Perturbation of retinoic acid (RA)-mediated limb development suggests a role for diminished RA signaling in the teratogenesis of ethanol

Birth Defects Research Part A - Clinical and Molecular Teratology

Volumn 79, Issue 9, 2007, Pages 631-641

  Johnson, Corey S ^a   Zucker, Robert M ^b   Hunter III, Edward Sidney ^b,c   Sulik, Kathleen K ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^c NHEERL ^*  (United States)

Author keywords

Ethanol; Fetal alcohol spectrum disorders; Limb defects; Limb development; Retinoic acid

Indexed keywords

ALCIAN BLUE; ALCOHOL; ALIZARIN RED S; BMS 189453; DISULFIRAM; DYE; NILE BLUE SULFATE; RECEPTOR BLOCKING AGENT; RETINOIC ACID; RETINOIC ACID RECEPTOR INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CONTROLLED STUDY; DISEASE MODEL; FORELIMB; GENE; GENETIC TRANSCRIPTION; GESTATIONAL AGE; IN SITU HYBRIDIZATION; LIMB DEFECT; LIMB DEVELOPMENT; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRENATAL EXPOSURE; PRIORITY JOURNAL; RISK FACTOR; SHH GENE; TBX5 GENE; TERATOGENESIS; VITAL STAIN;

ABNORMALITIES, DRUG-INDUCED; ANIMALS; CELL DEATH; ETHANOL; FEMALE; HEDGEHOG PROTEINS; IN SITU HYBRIDIZATION; LIMB DEFORMITIES, CONGENITAL; MICE; POLYMERASE CHAIN REACTION; PREGNANCY; RNA, MESSENGER; SIGNAL TRANSDUCTION; T-BOX DOMAIN PROTEINS; TERATOGENS; TRETINOIN;

MUS;

EID: 34848832404     PISSN: 15420752     EISSN: 15420760     Source Type: Journal    
DOI: 10.1002/bdra.20385     Document Type: Article

References (55)

1. Ahlgren SC, Thakur V, Bronner-Fraser M. 2002. Sonic hedgehog rescues cranial neural crest from cell death induced by ethanol exposure. Proc Natl Acad Sci USA 99:10476-10481.
2. Ali-Khan SE, Hales BF. 2006. Novel Retinoid Targets in the Mouse Limb during Organogenesis. Toxicol Sci 94:139-152.
3. Allen RT, Hunter WJ 3rd, Agrawal DK. 1997. Morphological and biochemical characterization and analysis of apoptosis. J Pharmacol Toxicol Meth 37:215-228.
4. Bell SM, Schreiner CM, Goetz JA, et al. 2005. Shh signaling in limb bud ectoderm: potential role in teratogen-induced postaxial ectrodactyly. Dev Dyn 233:313-325.
5. Bell SM, Schreiner CM, Scott WJ. 1999. Disrupting the establishment of polarizing activity by teratogen exposure. Mech Dev 88:147-157.
6. Chen JY, Pento S, Ostrowski J, et al. 1995. RAR-specific agonist/antagonists which dissociate transactivation and AP1 transrepression inhibit anchorage-independent cell proliferation. EMBO J 14:1187-1197.
7. Chrisman K, Kenney R, Comin J, et al. 2004. Gestational ethanol exposure disrupts the expression of Fgf8 and Sonic hedgehog during limb patterning. Birth Defects Res A Clin Mol Teratol 70:163-171.
8. Correia KM, Conlon RA. 2001. Whole-mount in situ hybridization to mouse embryos. Methods 23:335-338.
9. Cremin BJ, Jaffer Z. 1981. Radiological aspects of the fetal alcohol syndrome. Pediatr Radiol 11:151-153.
10. Deltour L, Ang HL, Duester G. 1996. Ethanol inhibition of retinoic acid synthesis as a potential mechanism for fetal alcohol syndrome. FASEB J 10:1050-1057.
11. Duester G. 1991. A hypothetical mechanism for fetal alcohol syndrome involving ethanol inhibition of retinoic acid synthesis at the alcohol dehydrogenase step. Alcohol Clin Exp Res 15:568-572.
12. Fernandez-Teran M, Piedra ME, Kathiriya IS, et al. 2000. Role of dHand in the arterior-posterior polarization of the limb bud: implications for the Sonic hedgehog pathway. Development 127:2133-2142.
13. Froster UG, Baird PA. 1992. Congenital defects of the limbs and alcohol exposure in pregnancy: data from a population based study. Am J Med Genet 44:782-785.
14. Helms J, Thaller C, Eichele G. 1994. Relationship between retinoic acid and sonic hedgehog, two polarizing signals in the chick wing bud. Development 120:3267-3274.
15. Helms JA, Kim CH, Eichele G, et al. 1996. Retinoic acid signaling is required during early chick limb development. Development 122:1385-1394.
16. Herrmann J, Pallister PD, Opitz JM. 1980. Tetraectrodactyly and other skeletal manifestations in the fetal alcohol syndrome. Eur J Pediatr 133:221-226.
17. Jones KL, Smith DW. 1973. Recognition of the fetal alcohol syndrome in early infancy. Lancet 2:999-1001.
18. Jones KL, Smith DW, Ulleland CN, et al. 1973. Pattern of malformation in offspring of chronic alcoholic mothers. Lancet 1:1267-1271.
19. Kotch LE, Dehart DB, Alles AJ, et al. 1992. Pathogenesis of ethanol-induced limb reduction defects in mice. Teratology 46:323-332.
20. Kronick JB. 1976. Teratogenic effects of ethyl alcohol administered to pregnant mice. Am J Obstet Gynecol 124:676-680.
21. Lemoine P, Harousseau H, Borteyru JP, et al. 1968. Les enfants de parents alcooliques: Anomalies observŕes s̀ propos de 127 cas. Ouest Med 21:476-482.
22. Lewandoski M, Sun X, Martin GR. 2000. Fgf8 signalling from the AER is essential for normal limb development. Nat Genet 26:460-463.
23. Lohnes D, Mark M, Mendelsohn C, et al. 1994. Function of the retinoic acid receptors (RARs) during development (I). Craniofacial and skeletal abnormalities in RAR double mutants. Development 120:2723-2748.
24. MacLean G, Abu-Abed S, Dolle P, et al. 2001. Cloning of a novel retinoic-acid metabolizing cytochrome P450, Cyp26B1, and comparative expression analysis with Cyp26A1 during early murine development. Mech Dev 107:195-201.
25. Mahmood R, Bresnick J, Hornbruch A, et al. 1995. A role for Fgf8 in the initiation and maintenance of vertebrate limb bud outgrowth. Curr Biol 5:797-806.
26. Mic FA, Sirbu IO, Duester G. 2004. Retinoic acid synthesis controlled by Raldh2 is required early for limb bud initiation and then later as a proximodistal signal during apical ectodermal ridge formation. J Biol Chem 279:26698-26706.
27. Moon AM, Capecchi MR. 2000. Fgf8 is required for outgrowth and patterning of the limbs. Nat Genet 26:455-459.
28. Motoyama J. 2006. Essential roles of Gli3 and sonic hedgehog in pattern formation and developmental anomalies caused by their dysfunction. Congenit Anom (Kyoto) 46:123-128.
29. Niederreither K, Vermot J, Schuhbaur B, et al. 2002. Embryonic retinoic acid synthesis is required for forelimb growth and anteroposterior patterning in the mouse. Development 129:3563-3574.
30. Nora AH, Nora JJ, Blu J. 1977. Limb-reduction anomalies in infants born to Disulfiram-treated alcoholic mothers. Lancet 2:664.
31. Ohuchi H, Nakagawa T, Yamamoto A, et al. 1997. The mesenchymal factor, Fgf10, initiates and maintains the outgrowth of the chick limb bud through interaction with Fgf8, an apical ectodermal factor. Development 124:2235-2244.
32. Pullarkat RK. 1991. Hypothesis: prenatal ethanol-induced birth defects and retinoic acid. Alcohol Clin Exp Res 15:565-567.
33. Riddle RD, Johnson RL, Laufer E, et al. 1993. Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75:1401-1416.
34. Schulze GE, Clay RJ, Mezza LE, et al. 2001. BMS-189453, a novel retinoid receptor antagonist, is a potent testicular toxin. Toxicol Sci 59:297-308.
35. Scott WJ Jr, Schreiner CM, Goetz JA, et al. 2005. Cadmium-induced post-axial forelimb ectrodactyly: association with altered sonic hedgehog signaling. Reprod Toxicol 19:479-485.
36. Spiegel PG, Pekman WM, Rich BH, et al. 1979. The orthopedic aspects of the fetal alcohol syndrome. Clin Orthop Relat Res 139:58-63.
37. Stratford T, Horton C, Maden M. 1996. Retinoic acid is required for the initiation of outgrowth in the chick limb bud. Curr Biol 6:1124-1133.
38. Stratford TH, Kostakopoulou K, Maden M. 1997. Hoxb-8 has a role in establishing early anterior-posterior polarity in chick forelimb but not hindlimb. Development 124:4225-4234.
39. Sulik KK, Johnston MC, Webb MA. 1981. Fetal alcohol syndrome: embryogenesis in a mouse model. Science 214:936-938.
40. Sun X, Mariani FV, Martin GR. 2002. Functions of Fgf signalling from the apical ectodermal ridge in limb development. Nature 418:501-508.
41. Swindell EC, Thaller C, Sockanathan S, et al. 1999. Complementary domains of retinoic acid production and degradation in the early chick embryo. Dev Biol 216:282-296.
42. Tillner I, Majewski F. 1978. Furrows and dermal ridges of the hand in patients with alcohol embryopathy. Hum Genet 42:307-314.
43. Vallari RC, Pietruszko R. 1982. Human aldehyde dehydrogenase: mechanism of inhibition of Disulfiram. Science 216:637-639.
44. van Rensburg LJ. 1981. Major skeletal defects in the fetal alcohol syndrome. A case report. S Afr Med J 59:687-688.
45. Van Thiel DH, Gavaler J, Lester R. 1974. Ethanol inhibition of vitamin A metabolism in the testes: possible mechanism for sterility in alcoholics. Science 186:941-942.
46. Viljoen DL, Gossage JP, Brooke L, et al. 2005. Fetal alcohol syndrome epidemiology in a South African community: a second study of a very high prevalence area. J Stud Alcohol 66:593-604.
47. Vogel A, Rodriguez C, Izpisua-Belmonte JC. 1996. Involvement of Fgf8 in initiation, outgrowth and patterning of the vertebrate limb. Development 122:1737-1750.
48. Webster WS, Walsh DA, McEwen SE, et al. 1983. Some teratogenic properties of ethanol and acetaldehyde in C57BL/6J mice: implications for the study of the fetal alcohol syndrome. Teratology 27:231-243.
49. White JA, Beckett-Jones B, Guo YD, et al. 1997. cDNA cloning of human retinoic acid-metabolizing enzyme (hP450RAI) identifies a novel family of cytochromes P450. J Biol Chem 272:18538-18541.
50. Wilson L, Maden M. 2005. The mechanisms of dorsoventral patterning in the vertebrate neural tube. Dev Biol 282:1-13.
51. Yang L, Munoz-Medellin D, Kim HT, et al. 1999. Retinoic acid receptor antagonist BMS453 inhibits the growth of normal and malignant breast cells without activating RAR-dependent gene expression. Breast Cancer Res Treat 56:277-291.
52. Zachman RD, Grummer MA. 1998. The interaction of ethanol and vitamin A as a potential mechanism for the pathogenesis of Fetal Alcohol syndrome. Alcohol Clin Exp Res 22:1544-1556.
53. Zucker RM. 2006. Whole insect and mammalian embryo imaging with confocal microscopy: morphology and apoptosis. Cytometry A 69:1143-1152.
54. Zucker RM, Hunter ES 3rd, Rogers JM. 2000. Confocal laser scanning microscopy of morphology and apoptosis in organogenesis-stage mouse embryos. Methods Mol Biol 135:191-202.
55. Zucker RM, Jeffay SC. 2006. Confocal laser scanning microscopy of whole mouse ovaries: excellent morphology, apoptosis detection, and spectroscopy. Cytometry A 69:930-939.