncol 1: 25, 2006.
48. Suzuki T: Explorative study on isoform-selective histone deacetylase inhibitors. Chem Pharm Bull (Tokyo) 57: 897-906, 2009.
49. Chung YL, Wang AJ and Yao LF: Antitumor histone deacetylase inhibitors suppress cutaneous radiation syndrome: Implications for increasing therapeutic gain in cancer radiotherapy. Mol Cancer Ther 3: 317-325, 2004.
50. Chung YL, Lee MY and Pui NN: Epigenetic therapy using the histone deacetylase inhibitor for increasing therapeutic gain in oral cancer: prevention of radiation-induced oral mucositis and inhibition of chemical-induced oral carcinogenesis. Carcinogenesis 30: 1387-1397, 2009.