Valproic acid, but not levetiracetam, selectively decreases HDAC7 and HDAC2 expression in human ovarian cancer cells

Toxicology Letters

Volumn 224, Issue 2, 2014, Pages 225-232

  Kwiecińska, Patrycja ^a   Wróbel, Anna ^a   Taubøll, Erik ^b   Gregoraszczuk, Ewa Lucja ^a  

^a JAGIELLONIAN UNIVERSITY   (Poland)

^b OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

Histone deacetylases; Levetiracetam; Ovarian cancer cell line OVCAR 3; Valproic acid

Indexed keywords

2 PYRROLIDINONE N BUTYRIC ACID; ETIRACETAM; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 10; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE 3; HISTONE DEACETYLASE 4; HISTONE DEACETYLASE 5; HISTONE DEACETYLASE 7; HISTONE DEACETYLASE 8; HISTONE DEACETYLASE 9; HISTONE H3; HISTONE H4; UNCLASSIFIED DRUG; VALPROIC ACID;

ARTICLE; CANCER CELL CULTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG TRANSFORMATION; ENZYME ACTIVITY; FEMALE; FLUOROMETRY; GENE EXPRESSION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HISTONE ACETYLATION; HUMAN; HUMAN CELL; IN VITRO STUDY; OVARY CARCINOMA; PLASMA CONCENTRATION-TIME CURVE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

HISTONE DEACETYLASES; LEVETIRACETAM; OVARIAN CANCER CELL LINE OVCAR-3; VALPROIC ACID;

ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; FEMALE; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HUMANS; OVARIAN NEOPLASMS; PIRACETAM; VALPROIC ACID;

EID: 84888158694     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2013.10.035     Document Type: Article

References (50)

1. Bakin R.E., Jung M.O. Cytoplasmic sequestration of HDAC7 from mitochondrial and nuclear compartments upon initiation of apoptosis. J. Biol. Chem. 2004, 279:51218-51225.
2. Bobustuc G.C., Baker C.H., Limaye A., Jenkins W.D., Pearl G., Avgeropoulos N.G., et al. Levetiracetam enhances p53-mediated MGMT inhibition and sensitizes glioblastoma cells to temozolomide. Neuro Oncol. 2010, 12:917-927.
3. Bokelmann I., Mahlknecht U. Valproic acid sensitizes chronic lymphocytic leukemia cells to apoptosis and restores the balance between pro- and antiapoptotic proteins. Mol. Med. 2008, 14:20-27.
4. Bosetti F., Bell J.M., Manickam P. Microarray analysis of rat brain gene expression after chronic administration of sodium valproate. Brain Res. Bull. 2005, 65:331-338.
5. Buckley K., Kelly R.B. Identification of a transmembrane glycoprotein specific for secretory vesicles of neural and endocrine cells. J. Cell Biol. 1985, 100:1284-1294.
6. Candelaria M., Gallardo-Rincón D., Arce C., Cetina L., Aguilar-Ponce J.L., Arrieta O., et al. A phase II study of epigenetic therapy with hydralazine and magnesium valproate to overcome chemotherapy resistance in refractory solid tumors. Ann. Oncol. 2007, 18:1529-1538.
7. Chavez-Blanco A., Segura-Pacheco B., Perez-Cardenas E., Taja-Chayeb L., Cetina L., Candelaria M., et al. Histone acetylation and histone deacetylase activity of magnesium valproate in tumor and peripheral blood of patients with cervical cancer. A phase I study. Mol. Cancer 2005, 4:22.
8. Coupez R., Nicolas J.M., Browne T.R. Levetiracetam, a new antiepileptic agent: lack of in vitro and in vivo pharmacokinetic interaction with valproic acid. Epilepsia 2003, 44:171-178.
9. Detich N., Bovenzi V., Szyf M. Valproate induces replication independent active DNA demethylation. J. Biol. Chem. 2003, 278:27586-27592.
10. Dokmanovic M., Perez G., Xu W., Ngo L., Clarke C., Parmigiani R.B., et al. Histone deacetylase inhibitors selectively suppress expression of HDAC7. Mol. Cancer Ther. 2007, 6:2525-2534.
11. Duong V., Bret C., Altucci L., Mai A., Duraffourd C., Loubersac J., et al. Specific activity of class II histone deacetylases in human breast cancer cells. Mol. Cancer Res. 2008, 6:1908-1919.
12. Eyal S., Yagen B., Sobol E., Altschuler Y., Shmuel M., Bialer M. The activity of antiepileptic drugs as histone deacetylase inhibitors. Epilepsia 2004, 45:737-744.
13. Fakhry H., Miyamoto T., Kashima H., Suzuki A., Ke H., Konishi I., et al. Immunohistochemical detection of histone deacetylases in endometrial carcinoma: involvement of histone deacetylase 2 in the proliferation of endometrial carcinoma cells. Hum. Pathol. 2010, 41:848-858.
14. Göttlicher M., Minucci S., Zhu P., Krämer O.H., Schimpf A., Giavara S., et al. Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. EMBO J. 2001, 20:6969-6978.
15. Gray S.G., Ekstroem T.J. The human histone deacetylase family. Exp. Cell Res. 2001, 262:75-83.
16. Gurvich N., Tsygankova O.M., Meinkoth J.L., Klein P.S. Histone deacetylase is a target of valproic acid-mediated cellular differentiation. Cancer Res. 2004, 64:1079-1086.
17. Hrzenjak A., Moinfar F., Kremser M.L., Strohmeier B., Staber P.B., Zatloukal K., et al. Valproate inhibition of histone deacetylase 2 affects differentiation and decreases proliferation of endometrial stromal sarcoma cells. Mol. Cancer Ther. 2006, 5:2203-2210.
18. Huang B.H., Laban M., Leung C.H., Lee L., Lee C.K., Salto-Tellez M., et al. Inhibition of histone deacetylase 2 increases apoptosis and p21Cip1/WAF1 expression, independent of histone deacetylase 1. Cell Death Differ. 2005, 12:395-404.
19. Jemal A., Siegel R., Ward E., Hao Y., Xu J., Thun M.J. Cancer statistics. CA: Cancer J. Clin. 2009, 59:225-249.
20. Jin K.L., Pak J.H., Park J.Y., Choi W.H., Lee J.Y., Kim J.H., et al. Expression profile of histone deacetylases 1, 2 and 3 in ovarian cancer tissues. J. Gynecol. Oncol. 2008, 19:185-190.
21. Johannessen C.U., Johannessen S.I. Valproate: past, present, and future. CNS Drug Rev. 2003, 9:199-216.
22. Jones J., Juengel E., Mickuckyte A., Hudak L., Wedel S., Jonas D., et al. The histone deacetylase inhibitor valproic acid alters growth properties of renal cell carcinoma in vitro and in vivo. J. Cell. Mol. Med. 2009, 13:2376-2385.
23. Khabele D., Son D.S., Parl A.K., Goldberg G.L., Augenlicht L.H., Mariadason J.M., et al. Drug-induced inactivation or gene silencing of class I histone deacetylases suppresses ovarian cancer cell growth: implications for therapy. Cancer Biol. Ther. 2007, 6:795-801.
24. Kim M.G., Pak J.H., Choi W.H., Park J.Y., Nam J.H., Kim J.H. The relationship between cisplatin resistance and histone deacetylase isoform overexpression in epithelial ovarian cancer cell lines. J. Gynecol. Oncol. 2012, 23:182-189.
25. Krämer O.H., Zhu P., Ostendorff H.P., Golebiewski M., Tiefenbach J., Peters M.A., et al. The histone deacetylase inhibitor valproic acid selectively induces proteasomal degradation of HDAC2. EMBO J. 2003, 22:3411-3420.
26. Kwiecińska P., Tauboll E., Gregoraszczuk EŁ Effects of valproic acid and levetiracetam on viability and cell cycle regulatory genes expression in the OVCAR-3 cell line. Pharmacol. Rep. 2012, 64:157-165.
27. Kwiecińska P., Taubøll E., Gregoraszczuk E.L. Comparison of the effects of valproic acid and levetiracetam on apoptosis in the human ovarian cancer cell line OVCAR-3. Pharmacol. Rep. 2012, 64:603-614.
28. Li X.N., Shu Q., Su J.M., Perlaky L., Blaney S.M., Lau C.C. Valproic acid induces growth arrest, apoptosis, and senescence in medulloblastomas by increasing histone hyperacetylation and regulating expression of p21Cip1, CDK4, and CMYC. Mol. Cancer Ther. 2005, 4:1912-1922.
29. Lin C.T., Lai H.C., Lee H.Y., Lin W.H., Chang C.C., Chu T.Y., et al. Valproic acid resensitizes cisplatin-resistant ovarian cancer cells. Cancer Sci. 2008, 99:1218-1226.
30. Lyseng-Williamson K.A. Levetiracetam: a review of its use in epilepsy. Drugs 2011, 71:489-514.
31. Marchion D.C., Bicaku E., Daud A.I., Sullivan D.M., Munster P.N. Valproic acid alters chromatin structure by regulation of chromatin modulation proteins. Cancer Res. 2005, 65:3815-3822.
32. Marks P.A., Miller T., Richon V.M. Histone deacetylases. Curr. Opin. Pharmacol. 2003, 3:344-351.
33. Minucci S., Pelicci P.G. Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat. Rev. Cancer 2006, 6:38-51.
34. Modesitt S.C., Sill M., Hoffman J.S., Bender D.P. Gynecologic oncology group, a phase II study of vorinostat in the treatment of persistent or recurrent epithelial ovarian or primary peritoneal carcinoma: a gynecologic oncology group study. Gynecol. Oncol. 2008, 109:182-186.
35. Moreno D.A., Scrideli C.A., Cortez M.A., de Paula Queiroz R., Valera E.T., da Silva Silveira V., et al. Differential expression of HDAC3, HDAC7 and HDAC9 is associated with prognosis and survival in childhood acute lymphoblastic leukaemia. Br. J. Haematol. 2010, 150:665-673.
36. Mottet D., Bellahcène A., Pirotte S., Waltregny D., Deroanne C., Lamour V., et al. Histone deacetylase 7 silencing alters endothelial cell migration, a key step in angiogenesis. Circ. Res. 2007, 101:1237-1246.
37. Osada H., Tatematsu Y., Saito H., Yatabe Y., Mitsudomi T., Takahashi T. Reduced expression of class II histone deacetylase genes is associated with poor prognosis in lung cancer patients. Int. J. Cancer 2004, 112:26-32.
38. Ouaïssi M., Sielezneff I., Silvestre R., Sastre B., Bernard J.P., Lafontaine J.S., et al. High histone deacetylase 7 (HDAC7) expression is significantly associated with adenocarcinomas of the pancreas. Ann. Surg. Oncol. 2008, 15:2318-2328.
39. Ozdaǧ H., Teschendorff A.E., Ahmed A.A., Hyland S.J., Blenkiron C., Bobrow L., et al. Differential expression of selected histone modifier genes in human solid cancers. BMC Genomics 2006, 7:90.
40. Patsalos P.N. Pharmacokinetic profile of levetiracetam: toward ideal characteristics. Pharmacol. Ther. 2000, 85:77-85.
41. Phiel C.J., Zhang F., Huang E.Y., Guenther M.G., Lazar M.A., Klein P.S. Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J. Biol. Chem. 2001, 276:36734-36741.
42. Portela-Gomes G.M., Lukinius A., Grimelius L. Synaptic vesicle protein 2, a new neuroendocrine cell marker. Am. J. Pathol. 2000, 157:1299-1309.
43. Quint K., Agaimy A., Di Fazio P., Montalbano R., Steindorf C., Jung R., et al. Clinical significance of histone deacetylases 1, 2, 3, and 7: HDAC2 is an independent predictor of survival in HCC. Virchows Arch. 2011, 459:129-139.
44. Sharma S., Symanowski J., Wong B., Dino P., Manno P., Vogelzang N. A phase II clinical trial of oral valproic acid in patients with castration-resistant prostate cancers using an intensive biomarker sampling strategy. Transl. Oncol. 2008, 1:141-147.
45. Song J., Noh J.H., Lee J.H., Eun J.W., Ahn Y.M., Kim S.Y., et al. Increased expression of histone deacetylase 2 is found in human gastric cancer. APMIS 2005, 113:264-268.
46. Stettner M., Krämer G., Strauss A., Kvitkina T., Ohle S., Kieseier B.C., et al. Long-term antiepileptic treatment with histone deacetylase inhibitors may reduce the risk of prostate cancer. Eur. J. Cancer Prev. 2012, 21:55-64.
47. Strahl B.D., Allis C.D. The language of covalent histone modifications. Nature 2000, 403:41-45.
48. Takai N., Kawamata N., Gui D., Said J.W., Miyakawa I., Koeffler H.P. Human ovarian carcinoma cells: histone deacetylase inhibitors exhibit antiproliferative activity and potently induce apoptosis. Cancer 2004, 101:2760-2770.
49. Travaglini L., Vian L., Billi M., Grignani F., Nervi C. Epigenetic reprogramming of breast cancer cells by valproic acid occurs regardless of estrogen receptor status. Int. J. Biochem. Cell Biol. 2009, 41:225-234.
50. Zhu C., Chen Q., Xie Z., Ai J., Tong L., Ding J., et al. The role of histone deacetylase 7 (HDAC7) in cancer cell proliferation: regulation on c-Myc. J. Mol. Med. (Berl) 2011, 89:279-289.