Valproate synergizes with purine nucleoside analogues to induce apoptosis of B-chronic lymphocytic leukaemia cells

British Journal of Haematology

Volumn 144, Issue 1, 2009, Pages 41-52

  Bouzar, Amel Baya ^a   Boxus, Mathieu ^a   Defoiche, Julien ^a   Berchem, Guy ^b   Macallan, Derek ^c   Pettengell, Ruth ^c   Willis, Fenella ^c   Burny, Arsène ^a   Lagneaux, Laurence ^d   Bron, Dominique ^d   Chatelain, Bernard ^e   Chatelain, Christian ^e   Willems, Luc ^a  

^a FUND FOR SCIENTIFIC RESEARCH   (Belgium)

^b CENTRE HOSPITALIER DE LUXEMBOURG   (Luxembourg)

^c ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

^d JULES BORDET INSTITUTE   (Belgium)

^e UNIVERSITY HOSPITAL OF MONT GODINNE   (Belgium)

Author keywords

Apoptosis; Chronic lymphocytic leukaemia; Cladribine; Fludarabine; Valproate

Indexed keywords

ACETYLCYSTEINE; CASPASE; CLADRIBINE; CYCLOPHOSPHAMIDE; CYTARABINE; CYTOCHROME C; DOXORUBICIN; FAS ANTIGEN; FLUDARABINE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PREDNISOLONE; PROTEIN BAX; REACTIVE OXYGEN METABOLITE; RITUXIMAB; VALPROIC ACID; VINCRISTINE; VINCRISTINE SULFATE;

ADULT; AGED; APOPTOSIS; ARTICLE; B CELL LEUKEMIA; B LYMPHOCYTE; CHRONIC LYMPHATIC LEUKEMIA; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG INHIBITION; DRUG POTENTIATION; DRUG SENSITIVITY; EPIGENETICS; FEMALE; HUMAN; HUMAN CELL; LEUKEMIA CELL; MALE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; STIMULATION;

ADULT; AGED; AGED, 80 AND OVER; ANTINEOPLASTIC AGENTS; APOPTOSIS; BLOTTING, WESTERN; CLADRIBINE; DRUG SYNERGISM; ENZYME INHIBITORS; FEMALE; HISTONE DEACETYLASES; HUMANS; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; MALE; MICROSCOPY, CONFOCAL; MIDDLE AGED; REACTIVE OXYGEN SPECIES; TUMOR CELLS, CULTURED; VALPROIC ACID; VIDARABINE;

EID: 57449103563     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/j.1365-2141.2008.07426.x     Document Type: Article

References (56)

1. Achachi, A., Florins, A., Gillet, N., Debacq, C., Urbain, P., Foutsop, G.M., Vandermeers, F., Jasik, A., Reichert, M., Kerkhofs, P., Lagneaux, L., Burny, A., Kettmann, R. Willems, L. (2005) Valproate activates bovine leukemia virus gene expression, triggers apoptosis, and induces leukemia/lymphoma regression in vivo. Proceedings of the National Academy of Sciences of the United States of America, 102, 10309 10314.
2. Adrain, C., Creagh, E.M. Martin, S.J. (2001) Apoptosis-associated release of Smac/DIABLO from mitochondria requires active caspases and is blocked by Bcl-2. EMBO Journal, 20, 6627 6636.
3. Anaissie, E.J., Kontoyiannis, D.P., O'Brien, S., Kantarjian, H., Robertson, L., Lerner, S. Keating, M.J. (1998) Infections in patients with chronic lymphocytic leukemia treated with fludarabine. Annals of Internal Medicine, 129, 559 566.
4. Bialer, M. Yagen, B. (2007) Valproic acid: second generation. Neurotherapeutics, 4, 130 137.
5. Blaheta, R.A., Nau, H., Michaelis, M. Cinatl, J. (2002) Valproate and valproate-analogues: potent tools to fight against cancer. Current Medicinal Chemistry, 9, 1417 1433.
6. Bokelmann, I. Mahlknecht, U. (2007) Valproic acid sensitizes chronic lymphocytic leukemia cells to apoptosis and restores the balance between pro- and antiapoptotic proteins. Molecular Medicine, 14 (1-2 20 7.
7. Byrd, J.C., Rai, K., Peterson, B.L., Appelbaum, F.R., Morrison, V.A., Kolitz, J.E., Shepherd, L., Hines, J.D., Schiffer, C.A. Larson, R.A. (2005a) Addition of rituximab to fludarabine may prolong progression-free survival and overall survival in patients with previously untreated chronic lymphocytic leukemia: an updated retrospective comparative analysis of CALGB 9712 and CALGB 9011. Blood, 105, 49 53.
8. Byrd, J.C., Marcucci, G., Parthun, M.R., Xiao, J.J., Klisovic, R.B., Moran, M., Lin, T.S., Liu, S., Sklenar, A.R., Davis, M.E., Lucas, D.M., Fischer, B., Shank, R., Tejaswi, S.L., Binkley, P., Wright, J., Chan, K.K. Grever, M.R. (2005b) A phase 1 and pharmacodynamic study of depsipeptide (FK228) in chronic lymphocytic leukemia and acute myeloid leukemia. Blood, 105, 959 967.
9. Cameron, E.E., Bachman, K.E., Myohanen, S., Herman, J.G. Baylin, S.B. (1999) Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer. Nature Genetics, 21, 103 107.
10. Catalano, M.G., Fortunati, N., Pugliese, M., Costantino, L., Poli, R., Bosco, O. Boccuzzi, G. (2005) Valproic acid induces apoptosis and cell cycle arrest in poorly differentiated thyroid cancer cells. Journal of Clinical Endocrinology and Metabolism, 90, 1383 1389.
11. ten Cate, B., Samplonius, D.F., Bijma, T., de Leij, L.F., Helfrich, W. Bremer, E. (2007) The histone deacetylase inhibitor valproic acid potently augments gemtuzumab ozogamicin-induced apoptosis in acute myeloid leukemic cells. Leukemia, 21, 248 252.
12. Chapman, A., Keane, P.E., Meldrum, B.S., Simiand, J. Vernieres, J.C. (1982) Mechanism of anticonvulsant action of valproate. Progress in Neurobiology, 19, 315 359.
13. Chen, J., Ghazawi, F.M., Bakkar, W. Li, Q. (2006) Valproic acid and butyrate induce apoptosis in human cancer cells through inhibition of gene expression of Akt/protein kinase B. Molecular Cancer, 5, 71.
14. Cheson, B.D. (1995) Infectious and immunosuppressive complications of purine analog therapy. Journal of Clinical Oncology, 13, 2431 2448.
15. Cheson, B.D., Vena, D.A., Barrett, J. Freidlin, B. (1999) Second malignancies as a consequence of nucleoside analog therapy for chronic lymphoid leukemias. Journal of Clinical Oncology, 17, 2454 2460.
16. Cinatl, J., Cinatl, J., Scholz, M., Driever, P.H., Henrich, D., Kabickova, H., Vogel, J.U., Doerr, H.W. Kornhuber, B. (1996) Antitumor activity of sodium valproate in cultures of human neuroblastoma cells. Anti-Cancer Drugs, 7, 766 773.
17. Cinatl, J., Kotchetkov, R., Blaheta, R., Driever, P.H., Vogel, J.U. Cinatl, J. (2002) Induction of differentiation and suppression of malignant phenotype of human neuroblastoma BE(2)-C cells by valproic acid: enhancement by combination with interferon-alpha. International Journal of Oncology, 20, 97 106.
18. Deng, Y., Lin, Y. Wu, X. (2002) TRAIL-induced apoptosis requires Bax-dependent mitochondrial release of Smac/DIABLO. Genes and Development, 16, 33 45.
19. Dohner, H., Fischer, K., Bentz, M., Hansen, K., Benner, A., Cabot, G., Diehl, D., Schlenk, R., Coy, J. Stilgenbauer, S. (1995) p53 gene deletion predicts for poor survival and non-response to therapy with purine analogs in chronic B-cell leukemias. Blood, 85, 1580 1589.
20. Gallinari, P., Di Marco, S., Jones, P., Pallaoro, M. Steinkuhler, C. (2007) HDACs, histone deacetylation and gene transcription: from molecular biology to cancer therapeutics. Cell Research, 17, 195 211.
21. Gao, S., Mobley, A., Miller, C., Boklan, J. Chandra, J. (2008) Potentiation of reactive oxygen species is a marker for synergistic cytotoxicity of MS-275 and 5-azacytidine in leukemic cells. Leukemia Research, 32, 771 780.
22. Genini, D., Adachi, S., Chao, Q., Rose, D.W., Carrera, C.J., Cottam, H.B., Carson, D.A. Leoni, L.M. (2000) Deoxyadenosine analogs induce programmed cell death in chronic lymphocytic leukemia cells by damaging the DNA and by directly affecting the mitochondria. Blood, 96, 3537 3543.
23. Gottlicher, M., Minucci, S., Zhu, P., Kramer, O.H., Schimpf, A., Giavara, S., Sleeman, J.P., Lo, C.F., Nervi, C., Pelicci, P.G. Heinzel, T. (2001) Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. EMBO Journal, 20, 6969 6978.
24. Insinga, A., Monestiroli, S., Ronzoni, S., Gelmetti, V., Marchesi, F., Viale, A., Altucci, L., Nervi, C., Minucci, S. Pelicci, P.G. (2005) Inhibitors of histone deacetylases induce tumor-selective apoptosis through activation of the death receptor pathway. Nature Medicine, 11, 71 76.
25. Johannessen, C.U. Johannessen, S.I. (2003) Valproate: past, present, and future. CNS Drug Reviews, 9, 199 216.
26. Keating, M.J., Kantarjian, H., Talpaz, M., Redman, J. Mccredie, K.B. (1988) Fludarabine therapy in chronic lymphocytic-leukemia (Cll). Nouvelle Revue Francaise D Hematologie, 30, 461 466.
27. Keating, M.J., O'Brien, S., Kantarjian, H., Plunkett, W., Estey, E., Koller, C., Beran, M. Freireich, E.J. (1993) Long-term follow-up of patients with chronic lymphocytic leukemia treated with fludarabine as a single agent. Blood, 81, 2878 2884.
28. Keating, M.J., O'Brien, S., Lerner, S., Koller, C., Beran, M., Robertson, L.E., Freireich, E.J., Estey, E. Kantarjian, H. (1998) Long-term follow-up of patients with chronic lymphocytic leukemia (CLL) receiving fludarabine regimens as initial therapy. Blood, 92, 1165 1171.
29. Keating, M.J., O'Brien, S., Albitar, M., Lerner, S., Plunkett, W., Giles, F., Andreeff, M., Cortes, J., Faderl, S., Thomas, D., Koller, C., Wierda, W., Detry, M.A., Lynn, A. Kantarjian, H. (2005) Early results of a chemoimmunotherapy regimen of fludarabine, cyclophosphamide, and rituximab as initial therapy for chronic lymphocytic leukemia. Journal of Clinical Oncology, 23, 4079 4088.
30. Kostrouchova, M., Kostrouch, Z. Kostrouchova, M. (2007) Valproic acid, a molecular lead to multiple regulatory pathways. Folia Biologica (Praha), 53, 37 49.
31. Kroft, S.H., Tallman, M.S., Shaw, J.M., Thangavelu, M. Peterson, L.C. (1997) Myelodysplasia following treatment of chronic lymphocytic leukemia (CLL) with 2-chlorodeoxyadenosine (2-CdA). Leukemia, 11, 170.
32. Lagneaux, L., Gillet, N., Stamatopoulos, B., Delforge, A., Dejeneffe, M., Massy, M., Meuleman, N., Kentos, A., Martiat, P., Willems, L. Bron, D. (2007) Valproic acid induces apoptosis in chronic lymphocytic leukemia cells through activation of the death receptor pathway and potentiates TRAIL response. Experimental Hematology, 35, 1527 1537.
33. Lin, H.Y., Chen, C.S., Lin, S.P., Weng, J.R. Chen, C.S. (2006) Targeting histone deacetylase in cancer therapy. Medicinal Research Reviews, 26, 397 413.
34. Lin, C.T., Lai, H.C., Lee, H.Y., Lin, W.H., Chang, C.C., Chu, T.Y., Lin, Y.W., Lee, K.D. Yu, M.H. (2008) Valproic acid resensitizes cisplatin-resistant ovarian cancer cells. Cancer Science, 99, 1218 1226.
35. Lucas, D.M., Davis, M.E., Parthun, M.R., Mone, A.P., Kitada, S., Cunningham, K.D., Flax, E.L., Wickham, J., Reed, J.C., Byrd, J.C. Grever, M.R. (2004) The histone deacetylase inhibitor MS-275 induces caspase-dependent apoptosis in B-cell chronic lymphocytic leukemia cells. Leukemia, 18, 1207 1214.
36. Maggio, S.C., Rosato, R.R., Kramer, L.B., Dai, Y., Rahmani, M., Paik, D.S., Czarnik, A.C., Payne, S.G., Spiegel, S. Grant, S. (2004) The histone deacetylase inhibitor MS-275 interacts synergistically with fludarabine to induce apoptosis in human leukemia cells. Cancer Research, 64, 2590 2600.
37. Marzo, I., Perez-Galan, P., Giraldo, P., Rubio-Felix, D., Anel, A. Naval, J. (2001) Cladribine induces apoptosis in human leukaemia cells by caspase-dependent and -independent pathways acting on mitochondria. Biochemical Journal, 359, 537 546.
38. Miller, C.P., Ban, K., Dujka, M.E., McConkey, D.J., Munsell, M., Palladino, M. Chandra, J. (2007) NPI-0052, a novel proteasome inhibitor, induces caspase-8 and ROS-dependent apoptosis alone and in combination with HDAC inhibitors in leukemia cells. Blood, 110, 267 277.
39. Montserrat, E. (2004) Treatment options in chronic lymphocytic leukemia. Hematology Journal, 5, S2 S9.
40. Nechushtan, A., Smith, C.L., Hsu, Y.T. Youle, R.J. (1999) Conformation of the Bax C-terminus regulates subcellular location and cell death. EMBO Journal, 18, 2330 2341.
41. O'Brien, S.M., Kantarjian, A.M., Cortes, J., Beran, M., Koller, C.A., Giles, F.J., Lerner, S. Keating, M. (2001) Results of the fludarabine and cyclophosphamide combination regimen in chronic lymphocytic leukemia. Journal of Clinical Oncology, 19, 1414 1420.
42. Ozaki, K., Kishikawa, F., Tanaka, M., Sakamoto, T., Tanimura, S. Kohno, M. (2008) Histone deacetylase inhibitors enhance the chemosensitivity of tumor cells with cross-resistance to a wide range of DNA-damaging drugs. Cancer Science, 99, 376 384.
43. Rahmani, M., Reese, E., Dai, Y., Bauer, C., Payne, S.G., Dent, P., Spiegel, S. Grant, S. (2005) Coadministration of histone deacetylase inhibitors and perifosine synergistically induces apoptosis in human leukemia cells through Akt and ERK1/2 inactivation and the generation of ceramide and reactive oxygen species. Cancer Research, 65, 2422 2432.
44. Rasheed, W.K., Johnstone, R.W. Prince, H.M. (2007) Histone deacetylase inhibitors in cancer therapy. Expert Opinion on Investigational Drugs, 16, 659 678.
45. Riester, D., Hildmann, C. Schwienhorst, A. (2007) Histone deacetylase inhibitors-turning epigenic mechanisms of gene regulation into tools of therapeutic intervention in malignant and other diseases. Applied Microbiology and Biotechnology, 75, 499 514.
46. Robak, T., Blonski, J.Z., Urbanska-Rys, H., Blasinska-Morawiec, M. Skotnicki, A.B. (1999) 2-chlorodeoxyadenosine (cladribine) in the treatment of patients with chronic lymphocytic leukemia 55 years old and younger. Leukemia, 13, 518 523.
47. Rosato, R.R., Maggio, S.C., Almenara, J.A., Payne, S.G., Atadja, P., Spiegel, S., Dent, P. Grant, S. (2006) The histone deacetylase inhibitor LAQ824 induces human leukemia cell death through a process involving XIAP down-regulation, oxidative injury, and the acid sphingomyelinase-dependent generation of ceramide. Molecular Pharmacology, 69, 216 225.
48. Ruefli, A.A., Ausserlechner, M.J., Bernhard, D., Sutton, V.R., Tainton, K.M., Kofler, R., Smyth, M.J. Johnstone, R.W. (2001) The histone deacetylase inhibitor and chemotherapeutic agent suberoylanilide hydroxamic acid (SAHA) induces a cell-death pathway characterized by cleavage of Bid and production of reactive oxygen species. Proceedings of the National Academy of Sciences of the United States of America, 98, 10833 10838.
49. Tallman, M.S. Hakimian, D. (1995) Purine nucleoside analogs - emerging roles in indolent lymphoproliferative disorders. Blood, 86, 2463 2474.
50. Tsapis, M., Lieb, M., Manzo, F., Shankaranarayanan, P., Herbrecht, R., Lutz, P. Gronemeyer, H. (2007) HDAC inhibitors induce apoptosis in glucocorticoid-resistant acute lymphatic leukemia cells despite a switch from the extrinsic to the intrinsic death pathway. International Journal of Biochemistry and Cell Biology, 39, 1500 1509.
51. Van Den Neste, E., Cardoen, S., Offner, F. Bontemps, F. (2005) Old and new insights into the mechanisms of action of two nucleoside analogs active in lymphoid malignancies: fludarabine and cladribine (review). International Journal of Oncology, 27, 1113 1124.
52. Wierda, W., O'Brien, S., Wen, S., Faderl, S., Garcia-Manero, G., Thomas, D., Do, K.A., Cortes, J., Koller, C., Beran, M., Ferrajoli, A., Giles, F., Lerner, S., Albitar, M., Kantarjian, H. Keating, M. (2005) Chemoimmunotherapy with fludarabine, cyclophosphamide, and rituximab for relapsed and refractory chronic lymphocytic leukemia. Journal of Clinical Oncology, 23, 4070 4078.
53. Wierda, W., O'Brien, S., Faderl, S., Ferrajoli, A., Wang, X., Do, K.A., Garcia-Manero, G., Thomas, D., Cortes, J., Ravandi-Kashani, F., Giles, F., Lerner, S., Kantarjian, H. Keating, M. (2006) A retrospective comparison of three sequential groups of patients with Recurrent/Refractory chronic lymphocytic leukemia treated with fludarabine-based regimens. Cancer, 106, 337 345.
54. Witzig, T.E., Timm, M., Stenson, M., Svingen, P.A. Kaufmann, S.H. (2000) Induction of apoptosis in malignant B cells by phenylbutyrate or phenylacetate in combination with chemotherapeutic agents. Clinical Cancer Research, 6, 681 692.
55. Zaskodova, D., Rezacova, M., Vavrova, J., Vokurkova, D. Tichy, A. (2006) Effect of valproic acid, a histone deacetylase inhibitor, on cell death and molecular changes caused by low-dose irradiation. Annals of the New York Academy of Sciences, 1091, 385 398.
56. Zinzani, P.L. (2001) A randomized trial of fludarabine and mitoxantrone plus rituximab versus CHOP plus rituximab as first-line treatment in patients with follicular lymphoma. Blood, 98, 842A.