Romidepsin in peripheral and cutaneous T-cell lymphoma: Mechanistic implications from clinical and correlative data

British Journal of Haematology

Volumn 170, Issue 1, 2015, Pages 96-109

  Bates, Susan E ^a   Eisch, Robin ^a   Ling, Alexander ^b   Rosing, Douglas ^a   Turner, Maria ^c   Pittaluga, Stefania ^c   Prince, H Miles ^d   Kirschbaum, Mark H ^e   Allen, Steven L ^f   Zain, Jasmine ^g   Geskin, Larisa J ^h   Joske, David ⁱ   Popplewell, Leslie ^j   Cowen, Edward W ^c   Jaffe, Elaine S ^c   Nichols, Jean ^k   Kennedy, Sally ^l   Steinberg, Seth M ^c   Liewehr, David J ^c   Showe, Louise C ^m   Steakley, Caryn ^c   Wright, John ^c   Fojo, Tito ^c   Litman, Thomas ⁿ   Piekarz, Richard L ^c   more..

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d PETER MACCALLUM CANCER CENTRE   (Australia)

^e PENN STATE MILTON S HERSHEY MEDICAL CENTER   (United States)

^f DONALD AND BARBARA ZUCKER SCHOOL OF MEDICINE AT HOFSTRA NORTHWELL   (United States)

^g Howard Hughes Medical Institute   (United States)

^h UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

ⁱ SIR CHARLES GAIRDNER HOSPITAL   (Australia)

^j CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^k CELGENE CORPORATION   (United States)

^l LEO Pharma A/S ^*  (United States)

^m WISTAR INSTITUTE   (United States)

ⁿ LEO PHARMA A S   (Denmark)

more..

Author keywords

Chromatin; Epigenetic therapy; Histone deacetylase inhibitor; Romidepsin; T cell lymphoma

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; BILIRUBIN; COMPLEMENTARY DNA; ROMIDEPSIN; ANTINEOPLASTIC ANTIBIOTIC; DEPSIPEPTIDE; HISTONE DEACETYLASE INHIBITOR;

ADULT; AGE DISTRIBUTION; AGED; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANOREXIA; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BILIRUBIN BLOOD LEVEL; CLINICAL EFFECTIVENESS; CUTANEOUS T CELL LYMPHOMA; DOSE RESPONSE; DRUG DOSE REDUCTION; DRUG EFFICACY; DRUG SAFETY; DRUG TOLERABILITY; DYSGEUSIA; EPIGENETICS; FATIGUE; FEMALE; GASTROINTESTINAL SYMPTOM; GENE EXPRESSION PROFILING; GENE INDUCTION; GENE REPRESSION; HUMAN; MAJOR CLINICAL STUDY; MALE; MICROARRAY ANALYSIS; MIDDLE AGED; MULTICENTER STUDY; MULTIPLE CYCLE TREATMENT; NAUSEA; NEUTROPENIA; PERIPHERAL T CELL LYMPHOMA; PHASE 2 CLINICAL TRIAL; POPULATION RESEARCH; PRIORITY JOURNAL; SEX DIFFERENCE; THROMBOCYTOPENIA; TREATMENT DURATION; TREATMENT OUTCOME; VOMITING; CLINICAL TRIAL; LYMPHOMA, T-CELL, CUTANEOUS; PATHOLOGY; PROSPECTIVE STUDY; SKIN NEOPLASMS; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; ANTIBIOTICS, ANTINEOPLASTIC; DEPSIPEPTIDES; EPIGENOMICS; FEMALE; HISTONE DEACETYLASE INHIBITORS; HUMANS; LYMPHOMA, T-CELL, CUTANEOUS; MALE; MIDDLE AGED; PROSPECTIVE STUDIES; SKIN NEOPLASMS;

EID: 84931569035     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/bjh.13400     Document Type: Article

References (67)

1. Bates, S., Zhan, Z., Steadman, K., Obrzut, T., Luchenko, V., Frye, R., Robey, R., Turner, M., Gardner, E., Figg, W., Steinberg, S., Ling, A., Fojo, T., To, K. & Piekarz, R. (2010) Laboratory correlates for a phase II trial of romidepsin in cutaneous and peripheral T-cell lymphoma. British Journal of Haematology, 148, 256-267.
2. Bhalla, S., Balasubramanian, S., David, K., Sirisawad, M., Buggy, J., Mauro, L., Prachand, S., Miller, R., Gordon, L.I. & Evens, A.M. (2009) PCI-24781 induces caspase and reactive oxygen species-dependent apoptosis through NF-kappaB mechanisms and is synergistic with bortezomib in lymphoma cells. Clinical Cancer Research, 15, 3354-3365.
3. Bolden, J.E., Shi, W., Jankowski, K., Kan, C.Y., Cluse, L., Martin, B.P., MacKenzie, K.L., Smyth, G.K. & Johnstone, R.W. (2013) HDAC inhibitors induce tumor-cell-selective pro-apoptotic transcriptional responses. Cell Death and Disease, 4, e519.
4. Cabell, C., Bates, S., Piekarz, R., Whittaker, S., Kim, Y.H., Currie, M., Godfrey, C.J., Schoonmaker, C., Nichols, J., Nix, D. & Burris, H.A. (2009) Systematic assessment of potential cardiac effects of the novel histone deacetylase (HDAC) inhibitor romidepsin. Blood (American Society of Hematology Annual Meeting Abstracts), 114, 3709.
5. Campbell, J.J., Clark, R.A., Watanabe, R. & Kupper, T.S. (2010) Sezary syndrome and mycosis fungoides arise from distinct T-cell subsets: a biologic rationale for their distinct clinical behaviors. Blood, 116, 767-771.
6. Chakraborty, A.R., Robey, R.W., Luchenko, V.L., Zhan, Z., Piekarz, R.L., Gillet, J.P., Kossenkov, A.V., Wilkerson, J., Showe, L.C., Gottesman, M.M., Collie, N.L. & Bates, S.E. (2013) MAPK pathway activation leads to Bim loss and histone deacetylase inhibitor resistance: rationale to combine romidepsin with an MEK inhibitor. Blood, 121, 4115-4125.
7. Chen, S., Dai, Y., Pei, X. & Grant, S. (2009) Bim upregulation by histone deacetylase inhibitors mediates interactions with the Bcl-2 antagonist ABT-737: evidence for distinct roles for Bcl-2, Bcl-xL, and Mcl-1. Molecular and Cellular Biology, 29, 6149-6169.
8. Cheson, B., Horning, S., Coiffier, B., Shipp, M., Fisher, R., Connors, J., Lister, T., Vose, J., Grillo-López, A., Hagenbeek, A., Cabanillas, F., Klippensten, D., Hiddemann, W., Castellino, R., Harris, N., Armitage, J., Carter, W., Hoppe, R. & Canellos, G. (1999) Report of an international workshop to standardize response criteria for non-Hodgkin's lymphomas. NCI Sponsored International Working Group. Journal of Clinical Oncology, 17, 1244.
9. Chien, W., Lee, D.H., Zheng, Y., Wuensche, P., Alvarez, R., Wen, D.L., Aribi, A.M., Thean, S.M., Doan, N.B., Said, J.W. & Koeffler, H.P. (2014) Growth inhibition of pancreatic cancer cells by histone deacetylase inhibitor belinostat through suppression of multiple pathways including HIF, NFkB, and mTOR signaling in vitro and in vivo. Molecular Carcinogenesis, 53, 722-735.
10. Coiffier, B., Pro, B., Prince, H.M., Foss, F., Sokol, L., Greenwood, M., Caballero, D., Borchmann, P., Morschhauser, F., Wilhelm, M., Pinter-Brown, L., Padmanabhan, S., Shustov, A., Nichols, J., Carroll, S., Balser, J., Balser, B. & Horwitz, S. (2012) Results from a pivotal, open-label, phase II study of romidepsin in relapsed or refractory peripheral T-cell lymphoma after prior systemic therapy. Journal of Clinical Oncology, 30, 631-636.
11. Coiffier, B., Pro, B., Prince, H.M., Foss, F., Sokol, L., Greenwood, M., Caballero, D., Morschhauser, F., Wilhelm, M., Pinter-Brown, L., Padmanabhan Iyer, S., Shustov, A., Nielsen, T., Nichols, J., Wolfson, J., Balser, B. & Horwitz, S. (2014) Romidepsin for the treatment of relapsed/refractory peripheral T-cell lymphoma: pivotal study update demonstrates durable responses. Journal of Hematology & Oncology, 7, 11.
12. Conti, C., Leo, E., Eichler, G.S., Sordet, O., Martin, M.M., Fan, A., Aladjem, M.I. & Pommier, Y. (2010) Inhibition of histone deacetylase in cancer cells slows down replication forks, activates dormant origins, and induces DNA damage. Cancer Research, 70, 4470-4480.
13. Dupuis, J., Casasnovas, R.-O., Ghesquieres, H., Morschhauser, F., Tilly, H., Thieblemont, C., Ribrag, V. & Coiffier, B. (2012) A Phase Ib trial of romidepsin in association with CHOP in patients with peripheral t-cell lymphoma (PTCL): the Ro-CHOP study. Blood (American Society of Hematology Annual Meeting Abstracts), 120, 1617.
14. Duvic, M., Talpur, R., Ni, X., Zhang, C., Hazarika, P., Kelly, C., Chiao, J., Reilly, J., Ricker, J., Richon, V. & Frankel, S. (2007) Phase 2 trial of oral vorinostat (suberoylanilide hydroxamic acid, SAHA) for refractory cutaneous T-cell lymphoma (CTCL). Blood, 109, 31-39.
15. Ellis, L., Pan, Y., Smyth, G., George, D., McCormack, C., Williams-Truax, R., Mita, M., Beck, J., Burris, H., Ryan, G., Atadja, P., Butterfoss, D., Dugan, M., Culver, K., Johnstone, R. & Prince, H. (2008) Histone deacetylase inhibitor panobinostat induces clinical responses with associated alterations in gene expression profiles in cutaneous T-cell lymphoma. Clinical Cancer Research, 14, 4500-4510.
16. Ellis, L., Bots, M., Lindemann, R.K., Bolden, J.E., Newbold, A., Cluse, L.A., Scott, C.L., Strasser, A., Atadja, P., Lowe, S.W. & Johnstone, R.W. (2009) The histone deacetylase inhibitors LAQ824 and LBH589 do not require death receptor signaling or a functional apoptosome to mediate tumor cell death or therapeutic efficacy. Blood, 114, 380-393.
17. Fabre, C., Grosjean, J., Tailler, M., Boehrer, S., Adès, L., Perfettini, J.L., de Botton, S., Fenaux, P. & Kroemer, G. (2008) A novel effect of DNA methyltransferase and histone deacetylase inhibitors: NFkappaB inhibition in malignant myeloblasts. Cell Cycle, 7, 2139-2145.
18. Ferrara, G., Pancione, M., Votino, C., Quaglino, P., Tomasini, C., Santucci, M., Pimpinelli, N., Cusano, F., Sabatino, L. & Colantuoni, V. (2013) A specific DNA methylation profile correlates with a high risk of disease progression in stage I classical (Alibert-Bazin type) mycosis fungoides. British Journal of Dermatology, 170, 1266-1275.
19. Foss, F., Advani, R., Duvic, M., Hymes, K.B., Intragumtornchai, T., Lekhakula, A., Shpilberg, O., Lerner, A., Belt, R.J., Jacobsen, E.D., Laurent, G., Ben-Yehuda, D., Beylot-Barry, M., Hillen, U., Knoblauch, P., Bhat, G., Chawla, S., Allen, L.F. & Pohlman, B. (2015) A Phase II trial of Belinostat (PXD101) in patients with relapsed or refractory peripheral or cutaneous T-cell lymphoma. British Journal of Haematology, 168, 811-819.
20. Frye, R., Myers, M., Axelrod, K.C., Ness, E.A., Piekarz, R.L., Bates, S.E. & Booher, S. (2012) Romidepsin: a new drug for the treatment of cutaneous T-cell lymphoma. Clinical Journal of Oncology Nursing, 16, 195-204.
21. Gaymes, T.J., Padua, R.A., Pla, M., Orr, S., Omidvar, N., Chomienne, C., Mufti, G.J. & Rassool, F.V. (2006) Histone deacetylase inhibitors (HDI) cause DNA damage in leukemia cells: a mechanism for leukemia-specific HDI-dependent apoptosis? Molecular Cancer Research, 4, 563-573.
22. Grant, C., Rahman, F., Piekarz, R., Peer, C., Frye, R., Robey, R.W., Gardner, E.R., Figg, W.D. & Bates, S.E. (2010) Romidepsin: a new therapy for cutaneous T-cell lymphoma and a potential therapy for solid tumors. Expert Review of Anticancer Therapy, 10, 997-1008.
23. Ierano, C., Chakraborty, A.R., Nicolae, A., Bahr, J.C., Zhan, Z., Pittaluga, S., Bates, S.E. & Robey, R.W. (2013) Loss of the proteins Bak and Bax prevents apoptosis mediated by histone deacetylase inhibitors. Cell Cycle, 12, 2829-2838.
24. Jóna, A., Khaskhely, N., Buglio, D., Shafer, J.A., Derenzini, E., Bollard, C.M., Medeiros, L.J., Illés, A., Ji, Y. & Younes, A. (2011) The histone deacetylase inhibitor entinostat (SNDX-275) induces apoptosis in Hodgkin lymphoma cells and synergizes with Bcl-2 family inhibitors. Experimental Hematology, 39, e1001.
25. LaBonte, M.J., Wilson, P.M., Fazzone, W., Groshen, S., Lenz, H.J. & Ladner, R.D. (2009) DNA microarray profiling of genes differentially regulated by the histone deacetylase inhibitors vorinostat and LBH589 in colon cancer cell lines. BMC Medical Genomics, 2, 67.
26. Lemonnier, F., Couronné, L., Parrens, M., Jaïs, J.P., Travert, M., Lamant, L., Tournillac, O., Rousset, T., Fabiani, B., Cairns, R.A., Mak, T., Bastard, C., Bernard, O.A., de Leval, L. & Gaulard, P. (2012) Recurrent TET2 mutations in peripheral T-cell lymphomas correlate with TFH-like features and adverse clinical parameters. Blood, 120, 1466-1469.
27. Lindemann, R.K., Newbold, A., Whitecross, K.F., Cluse, L.A., Frew, A.J., Ellis, L., Williams, S., Wiegmans, A.P., Dear, A.E., Scott, C.L., Pellegrini, M., Wei, A., Richon, V.M., Marks, P.A., Lowe, S.W., Smyth, M.J. & Johnstone, R.W. (2007) Analysis of the apoptotic and therapeutic activities of histone deacetylase inhibitors by using a mouse model of B cell lymphoma. Proceedings of the National Academy of Science of the United States of America, 104, 8071-8076.
28. Luchenko, V.L., Litman, T., Chakraborty, A.R., Heffner, A., Devor, C., Wilkerson, J., Stein, W., Robey, R.W., Bangiolo, L., Levens, D. & Bates, S.E. (2014) Global histone changes induced by romidepsin and vorinostat do not explain apoptosis-a study of cell context-specific effects. Molecular Oncology, 8, 1379-1392.
29. Ma, T., Galimberti, F., Erkmen, C.P., Memoli, V., Chinyengetere, F., Sempere, L., Beumer, J.H., Anyang, B.N., Nugent, W., Johnstone, D., Tsongalis, G.J., Kurie, J.M., Li, H., Direnzo, J., Guo, Y., Freemantle, S.J., Dragnev, K.H. & Dmitrovsky, E. (2013) Comparing histone deacetylase inhibitor responses in genetically engineered mouse lung cancer models and a window of opportunity trial in patients with lung cancer. Molecular Cancer Therapeutics, 12, 1545-1555.
30. Mak, V., Hamm, J., Chhanabhai, M., Shenkier, T., Klasa, R., Sehn, L.H., Villa, D., Gascoyne, R.D., Connors, J.M. & Savage, K.J. (2013) Survival of patients with peripheral T-cell lymphoma after first relapse or progression: spectrum of disease and rare long-term survivors. Journal of Clinical Oncology, 31, 1970-1976.
31. Marshall, J., Rizvi, N., Kauh, J., Dahut, W., Figuera, M., Kang, M., Figg, W., Wainer, I., Chaissang, C., Li, M. & Hawkins, M. (2002) A phase I trial of depsipeptide (FR901228) in patients with advanced cancer. Journal of Experimental Therapeutics and Oncology, 2, 325-332.
32. McKenzie, R.C., Jones, C.L., Tosi, I., Caesar, J.A., Whittaker, S.J. & Mitchell, T.J. (2012) Constitutive activation of STAT3 in Sézary syndrome is independent of SHP-1. Leukemia, 26, 323-331.
33. Newbold, A., Lindemann, R.K., Cluse, L.A., Whitecross, K.F., Dear, A.E. & Johnstone, R.W. (2008) Characterisation of the novel apoptotic and therapeutic activities of the histone deacetylase inhibitor romidepsin. Molecular Cancer Therapeutics, 7, 1066-1079.
34. Noonan, A.M., Eisch, R.A., Liewehr, D.J., Sissung, T.M., Venzon, D., Flagg, T.P., Haigney, M.C., Steinberg, S.M., Figg, W.D., Piekarz, R.L. & Bates, S.E. (2013) Electrocardiographic studies of romidepsin demonstrate its safety and identify a potential role for the KATP channel. Clinical Cancer Research, 19, 3095-3104.
35. O'Connor, O., Masszi, T., Savage, K., Pinter-Brown, L., Foss, F., Popplewell, L., Cashen, A., Doorduijn, J., Chawla, S., Knoblauch, P., Zinzani, P., Brown, P., Hess, G., Van Hoof, A., Horwitz, S. & Shustov, A. (2013) Belinostat, a novel pan-histone deacetylase inhibitor (HDACi), in relapsed or refractory peripheral T-cell lymphoma (R/R PTCL): results from the BELIEF trial. Journal of Clinical Oncology, 31(Suppl.), abstr 8507.
36. O'Connor, O.A., Bhagat, G., Ganapathi, K., Pedersen, M.B., D'Amore, F., Radeski, D. & Bates, S.E. (2014) Changing the paradigms of treatment in peripheral T-cell lymphoma: from biology to clinical practice. Clinical Cancer Research, 20, 5240-5254.
37. Oki, Y., Younes, A., Copeland, A., Hagemeister, F., Fayad, L.E., McLaughlin, P., Shah, J., Fowler, N., Romaguera, J., Kwak, L.W. & Pro, B. (2013) Phase I study of vorinostat in combination with standard CHOP in patients with newly diagnosed peripheral T-cell lymphoma. British Journal of Haematology, 162, 138-141.
38. Olsen, E., Kim, Y., Kuzel, T., Pacheco, T., Foss, F., Parker, S., Frankel, S., Chen, C., Ricker, J., Arduino, J. & 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.
39. Palomero, T., Couronné, L., Khiabanian, H., Kim, M.Y., Ambesi-Impiombato, A., Perez-Garcia, A., Carpenter, Z., Abate, F., Allegretta, M., Haydu, J.E., Jiang, X., Lossos, I.S., Nicolas, C., Balbin, M., Bastard, C., Bhagat, G., Piris, M.A., Campo, E., Bernard, O.A., Rabadan, R. & Ferrando, A.A. (2014) Recurrent mutations in epigenetic regulators, RHOA and FYN kinase in peripheral T cell lymphomas. Nature Genetics, 46, 166-170.
40. Paoluzzi, L. & O'Connor, O.A. (2010) Targeting survival pathways in lymphoma. Advances in Experimental Medicine and Biology, 687, 79-96.
41. Piccaluga, P.P., Fuligni, F., De Leo, A., Bertuzzi, C., Rossi, M., Bacci, F., Sabattini, E., Agostinelli, C., Gazzola, A., Laginestra, M.A., Mannu, C., Sapienza, M.R., Hartmann, S., Hansmann, M.L., Piva, R., Iqbal, J., Chan, J.C., Weisenburger, D., Vose, J.M., Bellei, M., Federico, M., Inghirami, G., Zinzani, P.L. & Pileri, S.A. (2013) Molecular profiling improves classification and prognostication of nodal peripheral T-cell lymphomas: results of a phase III diagnostic accuracy study. Journal of Clinical Oncology, 31, 3019-3025.
42. Piekarz, R.L., Robey, R., Sandor, V., Bakke, S., Wilson, W.H., Dahmoush, L., Kingma, D.M., Turner, M.L., Altemus, R. & Bates, S.E. (2001) Inhibitor of histone deacetylation, depsipeptide (FR901228), in the treatment of peripheral and cutaneous T-cell lymphoma: a case report. Blood, 98, 2865-2868.
43. Piekarz, R.L., Robey, R.W., Zhan, Z., Kayastha, G., Sayah, A., Abdeldaim, A.H., Torrico, S. & Bates, S.E. (2004) T-cell lymphoma as a model for the use of histone deacetylase inhibitors in cancer therapy: impact of depsipeptide on molecular markers, therapeutic targets, and mechanisms of resistance. Blood, 103, 4636-4643.
44. Piekarz, R.L., Frye, A.R., Wright, J.J., Steinberg, S.M., Liewehr, D.J., Rosing, D.R., Sachdev, V., Fojo, T. & Bates, S.E. (2006) Cardiac studies in patients treated with depsipeptide, FK228, in a phase II trial for T-cell lymphoma. Clinical Cancer Research, 12, 3762-3773.
45. Piekarz, R., Frye, R., Turner, M., Wright, J., Allen, S., Kirschbaum, M., Zain, J., Prince, H., Leonard, J., Geskin, L., Reeder, C., Joske, D., Figg, W., Gardner, E., Steinberg, S., Jaffe, E., Stetler-Stevenson, M., Lade, S., Fojo, A. & Bates, S. (2009) Phase II multi-institutional trial of the histone deacetylase inhibitor romidepsin as monotherapy for patients with cutaneous T-cell lymphoma. Journal of Clinical Oncology, 27, 5410-5417.
46. Piekarz, R.L., Frye, R., Prince, H.M., Kirschbaum, M.H., Zain, J., Allen, S.L., Jaffe, E.S., Ling, A., Turner, M., Peer, C.J., Figg, W.D., Steinberg, S.M., Smith, S., Joske, D., Lewis, I., Hutchins, L., Craig, M., Fojo, A.T., Wright, J.J. & Bates, S.E. (2011) Phase 2 trial of romidepsin in patients with peripheral T-cell lymphoma. Blood, 117, 5827-5834.
47. Ritchie, D., Piekarz, R., Blombery, P., Karai, L., Pittaluga, S., Jaffe, E., Raffeld, M., Janik, J., Prince, H. & Bates, S. (2009) Reactivation of DNA viruses in association with histone deacetylase inhibitor therapy: a case series report. Haematologica, 94, 1618-1622.
48. Robbins, A.R., Jablonski, S.A., Yen, T.J., Yoda, K., Robey, R., Bates, S.E. & Sackett, D.L. (2005) Inhibitors of histone deacetylases alter kinetochore assembly by disrupting pericentromeric heterochromatin. Cell Cycle, 4, 717-726.
49. Robert, C. & Rassool, F.V. (2012) HDAC inhibitors: roles of DNA damage and repair. Advances in Cancer Research, 116, 87-129.
50. Sandor, V., Robbins, A.R., Robey, R., Myers, T., Sausville, E., Bates, S.E. & Sackett, D.L. (2000) FR901228 causes mitotic arrest but does not alter microtubule polymerization. Anti-Cancer Drugs, 11, 445-454.
51. Sandor, V., Bakke, S., Robey, R.W., Kang, M.H., Blagosklonny, M.V., Bender, J., Brooks, R., Piekarz, R.L., Tucker, E., Figg, W.D., Chan, K.K., Goldspiel, B., Fojo, A.T., Balcerzak, S.P. & Bates, S.E. (2002) Phase I trial of the histone deacetylase inhibitor, depsipeptide (FR901228, NSC 630176), in patients with refractory neoplasms. Clinical Cancer Research, 8, 718-728.
52. Sarkar, S., Abujamra, A.L., Loew, J.E., Forman, L.W., Perrine, S.P. & Faller, D.V. (2011) Histone deacetylase inhibitors reverse CpG methylation by regulating DNMT1 through ERK signaling. Anticancer Research, 31, 2723-2732.
53. Schrump, D.S., Fischette, M.R., Nguyen, D.M., Zhao, M., Li, X., Kunst, T.F., Hancox, A., Hong, J.A., Chen, G.A., Kruchin, E., Wright, J.J., Rosing, D.R., Sparreboom, A., Figg, W.D. & Steinberg, S.M. (2008) Clinical and molecular responses in lung cancer patients receiving Romidepsin. Clinical Cancer Research, 14, 188-198.
54. Shao, W., Growney, J.D., Feng, Y., O'Connor, G., Pu, M., Zhu, W., Yao, Y.M., Kwon, P., Fawell, S. & Atadja, P. (2010) Activity of deacetylase inhibitor panobinostat (LBH589) in cutaneous T-cell lymphoma models: defining molecular mechanisms of resistance. International Journal of Cancer, 127, 2199-2208.
55. Shin, J., Monti, S., Aires, D.J., Duvic, M., Golub, T., Jones, D.A. & Kupper, T.S. (2007) Lesional gene expression profiling in cutaneous T-cell lymphoma reveals natural clusters associated with disease outcome. Blood, 110, 3015-3027.
56. Shiraga, T., Tozuka, Z., Ishimura, R., Kawamura, A. & Kagayama, A. (2005) Identification of cytochrome P450 enzymes involved in the metabolism of FK228, a potent histone deacetylase inhibitor, in human liver microsomes. Biological and Pharmaceutical Bulletin, 28, 124-129.
57. Staffolani, E., Nicolais, R., Manca di Villahermosa, S., Galli, D., Postorino, M. & Di Daniele, N. (2012) Cytokine removal under hemodiafiltration with endogenous reinfusion in acute kidney injury secondary to angioimmunoblastic T-cell lymphoma: a case report. Blood Purification, 34, 349-353.
58. Steinhoff, M., Beyer, M., Roewert-Huber, J., Lukowsky, A., Assaf, C. & Sterry, W. (2008) Complete clinical remission of tumor-stage mycosis fungoides after acute extensive skin necroses, granulomatous reaction, and fever under treatment with bexarotene, vorinostat, and high-dose fenofibrate. Journal of the American Academy of Dermatology, 58, S88-S91.
59. Takada, Y., Gillenwater, A., Ichikawa, H. & Aggarwal, B.B. (2006) Suberoylanilide hydroxamic acid potentiates apoptosis, inhibits invasion, and abolishes osteoclastogenesis by suppressing nuclear factor-kappaB activation. Journal of Biological Chemistry, 281, 5612-5622.
60. Teachey, D.T., Rheingold, S.R., Maude, S.L., Zugmaier, G., Barrett, D.M., Seif, A.E., Nichols, K.E., Suppa, E.K., Kalos, M., Berg, R.A., Fitzgerald, J.C., Aplenc, R., Gore, L. & Grupp, S.A. (2013) Cytokine release syndrome after blinatumomab treatment related to abnormal macrophage activation and ameliorated with cytokine-directed therapy. Blood, 121, 5154-5157.
61. Therasse, P., Arbuck, S.G., Eisenhauer, E.A., Wanders, J., Kaplan, R.S., Rubinstein, L., Verweij, J., Van Glabbeke, M., van Oosterom, A.T., Christian, M.C. & Gwyther, S.G. (2000) New guidelines to evaluate the response to treatment in solid tumors. European Organization for Research and Treatment of Cancer, National Cancer Institute of the United States, National Cancer Institute of Canada. Journal of the National Cancer Institute, 92, 205-216.
62. Tiffon, C., Adams, J., van der Fits, L., Wen, S., Townsend, P., Ganesan, A., Hodges, E., Vermeer, M. & Packham, G. (2011) The histone deacetylase inhibitors vorinostat and romidepsin downmodulate IL-10 expression in cutaneous T-cell lymphoma cells. British Journal of Pharmacology, 162, 1590-1602.
63. Van Waes, C. (2007) Nuclear factor-kappaB in development, prevention, and therapy of cancer. Clinical Cancer Research, 13, 1076-1082.
64. Whittaker, S.J., Demierre, M.F., Kim, E.J., Rook, A.H., Lerner, A., Duvic, M., Scarisbrick, J., Reddy, S., Robak, T., Becker, J.C., Samtsov, A., McCulloch, W. & Kim, Y.H. (2010) Final results from a multicenter, international, pivotal study of romidepsin in refractory cutaneous T-cell lymphoma. Journal of Clinical Oncology, 28, 4485-4491.
65. Wiegmans, A.P., Alsop, A.E., Bots, M., Cluse, L.A., Williams, S.P., Banks, K.M., Ralli, R., Scott, C.L., Frenzel, A., Villunger, A. & Johnstone, R.W. (2011) Deciphering the molecular events necessary for synergistic tumor cell apoptosis mediated by the histone deacetylase inhibitor vorinostat and the BH3 mimetic ABT-737. Cancer Research, 71, 3603-3615.
66. Wozniak, M.B., Villuendas, R., Bischoff, J.R., Aparicio, C.B., Martínez Leal, J.F., de La Cueva, P., Rodriguez, M.E., Herreros, B., Martin-Perez, D., Longo, M.I., Herrera, M., Piris, M.A. & Ortiz-Romero, P.L. (2010) Vorinostat interferes with the signaling transduction pathway of T-cell receptor and synergizes with phosphoinositide-3 kinase inhibitors in cutaneous T-cell lymphoma. Haematologica, 95, 613-621.
67. Zhang, C., Richon, V., Ni, X., Talpur, R. & Duvic, M. (2005) Selective induction of apoptosis by histone deacetylase inhibitor SAHA in cutaneous T-cell lymphoma cells: relevance to mechanism of therapeutic action. Journal of Investigative Dermatology, 125, 1045-1052.