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J. Biol. Chem., Vol. 276, Issue 39, 36734-36741, September 28, 2001
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From the Valproic acid is widely used to treat epilepsy
and bipolar disorder and is also a potent teratogen, but its mechanisms
of action in any of these settings are unknown. We report that valproic acid activates Wntdependent gene expression, similar to
lithium, the mainstay of therapy for bipolar disorder. Valproic acid,
however, acts through a distinct pathway that involves direct
inhibition of histone deacetylase (IC50 for
HDAC1 = 0.4 mM). At therapeutic levels, valproic acid
mimics the histone deacetylase inhibitor trichostatin A, causing
hyperacetylation of histones in cultured cells. Valproic acid, like
trichostatin A, also activates transcription from diverse exogenous and
endogenous promoters. Furthermore, valproic acid and trichostatin A
have remarkably similar teratogenic effects in vertebrate embryos,
while non-teratogenic analogues of valproic acid do not inhibit histone
deacetylase and do not activate transcription. Based on these
observations, we propose that inhibition of histone deacetylase
provides a mechanism for valproic acid-induced birth defects and could
also explain the efficacy of valproic acid in the treatment of bipolar disorder.
Histone Deacetylase Is a Direct Target of Valproic
Acid, a Potent Anticonvulsant, Mood Stabilizer, and Teratogen*
,
**, and§¶§§¶¶
Howard Hughes Medical Institute, Graduate
Programs in § Pharmacology and ¶ Cell and Molecular
Biology, and the Department of Medicine, ** Division of
Endocrinology, Diabetes, and Metabolism and §§ Division of
Hematology-Oncology, University of Pennsylvania School of Medicine,
Philadelphia, Pennsylvania 19104-6148
*
The costs of publication of this
article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement" in
accordance with 18 U.S.C. Section
1734 solely to indicate this fact.
Supported by Grants DK43806 and DK45586 from the NIDDK,
National Institutes of Health.
¶¶
Supported by a grant from the National Institute of
Mental Health and is an assistant investigator in the Howard Hughes
Medical Institute. To whom correspondence should be addressed: CRB
370/UPenn, 415 Curie Blvd., Philadelphia, PA 19104-6148. Tel.:
215-898-2179; Fax: 215-573-4320; E-mail:
pklein@mail.med.upenn.edu.
Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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R. Zhou, N. A. Gray, P. Yuan, X. Li, J. Chen, G. Chen, P. Damschroder-Williams, J. Du, L. Zhang, and H. K. Manji The Anti-Apoptotic, Glucocorticoid Receptor Cochaperone Protein BAG-1 Is a Long-Term Target for the Actions of Mood Stabilizers J. Neurosci., May 4, 2005; 25(18): 4493 - 4502. [Abstract] [Full Text] [PDF]
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D. C. Marchion, E. Bicaku, A. I. Daud, D. M. Sullivan, and P. N. Munster Valproic Acid Alters Chromatin Structure by Regulation of Chromatin Modulation Proteins Cancer Res., May 1, 2005; 65(9): 3815 - 3822. [Abstract] [Full Text] [PDF]
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B. J. Eickholt, G. J. Towers, W. J. Ryves, D. Eikel, K. Adley, L. M. J. Ylinen, N. H. Chadborn, A. J. Harwood, H. Nau, and R. S. B. Williams Effects of Valproic Acid Derivatives on Inositol Trisphosphate Depletion, Teratogenicity, Glycogen Synthase Kinase-3{beta} Inhibition, and Viral Replication: A Screening Approach for New Bipolar Disorder Drugs Derived from the Valproic Acid Core Structure Mol. Pharmacol., May 1, 2005; 67(5): 1426 - 1433. [Abstract] [Full Text] [PDF]
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X.-J. Yang and S. Gregoire Class II Histone Deacetylases: from Sequence to Function, Regulation, and Clinical Implication Mol. Cell. Biol., April 15, 2005; 25(8): 2873 - 2884. [Full Text] [PDF]
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 D. Sinha, Z. Wang, K. L. Ruchalski, J. S. Levine, S. Krishnan, W. Lieberthal, J. H. Schwartz, and S. C. Borkan Lithium activates the Wnt and phosphatidylinositol 3-kinase Akt signaling pathways to promote cell survival in the absence of soluble survival factors Am J Physiol Renal Physiol, April 1, 2005; 288(4): F703 - F713. [Abstract] [Full Text] [PDF]
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 M. G. Catalano, N. Fortunati, M. Pugliese, L. Costantino, R. Poli, O. Bosco, and G. Boccuzzi Valproic Acid Induces Apoptosis and Cell Cycle Arrest in Poorly Differentiated Thyroid Cancer Cells J. Clin. Endocrinol. Metab., March 1, 2005; 90(3): 1383 - 1389. [Abstract] [Full Text] [PDF]
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N. P. Mongan and L. J. Gudas Valproic acid, in combination with all-trans retinoic acid and 5-aza-2'-deoxycytidine, restores expression of silenced RAR{beta}2 in breast cancer cells Mol. Cancer Ther., March 1, 2005; 4(3): 477 - 486. [Abstract] [Full Text] [PDF]
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 J. R. Wood, V. L. Nelson-Degrave, E. Jansen, J. M. McAllister, S. Mosselman, and J. F. Strauss III Valproate-induced alterations in human theca cell gene expression: clues to the association between valproate use and metabolic side effects Physiol Genomics, February 10, 2005; 20(3): 233 - 243. [Abstract] [Full Text] [PDF]
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M. Veldic, A. Guidotti, E. Maloku, J. M. Davis, and E. Costa In psychosis, cortical interneurons overexpress DNA-methyltransferase 1 PNAS, February 8, 2005; 102(6): 2152 - 2157. [Abstract] [Full Text] [PDF]
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J. Chen, J. R. St-Germain, and Q. Li B56 Regulatory Subunit of Protein Phosphatase 2A Mediates Valproic Acid-Induced p300 Degradation Mol. Cell. Biol., January 15, 2005; 25(2): 525 - 532. [Abstract] [Full Text] [PDF]
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 A. J. Kim, Y. Shi, R. C. Austin, and G. H. Werstuck Valproate protects cells from ER stress-induced lipid accumulation and apoptosis by inhibiting glycogen synthase kinase-3 J. Cell Sci., January 1, 2005; 118(1): 89 - 99. [Abstract] [Full Text] [PDF]
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 C. Calomme, A. Dekoninck, S. Nizet, E. Adam, T. L.-A. Nguyen, A. Van Den Broeke, L. Willems, R. Kettmann, A. Burny, and C. Van Lint Overlapping CRE and E Box Motifs in the Enhancer Sequences of the Bovine Leukemia Virus 5' Long Terminal Repeat Are Critical for Basal and Acetylation-Dependent Transcriptional Activity of the Viral Promoter: Implications for Viral Latency J. Virol., December 15, 2004; 78(24): 13848 - 13864. [Abstract] [Full Text] [PDF]
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D. C. Lagace, R. S. McLeod, and M. W. Nachtigal Valproic Acid Inhibits Leptin Secretion and Reduces Leptin Messenger Ribonucleic Acid Levels in Adipocytes Endocrinology, December 1, 2004; 145(12): 5493 - 5503. [Abstract] [Full Text] [PDF]
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J. Hsieh, K. Nakashima, T. Kuwabara, E. Mejia, and F. H. Gage Histone deacetylase inhibition-mediated neuronal differentiation of multipotent adult neural progenitor cells PNAS, November 23, 2004; 101(47): 16659 - 16664. [Abstract] [Full Text] [PDF]
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 P. M. Das and R. Singal DNA Methylation and Cancer J. Clin. Oncol., November 15, 2004; 22(22): 4632 - 4642. [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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Y. Hao, T. Creson, L. Zhang, P. Li, F. Du, P. Yuan, T. D. Gould, H. K. Manji, and G. Chen Mood Stabilizer Valproate Promotes ERK Pathway-Dependent Cortical Neuronal Growth and Neurogenesis J. Neurosci., July 21, 2004; 24(29): 6590 - 6599. [Abstract] [Full Text] [PDF]
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M. S. Jansen, S. C. Nagel, P. J. Miranda, E. K. Lobenhofer, C. A. Afshari, and D. P. McDonnell Short-chain fatty acids enhance nuclear receptor activity through mitogen-activated protein kinase activation and histone deacetylase inhibition PNAS, May 4, 2004; 101(18): 7199 - 7204. [Abstract] [Full Text] [PDF]
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D. C. Lagace and M. W. Nachtigal Inhibition of Histone Deacetylase Activity by Valproic Acid Blocks Adipogenesis J. Biol. Chem., April 30, 2004; 279(18): 18851 - 18860. [Abstract] [Full Text] [PDF]
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L. Tou, Q. Liu, and R. A. Shivdasani Regulation of Mammalian Epithelial Differentiation and Intestine Development by Class I Histone Deacetylases Mol. Cell. Biol., April 15, 2004; 24(8): 3132 - 3139. [Abstract] [Full Text] [PDF]
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 P. M. Rodier Environmental Causes of Central Nervous System Maldevelopment Pediatrics, April 1, 2004; 113(4/S1): 1076 - 1083. [Abstract] [Full Text] [PDF]
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C. Konradi, M. Eaton, M. L. MacDonald, J. Walsh, F. M. Benes, and S. Heckers Molecular Evidence for Mitochondrial Dysfunction in Bipolar Disorder Arch Gen Psychiatry, March 1, 2004; 61(3): 300 - 308. [Abstract] [Full Text] [PDF]
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M. Michaelis, U. R. Michaelis, I. Fleming, T. Suhan, J. Cinatl, R. A. Blaheta, K. Hoffmann, R. Kotchetkov, R. Busse, H. Nau, et al. Valproic Acid Inhibits Angiogenesis in Vitro and in Vivo Mol. Pharmacol., March 1, 2004; 65(3): 520 - 527. [Abstract] [Full Text] [PDF]
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N. Gurvich, O. M. Tsygankova, J. L. Meinkoth, and P. S. Klein Histone Deacetylase Is a Target of Valproic Acid-Mediated Cellular Differentiation Cancer Res., February 1, 2004; 64(3): 1079 - 1086. [Abstract] [Full Text] [PDF]
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V. L. Nelson-DeGrave, J. K. Wickenheisser, J. E. Cockrell, J. R. Wood, R. S. Legro, J. F. Strauss III, and J. M. McAllister Valproate Potentiates Androgen Biosynthesis in Human Ovarian Theca Cells Endocrinology, February 1, 2004; 145(2): 799 - 808. [Abstract] [Full Text] [PDF]
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 H. K. Manji, I. I. Gottesman, and T. D. Gould Signal Transduction and Genes-to-Behaviors Pathways in Psychiatric Diseases Sci. Signal., November 4, 2003; 2003(207): pe49 - pe49. [Abstract] [Full Text] [PDF]
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F. Zhang, C. J. Phiel, L. Spece, N. Gurvich, and P. S. Klein Inhibitory Phosphorylation of Glycogen Synthase Kinase-3 (GSK-3) in Response to Lithium: EVIDENCE FOR AUTOREGULATION OF GSK-3 J. Biol. Chem., August 29, 2003; 278(35): 33067 - 33077. [Abstract] [Full Text] [PDF]
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N. Detich, V. Bovenzi, and M. Szyf Valproate Induces Replication-independent Active DNA Demethylation J. Biol. Chem., July 18, 2003; 278(30): 27586 - 27592. [Abstract] [Full Text] [PDF]
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G. Graziani, L. Tentori, I. Portarena, M. Vergati, and P. Navarra Valproic Acid Increases the Stimulatory Effect of Estrogens on Proliferation of Human Endometrial Adenocarcinoma Cells Endocrinology, July 1, 2003; 144(7): 2822 - 2828. [Abstract] [Full Text] [PDF]
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N. Mitsiades, C. S. Mitsiades, P. G. Richardson, C. McMullan, V. Poulaki, G. Fanourakis, R. Schlossman, D. Chauhan, N. C. Munshi, T. Hideshima, et al. Molecular sequelae of histone deacetylase inhibition in human malignant B cells Blood, May 15, 2003; 101(10): 4055 - 4062. [Abstract] [Full Text] [PDF]
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I. J. Arinze and Y. Kawai Sp Family of Transcription Factors Is Involved in Valproic Acid-induced Expression of Galpha i2 J. Biol. Chem., May 9, 2003; 278(20): 17785 - 17791. [Abstract] [Full Text] [PDF]
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S. J. Haggarty, K. M. Koeller, J. C. Wong, C. M. Grozinger, and S. L. Schreiber Domain-selective small-molecule inhibitor of histone deacetylase 6 (HDAC6)-mediated tubulin deacetylation PNAS, April 15, 2003; 100(8): 4389 - 4394. [Abstract] [Full Text] [PDF]
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