© 2000 by Oxford University Press
Journal of the National Cancer Institute, Vol. 92, No. 15, 1210-1216,
August 2, 2000
© 2000 Oxford University Press
REVIEW |
Histone Deacetylase Inhibitors: Inducers of Differentiation or Apoptosis of Transformed Cells
Affiliations of authors: Cell Biology Program, Memorial Sloan-Kettering Cancer Center, New York, NY, and Sloan-Kettering Institute Graduate School of Medical Sciences of Joan and Sanford I. Weill Graduate School of Medical Sciences of Cornell University, New York, NY.
Correspondence to: Paul A. Marks, M.D., Memorial Sloan-Kettering Cancer Center, 1275 York Ave., New York, NY 10021 (e-mail: paula_marks{at}mskcc.org).
Histone deacetylase (HDAC) inhibitors have been shown to be potent inducers of growth arrest, differentiation, and/or apoptotic cell death of transformed cells in vitro and in vivo. One class of HDAC inhibitors, hydroxamic acid-based hybrid polar compounds (HPCs), induce differentiation at micromolar or lower concentrations. Studies (x-ray crystallographic) showed that the catalytic site of HDAC has a tubular structure with a zinc atom at its base and that these HDAC inhibitors, such as suberoylanilide hydroxamic acid and trichostatin A, fit into this structure with the hydroxamic moiety of the inhibitor binding to the zinc. HDAC inhibitors cause acetylated histones to accumulate in both tumor and normal tissues, and this accumulation can be used as a marker of the biologic activity of the HDAC inhibitors. Hydroxamic acid-based HPCs act selectively to inhibit tumor cell growth at levels that have little or no toxicity for normal cells. These compounds also act selectively on gene expression, altering the expression of only about 2% of the genes expressed in cultured tumor cells. In general, chromatin fractions enriched in actively transcribed genes are also enriched in highly acetylated core histones, whereas silent genes are associated with nucleosomes with a low level of acetylation. However, HDACs can also acetylate proteins other than histones in nucleosomes. The role that these other targets play in the induction of cell growth arrest, differentiation, and/or apoptotic cell death has not been determined. Our working hypothesis is that inhibition of HDAC activity leads to the modulation of expression of a specific set of genes that, in turn, result in growth arrest, differentiation, and/or apoptotic cell death. The hydroxamic acid-based HPCs are potentially effective agents for cancer therapy and, possibly, cancer chemoprevention.
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D. Z. Qian, Y. Kato, S. Shabbeer, Y. Wei, H. M.W. Verheul, B. Salumbides, T. Sanni, P. Atadja, and R. Pili Targeting Tumor Angiogenesis with Histone Deacetylase Inhibitors: the Hydroxamic Acid Derivative LBH589 Clin. Cancer Res., January 15, 2006; 12(2): 634 - 642. [Abstract] [Full Text] [PDF]
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 H. J. Kee, I. S. Sohn, K. I. Nam, J. E. Park, Y. R. Qian, Z. Yin, Y. Ahn, M. H. Jeong, Y.-J. Bang, N. Kim, et al. Inhibition of Histone Deacetylation Blocks Cardiac Hypertrophy Induced by Angiotensin II Infusion and Aortic Banding Circulation, January 3, 2006; 113(1): 51 - 59. [Abstract] [Full Text] [PDF]
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J. K. Earel Jr., R. L. VanOosten, and T. S. Griffith Histone Deacetylase Inhibitors Modulate the Sensitivity of Tumor Necrosis Factor-Related Apoptosis-Inducing Ligand-Resistant Bladder Tumor Cells Cancer Res., January 1, 2006; 66(1): 499 - 507. [Abstract] [Full Text] [PDF]
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O. A. O'Connor, M. L. Heaney, L. Schwartz, S. Richardson, R. Willim, B. MacGregor-Cortelli, T. Curly, C. Moskowitz, C. Portlock, S. Horwitz, et al. 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., January 1, 2006; 24(1): 166 - 173. [Abstract] [Full Text] [PDF]
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 J.-H. Choi, K.-H. Nam, J. Kim, M. W. Baek, J.-E. Park, H.-Y. Park, H. J. Kwon, O.-S. Kwon, D.-Y. Kim, and G. T. Oh Trichostatin A Exacerbates Atherosclerosis in Low Density Lipoprotein Receptor-Deficient Mice Arterioscler Thromb Vasc Biol, November 1, 2005; 25(11): 2404 - 2409. [Abstract] [Full Text] [PDF]
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M. R. Acharya, A. Sparreboom, J. Venitz, and W. D. Figg Rational Development of Histone Deacetylase Inhibitors as Anticancer Agents: A Review Mol. Pharmacol., October 1, 2005; 68(4): 917 - 932. [Abstract] [Full Text] [PDF]
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O. A. O'Connor Targeting Histones and Proteasomes: New Strategies for the Treatment of Lymphoma J. Clin. Oncol., September 10, 2005; 23(26): 6429 - 6436. [Abstract] [Full Text] [PDF]
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P. Bali, M. Pranpat, R. Swaby, W. Fiskus, H. Yamaguchi, M. Balasis, K. Rocha, H.-G. Wang, V. Richon, and K. Bhalla Activity of Suberoylanilide Hydroxamic Acid Against Human Breast Cancer Cells with Amplification of Her-2 Clin. Cancer Res., September 1, 2005; 11(17): 6382 - 6389. [Abstract] [Full Text] [PDF]
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M. V. Blagosklonny, S. Trostel, G. Kayastha, Z. N. Demidenko, L. T. Vassilev, L. Y. Romanova, S. Bates, and T. Fojo Depletion of Mutant p53 and Cytotoxicity of Histone Deacetylase Inhibitors Cancer Res., August 15, 2005; 65(16): 7386 - 7392. [Abstract] [Full Text] [PDF]
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R. L. Bevins and S. G. Zimmer It's About Time: Scheduling Alters Effect of Histone Deacetylase Inhibitors on Camptothecin-Treated Cells Cancer Res., August 1, 2005; 65(15): 6957 - 6966. [Abstract] [Full Text] [PDF]
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J. J. Xiao, Y. Huang, Z. Dai, W. Sadee, J. Chen, S. Liu, G. Marcucci, J. Byrd, J. M. Covey, J. Wright, et al. Chemoresistance to Depsipeptide FK228 [(E)-(1S,4S,10S,21R)-7-[(Z)-Ethylidene]-4,21-diisopropyl-2-oxa-12,13-dithia-5,8,20,23-tetraazabicyclo[8,7,6]-tricos-16-ene-3,6,9,22-pentanone] Is Mediated by Reversible MDR1 Induction in Human Cancer Cell Lines J. Pharmacol. Exp. Ther., July 1, 2005; 314(1): 467 - 475. [Abstract] [Full Text] [PDF]
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Q. C. Ryan, D. Headlee, M. Acharya, A. Sparreboom, J. B. Trepel, J. Ye, W. D. Figg, K. Hwang, E. J. Chung, A. Murgo, et al. Phase I and Pharmacokinetic Study of MS-275, a Histone Deacetylase Inhibitor, in Patients With Advanced and Refractory Solid Tumors or Lymphoma J. Clin. Oncol., June 10, 2005; 23(17): 3912 - 3922. [Abstract] [Full Text] [PDF]
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K. N. Bhalla Epigenetic and Chromatin Modifiers As Targeted Therapy of Hematologic Malignancies J. Clin. Oncol., June 10, 2005; 23(17): 3971 - 3993. [Abstract] [Full Text] [PDF]
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B. L. Pool-Zobel, V. Selvaraju, J. Sauer, T. Kautenburger, J. Kiefer, K. K. Richter, M. Soom, and S. Wolfl Butyrate may enhance toxicological defence in primary, adenoma and tumor human colon cells by favourably modulating expression of glutathione S-transferases genes, an approach in nutrigenomics Carcinogenesis, June 1, 2005; 26(6): 1064 - 1076. [Abstract] [Full Text] [PDF]
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T. Tran, A. Shatnawi, X. Zheng, K. M.M. Kelley, and M. Ratnam Enhancement of Folate Receptor {alpha} Expression in Tumor Cells Through the Glucocorticoid Receptor: A Promising Means to Improved Tumor Detection and Targeting Cancer Res., May 15, 2005; 65(10): 4431 - 4441. [Abstract] [Full Text] [PDF]
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C. S. Mitsiades, V. Poulaki, C. McMullan, J. Negri, G. Fanourakis, A. Goudopoulou, V. M. Richon, P. A. Marks, and N. Mitsiades Novel Histone Deacetylase Inhibitors in the Treatment of Thyroid Cancer Clin. Cancer Res., May 15, 2005; 11(10): 3958 - 3965. [Abstract] [Full Text] [PDF]
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J. J. Xiao, A. B. Foraker, P. W. Swaan, S. Liu, Y. Huang, Z. Dai, J. Chen, W. Sadee, J. Byrd, G. Marcucci, et al. Efflux of Depsipeptide FK228 (FR901228, NSC-630176) Is Mediated by P-Glycoprotein and Multidrug Resistance-Associated Protein 1 J. Pharmacol. Exp. Ther., April 1, 2005; 313(1): 268 - 276. [Abstract] [Full Text] [PDF]
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K. A. Strait, C. T. Warnick, C. D. Ford, B. Dabbas, E. H. Hammond, and S. J. Ilstrup Histone deacetylase inhibitors induce G2-checkpoint arrest and apoptosis in cisplatinum-resistant ovarian cancer cells associated with overexpression of the Bcl-2-related protein Bad Mol. Cancer Ther., April 1, 2005; 4(4): 603 - 611. [Abstract] [Full Text] [PDF]
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C. Subramanian, A. W. Opipari Jr., X. Bian, V. P. Castle, and R. P. S. Kwok Ku70 acetylation mediates neuroblastoma cell death induced by histone deacetylase inhibitors PNAS, March 29, 2005; 102(13): 4842 - 4847. [Abstract] [Full Text] [PDF]
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H. Duan, C. A. Heckman, and L. M. Boxer Histone Deacetylase Inhibitors Down-Regulate bcl-2 Expression and Induce Apoptosis in t(14;18) Lymphomas Mol. Cell. Biol., March 1, 2005; 25(5): 1608 - 1619. [Abstract] [Full Text] [PDF]
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F. J. Davis, J. B Pillai, M. Gupta, and M. P. Gupta Concurrent opposite effects of trichostatin A, an inhibitor of histone deacetylases, on expression of {alpha}-MHC and cardiac tubulins: implication for gain in cardiac muscle contractility Am J Physiol Heart Circ Physiol, March 1, 2005; 288(3): H1477 - H1490. [Abstract] [Full Text] [PDF]
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L. De Felice, C. Tatarelli, M. G. Mascolo, C. Gregorj, F. Agostini, R. Fiorini, V. Gelmetti, S. Pascale, F. Padula, M. T. Petrucci, et al. Histone Deacetylase Inhibitor Valproic Acid Enhances the Cytokine-Induced Expansion of Human Hematopoietic Stem Cells Cancer Res., February 15, 2005; 65(4): 1505 - 1513. [Abstract] [Full Text] [PDF]
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M. Nevels, C. Paulus, and T. Shenk Human cytomegalovirus immediate-early 1 protein facilitates viral replication by antagonizing histone deacetylation PNAS, December 7, 2004; 101(49): 17234 - 17239. [Abstract] [Full Text] [PDF]
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L. C. Hsi, X. Xi, R. Lotan, I. Shureiqi, and S. M. Lippman The Histone Deacetylase Inhibitor Suberoylanilide Hydroxamic Acid Induces Apoptosis via Induction of 15-Lipoxygenase-1 in Colorectal Cancer Cells Cancer Res., December 1, 2004; 64(23): 8778 - 8781. [Abstract] [Full Text] [PDF]
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D. Z. Qian, X. Wang, S. K. Kachhap, Y. Kato, Y. Wei, L. Zhang, P. Atadja, and R. Pili The Histone Deacetylase Inhibitor NVP-LAQ824 Inhibits Angiogenesis and Has a Greater Antitumor Effect in Combination with the Vascular Endothelial Growth Factor Receptor Tyrosine Kinase Inhibitor PTK787/ZK222584 Cancer Res., September 15, 2004; 64(18): 6626 - 6634. [Abstract] [Full Text] [PDF]
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C. M. Reilly, N. Mishra, J. M. Miller, D. Joshi, P. Ruiz, V. M. Richon, P. A. Marks, and G. S. Gilkeson Modulation of Renal Disease in MRL/lpr Mice by Suberoylanilide Hydroxamic Acid J. Immunol., September 15, 2004; 173(6): 4171 - 4178. [Abstract] [Full Text] [PDF]
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I. Fenic, V. Sonnack, K. Failing, M. Bergmann, and K. Steger In Vivo Effects of Histone-Deacetylase Inhibitor Trichostatin-A on Murine Spermatogenesis J Androl, September 1, 2004; 25(5): 811 - 818. [Abstract] [Full Text] [PDF]
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A. Kuendgen, C. Strupp, M. Aivado, A. Bernhardt, B. Hildebrandt, R. Haas, U. Germing, and N. Gattermann Treatment of myelodysplastic syndromes with valproic acid alone or in combination with all-trans retinoic acid Blood, September 1, 2004; 104(5): 1266 - 1269. [Abstract] [Full Text] [PDF]
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M. C. Myzak, P. A. Karplus, F.-L. Chung, and R. H. Dashwood A Novel Mechanism of Chemoprotection by Sulforaphane: Inhibition of Histone Deacetylase Cancer Res., August 15, 2004; 64(16): 5767 - 5774. [Abstract] [Full Text] [PDF]
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J. P. Klopper, W. R. Hays, V. Sharma, M. A. Baumbusch, J. M. Hershman, and B. R. Haugen Retinoid X receptor-{gamma} and peroxisome proliferator-activated receptor-{gamma} expression predicts thyroid carcinoma cell response to retinoid and thiazolidinedione treatment Mol. Cancer Ther., August 1, 2004; 3(8): 1011 - 1020. [Abstract] [Full Text] [PDF]
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S. Ammanamanchi and M. G. Brattain Restoration of Transforming Growth Factor-{beta} Signaling through Receptor RI Induction by Histone Deacetylase Activity Inhibition in Breast Cancer Cells J. Biol. Chem., July 30, 2004; 279(31): 32620 - 32625. [Abstract] [Full Text] [PDF]
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X. Zhang, W. Wharton, Z. Yuan, S.-C. Tsai, N. Olashaw, and E. Seto Activation of the Growth-Differentiation Factor 11 Gene by the Histone Deacetylase (HDAC) Inhibitor Trichostatin A and Repression by HDAC3 Mol. Cell. Biol., June 15, 2004; 24(12): 5106 - 5118. [Abstract] [Full Text] [PDF]
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