The novel inhibitor of histone deacetylase resminostat (RAS2410) inhibits proliferation and induces apoptosis in multiple myeloma (MM) cells

British Journal of Haematology

Volumn 149, Issue 4, 2010, Pages 518-528

  Mandl Weber, Sonja ^a   Meinel, Felix G ^a   Jankowsky, Rüdiger ^b   Oduncu, Fuat ^a   Schmidmaier, Ralf ^a   Baumann, Philipp ^a  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b NONE

Author keywords

Apoptosis; Cell cycle; Histone deacetylase; Multiple myeloma; Resminostat

Indexed keywords

BIM PROTEIN; BORTEZOMIB; CASPASE 3; CASPASE 8; CASPASE 9; CELL PROTEIN; CYCLIN D1; CYCLIN DEPENDENT KINASE 4; HISTONE DEACETYLASE INHIBITOR; HISTONE H4; INITIATION FACTOR 4E BINDING PROTEIN 1; MELPHALAN; PROTEASOME INHIBITOR; PROTEIN BAX; PROTEIN BCL XL; PROTEIN CDC25A; PROTEIN KINASE B; PROTEIN P21; RAS 2410; RESMINOSTAT; RETINOBLASTOMA PROTEIN; S 2209; S6 KINASE; UNCLASSIFIED DRUG;

ACETYLATION; ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL CYCLE ARREST; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL STRAIN HEK293; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG POTENCY; DRUG POTENTIATION; ENZYME ACTIVATION; GROWTH INHIBITION; HUMAN; HUMAN CELL; IC 50; IN VITRO STUDY; INSECT CELL; MITOSIS INHIBITION; MULTIPLE MYELOMA; MYELOMA CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ACETYLATION; ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; CELL PROLIFERATION; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SYNERGISM; HISTONE DEACETYLASE INHIBITORS; HISTONES; HUMANS; HYDROXAMIC ACIDS; MULTIPLE MYELOMA; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-BCL-2; SIGNAL TRANSDUCTION; SULFONAMIDES; TUMOR CELLS, CULTURED;

EID: 77951685547     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/j.1365-2141.2010.08124.x     Document Type: Article

References (57)

1. Badros, A., Burger, A.M., Philip, S., Niesvizky, R., Kolla, S.S., Goloubeva, O., Harris, C., Zwiebel, J., Wright, J.J., Espinoza-Delgado, I., Baer, M.R., Holleran, J.L., Egorin, M.J. Grant, S. (2009) Phase I study of vorinostat in combination with bortezomib for relapsed and refractory multiple myeloma. Clinical Cancer Research, 15, 5250 5257.
2. Batty, N., Malouf, G.G. Issa, J.P. (2009) Histone deacetylase inhibitors as anti-neoplastic agents. Cancer Letters, 280, 192 200.
3. Baumann, P., Müller, K., Mandl-Weber, S., Leban, J., Doblhofer, R., Ammendola, A., Baumgartner, R., Oduncu, F. Schmidmaier, R. (2009) The peptide-semicarbazone S-2209, a representative of a new class of proteasome inhibitors, induces apoptosis and cell growth arrest in multiple myeloma cells. British Journal of Haematology, 144, 875 886.
4. Baylin, S.B. Ohm, J.E. (2006) Epigenetic gene silencing in cancer - a mechanism for early oncogenic pathway addiction? Nature Reviews. Cancer, 6, 107 116.
5. Bolden, J.E., Peart, M.J. Johnstone, R.W. (2006) Anticancer activities of histone deacetylase inhibitos. Nature Reviews. Drug Discovery, 5, 769 784.
6. Catley, L., Weisberg, E., Tai, Y.T., Atadja, P., Remiszewski, S., Hideshima, T., Mitsiades, N., Shringarpure, R., LeBlanc, R., Chauhan, D., Munshi, N.C., Schlossman, R., Richardson, P., Griffin, J. Anderson, K.C. (2003) NVP-LAQ824 is a potent novel histone deacetylase inhibitor with significant activity against multiple myeloma. Blood, 102, 2615 2622. (Pubitemid 37193603)
7. Clayton, A.L., Hazzalin, C.A. Mahadevan, L.C. (2006) Enhanced histone acetylation and transcription: a dynamic perspective. Molecular Cell, 23, 289 296. (Pubitemid 44128853)
8. De Nadal, E., Zapater, M., Alepuz, P.M., Sumoy, L., Mas, G. Posas, F. (2004) The MAPK Hog1 recruits Rpd3 histone deacetylase to activate osmoresponsive genes. Nature, 427, 370 374. (Pubitemid 38133666)
9. Deleu, S., Lemaire, M., Arts, J., Menu, E., Van Valckenborgh, E., King, P., Vande Broek, I., De Raeve, H., Van Camp, B., Croucher, P. Vanderkerken, K. (2009a) The effects of JNJ-26481585, a novel hydroxamate-based histone deacetylase inhibitor, on the development of multiple myeloma in the 5T2MM and 5T33MM murine models. Leukemia, 23, 1894 1903.
10. Deleu, S., Lemaire, M., Arts, J., Menu, E., Van Valckenborgh, E., Vande Broek, I., De Raeve, H., Coulton, L., Van Camp, B., Croucher, P. Vanderkerken, K. (2009b) Bortezomib alone or in combination with the histone deacetylase inhibitor JNJ-26481585: effect on myeloma bone disease in the 5T2MM murine model of myeloma. Cancer Research, 69, 5307 5311.
11. Drummond, D.C., Noble, C.O., Kirpotin, D.B., Guo, Z., Scott, G.K. Benz, C.C. (2005) Clinical development of histone deacetylase inhibitors as anticancer agents. Annual Review of Pharmacology and Toxicology, 45, 495 528. (Pubitemid 40261815)
12. Duvic, M. Vu, J. (2007a) Vorinostat in cutaneous T-cell lymphoma. Drugs of today (Barcelona, Spain: 1998), 43, 585 599. (Pubitemid 350004865)
13. Duvic, M. Vu, J. (2007b) Vorinostat: a new oral histone deacetylase inhibitor approved for cutaneous T-cell lymphoma. Expert Opinion on Investigational Drugs, 16, 1111 1120. (Pubitemid 47074165)
14. Feng, R., Oton, A., Mapara, M.Y., Anderson, G., Belani, C. Lentzsch, S. (2007) The histone deacetylase inhibitor, PXD101, potentiates bortezomib-induced anti-multiple myeloma effect by induction of oxidative stress and DNA damage. British Journal of Haematology, 139, 385 397. (Pubitemid 47512171)
15. Feng, R., Ma, H., Hassig, C.A., Payne, J.E., Smith, N.D., Mapara, M.Y., Hager, J.H. Lentzsch, S. (2008) KD5170, a novel mercaptoketone-based histone deacetylase inhibitor, exerts antimyeloma effects by DNA damage and mitochondrial signaling. Molecular Cancer Therapeutics, 7, 1494 1505.
16. Fischle, W., Dequiedt, F., Hendzel, M.J., Guenther, M.G., Lazar, M.A., Voelter, W. Verdin, E. (2002) Enzymatic activity associated with class II HDACs is dependent on a multiprotein complex containing HDAC3 and SMRT/N-CoR. Molecular Cell, 9, 45 57. (Pubitemid 34127770)
17. Fraga, M.F., Ballestar, E., Villar-Garea, A., Boix-Chornet, M., Espada, J., Schotta, G., Bonaldi, T., Haydon, C., Ropero, S., Petrie, K., Iyer, N.G., Pérez-Rosado, A., Calvo, E., Lopez, J.A., Cano, A., Calasanz, M.J., Colomer, D., Piris, M.A., Ahn, N., Imhof, A., Caldas, C., Jenuwein, T. Esteller, M. (2005) Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nature Genetics, 37, 391 400. (Pubitemid 40490489)
18. Galli, M., Salmoiraghi, S., Golay, J., Gozzini, A., Crippa, C., Pescosta, N. Rambaldi, A. (2010) A phase II multiple dose clinical trial of histone deacetylase inhibitor ITF2357 in patients with relapsed or progressive multiple myeloma. Annals of Hematology, 89, 185 190.
19. Glaser, K.B., Li, J., Staver, M.J., Wei, R.Q., Albert, D.H. Davidsen, S.K. (2003) Role of class I and class II histone deacetylases in carcinoma cells using siRNA. Biochemical and Biophysical Research Communications, 310, 529 536. (Pubitemid 37163696)
20. Grunstein, M. (1997) Histone acetylation in chromatin structure and transcription. Nature, 389, 349 352. (Pubitemid 27415209)
21. Guarente, L. (2006) Sirtuins as potential targets for metabolic syndrome. Nature, 444, 868 874. (Pubitemid 46024994)
22. Gupta, M., Ansell, S.M., Novak, A.J., Kumar, S., Kaufmann, S.H. Witzig, T.E. (2009) Inhibition of histone deacetylase overcomes rapamycin- mediated resistance in diffuse large B cell lymphoma by inhibiting Akt signaling through mTORC2. Blood, 114, 2926 2935.
23. Haberland, M., Montgomery, R.L. Olson, E.N. (2009) The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nature Reviews Genetics, 10, 32 42.
24. Huang, L., Sowa, Y., Sakai, T. Pardee, A.B. (2000) Activation of the p21WAF1/CIP1 promoter independent of p53 by the histone deacetylase inhibitor suberoylanilide hydroxamic acid (SAHA) through the Sp1 sites. Oncogene, 19, 5712 5719.
25. Johnstone, R.W. (2002) Histone-deacetylase inhibitors: novel drugs for the treatment of cancer. Nature Reviews. Drug Discovery, 1, 287 299. (Pubitemid 37361445)
26. Khan, S.B., Maududi, T., Barton, K., Ayers, J. Alkan, S. (2004) Analysis of histone deacetylase inhibitor, depsipeptide (FR901228), effect on multiple myeloma. British Journal of Haematology, 125, 156 161. (Pubitemid 38534966)
27. Kitazoe, K., Abe, M., Hiasa, M., Oda, A., Amou, H., Harada, T., Nakano, A., Takeuchi, K., Hashimoto, T., Ozaki, S. Matsumoto, T. (2009) Valproic acid exerts anti-tumor as well as anti-angiogenic effects on myeloma. International Journal of Hematology, 89, 45 57.
28. Lahm, A., Paolini, C., Pallaoro, M., Nardi, M.C., Jones, P., Neddermann, P., Sambucini, S., Bottomley, M.J., Lo Surdo, P., Carfí, A., Koch, U., De Francesco, R., Steinkühler, C. Gallinari, P. (2007) Unraveling the hidden catalytic activity of vertebrate class IIa histone deacetylases. Proceedings of the National Academy of Sciences of the United States of America, 104, 17335 17340. (Pubitemid 350219843)
29. Lane, D.P. (1992) Cancer. p53, guardian of the genome. Nature, 358, 15 16.
30. Lin, R.J., Sternsdorf, T., Tini, M. Evans, R.M. (2001) Transcriptional regulation in acute promyelocytic leukemia. Oncogene, 20, 7204 7215. (Pubitemid 33105009)
31. Longo, V.D. Kennedy, B.K. (2006) Sirtuins in aging and age-related disease. Cell, 126, 257 268.
32. Lund, A.H. van Lohuizen, M. (2004) Epigenetics and cancer. Genes & Development, 18, 2315 2335. (Pubitemid 39310518)
33. Maiso, P., Carvajal-Vergara, X., Ocio, E.M., López-Pérez, R., Mateo, G., Gutiérrez, N., Atadja, P., Pandiella, A. San Miguel, J.F. (2006) The histone deacetylase inhibitor LBH589 is a potent antimyeloma agent that overcomes drug resistance. Cancer Research, 66, 5781 5789. (Pubitemid 43927132)
34. Marks, P., Rifkind, R.A., Richon, V.M., Breslow, R., Miller, T. Kelly, W.K. (2001) Histone deacetylases and cancer: causes and therapies. Nature Reviews. Cancer, 1, 194 202. (Pubitemid 33741894)
35. Minucci, S. Pelicci, P.G. (2006) Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nature Reviews. Cancer, 6, 38 51. (Pubitemid 43054973)
36. Mitsiades, N., Mitsiades, C.S., Richardson, P.G., McMullan, C., Poulaki, V., Fanourakis, G., Schlossman, R., Chauhan, D., Munshi, N.C., Hideshima, T., Richon, V.M., Marks, P.A. Anderson, K.C. (2003) Molecular sequelae of histone deacetylase inhibition in human malignant B cells. Blood, 101, 4055 4062. (Pubitemid 36857886)
37. Mitsiades, C.S., Mitsiades, N.S., McMullan, C.J., Poulaki, V., Shringarpure, R., Hideshima, T., Akiyama, M., Chauhan, D., Munshi, N., Gu, X., Bailey, C., Joseph, M., Libermann, T.A., Richon, V.M., Marks, P.A. Anderson, K.C. (2004) Transcriptional signature of histone deacetylase inhibition in multiple myeloma: biological and clinical implications. Proceedings of the National Academy of Sciences of the United States of America, 101, 540 545. (Pubitemid 38084672)
38. Mitsiades, C.S., Hideshima, T., Chauhan, D., McMillin, D.W., Klippel, S., Laubach, J.P., Munshi, N.C., Anderson, K.C. Richardson, P.G. (2009) Emerging treatments for multiple myeloma: beyond immunomodulatory drugs and bortezomib. Seminars in Hematology, 46, 166 175.
39. Neri, P., Tagliaferri, P., Di Martino, M.T., Calimeri, T., Amodio, N., Bulotta, A., Ventura, M., Eramo, P.O., Viscomi, C., Arbitrio, M., Rossi, M., Caraglia, M., Munshi, N.C., Anderson, K.C. Tassone, P. (2008) In vivo anti-myeloma activity and modulation of gene expression profile induced by valproic acid, a histone deacetylase inhibitor. British Journal of Haematology, 143, 520 531.
40. Olsen, E.A., Kim, Y.H., Kuzel, T.M., Pacheco, T.R., Foss, F.M., Parker, S., Frankel, S.R., Chen, C., Ricker, J.L., Arduino, J.M. Duvic, M. (2007) Phase IIb multicenter trial of vorinostat in patients with persistent, progressive, or treatment refractory cutaneous T-cell lymphoma. Journal of Clinical Oncology, 25, 3109 3115. (Pubitemid 47218059)
41. Pei, X.Y., Dai, Y. Grant, S. (2004) Synergistic induction of oxidative injury and apoptosis in human multiple myeloma cells by the proteasome inhibitor bortezomib and histone deacetylase inhibitors. Clinical Cancer Research, 10, 3839 3852. (Pubitemid 38697620)
42. Raab, M.S., Podar, K., Breitkreutz, I., Richardson, P.G. Anderson, K.C. (2009) Multiple myeloma. Lancet, 374, 324 339.
43. Richardson, P., Mitsiades, C., Colson, K., Reilly, E., McBride, L., Chiao, J., Sun, L., Ricker, J., Rizvi, S., Oerth, C., Atkins, B., Fearen, I., Anderson, K. Siegel, D. (2008) Phase I trial of oral vorinostat (suberoylanilide hydroxamic acid, SAHA) in patients with advanced multiple myeloma. Leukemia & Lymphoma, 49, 502 507. (Pubitemid 351298334)
44. Richon, V.M., Sandhoff, T.W., Rifkind, R.A. Marks, P.A. (2000) Histone deacetylase inhibitor selectively induces p21WAF1 expression and gene-associated histone acetylation. Proceedings of the National Academy of Sciences of the United States of America, 97, 10014 10019.
45. Roth, S.Y., Denu, J.M. Allis, C.D. (2001) Histone acetyltransferases. Annual Review of Biochemistry, 70, 81 120.
46. Roussel, M.F. (1999) The INK4 family of cell cycle inhibitors in cancer. Oncogene, 18, 5311 5317. (Pubitemid 29462366)
47. Ruthenburg, A.J., Li, H., Patel, D.J. Allis, C.D. (2007) Multivalent engagement of chromatin modifications by linked binding modules. Nature Reviews Molecular Cell Biology, 8, 983 994. (Pubitemid 350174643)
48. Sarbassov, D.D., Ali, S.M. Sabatini, D.M. (2005) Growing roles for the mTOR pathway. Current Opinion in Cell Biology, 17, 596 603.
49. Siegel, D., Weber, D., Mitsiades, C.S., Rizvi, S., Garcia-Vargas, J., Howe, J., Reiser, D., Anderson, K.C. Richardson, P. (2008) A Phase I Study of Vorinostat in Combination with Lenalidomide and Dexamethasone in Patients with Relapsed or Refractory Multiple Myeloma. American Society of Hematology Annual Meeting Abstracts, 112, 3705. (Pubitemid 351958961)
50. Tang, Y., Zhao, W., Chen, Y., Zhao, Y. Gu, W. (2008) Acetylation is indispensable for p53 activation. Cell, 133, 612 626. (Pubitemid 351636297)
51. Toyota, M. Issa, J.P. (2005) Epigenetic changes in solid and hematopoietic tumors. Seminars in Oncology, 32, 521 530. (Pubitemid 41396429)
52. Wang, A., Kurdistani, S.K. Grunstein, M. (2002) Requirement of Hos2 histone deacetylase for gene activity in yeast. Science, 298, 1412 1414. (Pubitemid 35346139)
53. Weber, D., Badros, A.Z., Jagannath, S., Siegel, D., Richon, D., Rizvi, S., Garcia-Vargas, J., Reiser, D. Anderson, K.C. (2008a) Vorinostat Plus Bortezomib for the Treatment of Relapsed/Refractory Multiple Myeloma: Early Clinical Experience. American Society of Hematology Annual Meeting Abstracts, 112, 871.
54. Weber, D.M., Jagannath, S., Sobecks, R., Schiller, G., Chiaccierini, L., Reiser, D., Oerth, C., Garcia-Vargas, J. Rizvi, S. (2008b) Combination of Vorinostat Plus Bortezomib for the Treatment of Patients with Multiple Myeloma Who Have Previously Received Bortezomib. American Society of Hematology Annual Meeting Abstracts, 112, 3711.
55. Wegener, D., Wirsching, F., Riester, D. Schwienhorst, A. (2003) A fluorogenic histone deacetylase assay well suited for high-throughput activity screening. Chemistry & Biology, 10, 61 68. (Pubitemid 36154475)
56. Wilson, A.J., Byun, D.S., Popova, N., Murray, L.B., L'Italien, K., Sowa, Y., Arango, D., Velcich, A., Augenlicht, L.H. Mariadason, J.M. (2006) Histone deacetylase 3 (HDAC3) and other class I HDACs regulate colon cell maturation and p21 expression and are deregulated in human colon cancer. Journal of Biological Chemistry, 281, 13548 13558. (Pubitemid 43855268)
57. Zhu, P., Martin, E., Mengwasser, J., Schlag, P., Janssen, K.P. Göttlicher, M. (2004) Induction of HDAC2 expression upon loss of APC in colorectal tumorigenesis. Cancer Cell, 5, 455 463. (Pubitemid 38610247)