Mode of action: Inhibition of histone deacetylase, altering WNT-dependent gene expression, and regulation of beta-catenin - Developmental effects of valproic acid

Critical Reviews in Toxicology

Volumn 35, Issue 8-9, 2005, Pages 727-738

  Wiltse, Jeanette ^a,b  

^a U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^b ILSI Risk Science Institute   (United States)

Author keywords

Human Developmental Toxicity; Human Relevance; Neural Tube Defects; Spina Bifida; Wnt Signaling Pathway

Indexed keywords

BETA CATENIN; HISTONE DEACETYLASE; TRICHOSTATIN A; VALPROIC ACID; WNT1 PROTEIN;

ARTICLE; CELL DIFFERENTIATION; EMPIRICISM; ENZYME INHIBITION; GENE EXPRESSION; GENE STRUCTURE; HUMAN; LABORATORY TEST; NERVE CELL; NONHUMAN; SIGNAL TRANSDUCTION; SPINA BIFIDA;

ANIMALS; ANTICONVULSANTS; BETA CATENIN; ENZYME INHIBITORS; FEMALE; GENE EXPRESSION; HISTONE DEACETYLASES; HUMANS; PREGNANCY; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY; TERATOGENS; VALPROIC ACID; WNT PROTEINS;

ANIMALIA;

EID: 28144456841     PISSN: 10408444     EISSN: 15476898     Source Type: Journal    
DOI: 10.1080/10408440591007403     Document Type: Article

References (57)

1. Agathon, A., Thisse, C., and Thisse, B. (2003). The molecular nature of the zebrafish tail organizer. Nature 424:448-452.
2. Alonzo-Aperte, E., Ubeda, N., Achon, M, Perez-Miguelsanz, J., and Varela-Moreiras, G. (1999). Impaired methionine synthesis and hypomethylation in rats exposed to valproate during gestation. Neurology 52:750-756.
3. Amit, S., Hatzubia, A., Birman., J., Andersen, J.S., Ben-Shushan, E., Mann, M., Ben-Neriah, Y., and Alkalay, I. (2002). Axin-mediated CKI phosphorylation of β-catenin at Ser 45: A molecular switch for the Wnt pathway. Genes Dev. 16:1066-1076.
4. Arpino, C., Brescianini, S., Robert E., Castilla, E.E., Cocchi, G., Cornel, M.C., de Vigan, C., Lancaster, P.A., Merlob, P., Sumiyoshi, Y., Zampino, G., Renzi, C., Rosano, A., and Mastroiacovo, P. (2000). Teratogenic effects of antiepileptic drugs: Use of an international database on malformations and drug exposure (MADRE). Epilepsia 41(11):1435-1443.
5. Behrens, J., and Kühl, M. (2003). Wnt Signal Transduction Pathways: An Overview. In: Wnt signaling in Development. Kühl, M., ed. pp. 1-14. Kluwer Academic/Plenum Publishers, New York.
6. Biernacki, B., Bogdan, W., and Minta M. (2000). Effect of sodium valproate on rat embryo development in vitro. Bull. Vet. Inst. Pulawy 44:201-205.
7. Bilder, D., Graba, Y., and Scott, M.P. (1998). Wnt and TGFβ signals subdivide the AbdA Hox domain during Drosophila mesoderm patterning. Development 125:1781-1790.
8. Binkerd, P.E., Rowland, J.M., Nau. H., and Hendricks, A.G. (1988). Evaluation of valproic (VPA) developmental toxicity and pharmacokinetics in Sprague Dawley rats. Fundam. Appl. Toxicol. 11(3):485-493.
9. Blaheta, R.A., Nau, H., Michaelis, M., and Cinatl, J. (2002). Valproate and valproate-analogues: Potent tools to fight against cancer. Current Medicinal Chemistry 9:1417-1433.
10. Bogumil, B., Bogdan, W., and Minta, M. (2000). Effect of sodium valproate on rat embryo development in vitro. Bull. Vet. Inst. Pulawy 44:201-205.
11. Cadigan, K.M., and Nusse, R. (1997). Wnt signaling: A common theme in animal development. Genes Dev. 11:3286-3305.
12. Craig, J., Morrison, P., Morrow, J., and Patterson, V. (1999). Failure of periconceptual folic acid to prevent a neural tube defect in the offspring of a mother taking sodium valproate. Seizure 8:253-254.
13. Detich, N., Bovenzi, V., and Szyf, M. (2003). Valproate induces replication independent DNA demethylation. J. Biol. Chem.
14. Drevets, W.C. (2001). Neuroimaging and neuropathological studies of depression: Implications for the cognitive-emotional features of mood disorders. Curr. Opin. Neurobiol. 11:240-249.
15. Drevets, W.C., Price, J.L., Simpson, J.R., Jr., Todd, R.D., Reich, T., Vannier, M., and Raichle, M.E. (1997). Subgenual prefrontal cortex abnormalities in mood disorders. Nature 386:824-827.
16. Duncan, S., Mercho, S., Lopes-Cendes, I., Seni, M., Benjamin, A., Dubeau, F., Andermann, F., and Andermann, E. (2001). Repeated neural tube defects and valproate monotherapy suggest a pharmacogenetic abnormality. Epilepsia 42:750-753.
17. Ehlers, K., Sturjie, H., Merker, H.J., and Nau, H. (1992). Valproic acid-induced spinia bifida: A mouse model. Teratology 45(2):145-154.
18. Elmazar, M.M.A., and Nau, H. (1992). Methotrexate increases valproic acid-induced developmental toxicity, in particular neural tube defects in mice. Teratogenesis, Carcinogenesis, and Mutagenesis 12:203-210.
19. 12 on valproic acid-induced teratogenesis in mice. Fundamental and Applied Toxicology 18:389-394.
20. Faiella, A., Wernig, M., Consalez, G.G., Hostick, U., Hofmann, C., Hustert, E., Boncinelli, E., Balling, R., and Nadeau, J.H. (2000). A mouse model for valproate teratogenicity: Parental effects, homeotic transformations, and altered HOX expression. Hum. Mol. Genet. 9:227-236.
21. Finnell, R.H., Wlodarczyk, B.C., Craig, J.C., Piedrahita, J.A., and Bennett, G.D. (1997). Strain-dependent alterations in the expression of folate pathway genes following teratogenic exposure to valproic acid in a mouse model. Amer. J. Med. Genetics 70:303-311.
22. Fuller, L.G., Cornelius, S.K., Murphy, C.W., and Wiens, D.J. (2002). Neural crest cell motility in valproic acid. Reprod. Toxicol. 16:825-839.
23. Goold, R.G., Owen, R., and Gordon-Weeks, P.R. (1999). Glycogen synthase kinase 3beta phosphorylation of microtubule-associated protein 1B regulates the stability of micro tubules in growth cones. J. Cell Sci. 112:3373-3384.
24. Gould, T.D., and Manji, H.K. (2002). The Wnt signaling pathway in bipolar disorder. Neuroscientist 8:497-511.
25. Gurvich, N., and Klein, P.S. (2002). Lithium and valproic acid: Parallels and contrasts in diverse signaling contexts. Pharmacol. Ther. 96:45-66.
26. Hall, A.C., Lucas, F.R., and Salinas, P.C. (2000). Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling. Cell 100:525-535.
27. Hall, A.C., Brennan, A., Goold, R.G., Cleverley, K., Lucas, F.R., Gordon-Weeks, P.R., and Salinas, P.C. (2002). Valproate regulates GSK-3-mediated axonal remodeling and synapsin I clustering in developing neurons. Mol. Cell Neurosci. 20:257-270.
28. Hansen, D.K., Grafton, T.F., Dial, S.L., Gehring, T.A., and Siitonen, P.H. (1995). Effect of supplemental folic acid on valproic acid-induced embryotoxicity and tissue zinc levels in vivo. Teratology 52:277-285.
29. Holmes, L.B., Harvey, E.A., Coull, B.A., Huntington, B.A., Khoshbin, S., Hayes, A.M., and Ryan, L.M. (2001). The Teratogenicity of Anti Convulsant Drugs. N. Engl. J. Med. 344:1132-1135.
30. Huristone, F.L., Bethel, H., Korving, J., van Eeden, F., Cuppen, E., Ziukovic, D., Pasterk, R.H.A., and Clevers, H., (2003). The Wnt/β-catenin pathway regulates cardiac valve formation. Nature 425:633-637.
31. Jamora, C., DasGupta, R., Kocieniewski, P., and Fuchs, E. (2003). Links between signal transduction, transcription, and adhesion in epithelial bud development. Nature 422:317-322.
32. Kawagoe, R., Kawagoe, H., and Sano, K. (2002). Valproic acid induces apoptosis in human leukemia cells by stimulating both caspase-dependent and -independent apoptotic signaling pathways. Leukemia Res. 26:495-502.
33. Kliecker, C., and Niehrs, C. (2001). A morphogen gradient of Wnt/β-catenin signaling regulates anterioposterior neural patterning in Xenopus. Development 128:4189-4201.
34. Li, X., Bijur, G.N., and Jope, R.S. (2002). Glycogen synthase kinase-3beta, mood stabilizers, and neuroprotection. BipolarDisord. 4:137-144.
35. Lucas, F.R., and Salinas, P.C. (1997). WNT-7a induces axonal remodeling and increases synapsin I levels in cerebellar neurons. Dev. Biol. 192:31-44.
36. Manji, H.K., and Chen, G. (2002). PKC, MAP kinases and the bcl-2 family of proteins as long term targets for mood stabilizers. Mol. Psychiatry 7(suppl. 1):S46-S56.
37. Menegola, E., Broccia, M.L., Nau, H., Prate, M., Ricolfi, R., and Giavina, E. (1996). Teratogenic effects of sodium valproate in mice and rats at mid-gestation and at term. Teratogen. Carcinogen. Mutagen. 16(2):97-108.
38. Mlodzik, M. (2003). Epithelial planar cell polarity in Drosophila. Kühl, M., ed. pp. 90-101. Kluwer Academic/Plenum Publishers, New York.
39. Moon, R.T., Kohn, A.D., DeFarrari, G.V., and Kaykas, A. (2004). Wnt and β catenin signalling: Diseases and therapies. Nature Reviews Genetics 5:691-701.
40. Narotsky, M.G., Francis, E.Z., and Kavlock, R.J. (1994). Developmental toxicity and structure-activity relationship of aliphatic acids, including dose-response assessment of valproic acid in mice and rats. Fundam. Appl. Toxicol. 22(2):251-265.
41. Naruse, I., Collins, M.D., and Scott, W.J., Jr. (1988). Strain differences in the teratogenicity induced by sodium valproate in cultured mouse embryos. Teratology 38(1):87-96.
42. Padmanabhan, R., and Shafiullah, M.M. (2003). Amelioration of sodium valproate-induced neural tube defects in mouse fetuses by maternal folic acid supplementation during gestation. Congenital Abnormalities 43:29-40.
43. Peifer, M., and Polakis, P. (2000). Wnt signaling in oncogenesis and embryogenesis - A look outside the nucleus. Science 287:1606-1609.
44. Phiel, C.J., Zhang F., Huang, E.Y., Guenther, M.G., Lazar, M.A., and Klein, P.S. (2001). Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J. Biol. Chem. 276:36734-36741.
45. Pires-daSilva, A., and Sommer, R.J. (2003). The evolution of signaling pathways in animal development. Nature Reviews Genetics 4:39-49.
46. Pourquié, O. (2003). The segmentation clock: Converting embryonic time into spatial pattern. Science 301:328-330.
47. Robert, E., and Guibaud, P. (1982). Maternal valproic acid and congenital neural tube defects. Lancet 2:937.
48. Stambolic, V., Ruel, L., and Woodgett, J.R. (1996). Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signalling in intact cells. Curr. Biol. 6:1664-1668.
49. Svensson, K., Mattsson, R., James, T.C., Wentzel, P., Pilartz, M., MacLaughlin, J., Miller, S.J., Olsson, T., Eriksson, U.J., and Ohlsson, R. (1998). The paternal allele of the H19 gene is progressively silenced during early mouse development: The acetylation status of histones may be involved in the generation of variegated expression patterns. Development 125:61-69.
50. Sztajnkrycer, M.D. (2002). Valproic acid toxicity: Overview and management. J. Toxicology 40:789-801.
51. Trotz, M., Wegner, C., and Nau, H. (1987). Valproic acid-induced neural tube defects: Reduction by folinic acid in the mouse. Life Sciences 41:103-110.
52. Wallingford, J.B., and Harland, R.M. (2002). Neural tube closure requires Disheveled-dependent convergent extension of the midline. Development 129:5815-5825.
53. 2+, and cyclic GMP: Visualizing Frizzled functions. Science 300:1529-1530.
54. Wegner, C., and Nau, H. (1991). Diurnal variation of folate concentrations in mouse embryo and plasma: The protective effect of folinic acid on valproic acid-induced teratogenicity is time dependent. Reproductive Toxicology 5:465-471.
55. Wegner, C., and Nau, H. (1992). Alteration of embryonic folate metabolism by valproic acid during organogenesis: Implications for mechanism of teratogenesis. Neurology 42(suppl. 5):17-24.
56. Williams, R.S., Cheng, L., Mudge, A.W., and Harwood, A.J. (2002). A common mechanism of action for three mood stabilizing drugs. Nature 417:292-295.
57. Yost, C., Tones, M., Miller, J.R., Huang, E., Kimelman, D., and Moon, R.T. (1996). The axis-inducing activity, stability, and subcellular distribution of beta-catenin is regulated in Xenopus embryos by glycogen synthase kinase 3. Genes Devel. 10:1443-1454.