Drug Insight: Histone deacetylase inhibitor-based therapies for cutaneous T-cell lymphomas

Nature Clinical Practice Oncology

Volumn 5, Issue 12, 2008, Pages 714-726

  Khan, Omar ^a   La Thangue, Nicholas B ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

3 PHENYLSULFAMOYLCINNAMOHYDROXAMIC ACID; 4 [N (2 HYDROXYETHYL) N [2 (3 INDOLYL)ETHYL]AMINOMETHYL]CINNAMOHYDROXAMIC ACID; ALPHA INTERFERON; ANTINEOPLASTIC AGENT; AZACITIDINE; BEXAROTENE; BORTEZOMIB; CAMPTOTHECIN; CARBOPLATIN; CORTICOSTEROID; DENILEUKIN DIFTITOX; DEXAMETHASONE; FLUOROURACIL; GEMCITABINE; HEAT SHOCK PROTEIN 90 INHIBITOR; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; ISOTRETINOIN; N (2 AMINOPHENYL) 4 (3 PYRIDINYLMETHOXYCARBONYLAMINOMETHYL)BENZAMIDE; N (2 AMINOPHENYL) 4 [4 (3 PYRIDINYL) 2 PYRIMIDINYLAMINOMETHYL]BENZAMIDE; PACLITAXEL; PANOBINOSTAT; PROTEASOME INHIBITOR; RETINOIC ACID; ROMIDEPSIN; TRICHOSTATIN A; VALPROIC ACID; VORINOSTAT;

ANOREXIA; ANTINEOPLASTIC ACTIVITY; CANCER RELAPSE; CARCINOGENESIS; CD4+ T LYMPHOCYTE; CHEMOTHERAPY INDUCED EMESIS; CLINICAL TRIAL; COMBINATION CHEMOTHERAPY; CUTANEOUS T CELL LYMPHOMA; DEHYDRATION; DIARRHEA; DOSE RESPONSE; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENTIATION; DRUG STRUCTURE; DRUG TOLERABILITY; ECG ABNORMALITY; ENZYME INHIBITION; FATIGUE; FEVER; GASTROINTESTINAL SYMPTOM; GLIOBLASTOMA; GRANULOCYTOPENIA; HUMAN; LUNG NON SMALL CELL CANCER; MESOTHELIOMA; MONOTHERAPY; MULTIPLE CYCLE TREATMENT; NAUSEA; PRIORITY JOURNAL; PROSTATE CANCER; REVIEW; SEZARY SYNDROME; THROMBOCYTOPENIA; TUMOR SUPPRESSOR GENE;

ANTINEOPLASTIC AGENTS; HISTONE DEACETYLASES; HUMANS; HYDROXAMIC ACIDS; LYMPHOMA, T-CELL, CUTANEOUS;

EID: 57049120498     PISSN: 17434254     EISSN: 17434262     Source Type: Journal    
DOI: 10.1038/ncponc1238     Document Type: Review

References (99)

1. Ting AH et al. (2006) The cancer epigenome-components and functional correlates. Genes Dev 20: 3215-3231
2. Inche AG and La Thangue NB (2006) Chromatin control and cancer-drug discovery: Realizing the promise. Drug Discov Today 11: 97-109
3. Carey N and La Thangue NB (2006) Histone deacetylase inhibitors: gathering pace. Curr Opin Pharmacol 6: 369-375
4. Marks P et al. (2001) Histone deacetylases and cancer: Causes and therapies. Nat Rev Cancer 1: 194-202
5. Marks PA et al. (2004) Histone deacetylase inhibitors. Adv Cancer Res 91: 137-168
6. Marks PA and Breslow R (2007) Dimethyl sulfoxide to vorinostat: development of this histone deacetylase inhibitor as an anticancer drug. Nat Biotechnol 25: 84-90
7. Duvic M and Zhang C (2006) Clinical and laboratory experience of vorinostat (suberoylanilide hydroxamic acid) in the treatment of cutaneous T-cell lymphoma. Br J Cancer 95: S13-S19
8. Luger K et al. (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389: 251-260
9. Jenuwein T and Allis CD (2001) Translating the histone code. Science 293: 1074-1080
10. Spotswood HT and Turner BM (2002) An increasingly complex code. J Clin Invest 110: 577-582
11. Chan HM et al. (2001) Acetylation control of the retinoblastoma tumour-suppressor protein. Nat Cell Biol 3: 667-674
12. Bolden JE et al. (2006) Anticancer activities of histone deacetylase inhibitors. Nat Rev Drug Discov 5: 769-784
13. de Ruijter AJ et al. (2003) Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem J 370 737-749
14. Yoshida M et al. (1990) Potent and specific inhibition of mammalian histone deacetylase both in vivo and in vitro by trichostatin A. J Biol Chem 265: 17174-17179
15. Finnin MS et al. (1999) Structures of a histone deacetylase homologue bound to the TSA and SAHA inhibitors. Nature 401: 188-193
16. Glaser KB et al. (2003) Gene expression profiling of multiple histone deacetylase (HDAC) inhibitors: Defining a common gene set produced by HDAC inhibition in T24 and MDA carcinoma cell lines. Mol Cancer Ther 2: 151-163
17. Johnstone RW and Licht JD (2003) Histone deacetylase inhibitors in cancer therapy: Is transcription the primary target? Cancer Cell 4: 13-18
18. Mitsiades CS et al. (2004) Transcriptional signature of histone deacetylase inhibition in multiple myeloma: Biological and clinical implications. Proc Natl Acad Sci USA 101: 540-545
19. Dokmanovic M et al. (2007) Histone deacetylase inhibitors: overview and perspectives. Mol Cancer Res 5: 981-989
20. Kovacs JJ et al. (2005) HDAC6 regulates Hsp90 acetylation and chaperone-dependent activation of glucocorticoid receptor. Mol Cell 18: 601-607
21. Gu W and Roeder RG (1997) Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell 90 595-606
22. Martinez-Balbas MA et al. (2000) Regulation of E2F1 activity by acetylation. EMBO J 19: 662-671
23. Patel JH et al. (2004) The c-MYC oncoprotein is a substrate of the acetyltransferases hGCN5/PCAF and TIP60. Mol Cell Biol 24: 10826-10834
24. Billin AN et al. (2000) Beta-catenin-histone deacetylase interactions regulate the transition of LEF1 from a transcriptional repressor to an activator. Mol Cell Biol 20: 6882-6890
25. Park JH et al. (2004) Class I histone deacetylase-selective novel synthetic inhibitors potently inhibit human tumor proliferation. Clin Cancer Res 10: 5271-5281
26. Huang BH et al. (2005) Inhibition of histone deacetylase 2 increases apoptosis and p21Cip1/WAF1 expression, independent of histone deacetylase 1. Cell Death Differ 12: 395-404
27. Zhang Y et al. (2003) HDAC-6 interacts with and deacetylates tubulin and microtubules in vivo. EMBO J 22: 1168-1179
28. Kawaguchi Y et al. (2003) The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell 115: 727-738
29. Boyault C et al. (2006) HDAC6-p97/VCP controlled polyubiquitin chain turnover. EMBO J 25: 3357-3366
30. Zhang CL et al. (2002) Class II histone deacetylases act as signal-responsive repressors of cardiac hypertrophy. Cell 110 479-488
31. Vega K et al. (2004) Histone deacetylase 4 controls chondrocyte hypertrophy during skeletogenesis. Cell 119: 555-566
32. Arnold MA et al. (2007) MEF2C transcription factor controls chondrocyte hypertrophy and bone development. Dev Cell 12: 377-389
33. Dequiedt F et al. (2003) HDAC7, a thymus-specific class II histone deacetylase, regulates Nur77 transcription and TCR-mediated apoptosis. Immunity 18: 687-698
34. Zhu E et al. (2004) Induction of HDAC2 expression upon loss of APC in colorectal tumorigenesis. Cancer Cell 5: 455-463
35. Ropero S et al. (2006) A truncating mutation of HDAC2 in human cancers confers resistance to histone deacetylase inhibition. Nat Genet 38: 566-569
36. Minucci S and Pelicci PG (2006) Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat Rev Cancer 6: 38-51
37. Wu WS et al. (2001) The growth suppressor PML represses transcription by functionally and physically interacting with histone deacetylases. Mol Cell Biol 21: 2259-2268
38. Reddy P et al. (2004) Histone deacetylase inhibitor suberoylanilide hydroxamic acid reduces acute graft-versus-host disease and preserves graft-versus-leukaemia effect. Proc Natl Acad Sci USA 101: 3921-3926
39. Brogdon JL et al. (2006) Histone deacetylase activities are required for innate immune cell control of Th1 but Th2 effector cell function. Blood 109: 1123-1130
40. Tao R et al. (2007) Deacetylase inhibition promotes the generation and function of regulatory T cells. Nat Med 13: 1299-1307
41. Shao Y et al. (2004) Apoptotic and autophagic cell death induced by histone deacetylase inhibitors. Proc Natl Acad Sci USA 101 18030-18035
42. Yang X et al. (2001) Synergistic activation of functional estrogen receptor (ER)-alpha by DNA methyltransferase and histone deacetylase inhibition in human ER-alpha-negative breast cancer cells. Cancer Res 61: 7025-7029
43. Ferrara FF et al. (2001) Histone deacetylase-targeted treatment restores retinoic acid signaling and differentiation in acute myeloid leukemia. Cancer Res 61: 2-7
44. Rahmani M et al. (2003) Coadministration of the heat shock protein 90 antagonist 17-allylamino-17-demethoxygeldanamycin with suberoylanilide hydroxamic acid or sodium butyrate synergistically induces apoptosis in human leukemia cells. Cancer Res 63: 8420-8427
45. Hideshima T et al. (2005) Small-molecule inhibition of proteasome and aggresome function induces synergistic antitumor activity in multiple myeloma. Proc Natl Acad Sci USA 102: 8567-8572
46. Tumber A et al. (2007) The histone deacetylase inhibitor PXD101 synergises with 5-fluorouracil to inhibit colon cancer cell growth in vitro and in vivo. Cancer Chemother Pharmacol 60: 275-283
47. Marchion DC et al. (2004) Sequence-specific potentiation of topoisomerase II inhibitors by the histone deacetylase inhibitor suberoylanilide hydroxamic acid. J Cell Biochem 92: 223-237
48. Grant S et al. (2007) Vorinostat. Nat Rev Drug Discov 6 21-22
49. Glaser KB (2007) HDAC inhibitors: Clinical update and mechanism-based potential. Biochem Pharmacol 74: 659-671
50. Keehn CA et al. (2007) The diagnosis, staging, and treatment options for mycosis fungoides. Cancer Control 14: 102-111
51. Chuang TY et al. (1990) Incidence of cutaneous T cell lymphoma and other rare skin cancers in a defined population. J Am Acad Dermatol 23: 254-256
52. Willemze R et al. (2005) WHO-EORTC classification for cutaneous lymphomas. Blood 105: 3768-3785
53. Lessin SR et al. (1994) Retroviruses and cutaneous T-cell lymphoma. Dermatol Clin 12: 243-253
54. Kim EJ et al. (2006) Mycosis fungoides and Sézary syndrome: An update. Curr Oncol Rep 8: 376-386
55. van Doorn R et al. (2002) A novel splice variant of the Fas gene in patients with cutaneous T-cell lymphoma. Cancer Res 62: 5389-5392
56. Sommer VH et al. (2004) In vivo activation of STAT3 in cutaneous T-cell lymphoma: Evidence for an antiapoptotic function of STAT3. Leukemia 18: 1288-1295
57. Lauritzen AF et al. (1995) p53 protein expression in cutaneous T-cell lymphomas. Br J Dermatol 133: 32-36
58. Navas IC et al. (2000) p16(INK4a) gene alterations are frequent in lesions of mycosis fungoides. Am J Pathol 156: 1565-1572
59. Scarisbrick JJ et al. (2002) Frequent abnormalities of the p15 and p16 genes in mycosis fungoides and Sézary syndrome. J Invest Dermatol 118: 493-499
60. Scarisbrick JJ et al. (2003) Microsatellite instability is associated with hypermethylation of the hMLH1 gene and reduced gene expression in mycosis fungoides. J Invest Dermatol 121: 894-901
61. Zhang C et al. (2007) Consequences of p16 tumor suppressor gene inactivation in mycosis fungoides and Sézary syndrome and role of the bmi-1 and ras oncogenes in disease progression. Hum Pathol 38 995-1002
62. Sherr CJ and Roberts JM (1999) CDK inhibitors: Positive and negative regulators of G1-phase progression. Genes Dev 13: 1501-1512
63. van Doorn R et al. (2005) Epigenetic profiling of cutaneous T-cell lymphoma: Promoter hypermethylation of multiple tumor suppressor genes including BCL7a, PTPRG, and p73. J Clin Oncol 23: 3886-3896
64. Alizadeh AA et al. (2000) Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 403 503-511
65. Martinez-Delgado B et al. (2002) Frequent inactivation of the p73 gene by abnormal methylation or LOH in non-Hodgkin's lymphomas. Int J Cancer 102: 15-19
66. Siu LL et al. (2003) Aberrant promoter CpG methylation as a molecular marker for disease monitoring in natural killer cell lymphomas. Br J Haematol 122: 70-77
67. Querfeld C et al. (2003) Primary cutaneous lymphomas: A review with current treatment options. Blood Rev 17: 131-142
68. Bunn PA Jr and Lamberg SI (1979) Report of the Committee on Staging and Classification of Cutaneous T-Cell Lymphomas. Cancer Treat Rep 63: 725-728
69. Sausville EA et al. (1988) Histopathologic staging at initial diagnosis of mycosis fungoides and the Sézary syndrome: Definition of three distinctive prognostic groups. Ann Intern Med 109: 372-382
70. Trautinger F et al. (2006) EORTC consensus recommendations for the treatment of mycosis fungoides/Sézary syndrome. Eur J Cancer 42: 1014-1030
71. Budgin JB et al. (2005) Biological effects of bexarotene in cutaneous T-cell lymphoma. Arch Dermatol 141: 315-321
72. Zhang C et al. (2002) Induction of apoptosis by bexarotene in cutaneous T-cell lymphoma cells: Relevance to mechanism of therapeutic action. Clin Cancer Res 8: 1234-1240
73. Duvic M et al. (2001) Bexarotene is effective and safe for treatment of refractory advanced-stage cutaneous T-cell lymphoma: multinational phase II-III trial results. J Clin Oncol 19: 2456-2471
74. vanderSpek JC et al. (1993) Structure/function analysis of the transmembrane domain of DAB389-interleukin-2, an interleukin-2 receptor-targeted fusion toxin: The amphipathic helical region of the transmembrane domain is essential for the efficient delivery of the catalytic domain to the cytosol of target cells. J Biol Chem 268: 12077-12082
75. Foss FM et al. (2001) Biological correlates of acute hypersensitivity events with DAB(389)IL-2 (denileukin diftitox, ONTAK) in cutaneous T-cell lymphoma: Decreased frequency and severity with steroid premedication. Clin Lymphoma 1: 298-302
76. Olsen E et al. (2001) Pivotal phase III trial of two dose levels of denileukin diftitox for the treatment of cutaneous T-cell lymphoma. J Clin Oncol 19: 376-388
77. Kim EJ et al. (2005) Immunopathogenesis and therapy of cutaneous T cell lymphoma. J Clin Invest 115: 798-812
78. Mann BS et al. (2007) Vorinostat for treatment of cutaneous manifestations of advanced primary cutaneous T-cell lymphoma. Clin Cancer Res 13: 2318-2322
79. Piekarz RL et al. (2001) Inhibitor of histone deacetylation, depsipeptide (FR901228), in the treatment of peripheral and cutaneous T-cell lymphoma: A case report. Blood 98: 2865-2868
80. Kelly WK et al. (2005) Phase I study of an oral histone deacetylase inhibitor, suberoylanilide hydroxamic acid, in patients with advanced cancer. J Clin Oncol 23: 3923-3931
81. O'Connor OA et al. (2006) Clinical experience with intravenous and oral formulations of the novel histone deacetylase inhibitor suberoylanilide hydroxamic acid in patients with advanced hematologic malignancies. J Clin Oncol 24: 166-173
82. Duvic M et al. (2007) Phase 2 trial of oral vorinostat (suberoylanilide hydroxamic acid, SAHA) for refractory cutaneous T-cell lymphoma (CTCL). Blood 109: 31-39
83. Olsen EA et al. (2007) Phase IIb multicenter trial of vorinostat in patients with persistent, progressive, or treatment refractory cutaneous T-cell lymphoma. J Clin Oncol 25: 3109-3115
84. Traynor AM et al. (2007) A phase II study of vorinostat (NSC 701852) in patients (pts) with relapsed non-small cell lung cancer (NSCLC). J Clin Oncol 25 (suppl): 18044
85. Galanis E et al. (2007) N047B: NCCTG phase II trial of vorinostat (suberoylanilide hydroxamic acid) in recurrent glioblastoma multiforme (GBM). J Clin Oncol 25 (suppl): 2004
86. Hussain M et al. (2007) Suberoylanilide hydroxamic acid (vorinostat) post chemotherapy in hormone refractory prostate cancer (HRPC) patients (pts): A phase II trial by the Prostate Cancer Clinical Trials Consortium (NCI 6862). J Clin Oncol 25 (suppl): 5132
87. Krug LM et al. (2006) Potential role of histone deacetylase inhibitors in mesothelioma: Clinical experience with suberoylanilide hydroxamic acid. Clin Lung Cancer 7: 257-261
88. Piekarz R et al. (2007) Update of the NCI multiinstitutional phase II trial of romidepsin, FK228, for patients with cutaneous or peripheral T-cell lymphoma. J Clin Oncol 25 (suppl): 8027
89. Lerner A et al. (2006) Romidepsin (depsipeptide, FK228) induces clinically significant responses in treatment-refractory CTCL: Interim report of a phase II multicenter study [abstract #2468]. Blood 108: 699a
90. Parker C et al. (2007) Romidepsin (FK228), a histone deacetylase inhibitor: Final results of a phase II study in metastatic hormone refractory prostate cancer (HRPC). J Clin Oncol 25 (suppl): 15507
91. Molife R et al. (2006) Phase II study of FK228 in patients with metastatic hormone refractory prostate cancer (HRPC). J Clin Oncol 24 (suppl): 14554
92. Sullivan D et al. (2006) A phase II study of PXD101 in advanced multiple myeloma [poster 3583]. Presented at the American Society of Hematology Annual Meeting: 2006 December 10-13, Orlando, FL
93. Prince M et al. (2006) LBH589, a novel deacetylase inhibitor (DACi), treatment of patients with cutaneous T cell lymphoma (CTCL): skin expression profiles in the first 24 h related to clinical response following therapy [abstract #2715]. Blood 108 (AsH Meeting Abstracts)
94. Younes A et al. (2007) A phase II study of a novel oral isotype-selective histone deacetylase (HDAC) inhibitor in patients with relapsed or refractory Hodgkin lymphoma. J Clin Oncol 25 (suppl): 8000
95. Methylgene (online 21 August 2007) Methylgene and Pharmion announce US orphan drug designation granted for mgcd0103 for the treatment of Hodgkin's lymphoma [http://www.methylgene.com/content.asp?node=267] (accessed 13 February 2008)
96. Zhang C et al. (2005) Selective induction of apoptosis by histone deacetylase inhibitor SAHA in cutaneous T-cell lymphoma cells: Relevance to mechanism of therapeutic action. J Invest Dermatol 125: 1045-1052
97. Lee JH et al. (2006) Histone deacetylase inhibitor enhances 5-fluorouracil cytotoxicity by down-regulating thymidylate synthase in human cancer cells. Mol Cancer Ther 5: 3085-3095
98. Zhou DC et al. (2002) Frequent mutations in the ligand-binding domain of PML-RAR alpha after multiple relapses of acute promyelocytic leukemia: Analysis for functional relationship to response to all-trans retinoic acid and histone deacetylase inhibitors in vitro and in vivo. Blood 99: 1356-1363
99. Chung EJ et al. (2006) Assays for pharmacodynamic analysis of histone deacetylase inhibitors. Expert Opin Drug Metab Toxicol 2: 213-230