Reduction in Valproic Acid-Induced Neural Tube Defects by Maternal Immune Stimulation: Role of Apoptosis

Birth Defects Research Part B - Developmental and Reproductive Toxicology

Volumn 95, Issue 4, 2012, Pages 296-303

  Mallela, Mural ^a   Hrubec, Theresa ^b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EDWARD VIA COLLEGE OF OSTEOPATHIC MEDICINE   (United States)

Author keywords

apoptosis; maternal immune stimulation; mechanisms of teratogenesis; neural tube defects

Indexed keywords

GAMMA INTERFERON; VALPROIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; FLOW CYTOMETRY; IMMUNOSTIMULATION; MALE; MATERNAL IMMUNE STIMULATION; MOUSE; NEURAL TUBE DEFECT; NEUROPROTECTION; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; TERATOGENICITY;

ANIMALS; APOPTOSIS; EMBRYO, MAMMALIAN; FEMALE; IMMUNITY; INTERFERON-GAMMA; MALE; MATERNAL EXPOSURE; MICE; NEURAL TUBE DEFECTS; PREGNANCY; VALPROIC ACID;

EID: 84865147582     PISSN: 15429733     EISSN: 15429741     Source Type: Journal    
DOI: 10.1002/bdrb.21018     Document Type: Article

References (61)

1. Bai LY, Omar HA, Chiu CF, Chi ZP, Hu JL, Weng JR. 2011. Antitumor effects of (S)-HDAC42, a phenylbutyrate-derived histone deacetylase inhibitor, in multiple myeloma cells. Cancer Chemother Pharmacol 68(2):489-96.
2. Barrier M, Dix DJ, Mirkes PE. 2009. Inducible 70 kDa heat shock proteins protect embryos from teratogen-induced exencephaly: analysis using Hspa1a/a1b knockout mice. Birth Defects Res A Clin Mol Teratol 85(8):732-740.
3. Byun SS, Kim FJ, Khandrika L, Kumar B, Koul S, Wilson S, Koul HK. 2009. Differential effects of valproic acid on growth, proliferation and metastasis in HTB5 and HTB9 bladder cancer cell lines. Cancer Lett 281(2):196-202.
4. Cansu A, Erdogan D, Serdaroglu A, Take G, Coskun ZK, Gurgen SG. 2010. Histologic and morphologic effects of valproic acid and oxcarbazepine on rat uterine and ovarian cells. Epilepsia 51(1):98-107.
5. Chen B, Cyr DG, Hales BF. 1994. Role of apoptosis in mediating phosphoramide mustard-induced rat embryo malformations in vitro. Teratology 50(1):1-12.
6. Chen BY, Chang HH, Chen ST, Tsao ZJ, Yeh SM, Wu CY, Lin DP. 2009. Congenital eye malformations associated with extensive periocular neural crest apoptosis after influenza B virus infection during early embryogenesis. Mol Vis 15:2821-2828.
7. Christianson A, Howson CP, Model B. 2006. March of dimes global report, executive summary: the hidden toll of dying and disabled children. White Plains, NY: March of Dimes Foundation
8. Clayton-Smith J, Donnai D. 1995. Fetal valproate syndrome. J Med Genet 32(9):724-727.
9. Copp AJ. 2005. Neurulation in the cranial region-normal and abnormal. J Anat 207(5):623-635.
10. Dawson JE, Raymond AM, Winn LM. 2006. Folic acid and pantothenic acid protection against valproic acid-induced neural tube defects in CD-1 mice. Toxicol Appl Pharmacol 211(2):124-132.
11. Defoort EN, Kim PM, Winn LM. 2006. Valproic acid increases conservative homologous recombination frequency and reactive oxygen species formation: a potential mechanism for valproic acid-induced neural tube defects. Mol Pharmacol 69(4):1304-1310.
12. Dieterich E, Steveling A, Lukas A, Seyfeddinipur N, Spranger J. 1980. Congenital anomalies in children of epileptic mothers and fathers. Neuropediatrics 11(3):274-283.
13. 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.
14. Häcker S, Dittrich A, Mohr A, Schweitzer T, Rutkowski S, Krauss J, Debatin KM, Fulda S. 2009. Histone deacetylase inhibitors cooperate with IFN-gamma to restore caspase-8 expression and overcome TRAIL resistance in cancers with silencing of caspase-8. Oncogene 28(35):3097-3110.
15. Holladay SD, Sharova L, Smith BJ, Gogal RM Jr, Ward DL, Blaylock BL. 2000. Nonspecific stimulation of the maternal immune system. I. Effects on teratogen-induced fetal malformations. Teratology 62(6):413-419.
16. Hrubec TC, Yan M, Ye, K, Salafia CM, Holladay SD. 2006a. Valproic acid induced fetal malformations are reduced by maternal immune stimulation with granulocyte macrophage colony-stimulating factor or interferon. Anat Rec A 288A:1303-1309.
17. Hrubec TC, Prater MR, Toops KA, Holladay SD. 2006b. Reduction in diabetes-induced craniofacial defects by maternal immune stimulation. Birth Defects Res B Dev Reprod Toxicol 77(1):1-9.
18. Hrubec TC, Prater MR, Mallela MK, Gogal RM, Guo TL, Holladay SD. 2012. Diverse ability of maternal immune stimulation to reduce birth defects in mice exposed to teratogens: a review. J Dev Origins Health Dis 3:132-139.
19. Hsu CY, Chang NC, Lee MW, Lee KH, Sun DS, Lai C, Chang AC. 2008. LUZP deficiency affects neural tube closure during brain development. Biochem Biophys Res Commun 376(3):466-471.
20. Hubaux R, Vandermeers F, Crisanti MC, Kapoor V, Burny A, Mascaux C, Albelda SM, Willems L. 2010. Preclinical evidence for a beneficial impact of valproate on the response of small cell lung cancer to first-line chemotherapy. Eur J Cancer 46(9):1724-1734.
21. Jergil M, Kultima K, Gustafson AL, Dencker L, Stigson M. 2009. Valproic acid-induced deregulation in vitro of genes associated in vivo with neural tube defects. Toxicol Sci 108(1):132-148.
22. Jiang B, Kumar SD, Loh WT, Manikandan J, Ling EA, Tay SS, Dheen ST. 2008. Global gene expression analysis of cranial neural tubes in embryos of diabetic mice. J Neurosci Res 86(16):3481-3493.
23. Khaksary Mahabady M, Ranjbar R, Arzi A, Papahn AA, Najafzadeh H. 2006. A comparison study of effects of Echinacea extract and levamisole on phenytoin-induced cleft palate in mice. Regul Toxicol Pharmacol 46(3):163-166.
24. Kisseberth WC, Murahari S, London CA, Kulp SK, Chen CS. 2008. Evaluation of the effects of histone deacetylase inhibitors on cells from canine cancer cell lines. Am J Vet Res 69(7):938-945.
25. Kostrouchova M, Kostrouch Z. 2007. Valproic acid, a molecular lead to multiple regulatory pathways. Folia Biol (Praha) 53(2):37-49.
26. Kultima K, Nystrom AM, Scholz B, Gustafson AL, Dencker L, Stigson M. 2004. Valproic acid teratogenicity: a toxicogenomics approach. Environ Health Perspect 112(12):1225-1235.
27. Latorre AO, Hueza IM, Gorniak SL. 2007. Association of Ipomoea carnea and BCG reduces birth defects caused by cyclophosphamide in rats. Life Sci 80(5):430-435.
28. Laudermilch CL, Holladay SD, Sponenberg DP, Saunders GK, Ward DL, Prater MR. 2005. Placental improvement and reduced distal limb defects by maternal interferon-gamma injection in methylnitrosourea-exposed mice. Birth Defects Res A Clin Mol Teratol 73(9):597-604.
29. Lee JY, Bowden DS. 2000. Rubella virus replication and links to teratogenicity. Clin Microbiol Rev 13(4):571-587.
30. Levy RR, Cordonier H, Czyba JC, Guerin JF. 2001. Apoptosis in preimplantation mammalian embryo and genetics. Ital J Anat Embryol 106(2 Suppl 2):101-108.
31. Li Y, Chen X, Zhao X, Hu B. 1999. Relationship between homocysteine-induced apoptosis and teratogenesis in developing avian embryo. Wei Sheng Yan Jiu 28(5):275-278.
32. Li Y, Yu Z, Zhu H. 1998. Role of programmed cell death in mediating arsenic-induced rat embryo anomalies. Wei Sheng Yan Jiu 27(2):91-94.
33. Massa V, Savery D, Ybot-Gonzalez P, Ferraro E, Rongvaux A, Cecconi F, Flavell R, Greene ND, Copp AJ. 2009. Apoptosis is not required for mammalian neural tube closure. Proc Natl Acad Sci USA 106(20):8233-8238.
34. Nau H, Hauck RS, Ehlers K. 1991. Valproic acid-induced neural tube defects in mouse and human: aspects of chirality, alternative drug development, pharmacokinetics and possible mechanisms. Pharmacol Toxicol 69(5):310-321.
35. Nomura T, Hata S, Kusafuka T. 1990. Suppression of developmental anomalies by maternal macrophages in mice. J Exp Med 172(5):1325-1330.
36. Okada A, Kushima K, Aoki Y, Bialer M, Fujiwara M. 2005. Identification of early-responsive genes correlated to valproic acid-induced neural tube defects in mice. Birth Defects Res A Clin Mol Teratol 73(4):229-238.
37. Oyama K, Sugimura Y, Murase T, Uchida A, Hayasaka S, Oiso Y, Murata Y. 2009. Folic acid prevents congenital malformations in the offspring of diabetic mice. Endocr J 56(1):29-37.
38. Papi A, Ferreri AM, Rocchi P, Guerra F, Orlandi M. 2010. Epigenetic modifiers as anticancer drugs: effectiveness of valproic acid in neural crest-derived tumor cells. Anticancer Res 30(2):535-540.
39. Pei XY, Dai Y, Grant S. 2004. Synergistic induction of oxidative injury and apoptosis in human multiple myeloma cells by the proteasome inhibitor bortezomib and histone deacetylase inhibitors. Clin Cancer Res 10(11):3839-3852.
40. Prater MR, Zimmerman KL, Ward DL, Holladay SD. 2004. Reduced birth defects caused by maternal immune stimulation in methylnitrosourea-exposed mice: association with placental improvement. Birth Defects Res A Clin Mol Teratol 70(11):862-869.
41. Punareewattana K, Holladay SD. 2004. Immunostimulation by complete Freund's adjuvant, granulocyte macrophage colony-stimulating factor, or interferon-gamma reduces severity of diabetic embryopathy in ICR mice. Birth Defects Res A Clin Mol Teratol 70(1):20-27.
42. Sabapathy K, Jochum W, Hochedlinger K, Chang L, Karin M, Wagner EF. 1999. Defective neural tube morphogenesis and altered apoptosis in the absence of both JNK1 and JNK2. Mech Dev 89(1-2):115-124.
43. Sarkar SA, Sharma RP. 2002. Expression of c-Myc and other apoptosis-related genes in Swiss Webster mouse fetuses after maternal exposure to all trans-retinoic acid. Reprod Toxicol 16(3):245-252.
44. Savion S, Kamshitsky-Feldman A, Ivnitsky I, Orenstein H, Shepshelovich J, Carp H, Fein A, Torchinsky A, Toder V. 2003. Potentiation of the maternal immune system may modify the apoptotic process in embryos exposed to developmental toxicants. Am J Reprod Immunol 49(1):30-41.
45. Schluter G. 1973. Ultrastructural observations on cell necrosis during formation of the neural tube in mouse embryos. Z Anat Entwicklungsgesch 141(3):251-264.
46. Sharova L, Sura P, Smith BJ, Gogal RM, Jr., Sharov AA, Ward DL, Holladay SD. 2000. Nonspecific stimulation of the maternal immune system. II. Effects on gene expression in the fetus. Teratology 62(6):420-428.
47. Sharova LV, Sharov AA, Sura P, Gogal RM, Smith BJ, Holladay SD. 2003. Maternal immune stimulation reduces both placental morphologic damage and down-regulated placental growth-factor and cell cycle gene expression caused by urethane: are these events related to reduced teratogenesis? Int Immunopharmacol 3(7):945-955.
48. Shim M, Foley J, Anna C, Mishina Y, Eling T. 2010. Embryonic expression of cyclooxygenase-2 causes malformations in axial skeleton. J Biol Chem 285(21):16206-16217.
49. Shirane M, Ogawa M, Motoyama J, Nakayama KI. 2008. Regulation of apoptosis and neurite extension by FKBP38 is required for neural tube formation in the mouse. Genes Cells 13(6):635-651.
50. Singh G, Sinha N, Koushik CJ, Mathur SK, Srivastava S. 2005. Detecting role of apoptosis in mediating cyclophosphamide induced teratogenesis in vitro. Toxicol Mech Methods 15(6):391-397.
51. Singh G, Sinha N, Mahipag GS. 2009. Role of apoptosis in mediating salicylic acid-induced teratogenesis in vitro. Toxicol Mech Methods 19(2):161-168.
52. Singh G, Kumar A, Sinha N. 2011. Studying significance of apoptosis in mediating tolbutamide-induced teratogenesis in vitro. Fundam Clin Pharmacol. doi: 10.1111/j.1472-8206.2011.00946.x.[Epub ahead of print].
53. Sugimura Y, Murase T, Oyama K, Uchida A, Sato N, Hayasaka S, Kano Y, Takagishi Y, Hayashi Y, Oiso Y, Murata Y. 2009. Prevention of neural tube defects by loss of function of inducible nitric oxide synthase in fetuses of a mouse model of streptozotocin-induced diabetes. Diabetologia 52(5):962-971.
54. Sulik KK, Cook CS, Webster WS. 1988. Teratogens and craniofacial malformations: relationships to cell death. Development 103(Suppl):213-231.
55. Toder V, Savion S, Gorivodsky M, Shepshelovich J, Zaslavsky Z, Fein A, Torchinsky A. 1996. Teratogen-induced apoptosis may be affected by immunopotentiation. J Reprod Immunol 30(2-3):173-185.
56. Torchinsky A, Savion S, Gorivodsky M, Shepshelovich J, Zaslavsky Z, Fein A, Toder V. 1995. Cyclophosphamide-induced teratogenesis in ICR mice: the role of apoptosis. Teratog Carcinog Mutagen 15(4):179-190.
57. 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.
58. Voisard R, Krebs R, Baur R, Hombach V. 2010. Valproic acid inhibits proliferation of human coronary vascular cells (SI/MPL-ratio: 0.5): a novel candidate for systemic and local therapy of postinterventional restenosis. Coron Artery Dis 21(5):286-291.
59. Wong RL, Wlodarczyk BJ, Min KS, Scott ML, Kartiko S, Yu W, Merriweather MY, Vogel P, Zambrowicz BP, Finnell RH. 2008. Mouse Fkbp8 activity is required to inhibit cell death and establish dorso-ventral patterning in the posterior neural tube. Hum Mol Genet 17(4):587-601.
60. Yitzhakie D, Torchinsky A, Savion S, Toder V. 1999. Maternal immunopotentiation affects the teratogenic response to hyperthermia. J Reprod Immunol 45(1):49-66.
61. Zhao Y, Tan J, Zhuang L, Jiang X, Liu ET, Yu Q. 2005. Inhibitors of histone deacetylases target the Rb-E2F1 pathway for apoptosis induction through activation of proapoptotic protein Bim. Proc Natl Acad Sci USA 102(44):16090-16095.