Preclinical evidence for a beneficial impact of valproate on the response of small cell lung cancer to first-line chemotherapy

European Journal of Cancer

Volumn 46, Issue 9, 2010, Pages 1724-1734

  Hubaux, Roland ^a   Vandermeers, Fabian ^a   Crisanti, Cecilia ^b   Kapoor, Veena ^b   Burny, Arsène ^a   Mascaux, Céline ^c   Albelda, Steven M ^b   Willems, Luc ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c JULES BORDET INSTITUTE   (Belgium)

Author keywords

Chemotherapy; HDAC; Mice; Small cell lung cancer; Valproate

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CISPLATIN; CYTOCHROME C; DEATH RECEPTOR; ETOPOSIDE; HISTONE H2AX; HISTONE H3; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN BCL XL; PROTEIN BID; PROTEIN P21; VALPROIC ACID; ANTINEOPLASTIC AGENT; CASPASE; HISTONE DEACETYLASE INHIBITOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER CHEMOTHERAPY; CANCER RESISTANCE; CARCINOMA CELL; CONTROLLED STUDY; CYTOSOL; DRUG MECHANISM; DRUG POTENTIATION; DRUG RESPONSE; ENZYME RELEASE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN TISSUE; LUNG SMALL CELL CANCER; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; ANIMAL; CANCER TRANSPLANTATION; CELL PROLIFERATION; DRUG EFFECTS; FEMALE; GENE EXPRESSION; GENETICS; LUNG NEOPLASMS; METABOLISM; MICROARRAY ANALYSIS; SCID MOUSE; SMALL CELL LUNG CARCINOMA; TUMOR CELL LINE; WESTERN BLOTTING; XENOGRAFT;

ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; BLOTTING, WESTERN; CASPASES; CELL LINE, TUMOR; CELL PROLIFERATION; CISPLATIN; DRUG SYNERGISM; ETOPOSIDE; FEMALE; GENE EXPRESSION; HISTONE DEACETYLASE INHIBITORS; HUMANS; LUNG NEOPLASMS; MICE; MICE, SCID; MICROARRAY ANALYSIS; NEOPLASM TRANSPLANTATION; SMALL CELL LUNG CARCINOMA; TRANSPLANTATION, HETEROLOGOUS; VALPROIC ACID;

EID: 77952582492     PISSN: 09598049     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejca.2010.03.021     Document Type: Article

References (61)

1. Jackman D.M., and Johnson B.E. Small-cell lung cancer. Lancet 366 (2005) 1385-1396
2. Hoffman P.C., Mauer A.M., and Vokes E.E. Lung cancer. Lancet 355 (2000) 479-485
3. Govindan R., Page N., Morgensztern D., et al. Changing epidemiology of small-cell lung cancer in the United States over the last 30 years: analysis of the surveillance, epidemiologic, and end results database. J Clin Oncol 24 (2006) 4539-4544
4. Ferraldeschi R., Baka S., Jyoti B., et al. Modern management of small-cell lung cancer. Drugs 67 (2007) 2135-2152
5. Amarasena I.U., Walters J.A., Wood-Baker R., and Fong K. Platinum versus non-platinum chemotherapy regimens for small cell lung cancer. Cochrane Database Syst Rev (2008) CD006849
6. Simon G.R., and Wagner H. Small cell lung cancer. Chest 123 (2003) 259S-271S
7. Treatment of small cell lung cancer: extensive diseases. Guidelines of clinical practice made by the European Lung Cancer Working Party. Rev Med Brux 2008;29:455-70.
8. Mascaux C., Paesmans M., Berghmans T., et al. A systematic review of the role of etoposide and cisplatin in the chemotherapy of small cell lung cancer with methodology assessment and meta-analysis. Lung Cancer 30 (2000) 23-36
9. von Pawel J., Schiller J.H., Shepherd F.A., et al. Topotecan versus cyclophosphamide, doxorubicin, and vincristine for the treatment of recurrent small-cell lung cancer. J Clin Oncol 17 (1999) 658-667
10. Baylin S.B., and Ohm J.E. Epigenetic gene silencing in cancer - a mechanism for early oncogenic pathway addiction?. Nat Rev Cancer 6 (2006) 107-116
11. Gronbaek K., Treppendahl M., Asmar F., and Guldberg P. Epigenetic changes in cancer as potential targets for prophylaxis and maintenance therapy. Basic Clin Pharmacol Toxicol 103 (2008) 389-396
12. Helmbold P., Lahtz C., Herpel E., et al. Frequent hypermethylation of RASSF1A tumour suppressor gene promoter and presence of Merkel cell polyomavirus in small cell lung cancer. Eur J Cancer 45 (2009) 2207-2211
13. Platta C.S., Greenblatt D.Y., Kunnimalaiyaan M., and Chen H. The HDAC inhibitor trichostatin A inhibits growth of small cell lung cancer cells. J Surg Res 142 (2007) 219-226
14. Platta C.S., Greenblatt D.Y., Kunnimalaiyaan M., and Chen H. Valproic acid induces Notch1 signaling in small cell lung cancer cells. J Surg Res 148 (2008) 31-37
15. Tsurutani J., Soda H., Oka M., et al. Antiproliferative effects of the histone deacetylase inhibitor FR901228 on small-cell lung cancer lines and drug-resistant sublines. Int J Cancer 104 (2003) 238-242
16. Achachi A., Florins A., Gillet N., et al. Valproate activates bovine leukemia virus gene expression, triggers apoptosis, and induces leukemia/lymphoma regression in vivo. Proc Natl Acad Sci USA 102 (2005) 10309-10314
17. Bouzar A.B., Boxus M., Defoiche J., et al. Valproate synergizes with purine nucleoside analogues to induce apoptosis of B-chronic lymphocytic leukaemia cells. Br J Haematol 144 (2009) 41-52
18. Crisanti M.C., Wallace A.F., Kapoor V., et al. The HDAC inhibitor panobinostat (LBH589) inhibits mesothelioma and lung cancer cells in vitro and in vivo with particular efficacy for small cell lung cancer. Mol Cancer Ther 8 (2009) 2221-2231
19. Vandermeers F., Hubert P., Delvenne P., et al. Valproate, in combination with pemetrexed and cisplatin, provides additional efficacy to the treatment of malignant mesothelioma. Clin Cancer Res 15 (2009) 2818-2828
20. Brodie M.J., and Dichter M.A. Antiepileptic drugs. N Engl J Med 334 (1996) 168-175
21. Chapman A., Keane P.E., Meldrum B.S., et al. Mechanism of anticonvulsant action of valproate. Prog Neurobiol 19 (1982) 315-359
22. DeVane C.L. Pharmacokinetics, drug interactions, and tolerability of valproate. Psychopharmacol Bull 37 Suppl. 2 (2003) 25-42
23. Bjerkedal T., Czeizel A., Goujard J., et al. Valproic acid and spina bifida. Lancet 2 (1982) 1096
24. Cinatl Jr. J., Cinatl J., Scholz M., et al. Antitumor activity of sodium valproate in cultures of human neuroblastoma cells. Anticancer Drugs 7 (1996) 766-773
25. Gurvich N., Tsygankova O.M., Meinkoth J.L., and Klein P.S. Histone deacetylase is a target of valproic acid-mediated cellular differentiation. Cancer Res 64 (2004) 1079-1086
26. Phiel C.J., Zhang F., Huang E.Y., et al. Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J Biol Chem 276 (2001) 36734-36741
27. Roth S.Y., Denu J.M., and Allis C.D. Histone acetyltransferases. Annu Rev Biochem 70 (2001) 81-120
28. Wolffe A.P., and Hayes J.J. Chromatin disruption and modification. Nucl Acids Res 27 (1999) 711-720
29. Iizuka M., and Smith M.M. Functional consequences of histone modifications. Curr Opin Genet Dev 13 (2003) 154-160
30. Gottlicher M., Minucci S., Zhu P., et al. Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. EMBO J 20 (2001) 6969-6978
31. Hrzenjak A., Moinfar F., Kremser M.L., et al. Valproate inhibition of histone deacetylase 2 affects differentiation and decreases proliferation of endometrial stromal sarcoma cells. Mol Cancer Ther 5 (2006) 2203-2210
32. Li X.N., Shu Q., Su J.M., et al. 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 (2005) 1912-1922
33. Lin C.T., Lai H.C., Lee H.Y., et al. Valproic acid resensitizes cisplatin-resistant ovarian cancer cells. Cancer Sci 99 (2008) 1218-1226
34. Ziauddin M.F., Yeow W.S., Maxhimer J.B., et al. Valproic acid, an antiepileptic drug with histone deacetylase inhibitory activity, potentiates the cytotoxic effect of Apo2L/TRAIL on cultured thoracic cancer cells through mitochondria-dependent caspase activation. Neoplasia 8 (2006) 446-457
35. Duenas-Gonzalez A., Candelaria M., Perez-Plascencia C., et al. Valproic acid as epigenetic cancer drug: preclinical, clinical and transcriptional effects on solid tumors. Cancer Treat Rev 34 (2008) 206-222
36. Spiller H.A., Krenzelok E.P., Klein-Schwartz W., et al. Multicenter case series of valproic acid ingestion: serum concentrations and toxicity. J Toxicol Clin Toxicol 38 (2000) 755-760
37. Stewart DJ. Tumor and host factors that may limit efficacy of chemotherapy in non-small and small cell lung cancer. Crit Rev Oncol/Hematol 2009; in press. doi:10.1016/j.critrevonc.2009.11.006.
38. Bunn Jr. P.A., Soriano A., Johnson G., and Heasley L. New therapeutic strategies for lung cancer: biology and molecular biology come of age. Chest 117 (2000) 163S-168S
39. Doi S., Soda H., Oka M., et al. The histone deacetylase inhibitor FR901228 induces caspase-dependent apoptosis via the mitochondrial pathway in small cell lung cancer cells. Mol Cancer Ther 3 (2004) 1397-1402
40. Li H., Zhu H., Xu C.J., and Yuan J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94 (1998) 491-501
41. Luo X., Budihardjo I., Zou H., et al. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94 (1998) 481-490
42. Wang X. The expanding role of mitochondria in apoptosis. Genes Dev 15 (2001) 2922-2933
43. Billen L.P., Shamas-Din A., and Andrews D.W. Bid: a Bax-like BH3 protein. Oncogene 27S 1 (2008) S93-S104
44. Kumar B.S., Huang J., Persaud S., and Basu A. Down-regulation of Bcl-2 is associated with cisplatin resistance in human small cell lung cancer H69 cells. Mol Cancer Ther 3 (2004) 327-334
45. Ming L., Wang P., Bank A., et al. PUMA Dissociates Bax and Bcl-X(L) to induce apoptosis in colon cancer cells. J Biol Chem 281 (2006) 16034-16042
46. Yu J., Wang Z., Kinzler K.W., et al. PUMA mediates the apoptotic response to p53 in colorectal cancer cells. Proc Natl Acad Sci USA 100 (2003) 1931-1936
47. Cao X., Deng X., and May W.S. Cleavage of Bax to p18 Bax accelerates stress-induced apoptosis, and a cathepsin-like protease may rapidly degrade p18 Bax. Blood 102 (2003) 2605-2614
48. Choi W.S., Lee E.H., Chung C.W., et al. Cleavage of Bax is mediated by caspase-dependent or -independent calpain activation in dopaminergic neuronal cells: protective role of Bcl-2. J Neurochem 77 (2001) 1531-1541
49. Gao G., and Dou Q.P. N-terminal cleavage of bax by calpain generates a potent proapoptotic 18-kDa fragment that promotes bcl-2-independent cytochrome C release and apoptotic cell death. J Cell Biochem 80 (2000) 53-72
50. Wood D.E., Thomas A., Devi L.A., et al. Bax cleavage is mediated by calpain during drug-induced apoptosis. Oncogene 17 (1998) 1069-1078
51. Dokmanovic M., Clarke C., and Marks P.A. Histone deacetylase inhibitors: overview and perspectives. Mol Cancer Res 5 (2007) 981-989
52. Lindemann R.K., Gabrielli B., and Johnstone R.W. Histone-deacetylase inhibitors for the treatment of cancer. Cell Cycle 3 (2004) 779-788
53. Kim M.S., Blake M., Baek J.H., et al. Inhibition of histone deacetylase increases cytotoxicity to anticancer drugs targeting DNA. Cancer Res 63 (2003) 7291-7300
54. Tsai S.C., Valkov N., Yang W.M., et al. Histone deacetylase interacts directly with DNA topoisomerase II. Nat Genet 26 (2000) 349-353
55. Cohen H.Y., Lavu S., Bitterman K.J., et al. Acetylation of the C terminus of Ku70 by CBP and PCAF controls Bax-mediated apoptosis. Mol Cell 13 (2004) 627-638
56. Catalano M.G., Fortunati N., Pugliese M., et al. Valproic acid, a histone deacetylase inhibitor, enhances sensitivity to doxorubicin in anaplastic thyroid cancer cells. J Endocrinol 191 (2006) 465-472
57. Marchion D.C., Bicaku E., Daud A.I., et al. Valproic acid alters chromatin structure by regulation of chromatin modulation proteins. Cancer Res 65 (2005) 3815-3822
58. Hann C.L., and Rudin C.M. Management of small-cell lung cancer: incremental changes but hope for the future. Oncology 22 (2008) 1486-1492
59. Lara Jr. P.N., Natale R., Crowley J., et al. Phase III trial of irinotecan/cisplatin compared with etoposide/cisplatin in extensive-stage small-cell lung cancer: clinical and pharmacogenomic results from SWOG S0124. J Clin Oncol 27 (2009) 2530-2535
60. Munster P., Marchion D., Bicaku E., et al. 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 (2009) 2488-2496
61. Munster P., Marchion D., Bicaku E., et al. Phase I trial of histone deacetylase inhibition by valproic acid followed by the topoisomerase II inhibitor epirubicin in advanced solid tumors: a clinical and translational study. J Clin Oncol 25 (2007) 979-985