Hostname: page-component-6b989bf9dc-6f5p8 Total loading time: 0.001 Render date: 2024-04-10T21:19:54.579Z Has data issue: false hasContentIssue false

Prevention of retinoic acid-induced early craniofacial abnormalities by folinic acid and expression of endothelin-/HAND in the branchial arches in mouse

Published online by Cambridge University Press:  19 February 2008

Zhaofeng Zhang
Affiliation:
Department of Nutrition & Food Hygiene, Laboratory of Molecular Toxicology and Developmental Molecular Biology, School of Public Health, Peking University, Beijing 100083, P.R. China
Yajun Xu
Affiliation:
Department of Nutrition & Food Hygiene, Laboratory of Molecular Toxicology and Developmental Molecular Biology, School of Public Health, Peking University, Beijing 100083, P.R. China
Li Li
Affiliation:
Department of Nutrition & Food Hygiene, Laboratory of Molecular Toxicology and Developmental Molecular Biology, School of Public Health, Peking University, Beijing 100083, P.R. China
Jing Han
Affiliation:
Department of Nutrition & Food Hygiene, Laboratory of Molecular Toxicology and Developmental Molecular Biology, School of Public Health, Peking University, Beijing 100083, P.R. China
Liping Zheng
Affiliation:
Department of Nutrition & Food Hygiene, Laboratory of Molecular Toxicology and Developmental Molecular Biology, School of Public Health, Peking University, Beijing 100083, P.R. China
Peng Liu
Affiliation:
Department of Nutrition & Food Hygiene, Laboratory of Molecular Toxicology and Developmental Molecular Biology, School of Public Health, Peking University, Beijing 100083, P.R. China
Yong Li*
Affiliation:
Department of Nutrition & Food Hygiene, Laboratory of Molecular Toxicology and Developmental Molecular Biology, School of Public Health, Peking University, Beijing 100083, P.R. China
*
*Corresponding author: Professor Yong Li, fax +86 10 82801177, email liyong@bjmu.edu.cn
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Prevention of retinoic acid-induced craniofacial abnormalities by folinic acid, and endothelin-1 (ET-1)/dHAND protein and mRNA expression were investigated in mouse embryos using the whole embryo culture, streptavidin–biotin peroxidase complex method, and whole-mount in situ hybridization. In the whole embryo culture, 1·0 and 0·1mm-folinic acid dose dependently prevented branchial region malformations and decreased defects by 93% and 77%, respectively. Folinic acid at concentrations of 1·0 and 0·1mm significantly increased ET-1 and dHAND protein expression levels compared to retinoic acid-exposed values in embryonic branchial areas. Folinic acid also increased ET-1 and dHAND mRNA levels in the same region. The present results suggest that folinic acid may prevent retinoic acid-induced craniofacial abnormalities via increasing ET-1 and dHAND levels in the branchial region during the organogenic period.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2006

References

Andrew, EC, Laszlo, T & Andrea, S (1999) Dose-dependent effect of folic acid on the prevention of orofacial clefts. Pediatrics 104, 6672.Google Scholar
Antony, AC & Hansen, DK (2000) Hypothesis: folate-responsive neural tube defects and neurocristopathies. Teratology 62, 4250.3.0.CO;2-U>CrossRefGoogle ScholarPubMed
Bonilla, S, Redonnet, A, Noel-Suberville, C, Pallet, V, Garcin, H & Higueret, P (2000) High-fat diets affect the expression of nuclear retinoic acid receptor in rat liver. Br J Nutr 83, 665671.CrossRefGoogle ScholarPubMed
Chang, CB & Hemmati-Brivanlou, A (1998) Cell fate determination in embryonic ectoderm. J Neurobiol 36, 128151.3.0.CO;2-3>CrossRefGoogle ScholarPubMed
Choi, SW, Friso, S, Keyes, MK & Mason, JB (2005) Folate supplementation increases genomic DNA methylation in the liver of elder rats. Br J Nutr 93, 3135.CrossRefGoogle ScholarPubMed
Clagett-Dame, M & Deluca, HF (2002) The role of vitamin A in mammalian reproduction and embryonic development. Annu Rev Nutr 22, 347381.CrossRefGoogle ScholarPubMed
Clouthier, DE, Williams, SC, Yanagisawa, H, Wieduwilt, M, Richardson, JA & Yanagisawa, M (2000) Signaling pathways crucial for craniofacial development revealed by endothelin-A receptor-deficient mice. Dev Biol 217, 1024.CrossRefGoogle ScholarPubMed
Frenz, DA & Liu, W (2000) Treatment with all-trans-retinoic acid decreases levels of endogenous TGF-β1 in the mesenchyme of the developing mouse inner ear. Teratology 61, 297304.3.0.CO;2-H>CrossRefGoogle Scholar
Fukuhara, S, Kurihara, Y, Arima, Y, Yamada, N & Kurihara, H (2004) Temporal requirement of signaling cascade involving endothelin-/ndothelin receptor type A in branchial arch development. Mech Dev 121, 12231233.CrossRefGoogle Scholar
Gale, E, Prince, V, Lumsden, A, Clarke, J, Holder, N & Maden, M (1996) Late effects of retinoic acid on neural crest and aspects of thombomere. Development 122, 783793.CrossRefGoogle Scholar
Gelineau-Vanwaes, J, Bennett, GD & Finnell, RH (1999) Phenytoin-induced alterations in craniofacial gene expression. Teratology 59, 2334.3.0.CO;2-M>CrossRefGoogle Scholar
Husson, M, Enderlin, V, Alfos, S, Feart, C, Higueret, P & Pallet, V (2003) Triiodothyronine administration reverses vitamin A deficiency-related hypo-expression of retinoic acid and triiodothyronine nuclear receptors and of neurogranin in rat brain. Br J Nutr 90, 191198.CrossRefGoogle ScholarPubMed
Institute of Laboratory Animal Resources (1996) Guide for the Care and Use of Laboratory Animals. National Research Council, Washington, DC: National Academy Press.Google Scholar
Kempf, H, Linares, C, Corvol, P & Gasc, JM (1998) Pharmacological inactivation of the endothelin type A receptor in the early chick embryo: a model of mispatterning of the branchial arch derivatives. Development 125, 49314941.CrossRefGoogle Scholar
Kontges, G & Lumsden, A (1996) Rhombencephalic neural crest segmentation is preserved throughout craniofacial ontogeny. Development 122, 32293242.CrossRefGoogle ScholarPubMed
Kurihara, H, Kurihara, Y, Nagai, R & Yazaki, Y (1999) Endothelin and neural crest development. Cell Mol Biol 45, 639651.Google ScholarPubMed
Kurihara, Y, Kurihara, H, Suzuki, H, Kodama, T, Maemura, K, Nagai, R, Oda, H, Kuwaki, T, Cao, WH & Kamada, N (1994) Elevated blood pressure and craniofacial abnormalities in mice deficient in endothelin-1. Nature 368, 703710.CrossRefGoogle ScholarPubMed
Lee, YM, Osumi-Yumashita, N, Ninomiya, Y, Moon, CK, Eriksson, U & Eto, K (1995) Retinoic acid stage-dependently alters the migration pattern and identity of hindbrain neural crest cells. Development 121, 825837.CrossRefGoogle ScholarPubMed
Liu, P, Xu, Y, Yin, H, Wang, J, Chen, K & Li, Y (2005) Development toxicity research of ginsenoside Rb1 using a whole mouse embryo culture model. Birth Defects Res (Part B) 74, 207209.CrossRefGoogle ScholarPubMed
Lumsden, A, Sprawson, N & Graham, A (1991) Segmental origin and migration of neural crest cells in the hindbrain region of the chick embryo. Development 113, 12811291.CrossRefGoogle ScholarPubMed
MacLean, G, Abu-Abed, S, Dolle, P, Tahayato, A, Chambon, P & Petkovich, M (2001) Cloning of a novel retinoic-acid metabolizing cytochrome P450, Cyp26B1, and comparative expression analysis with Cyp26A1 during early murine development. Mech Dev 107, 195201.CrossRefGoogle ScholarPubMed
Maden, M (2001) Role and distribution of retinoic acid during CNS development. Int Rev Cytol 209, 177.CrossRefGoogle ScholarPubMed
Menegola, E, Marisa, LB, Francesca, DR, Massa, V & Giavini, E (2004) Relationship between hindbrain segmentation, neural crest cell migration and branchial arch abnormalities in rat embryos exposed to fluconazole and retinoic acid in vitro. Reprod Toxicol 18, 121130.CrossRefGoogle ScholarPubMed
Miller, CT, Schilling, TF, Lee, K, Parker, J & Kimmel, CB (2000) Sucker encodes a zebrafish endothelin-1 required for ventral branchial arch development. Development 127, 38153828.CrossRefGoogle Scholar
New, D (1978) Whole embryo culture and the study of mammalian embryo during organogenesis. Biol Rev 53, 81122.CrossRefGoogle Scholar
Niederreither, K, Vermot, J, Schuhbaur, B, Chambon, P & Dolle, P (2000) Retinoic acid synthesis and hindbrain patterning in the mouse embryo. Development 127, 7585.CrossRefGoogle ScholarPubMed
Noden, DM (1998) Interactions and fates of avian craniofacial mesenchyme. Development 103, 121140.CrossRefGoogle Scholar
Ozeki, H, Kukiko, Y, Tonami, K, Watatani, S & Kurihara, H (2004) Endothelin-1 regulates the dorsoventral branchial arch patterning in mice. Mech Dev 121, 387395.CrossRefGoogle ScholarPubMed
Paros, A & Beck, SL (1999) Folinic acid reduces cleft lip [CL(P)] in /ySn mice. Teratology 60, 344347.3.0.CO;2-M>CrossRefGoogle Scholar
Reynolds, PR, Schaalje, GB & Seegmiller, RE (2003) Combination therapy with folic acid and methionine in the prevention of retinoic acid-induced cleft palate in mice. Birth Defects Res (Part A) 67, 168173.CrossRefGoogle ScholarPubMed
Ruest, LB, Dager, M, Yanagisawa, H, Charite, J, Hammer, RE, Olson, EN, Yanagisawa, M & Clouthier, DE (2003) dHAND-Cre transgenic mice reveal specific potential functions of dHAND during craniofacial development. Dev Biol 257, 263277.CrossRefGoogle ScholarPubMed
Sadler, TW, Merrill, AH, Stevens, VL, Sullards, MC, Wang, E & Wang, P (2002) Prevention of fumonisin B1-induced neural tube defects by folic acid. Teratology 66, 169176.CrossRefGoogle ScholarPubMed
Scott, JM, Weir, DG, Molloy, A, McPartlin, J, Daly, L & Kirke, P (1994) Folic acid metabolism and mechanisms of neural tube defects. Ciba Found Symp 181, 180187.Google ScholarPubMed
Tahayato, A, Dolle, P & Petkovich, M (2003) Cyp26C1 encodes a novel retinoic acid-metabolizing enzyme expressed in the hindbrain, inner ear, first branchial arch and tooth buds during murine development. Gene Expr Patterns 3, 449454.CrossRefGoogle ScholarPubMed
Thomas, T, Kurihara, H, Yamagishi, H, Kurihara, Y, Yazaki, Y, Olson, EN & Srivastava, D (1998) A signaling cascade involving endothelin-1, dHAND and Msx1 regulates development of neural-crest-derived branchial arch mesenchyme. Development 125, 30053014.CrossRefGoogle ScholarPubMed
Tsuiki, H & Kishi, K (1999) Retinoid-induced limb defects 2: involvement of TGF-β2 in retinoid-induced inhibition of limb bud development. Reprod Toxicol 13, 113122.CrossRefGoogle ScholarPubMed
Van, MFG, Delhaise, F & Picard, JT (1990) Quantitation of mouse embryonic development in vitro: a morphological scoring system. Toxicol In Vitro 4, 149.Google Scholar
Wilkinson, D (1992) In Situ Hybridization: A Practical Approach. Oxford: IRL Press.Google Scholar
Yasui, H, Morishima, M, Nakazawa, M & Aikawa, E (1998) Anomalous looping, atrioventricular cushion dysplasia, and unilateral ventricular hypoplasia in the mouse embryos with right isomerism induced by retinoic acid. Anat Rec 250, 210219.3.0.CO;2-R>CrossRefGoogle ScholarPubMed
Yokota, J, Kawana, M, Hidai, C, Aoka, Y, Ichikawa, K, Iguchi, N, Okada, M, Kasanuki, H (2001) Retinoic acid suppresses endothelin-1 gene expression at the transcription level in endothelial cells. Atherosclerosis 159, 491496.CrossRefGoogle ScholarPubMed
Yu, Z, Lin, J, Xiao, Y, Han, J, Zhang, X, Jia, H, Tang, Y & Li, Y (2005) Induction of cell-cycle arrest by all-trans retinoic acid in mouse embryonic palatal mesenchymal (MEPM) cells. Toxicol Sci 83, 349354.CrossRefGoogle ScholarPubMed
Zhu, CC, Yamada, G & Blum, M (1997) Correlation between loss of middle ear bones and altered goosecoid gene expression in the branchial region following retinoic acid treatment of mouse embryos in vivo. Biochem Biophys Res Commun 235, 748753.CrossRefGoogle ScholarPubMed