© 1998 by Oxford University Press
Journal of the National Cancer Institute, Vol. 90, No. 21, 1621-1625,
November 4, 1998
©Copyright 1998 Oxford University Press
ACCELERATED DISCOVERY |
Therapeutic Targeting of Transcription in Acute Promyelocytic Leukemia by Use of an Inhibitor of Histone Deacetylase
Affiliations of authors: R. P. Warrell, Jr. (Developmental Chemotherapy and Leukemia Services, Department of Medicine), L.-Z. He (Department of Human Genetics and the Molecular Biology Program), V. Richon, (Cell Biology Program), E. Calleja (Department of Pediatrics), P. P. Pandolfi (Department of Human Genetics and the Molecular Biology Program), Memorial Sloan-Kettering Cancer Center, and the Cornell University Medical College, New York, NY.
Correspondence to: Pier Paolo Pandolfi, M.D., Ph.D., Memorial Sloan-Kettering Cancer Center, 1275 York Ave., New York, NY 10021 (e-mail:p-pandolfi{at}ski.mskcc.org).
Abstract
Background: Acetylation of DNA-associated histones is
linked to activation of gene
transcription, whereas histone deacetylation is associated with
transcriptional repression. Recent
studies have shown that inhibitors of histone deacetylases can
relieve transcriptional repression
caused by the products of certain oncogenes. We tested whether
these findings could be applied
clinically to a patient with highly resistant acute promyelocytic
leukemia. Methods: A
patient who had experienced multiple relapses was treated with
all-trans-retinoic acid
alone and in combination with sodium phenylbutyrate, an inhibitor
of histone deacetylases.
Immunohistochemistry and western blot analysis were used to assay
for histone hyperacetylation
in mononuclear cells from the patient's blood and bone
marrow. Marrow mononuclear
cells and reverse transcription-polymerase chain reaction
(RT-PCR) analysis of messenger RNA
encoded by the PML/RAR-
oncogene were used to assess minimal
residual disease. Results: The patient proved clinically
resistant to treatment with all-trans-retinoic
acid alone. However, 23 days after sodium phenylbutyrate was
added to the treatment regimen,
visible leukemic cells had been eliminated from her bone marrow,
and she achieved a complete
clinical and cytogenetic remission shortly thereafter. With a
second treatment course, analysis for
minimal residual disease by RT-PCR proved negative.
Immunofluorescence and western blot
analysis showed that phenylbutyrate caused a time-dependent
increase in histone acetylation in
blood and bone marrow mononuclear cells. Conclusions:
Clinical treatment with an
inhibitor of histone deacetylase induces histone hyperacetylation
in target cells and may restore
sensitivity to the anti-leukemic effects of all-trans-retinoic acid in acute promyelocytic
leukemia. Similar therapy may prove useful in other neoplastic
diseases that are associated with
oncogenic repression of gene transcription due to recruitment of
histone deacetylases. [J
Natl Cancer Inst 1998;90:1621-5]
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J. M. Amann, J. Nip, D. K. Strom, B. Lutterbach, H. Harada, N. Lenny, J. R. Downing, S. Meyers, and S. W. Hiebert ETO, a Target of t(8;21) in Acute Leukemia, Makes Distinct Contacts with Multiple Histone Deacetylases and Binds mSin3A through Its Oligomerization Domain Mol. Cell. Biol., October 1, 2001; 21(19): 6470 - 6483. [Abstract] [Full Text] [PDF]
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M. A. Smith and B. Anderson Where to Next with Retinoids for Cancer Therapy? Clin. Cancer Res., October 1, 2001; 7(10): 2955 - 2957. [Full Text] [PDF]
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D. Grimwade, H. Walker, G. Harrison, F. Oliver, S. Chatters, C. J. Harrison, K. Wheatley, A. K. Burnett, and A. H. Goldstone The predictive value of hierarchical cytogenetic classification in older adults with acute myeloid leukemia (AML): analysis of 1065 patients entered into the United Kingdom Medical Research Council AML11 trial Blood, September 1, 2001; 98(5): 1312 - 1320. [Abstract] [Full Text] [PDF]
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J. Gilbert, S. D. Baker, M. K. Bowling, L. Grochow, W. D. Figg, Y. Zabelina, R. C. Donehower, and M. A. Carducci A Phase I Dose Escalation and Bioavailability Study of Oral Sodium Phenylbutyrate in Patients with Refractory Solid Tumor Malignancies Clin. Cancer Res., August 1, 2001; 7(8): 2292 - 2300. [Abstract] [Full Text] [PDF]
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Y. Komatsu, K.-y. Tomizaki, M. Tsukamoto, T. Kato, N. Nishino, S. Sato, T. Yamori, T. Tsuruo, R. Furumai, M. Yoshida, et al. Cyclic Hydroxamic-acid-containing Peptide 31, a Potent Synthetic Histone Deacetylase Inhibitor with Antitumor Activity Cancer Res., June 1, 2001; 61(11): 4459 - 4466. [Abstract] [Full Text] [PDF]
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D. C. Coffey, M. C. Kutko, R. D. Glick, L. M. Butler, G. Heller, R. A. Rifkind, P. A. Marks, V. M. Richon, and M. P. La Quaglia The Histone Deacetylase Inhibitor, CBHA, Inhibits Growth of Human Neuroblastoma Xenografts in Vivo, Alone and Synergistically with All-Trans Retinoic Acid Cancer Res., May 1, 2001; 61(9): 3591 - 3594. [Abstract] [Full Text]
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S. Han, R. K. Wada, and N. Sidell Differentiation of Human Neuroblastoma by Phenylacetate Is Mediated by Peroxisome Proliferator-activated Receptor {{gamma}} Cancer Res., May 1, 2001; 61(10): 3998 - 4002. [Abstract] [Full Text]
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P. P. Pandolfi Oncogenes and tumor suppressors in the molecular pathogenesis of acute promyelocytic leukemia Hum. Mol. Genet., April 1, 2001; 10(7): 769 - 775. [Abstract] [Full Text] [PDF]
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C. Nervi, U. Borello, F. Fazi, V. Buffa, P. G. Pelicci, and G. Cossu Inhibition of Histone Deacetylase Activity by Trichostatin A Modulates Gene Expression during Mouse Embryogenesis without Apparent Toxicity Cancer Res., February 1, 2001; 61(4): 1247 - 1249. [Abstract] [Full Text]
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J. Zhang, B. A. Hug, E. Y. Huang, C. W. Chen, V. Gelmetti, M. Maccarana, S. Minucci, P. G. Pelicci, and M. A. Lazar Oligomerization of ETO Is Obligatory for Corepressor Interaction Mol. Cell. Biol., January 1, 2001; 21(1): 156 - 163. [Abstract] [Full Text]
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F. F. Ferrara, F. Fazi, A. Bianchini, F. Padula, V. Gelmetti, S. Minucci, M. Mancini, P. G. Pelicci, F. L. Coco, and C. Nervi Histone Deacetylase-targeted Treatment Restores Retinoic Acid Signaling and Differentiation in Acute Myeloid Leukemia Cancer Res., January 1, 2001; 61(1): 2 - 7. [Abstract] [Full Text]
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T. Maeda, M. Towatari, H. Kosugi, and H. Saito Up-regulation of costimulatory/adhesion molecules by histone deacetylase inhibitors in acute myeloid leukemia cells Blood, December 1, 2000; 96(12): 3847 - 3856. [Abstract] [Full Text] [PDF]
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S. Cote, D. Zhou, A. Bianchini, C. Nervi, R. E. Gallagher, and W. H. Miller Jr Altered ligand binding and transcriptional regulation by mutations in the PML/RARalpha ligand-binding domain arising in retinoic acid-resistant patients with acute promyelocytic leukemia Blood, November 1, 2000; 96(9): 3200 - 3208. [Abstract] [Full Text] [PDF]
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L. A. Hansen, C. C. Sigman, F. Andreola, S. A. Ross, G. J. Kelloff, and L. M. De Luca Retinoids in chemoprevention and differentiation therapy Carcinogenesis, July 1, 2000; 21(7): 1271 - 1279. [Abstract] [Full Text] [PDF]
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Q. M. Wang, R. Feinman, F. Kashanchi, J. M. Houghton, G. P. Studzinski, and L. E. Harrison Changes in E2F Binding after Phenylbutyrate-induced Differentiation of Caco-2 Colon Cancer Cells Clin. Cancer Res., July 1, 2000; 6(7): 2951 - 2958. [Abstract] [Full Text]
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R. L. Redner, J. D. Chen, E. A. Rush, H. Li, and S. L. Pollock The t(5;17) acute promyelocytic leukemia fusion protein NPM-RAR interacts with co-repressor and co-activator proteins and exhibits both positive and negative transcriptional properties Blood, April 15, 2000; 95(8): 2683 - 2690. [Abstract] [Full Text] [PDF]
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Y.-L. Chung, Y.-H. W. Lee, S.-H. Yen, and K.-H. Chi A Novel Approach for Nasopharyngeal Carcinoma Treatment Uses Phenylbutyrate as a Protein Kinase C Modulator: Implications for Radiosensitization and EBV-targeted Therapy Clin. Cancer Res., April 1, 2000; 6(4): 1452 - 1458. [Abstract] [Full Text]
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D. Samid, M. Wells, M. E. Greene, W. Shen, C. N. A. Palmer, and A. Thibault Peroxisome Proliferator-activated Receptor {{gamma}} as a Novel Target in Cancer Therapy: Binding and Activation by an Aromatic Fatty Acid with Clinical Antitumor Activity Clin. Cancer Res., March 1, 2000; 6(3): 933 - 941. [Abstract] [Full Text]
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T. E. Witzig, M. Timm, M. Stenson, P. A. Svingen, and S. H. Kaufmann Induction of Apoptosis in Malignant B Cells by Phenylbutyrate or Phenylacetate in Combination with Chemotherapeutic Agents Clin. Cancer Res., February 1, 2000; 6(2): 681 - 692. [Abstract] [Full Text]
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C. Perkins, C. N. Kim, G. Fang, and K. N. Bhalla Arsenic induces apoptosis of multidrug-resistant human myeloid leukemia cells that express Bcr-Abl or overexpress MDR, MRP, Bcl-2, or Bcl-xL Blood, February 1, 2000; 95(3): 1014 - 1022. [Abstract] [Full Text] [PDF]
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N. C. Gorin, E. Estey, R. J. Jones, H. I. Levitsky, I. Borrello, and S. Slavin New Developments in the Therapy of Acute Myelocytic Leukemia Hematology, January 1, 2000; 2000(1): 69 - 89. [Abstract] [Full Text] [PDF]
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L. C. Sambucetti, D. D. Fischer, S. Zabludoff, P. O. Kwon, H. Chamberlin, N. Trogani, H. Xu, and D. Cohen Histone Deacetylase Inhibition Selectively Alters the Activity and Expression of Cell Cycle Proteins Leading to Specific Chromatin Acetylation and Antiproliferative Effects J. Biol. Chem., December 3, 1999; 274(49): 34940 - 34947. [Abstract] [Full Text] [PDF]
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Y. Sowa, T. Orita, S. Minamikawa-Hiranabe, T. Mizuno, H. Nomura, and T. Sakai Sp3, but not Sp1, Mediates the Transcriptional Activation of the p21/WAF1/Cip1 Gene Promoter by Histone Deacetylase Inhibitor Cancer Res., September 1, 1999; 59(17): 4266 - 4270. [Abstract] [Full Text] [PDF]
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R. D. Glick, S. L. Swendeman, D. C. Coffey, R. A. Rifkind, P. A. Marks, V. M. Richon, and M. P. La Quaglia Hybrid Polar Histone Deacetylase Inhibitor Induces Apoptosis and CD95/CD95 Ligand Expression in Human Neuroblastoma Cancer Res., September 1, 1999; 59(17): 4392 - 4399. [Abstract] [Full Text] [PDF]
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R. X. Luo and D. C. Dean Chromatin Remodeling and Transcriptional Regulation J Natl Cancer Inst, August 4, 1999; 91(15): 1288 - 1294. [Abstract] [Full Text] [PDF]
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R. L. Redner, J. Wang, and J. M. Liu Chromatin Remodeling and Leukemia: New Therapeutic Paradigms Blood, July 15, 1999; 94(2): 417 - 428. [Full Text] [PDF]
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J. Wang, Y. Saunthararajah, R. L. Redner, and J. M. Liu Inhibitors of Histone Deacetylase Relieve ETO-mediated Repression and Induce Differentiation of AML1-ETO Leukemia Cells Cancer Res., June 1, 1999; 59(12): 2766 - 2769. [Abstract] [Full Text] [PDF]
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H. Huang, C. P. Reed, J.-S. Zhang, V. Shridhar, L. Wang, and D. I. Smith Carboxypeptidase A3 (CPA3): A Novel Gene Highly Induced by Histone Deacetylase Inhibitors during Differentiation of Prostate Epithelial Cancer Cells Cancer Res., June 1, 1999; 59(12): 2981 - 2988. [Abstract] [Full Text] [PDF]
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M. Bar-Ner, A. Thibault, M. Tsokos, I. T. Magrath, and D. Samid Phenylbutyrate Induces Cell Differentiation and Modulates Epstein-Barr Virus Gene Expression in Burkitt's Lymphoma Cells Clin. Cancer Res., June 1, 1999; 5(6): 1509 - 1516. [Abstract] [Full Text] [PDF]
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G.-X. Cheng, X.-H. Zhu, X.-Q. Men, L. Wang, Q.-H. Huang, X. L. Jin, S.-M. Xiong, J. Zhu, W.-M. Guo, J.-Q. Chen, et al. Distinct leukemia phenotypes in transgenic mice and different corepressor interactions generated by promyelocytic leukemia variant fusion genes PLZF-RARalpha and NPM-RARalpha PNAS, May 25, 1999; 96(11): 6318 - 6323. [Abstract] [Full Text] [PDF]
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