Valproic acid-induced skeletal malformations: Associated gene expression cascades

Pharmacogenetics and Genomics

Volumn 15, Issue 11, 2005, Pages 787-800

  Massa, Valentina ^a   Cabrera, Robert M ^b   Menegola, Elena ^a   Giavini, Erminio ^a   Finnell, Richard H ^b,c  

^a UNIVERSITY OF MILAN   (Italy)

^b TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

^c TEXAS A AND M UNIVERSITY SYSTEM   (United States)

Author keywords

Gene expression; Skeletal defects; Somites; Valproic acid

Indexed keywords

COMPLEMENTARY DNA; COMPLEMENTARY RNA; GUANOSINE TRIPHOSPHATASE; HISTONE DEACETYLASE; RNA; VALPROIC ACID;

ANIMAL MODEL; ARTICLE; BONE DISEASE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOSKELETON; DISEASE ASSOCIATION; DISEASE COURSE; DNA MICROARRAY; DOSE RESPONSE; GENE AMPLIFICATION; GENE EXPRESSION; GENETIC IDENTIFICATION; HUMAN; MEDICAL EXAMINATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; SKELETON MALFORMATION; TERATOGENESIS; UNINDEXED SEQUENCE; VALIDATION PROCESS;

ANIMALIA;

EID: 27444442803     PISSN: 17446872     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.fpc.0000170914.11898.3a     Document Type: Article

References (67)

1. Lammer EJ, Sever LE, Oakley GP Jr. Teratogen update: valproic acid. Teratology 1987; 35:465-473.
2. Nau H, Rating D, Koch S, Hauser I, Helge H. Valproic acid and its metabolites: placental transfer, neonatal pharmacokinetics, transfer via mother's milk and clinical status in neonates of epileptic mothers. J Pharmacol Exp Ther 1981; 219:768-777.
3. Wide K, Winbladh B, Kallen B. Major malformations in infants exposed to antiepileptic drugs in utero, with emphasis on carbamazepine and valproic acid: a nation-wide, population-based register study. Acta Paediatr 2004; 93:174-176.
4. Nau H. Teratogenic valproic acid concentrations: infusion by implanted minipumps vs conventional injection regimen in the mouse. Toxicol Appl Pharmacol 1985; 80:243-250.
5. Nau H, Zierer R, Spielmann H, Neubert D, Gansau C. A new model for embryotoxicity testing: teratogenicity and pharmacokinetics of valproic acid following constant-rate administration in the mouse using human therapeutic drug and metabolite concentrations. Life Sci 1981; 29:2803-2814.
6. Paulson RB, Sucheston ME, Hayes TG, Paulson GW. Teratogenic effects of valproate in the CD-1 mouse fetus. Arch Neurol 1985; 42:980-983.
7. Yerby MS. Management issues for women with epilepsy: neural tube defects and folic acid supplementation. Neurology 2003; 61:S23-S26.
8. Finnell RH, Gelineau-van Waes J, Bennett GD, Barber RC, Wlodarczyk B, Shaw GM, et al. Genetic basis of susceptibility to environmentally induced neural tube defects. Ann N Y Acad Sci 2000; 919:261-277.
9. Oakeshott P. Sodium valproate, carbamazepine and spina bifida. Br J Gen Pract 1991; 41:478-479.
10. Menegola E, Broccia ML, Nau H, Prati M, Ricolfi R, Giavini E. Teratogenic effects of sodium valproate in mice and rats at midgestation and at term. Teratog Carcinog Mutagen 1996; 16:97-108.
11. Okada A, Kurihara H, Aoki Y, Bialer M, Fujiwara M. Amidic modification of valproic acid reduces skeletal teratogenicity in mice. Birth Defects Res Part B Dev Reprod Toxicol 2004; 71:47-53.
12. Kawanishi CY, Hartig P, Bobseine KL, Schmid J, Cardon M, Massenburg G, et al. Axial skeletal and Hox expression domain alterations induced by retinoic acid, valproic acid, and bromoxynil during murine development. J Biochem Mol Toxicol 2003; 17:346-356.
13. Menegola E, Broccia ML, Prati M, Giavini E. Stage-dependent skeletal malformations induced by valproic acid in rat. Int J Dev Biol 1998; 42:99-102.
14. Menegola E, Broccia ML, Prati M, Giavini E. Morphological alterations induced by sodium valproate on somites and spinal nerves in rat embryos. Teratology 1999; 59:110-119.
15. Tam PP. The control of somitogenesis in mouse embryos. J Embryol Exp Morphol 1981; 65(suppl):103-128.
16. Aulehla A, Herrmann BG. Segmentation in vertebrates: clock and gradient finally joined. Genes Dev 2004; 18:2060-2067.
17. Maroto M, Pourquie O. A molecular clock involved in somite segmentation. Curr Top Dev Biol 2001; 51:221-248.
18. Galis F. Why do almost all mammals have seven cervical vertebrae? Developmental constraints, Hox genes, and cancer. J Exp Zool 1999; 285:19-26.
19. Faiella A, Wernig M, Consalez GG, Hostick U, Hofmann C, Hustert E, et al. A mouse model for valproate teratogenicity: parental effects, homeotic transformations, and altered HOX expression. Hum Mol Genet 2000; 9:227-236.
20. Finnell RH. Genetic differences in susceptibility to anticonvulsant drug-induced developmental defects. Pharmacol Toxicol 1991; 69:223-227.
21. Finnell RH, Bennett GD, Karras SB, Mohl VK. Common hierarchies of susceptibility to the induction of neural tube defects in mouse embryos by valproic acid and its 4-propyl-4-pentenoic acid metabolite. Teratology 1988; 38:313-320.
22. Snell G, Fekete E, Hummel K. The relation of mating, ovulation and the estrus smear in the house mouse to the time of day. Anat Rec 1948; 76:30-54.
23. Lundberg YW, Cabrera RM, Greer KA, Zhao J, Garg R, Finnell RH. Mapping a chromosomal locus for valproic acid-induced exencephaly in mice. Mamm Genome 2004; 15:361-369.
24. Kappen C, Mello MA, Finnell RH, Salbaum JM. Folate modulates Hox gene-controlled skeletal phenotypes. Genesis 2004; 39:155-166.
25. Eberwine J, Yeh H, Miyashiro K, Cao Y, Nair S, Finnell RH, et al. Analysis of gene expression in single live neurons. Proc Natl Acad Sci USA 1992; 89:3010-3014.
26. Vinciotti V, Khanin R, D'Alimonte D, Liu X, Cattini N, Hotchkiss G, et al. An experimental evaluation of a loop versus a reference design for two-channel microarrays. Bioinformatics 2005; 21:492-501.
27. Diehn M, Sherlock G, Binkley G, Jin H, Matese JC, Hernandez-Boussard T, et al. SOURCE: a unified genomic resource of functional annotations, ontologies, and gene expression data. Nucl Acids Res 2003; 31:219-223.
28. Zeeberg BR, Feng W, Wang G, Wang MD, Fojo AT, Sunshine M, et al. GoMiner: a resource for biological interpretation of genomic and proteomic data. Genome Biol 2003; 4:R28.
29. Wery N, Narotsky MG, Pacico N, Kavlock RJ, Picard JJ, Gofflot F. Defects in cervical vertebrae in boric acid-exposed rat embryos are associated with anterior shifts of hox gene expression domains. Birth Defects Res Part A Clin Mol Teratol 2003; 67:59-67.
30. van den Akker E, Fromental-Ramain C, de Graaff W, Le Mouellic H, Brulet P, Chambon P, et al. Axial skeletal patterning in mice lacking all paralogous groups Hox genes. Development 2001; 128:1911-1921.
31. de la Cruz CC, Der-Avakian A, Spyropoulos DD, Tieu DD, Carpenter EM. Targeted disruption of Hoxd9 and Hoxd10 alters locomotor behavior, vertebral identity, and peripheral nervous system development. Dev Biol 1999; 216:595-610.
32. Lohnes D, Mark M, Mendelsohn C, Dolle P, Decimo D, LeMeur M, et al. Developmental roles of the retinoic acid receptors. J Steroid Biochem Mol Biol 1995; 53:475-486.
33. Kultima K, Nystrom AM, Scholz B, Gustafson AL, Dencker L, Stigson M. Valproic acid teratogenicity: a toxicogenomics approach. Environ Health Perspect 2004; 112:1225-1235.
34. Giavini E, Menegola E. Gene-teratogen interactions in chemically induced congenital malformations. Biol Neonate 2004; 85:73-81.
35. Finnell RH, Waes JG, Eudy JD, Rosenquist TH. Molecular basis of environmentally induced birth defects. Annu Rev Pharmacol Toxicol 2002; 42:181-208.
36. Gottlicher M, Minucci S, Zhu P, Kramer OH, Schimpf A, Giavara S, et al. Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. Embo J 2001; 20:6969-6978.
37. Gottlicher M. Valproic acid: an old drug newly discovered as inhibitor of histone deacetylases. Ann Hematol 2004; 83(suppl 1):91-92.
38. Yildirim E, Zhang Z, Uz T, Chen CQ, Manev R, Manev H. Valproate administration to mice increases histone acetylation and 5-lipoxygenase content in the hippocampus. Neurosci Lett 2003; 345:141-143.
39. Kanai H, Sawa A, Chen RW, Leeds P, Chuang DM. Valproic acid inhibits histone deacetylase activity and suppresses excitotoxicity-induced GAPDH nuclear accumulation and apoptotic death in neurons. Pharmacogenomics J 2004; 4:336-344.
40. Phiel CJ, Zhang F, Huang EY, Guenther MG, Lazar MA, Klein PS. Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J Biol Chem 2001; 276:36734-36741.
41. Ahringer J. NuRD and SIN3 histone deacetylase complexes in development. Trends Genet 2000; 16:351-356.
42. Luo J, Su F, Chen D, Shiloh A, Gu W. Deacetylation of p53 modulates its effect on cell growth and apoptosis. Nature 2000; 408:377-381.
43. Zhang Y, Iratni R, Erdjument-Bromage H, Tempst P, Reinberg D. Histone deacetylases and SAP18, a novel polypeptide, are components of a human Sin3 complex. Cell 1997; 89:357-364.
44. Loyola A, Almouzni G. Histone chaperones, a supporting role in the limelight. Biochim Biophys Acta 2004; 1677:3-11.
45. Nicolas E, Ait-Si-Ali S, Trouche D. The histone deacetylase HDAC3 targets RbAp48 to the retinoblastoma protein. Nucleic Acids Res 2001; 29:3131-3136.
46. Lai A, Kennedy BK, Barbie DA, Bertos NR, Yang XJ, Theberge MC, et al. RBP1 recruits the mSIN3-histone deacetylase complex to the pocket of retinoblastoma tumor suppressor family proteins found in limited discrete regions of the nucleus at growth arrest. Mol Cell Biol 2001; 21:2918-2932.
47. Nicolas E, Morales V, Magnaghi-Jaulin L, Harel-Bellan A, Richard-Foy H, Trouche D. RbAp48 belongs to the histone deacetylase complex that associates with the retinoblastoma protein. J Biol Chem 2000; 275:9797-9804.
48. Ch'ng Q, Kenyon C. egl-27 generates anteroposterior patterns of cell fusion in C. elegans by regulating Hox gene expression and Hox protein function. Development 1999; 126:3303-3312.
49. Glick RD, Swendeman SL, Coffey DC, Rifkind RA, Marks PA, Richon VM, et al. Hybrid polar histone deacetylase inhibitor induces apoptosis and CD95/CD95 ligand expression in human neuroblastoma. Cancer Res 1999; 59:4392-4399.
50. Kuefer R, Hofer MD, Altug V, Zorn C, Genze F, Kunzi-Rapp K, et al. Sodium butyrate and tributyrin induce in vivo growth inhibition and apoptosis in human prostate cancer. Br J Cancer 2004; 90:535-541.
51. Mitsiades CS, Mitsiades NS, McMullan CJ, Poulaki V, Shringarpure R, Hideshima T, et al. Transcriptional signature of histone deacetylase inhibition in multiple myeloma: biological and clinical implications. Proc Natl Acad Sci USA 2004; 101:540-545.
52. Zhao Q, Boschelli F, Caplan AJ, Arndt KT. Identification of a conserved sequence motif that promotes Cdc37 and cyclin D1 binding to Cdk4. J Biol Chem 2004; 279:12560-12564.
53. Bunnell BA, Heath LS, Adams DE, Lahti JM, Kidd VJ. Increased expression of a 58-kDa protein kinase leads to changes in the CHO cell cycle. Proc Natl Acad Sci USA 1990; 87:7467-7471.
54. Harbour JW, Luo RX, Dei Santi A, Postigo AA, Dean DC. Cdk phosphorylation triggers sequential intramolecular interactions that progressively block Rb functions as cells move through G1. Cell 1999; 98:859-869.
55. Xiao B, Smerdon SJ, Jones DH, Dodson GG, Soneji Y, Aitken A, et al. Structure of a 14-3-3 protein and implications for coordination of multiple signalling pathways. Nature 1995; 376:188-191.
56. Sato S, Fujita N, Tsuruo T. Regulation of kinase activity of 3-phosphoinositide-dependent protein kinase-1 by binding to 14-3-3. J Biol Chem 2002; 277:39360-39367.
57. Brouns MR, Matheson SF, Hu KQ, Delalle I, Caviness VS, Silver J, et al. The adhesion signaling molecule p190 RhoGAP is required for morphogenetic processes in neural development. Development 2000; 127:4891-4903.
58. Del Sal G, Ruaro ME, Philipson L, Schneider C. The growth arrest-specific gene, gas1, is involved in growth suppression. Cell 1992; 70:595-607
59. Cobourne MT, Miletich I, Sharpe PT. Restriction of sonic hedgehog signalling during early tooth development. Development 2004; 131:2875-2885.
60. Miller LD, Lee KC, Mochly-Rosen D, Cartwright CA. RACK1 regulates Src-mediated Sam68 and p190RhoGAP signaling. Oncogene 2004; 23:5682-5686.
61. Balch WE, Kahn RA, Schwaninger R. ADP-ribosylation factor is required for vesicular trafficking between the endoplasmic reticulum and the cis-Golgi compartment. J Biol Chem 1992; 267:13053-13061.
62. Olkkonen VM, Peterson JR, Dupree P, Lutcke A, Zerial M, Simons K. Isolation of a mouse cDNA encoding Rab23, a small novel GTPase expressed predominantly in the brain. Gene 1994; 138:207-211.
63. Evans TM, Ferguson C, Wainwright BJ, Parton RG, Wicking C. Rab23, a negative regulator of hedgehog signaling, localizes to the plasma membrane and the endocytic pathway. Traffic 2003; 4:869-884.
64. Eggenschwiler JT, Espinoza E, Anderson KV. Rab23 is an essential negative regulator of the mouse Sonic hedgehog signalling pathway. Nature 2001; 412:194-198.
65. Shippy R, Sendera TJ, Lockner R, Palaniappan C, Kaysser-Kranich T, Watts G, et al. Performance evaluation of commercial short-oligonucleotide microarrays and the impact of noise in making cross-platform correlations. BMC Genomics 2004; 5:61.
66. Spiess AN, Mueller N, Ivell R. Amplified RNA degradation in T7-amplification methods results in biased microarray hybridizations. BMC Genomics 2003; 4:44.
67. Horan GS, Wu K, Wolgemuth DJ, Behringer RR. Homeotic transformation of cervical vertebrae in Hoxa-4 mutant mice. Proc Natl Acad Sci USA 1994; 91:12644-12648.