Valproic Acid Induces the Hyperacetylation of P53, Expression of P53 Target Genes, and Markers of the Intrinsic Apoptotic Pathway in Midorganogenesis Murine Limbs

Birth Defects Research Part B - Developmental and Reproductive Toxicology

Volumn 104, Issue 5, 2015, Pages 177-183

  Paradis, France Hélène ^a   Hales, Barbara F ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Apoptosis; HDAC inhibitor; Limb; P53; Valproic acid; Valpromide

Indexed keywords

BIOLOGICAL MARKER; CASPASE 3; CASPASE 9; CYCLIN DEPENDENT KINASE INHIBITOR 1A; HISTONE H2AX; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BCL 2; PROTEIN P21; PROTEIN P53; SURVIVIN; VALPROIC ACID; VALPROMIDE; GAMMA-H2AX PROTEIN, MOUSE; HISTONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL CULTURE; CONCENTRATION (PARAMETERS); DISEASE MARKER; DNA DAMAGE; FEMALE; FORELIMB; GENE TARGETING; GESTATIONAL AGE; IN VITRO STUDY; LIMB DEVELOPMENT; MOUSE; NONHUMAN; ORGANOGENESIS; PRIORITY JOURNAL; PROTEIN ACETYLATION; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; TERATOGENICITY; ACETYLATION; ANALOGS AND DERIVATIVES; ANIMAL; DRUG EFFECTS; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; LIMB; METABOLISM; PHOSPHORYLATION;

ACETYLATION; ANIMALS; APOPTOSIS; BIOMARKERS; CASPASE 3; CASPASE 9; EXTREMITIES; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HISTONES; MICE; ORGANOGENESIS; PHOSPHORYLATION; POLY(ADP-RIBOSE) POLYMERASES; TUMOR SUPPRESSOR PROTEIN P53; VALPROIC ACID;

EID: 84944441490     PISSN: 15429733     EISSN: 15429741     Source Type: Journal    
DOI: 10.1002/bdrb.21149     Document Type: Article

References (38)

1. Ali-Khan SE, Hales BF. 2003. Caspase-3 mediates retinoid-induced apoptosis in the organogenesis-stage mouse limb. Birth Defects Res A Clin Mol Teratol 67(10):848-860.
2. Bodiford A, Bodge M, Talbott MS, Reddy NM. 2014. Profile of belinostat for the treatment of relapsed or refractory peripheral T-cell lymphoma. Onco Targets Ther 7:1971-1977.
3. Bowden CL. 2009. Anticonvulsants in bipolar disorders: current research and practice and future directions. Bipolar Disord 11(Suppl 2):20-33.
4. Cipro S, Hrebackova J, Hrabeta J, Poljakova J, Eckschlager T. 2012. Valproic acid overcomes hypoxia-induced resistance to apoptosis. Oncol Rep 27(4):1219-1226.
5. Dayan C, Hales BF. 2014. Effects of ethylene glycol monomethyl ether and its metabolite, 2-methoxyacetic acid, on organogenesis stage mouse limbs in vitro. Birth Defects Res B Dev Reprod Toxicol 101(3):254-261.
6. Di Renzo F, Broccia ML, Giavini E, Menegola E. 2010. VPA-related axial skeletal defects and apoptosis: a proposed event cascade. Reprod Toxicol 29(1):106-112.
7. Evers S. 2008. Treatment of migraine with prophylactic drugs. Exp Opin Pharmacother 9(15):2565-2573.
8. Fantauzzo KA, Soriano P. 2014. PI3K-mediated PDGFRalpha signaling regulates survival and proliferation in skeletal development through p53-dependent intracellular pathways. Genes Dev 28(9):1005-1017.
9. Fortson WS, Kayarthodi S, Fujimura Y, Xu H, Matthews R, Grizzle WE, Rao VN, Bhat GK, Reddy ES. 2011. Histone deacetylase inhibitors, valproic acid and trichostatin-A induce apoptosis and affect acetylation status of p53 in ERG-positive prostate cancer cells. Int J Oncol 39(1):111-119.
10. Glozak MA, Sengupta N, Zhang X, Seto E. 2005. Acetylation and deacetylation of non-histone proteins. Gene 363:15-23.
11. Hamard PJ, Barthelery N, Hogstad B, Mungamuri SK, Tonnessen CA, Carvajal LA, Senturk E, Gillespie V, Aaronson SA, Merad M, Manfredi JJ. 2013. The C terminus of p53 regulates gene expression by multiple mechanisms in a target- and tissue-specific manner in vivo. Genes Dev 27(17):1868-1885.
12. Huang C, Hales BF. 2002. Role of caspases in murine limb bud cell death induced by 4-hydroperoxycyclophosphamide, an activated analog of cyclophosphamide. Teratology 66(6):288-299.
13. Johannessen CU, Johannessen SI. 2003. Valproate: past, present, and future. CNS Drug Rev 9(2):199-216.
14. Jonkers J, Meuwissen R, van der Gulden H, Peterse H, van der Valk M, Berns A. 2001. Synergistic tumor suppressor activity of BRCA2 and p53 in a conditional mouse model for breast cancer. Nat Genet 29(4):418-425.
15. Lagneaux L, Gillet N, Stamatopoulos B, Delforge A, Dejeneffe M, Massy M, Meuleman N, Kentos A, Martiat P, Willems L, Bron D. 2007. Valproic acid induces apoptosis in chronic lymphocytic leukemia cells through activation of the death receptor pathway and potentiates TRAIL response. Exp Hematol 35(10):1527-1537.
16. Lavin MF, Gueven N. 2006. The complexity of p53 stabilization and activation. Cell Death Differ 13(6):941-950.
17. Liu L, Scolnick DM, Trievel RC, Zhang HB, Marmorstein R, Halazonetis TD, Berger SL. 1999. p53 sites acetylated in vitro by PCAF and p300 are acetylated in vivo in response to DNA damage. Mol Cell Biol 19(2):1202-1209.
18. Liu G, Terzian T, Xiong S, van Pelt CS, Audiffred A, Box NF, Lozano G. 2007. The p53-Mdm2 network in progenitor cell expansion during mouse postnatal development. J Pathol 213(4):360-368.
19. Luo J, Su F, Chen D, Shiloh A, Gu W. 2000. Deacetylation of p53 modulates its effect on cell growth and apoptosis. Nature 408(6810):377-381.
20. Mallela M, Hrubec T. 2012. Reduction in valproic acid-induced neural tube defects by maternal immune stimulation: role of apoptosis. Birth Defects Res B Dev Reprod Toxicol 95(4):296-303.
21. McCormack E, Haaland I, Venas G, Forthun RB, Huseby S, Gausdal G, Knappskog S, Micklem DR, Lorens JB, Bruserud O, Gjertsen BT. 2012. Synergistic induction of p53 mediated apoptosis by valproic acid and nutlin-3 in acute myeloid leukemia. Leukemia 26(5):910-917.
22. Mellert HS, Stanek TJ, Sykes SM, Rauscher FJ, 3rd, Schultz DC, McMahon SB. 2011. Deacetylation of the DNA-binding domain regulates p53-mediated apoptosis. J Biol Chem 286(6):4264-4270.
23. Menegola E, Di Renzo F, Broccia ML, Giavini E. 2006. Inhibition of histone deacetylase as a new mechanism of teratogenesis. Birth Defects Res C Embryo Today 78(4):345-353.
24. Meunier H, Carraz G, Neunier Y, Eymard P, Aimard M. 1963. [Pharmacodynamic properties of N-dipropylacetic acid]. Therapie 18:435-438.
25. Montes de Oca Luna R, Wagner DS, Lozano G. 1995. Rescue of early embryonic lethality in mdm2-deficient mice by deletion of p53. Nature 378(6553):203-206.
26. Nau H, Scott WJ, Jr. 1986. Weak acids may act as teratogens by accumulating in the basic milieu of the early mammalian embryo. Nature 323(6085):276-278.
27. Paradis FH, Hales BF. 2013. Exposure to valproic acid inhibits chondrogenesis and osteogenesis in mid-organogenesis mouse limbs. Toxicol Sci 131(1):234-241.
28. Paradis FH, Hales BF. 2015. The effects of class-specific histone deacetylase inhibitors on the development of limbs during organogenesis. Toxicol Sci Aug 6 pii: kfv174.
29. Paradis FH, Huang C, Hales BF. 2012. The murine limb bud in culture as an in vitro teratogenicity test system. Methods Mol Biol 889:197-213.
30. Peck B, Chen CY, Ho KK, Di Fruscia P, Myatt SS, Coombes RC, Fuchter MJ, Hsiao CD, Lam EW. 2010. SIRT inhibitors induce cell death and p53 acetylation through targeting both SIRT1 and SIRT2. Mol Cancer Ther 9(4):844-855.
31. Rangwala S, Zhang C, Duvic M. 2012. HDAC inhibitors for the treatment of cutaneous T-cell lymphomas. Future Med Chem 4(4):471-486.
32. Richardson L, Venkataraman S, Stevenson P, Yang Y, Moss J, Graham L, Burton N, Hill B, Rao J, Baldock RA, Armit C. 2014. EMAGE mouse embryo spatial gene expression database: 2014 update. Nucleic Acids Res 42(Database issue):D835-D844.
33. Rogakou EP, Nieves-Neira W, Boon C, Pommier Y, Bonner WM. 2000. Initiation of DNA fragmentation during apoptosis induces phosphorylation of H2AX histone at serine 139. J Biol Chem 275(13):9390-9395.
34. Shankar S, Srivastava RK. 2008. Histone deacetylase inhibitors: mechanisms and clinical significance in cancer: HDAC inhibitor-induced apoptosis. Adv Exp Med Biol 615:261-298.
35. Tung EW, Winn LM. 2011. Valproic acid increases formation of reactive oxygen species and induces apoptosis in postimplantation embryos: a role for oxidative stress in valproic acid-induced neural tube defects. Mol Pharmacol 80(6):979-987.
36. Vajda FJ, Eadie MJ. 2005. Maternal valproate dosage and foetal malformations. Acta Neurol Scand 112(3):137-143.
37. van den Berg RJ, Kok P, Voskuyl RA. 1993. Valproate and sodium currents in cultured hippocampal neurons. Exp Brain Res 93(2):279-287.
38. Voso MT, Santini V, Finelli C, Musto P, Pogliani E, Angelucci E, Fioritoni G, Alimena G, Maurillo L, Cortelezzi A, Buccisano F, Gobbi M, Borin L, Di Tucci A, Zini G, Petti MC, Martinelli G, Fabiani E, Fazi P, Vignetti M, Piciocchi A, Liso V, Amadori S, Leone G. 2009. Valproic acid at therapeutic plasma levels may increase 5-azacytidine efficacy in higher risk myelodysplastic syndromes. Clin Cancer Res 15(15):5002-5007.