Valproic acid induces p21 and topoisomerase-II (α/β) expression and synergistically enhances etoposide cytotoxicity in human glioblastoma cell lines

Journal of Neuro-Oncology

Volumn 85, Issue 2, 2007, Pages 159-170

  Das, Chandra M ^a   Aguilera, Dolly ^a   Vasquez, Hernan ^a   Prasad, Preethi ^a   Zhang, Ming ^a   Wolff, Johannes E ^a,b   Gopalakrishnan, Vidya ^a,b  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

Adjuvant; Etoposide; Glioblastoma; HDAC inhibitor; p21; Topoisomerase II; Valproic acid

Indexed keywords

3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; CASPASE 3; CELL DNA; CYCLIN DEPENDENT KINASE INHIBITOR 1; DNA TOPOISOMERASE (ATP HYDROLYSING) A; DNA TOPOISOMERASE (ATP HYDROLYSING) B; ETOPOSIDE; GLIAL FIBRILLARY ACIDIC PROTEIN; HISTONE H4; PROTEIN P21; VALPROIC ACID;

ACETYLATION; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER GROWTH; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL DIFFERENTIATION; COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; CYTOTOXICITY; DNA CONTENT; DRUG EXPOSURE; DRUG POTENTIATION; DRUG SENSITIZATION; ENZYME ACTIVITY; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GLIOBLASTOMA; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; IN VITRO STUDY; MONOTHERAPY; UPREGULATION; WESTERN BLOTTING;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; BRAIN NEOPLASMS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DNA TOPOISOMERASES, TYPE II; DRUG SYNERGISM; ENZYME INHIBITORS; ETOPOSIDE; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOBLASTOMA; HISTONE DEACETYLASES; HISTONES; HUMANS; ISOENZYMES; VALPROIC ACID;

EID: 35448999681     PISSN: 0167594X     EISSN: 15737373     Source Type: Journal    
DOI: 10.1007/s11060-007-9402-7     Document Type: Article

References (45)

1. Hanada R, Inaba T, Yaginuma A, Hayashi Y, Yamamoto K, Nishimoto H, Tsukiyama T (1989) [Effect of high-dose cyclophosphamide plus high-dose etoposide in malignant brain tumors of children followed by autologous bone marrow rescue]. Gan To Kagaku Ryoho 16:263-268
2. Leo E, Schlegel PG, Lindemann A (1997) Chemotherapeutic induction of long-term remission in metastatic medulloblastoma. J Neurooncol 32:149-154
3. Kageji T, Nagahiro S, Horiguchi H, Watanabe T, Suzuya H, Okamoto Y, Kuroda Y (2003) Successful high-dose chemotherapy for widespread neuroaxis dissemination of an optico-hypothalamic juvenile pilocytic astrocytoma in an infant: A case report. J Neurooncol 62:281-287
4. Postmus PE, Mulder NH, Sleijfer DT, Meinesz AF, Vriesendorp R, de Vries EG (1984) High-dose etoposide for refractory malignancies: A phase I study. Cancer Treat Rep 68:1471-1474
5. Parney IF, Chang SM (2003) Current chemotherapy for glioblastoma. Cancer J 9:149-156
6. Yin D, Tamaki N, Parent AD, Zhang JH (2005) Insulin-like growth factor-I decreased etoposide-induced apoptosis in glioma cells by increasing bcl-2 expression and decreasing CPP32 activity. Neurol Res 27:27-35
7. El-Deiry WS (2003) The role of p53 in chemosensitivity and radiosensitivity. Oncogene 22:7486-7495
8. Wu GS, El-Diery WS (1996) p53 and chemosensitivity. Nat Med 2:255-256
9. Valkov NI, Sullivan DM (2003) Tumor p53 status and response to topoisomerase II inhibitors. Drug Resist Updat 6:27-39
10. Kim EH, Kim HS, Kim SU, Noh EJ, Lee JS, Choi KS (2005) Sodium butyrate sensitizes human glioma cells to TRAIL-mediated apoptosis through inhibition of Cdc2 and the subsequent downregulation of survivin and XIAP. Oncogene 24:6877-6889
11. Kim TY, Zhong S, Fields CR, Kim JH, Robertson KD (2006) Epigenomic profiling reveals novel and frequent targets of aberrant DNA methylation-mediated silencing in malignant glioma. Cancer Res 66:7490-7501
12. Yin D, Ong JM, Hu J, Desmond JC, Kawamata N, Konda BM, Black KL, Koeffler HP (2007) Suberoylanilide hydroxamic acid, a histone deacetylase inhibitor: Effects on gene expression and growth of glioma cells in vitro and in vivo. Clin Cancer Res 13:1045-1052
13. Minucci S, Pelicci PG (2006) Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat Rev Cancer 6:38-51
14. Eyupoglu IY, Hahnen E, Trankle C, Savaskan NE, Siebzehnrubl FA, Buslei R, Lemke D, Wick W, Fahlbusch R, Blumcke I (2006) Experimental therapy of malignant gliomas using the inhibitor of histone deacetylase MS-275. Mol Cancer Ther 5:1248-1255
15. Wetzel M, Premkumar DR, Arnold B, Pollack IF (2005) Effect of trichostatin A, a histone deacetylase inhibitor, on glioma proliferation in vitro by inducing cell cycle arrest and apoptosis. J Neurosurg 103:549-556
16. Entin-Meer M, Rephaeli A, Yang X, Nudelman A, VandenBerg SR, Haas-Kogan DA (2005) Butyric acid prodrugs are histone deacetylase inhibitors that show antineoplastic activity and radiosensitizing capacity in the treatment of malignant gliomas. Mol Cancer Ther 4:1952-1961
17. Chapman A, Keane PE, Meldrum BS, Simiand J, Vernieres JC (1982) Mechanism of anticonvulsant action of valproate. Prog Neurobiol 19:315-359
18. Davis R, Peters DH, McTavish D (1994) Valproic acid. A reappraisal of its pharmacological properties and clinical efficacy in epilepsy. Drugs 47:332-372
19. Driever PH, Knupfer MM, Cinatl J, Wolff JE (1999) Valproic acid for the treatment of pediatric malignant glioma. Klin Padiatr 211:323-328
20. Witt O, Schweigerer L, Driever PH, Wolff J, Pekrun A (2004) Valproic acid treatment of glioblastoma multiforme in a child. Pediatr Blood Cancer 43:181
21. Hanson JA, Bentley DP, Bean EA, Nute SR, Moore JL (1991) In vitro chemosensitivity testing in chronic lymphocytic leukaemia patients. Leuk Res 15:565-569
22. Su X, Gopalakrishnan V, Stearns D, Aldape K, Lang FF, Fuller G, Snyder E, Eberhart CG, Majumder S (2006) Abnormal expression of REST/NRSF and Myc in neural stem/progenitor cells causes cerebellar tumors by blocking neuronal differentiation. Mol Cell Biol 26:1666-1678
23. Kagan VE, Gleiss B, Tyurina YY, Tyurin VA, Elenstrom-Magnusson C, Liu SX, Serinkan FB, Arroyo A, Chandra J, Orrenius S, Fadeel B (2002) A role for oxidative stress in apoptosis: Oxidation and externalization of phosphatidylserine is required for macrophage clearance of cells undergoing Fas-mediated apoptosis. J Immunol 169:487-499
24. Yang H, Hoshino K, Sanchez-Gonzalez B, Kantarjian H, Garcia-Manero G (2005) Antileukemia activity of the combination of 5-aza-2′-deoxycytidine with valproic acid. Leuk Res 29:739-748
25. Stockhausen MT, Sjolund J, Manetopoulos C, Axelson H (2005) Effects of the histone deacetylase inhibitor valproic acid on Notch signalling in human neuroblastoma cells. Br J Cancer 92:751-759
26. Li XN, Shu Q, Su JM, Perlaky L, Blaney SM, Lau CC (2005) 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 4:1912-1922
27. Yoo EJ, Chung JJ, Choe SS, Kim KH, Kim JB (2006) Down-regulation of histone deacetylases stimulates adipocyte differentiation. J Biol Chem 281:6608-6615
28. Wolff JE, Finlay JL (2004) High-dose chemotherapy in childhood brain tumors. Onkologie 27:239-245
29. Hake SB, Xiao A, Allis CD (2004) Linking the epigenetic 'language' of covalent histone modifications to cancer. Br J Cancer 90:761-769
30. Johnstone RW (2002) Histone-deacetylase inhibitors: Novel drugs for the treatment of cancer. Nat Rev Drug Discov 1:287-299
31. Dokmanovic M, Marks PA (2005) Prospects: Histone deacetylase inhibitors. J Cell Biochem 96:293-304
32. Takai N, Kawamata N, Gui D, Said JW, Miyakawa I, Koeffler HP (2004) Human ovarian carcinoma cells: Histone deacetylase inhibitors exhibit antiproliferative activity and potently induce apoptosis. Cancer 101:2760-2770
33. Peart MJ, Smyth GK, van Laar RK, Bowtell DD, Richon VM, Marks PA, Holloway AJ, Johnstone RW (2005) Identification and functional significance of genes regulated by structurally different histone deacetylase inhibitors. Proc Natl Acad Sci USA 102:3697-3702
34. Tsai SC, Valkov N, Yang WM, Gump J, Sullivan D, Seto E (2000) Histone deacetylase interacts directly with DNA topoisomerase II. Nat Genet 26:349-353
35. Kurz EU, Wilson SE, Leader KB, Sampey BP, Allan WP, Yalowich JC, Kroll DJ (2001) 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
36. Marchion DC, Bicaku E, Daud AI, Richon V, Sullivan DM, Munster PN (2004) Sequence-specific potentiation of topoisomerase II inhibitors by the histone deacetylase inhibitor suberoylanilide hydroxamic acid. J Cell Biochem 92:223-237
37. Marin-Husstege M, Muggironi M, Liu A, Casaccia-Bonnefil P (2002) Histone deacetylase activity is necessary for oligodendrocyte lineage progression. J Neurosci 22:10333-10345
38. Hsieh J, Nakashima K, Kuwabara T, Mejia E, Gage FH (2004) Histone deacetylase inhibition-mediated neuronal differentiation of multipotent adult neural progenitor cells. Proc Natl Acad Sci USA 101:16659-16664
39. Asklund T, Appelskog IB, Ammerpohl O, Ekstrom TJ, Almqvist PM (2004) Histone deacetylase inhibitor 4-phenylbutyrate modulates glial fibrillary acidic protein and connexin 43 expression, and enhances gap-junction communication, in human glioblastoma cells. Eur J Cancer 40:1073-1081
40. Marchion DC, Bicaku E, Turner JG, Daud AI, Sullivan DM, Munster PN (2005) Synergistic interaction between histone deacetylase and topoisomerase II inhibitors is mediated through topoisomerase IIbeta. Clin Cancer Res 11:8467-8475
41. Tews DS, Fleissner C, Tiziani B, Gaumann AK (2001) Intrinsic expression of drug resistance-associated factors in meningiomas. Appl Immunohistochem Mol Morphol 9:242-249
42. Takano H, Kohno K, Matsuo K, Matsuda T, Kuwano M (1992) DNA topoisomerase-targeting antitumor agents and drug resistance. Anticancer Drugs 3:323-330
43. Wang Q, Zambetti GP, Suttle DP (1997) Inhibition of DNA topoisomerase II alpha gene expression by the p53 tumor suppressor. Mol Cell Biol 17:389-397
44. Clifford B, Beljin M, Stark GR, Taylor WR (2003) G2 arrest in response to topoisomerase II inhibitors: The role of p53. Cancer Res 63:4074-4081
45. Kim MS, Blake M, Baek JH, Kohlhagen G, Pommier Y, Carrier F (2003) Inhibition of histone deacetylase increases cytotoxicity to anticancer drugs targeting DNA. Cancer Res 63:7291-7300