Retinoic acid and hindbrain patterning

Journal of Neurobiology

Volumn 66, Issue 7, 2006, Pages 705-725

  Glover, Joel C ^a   Renaud, Jean Sébastien ^a   Rijli, Filippo M ^b  

^a UNIVERSITY OF OSLO   (Norway)

^b INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

CYP26; Hox; RALDH2; RAR; Retinoid; Rhombomere; RXR

Indexed keywords

ALITRETINOIN; BETA GALACTOSIDASE; BINDING PROTEIN; CYTOCHROME P450 26; CYTOCHROME P450 ISOENZYME; ENZYME; RETINOIC ACID; RETINOID X RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL MODEL; ANTERIOR POSTERIOR AXIS; BRAIN DEVELOPMENT; BRAIN MALFORMATION; BRAIN MATURATION; BRAIN REGION; DEVELOPMENTAL STAGE; EMBRYO PATTERN FORMATION; FETUS LUNG MATURATION; GENE ACTIVITY; GENE EXPRESSION; HOX GENE; MESODERM; NEUROEPITHELIUM; NONHUMAN; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REGULATOR GENE; REPORTER GENE; RETINOL DEFICIENCY; RETINOL INTOXICATION; REVIEW; RHOMBENCEPHALON; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; TERATOGENICITY;

ANIMALS; BODY PATTERNING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, HOMEOBOX; HUMANS; PHYLOGENY; RECEPTORS, RETINOIC ACID; RHOMBENCEPHALON; SIGNAL TRANSDUCTION; TRETINOIN;

EID: 33745297531     PISSN: 00223034     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/neu.20272     Document Type: Review

References (178)

1. Abu-Abed S, Dolle P, Metzger D, Beckett B, Chambon P, Petkovich M. 2001. The retinoic acid-metabolizing enzyme, CYP26A1, is essential for normal hindbrain patterning, vertebral identity, and development of posterior structures. Genes Dev 15:226-240.
2. Agarwal VR, Sato SM. 1993. Retinoic acid affects central nervous system development of Xenopus by changing cell fate. Mech Dev 44:167-173.
3. Allenby G, Bocquel MT, Saunders M, Kazmer S, Speck J, Rosenberger M, Lovey A, et al. 1993. Retinoic acid receptors and retinoid X receptors: interactions with endogenous retinoic acids. Proc Natl Acad Sci USA 90:30-34.
4. Avantaggiato V, Acampora D, Tuorto F, Simeone A. 1996. Retinoic acid induces stage-specific repatterning of the rostral central nervous system. Dev Biol 175:347-357.
5. Balkan W, Colbert M, Bock C, Linney E. 1992. Transgenic indicator mice for studying activated retinoic acid receptors during development. Proc Natl Acad Sci USA 89:3347-3351.
6. Begemann G, Marx M, Mebus K, Meyer A, Bastmeyer M. 2004. Beyond the neckless phenotype: influence of reduced retinoic acid signaling on motor neuron development in the zebrafish hindbrain. Dev Biol 271:119-129.
7. Begemann G, Schilling TF, Rauch GJ, Geisler R, Ingham PW. 2001. The zebrafish neckless mutation reveals a requirement for raldh2 in mesodermal signals that pattern the hindbrain. Development 128:3081-3094.
8. Bel-Vialar S, Itasaki N, Krumlauf R. 2002. Initiating Hox gene expression: in the early chick neural tube differential sensitivity to FGF and RA signaling subdivides the HoxB genes in two distinct groups. Development 129:5103-5115.
9. Berggren K, McCaffery P, Drager U, Forehand CJ. 1999. Differential distribution of retinoic acid synthesis in the chicken embryo as determined by immunolocalization of the retinoic acid synthetic enzyme, RALDH-2. Dev Biol 210:288-304.
10. Blentic A, Gale E, Maden M. 2003. Retinoic acid signalling centres in the avian embryo identified by sites of expression of synthesising and catabolising enzymes. Dev Dyn 227:114-127.
11. Blumberg B, Bolado J, Jr., Derguini F, Craig AG, Moreno TA, Chakravarti D, Heyman RA, et al. 1996. Novel retinoic acid receptor ligands in Xenopus embryos. Proc Natl Acad Sci USA 93:4873-4878.
12. Blumberg B, Bolado J, Jr., Moreno TA, Kintner C, Evans RM, Papalopulu N. 1997. An essential role for retinoid signaling in anteroposterior neural patterning. Development 124:373-379.
13. Blumberg B, Mangelsdorf DJ, Dyck JA, Bittner DA, Evans RM, De Robertis EM. 1992. Multiple retinoid-responsive receptors in a single cell: families of retinoid "X" receptors and retinoic acid receptors in the Xenopus egg. Proc Natl Acad Sci USA 89:2321-2325.
14. Chambon P. 1996. A decade of molecular biology of retinoic acid receptors. FASEB J 10:940-954.
15. Chen Y, Huang L, Russo AF, Solursh M. 1992. Retinoic acid is enriched in Hensen's node and is developmentally regulated in the early chicken embryo. Proc Natl Acad Sci USA 89:10056-10059.
16. Chen Y, Huang L, Solursh M. 1994. A concentration gradient of retinoids in the early Xenopus laevis embryo. Dev Biol 161:70-76.
17. Chen Y, Pollet N, Niehrs C, Pieler T. 2001. Increased XRALDH2 activity has a posteriorizing effect on the central nervous system of Xenopus embryos. Mech Dev 101:91-103.
18. Colbert MC, Linney E, LaMantia AS. 1993. Local sources of retinoic acid coincide with retinoid-mediated transgene activity during embryonic development. Proc Natl Acad Sci USA 90:6572-6576.
19. Conlon RA, Rossant J. 1992. Exogenous retinoic acid rapidly induces anterior ectopic expression of murine Hox-2 genes in vivo. Development 116:357-368.
20. Cordes SP, Barsh GS. 1994. The mouse segmentation gene kr encodes a novel basic domain-leucine zipper transcription factor. Cell 79:1025-1034.
21. Costaridis P, Horton C, Zeitlinger J, Holder N, Maden M. 1996. Endogenous retinoids in the zebrafish embryo and adult. Dev Dyn 205:41-51.
22. Crawford MJ, Liversage RA, Varmuza SL. 1995. Two isoforms of Xenopus retinoic acid receptor gamma 2 (B) exhibit differential expression and sensitivity to retinoic acid during embryogenesis. Dev Genet 17:291-302.
23. Davenne M, Maconochie MK, Neun R, Pattyn A, Chambon P, Krumlauf R, Rijli FM. 1999. Hoxa2 and Hoxb2 control dorsoventral patterns of neuronal development in the rostral hindbrain. Neuron 22:677-691.
24. Dekker EJ, Pannese M, Houtzager E, Timmermans A, Boncinelli E, Durston A. 1992. Xenopus Hox-2 genes are expressed sequentially after the onset of gastrulation and are differentially inducible by retinoic acid. Dev Suppl 195-202.
25. Dekker EJ, Vaessen MJ, van den Berg C, Timmermans A, Godsave S, Holling T, Nieuwkoop P, et al. 1994. Overexpression of a cellular retinoic acid binding protein (xCRABP) causes anteroposterior defects in developing Xenopus embryos. Development 120:973-985.
26. de Roos K, Sonneveld E, Compaan B, ten Berge D, Durston AJ, van der Saag PT. 1999. Expression of retinoic acid 4-hydroxylase (CYP26) during mouse and Xenopus laevis embryogenesis. Mech Dev 82:205-211.
27. Dersch H, Zile MH. 1993. Induction of normal cardiovascular development in the vitamin A-deprived quail embryo by natural retinoids. Dev Biol 160:424-433.
28. Diez del Corral R, Olivera-Martinez I, Goriely A, Gale E, Maden M, Storey K. 2003. Opposing FGF and retinoid pathways control ventral neural pattern, neuronal differentiation, and segmentation during body axis extension. Neuron 40:65-79.
29. Diez del Corral R, Storey KG. 2004. Opposing FGF and retinoid pathways: a signalling switch that controls differentiation and patterning onset in the extending vertebrate body axis. Bioessays 26:857-869.
30. Dobbs-McAuliffe B, Zhao Q, Linney E. 2004. Feedback mechanisms regulate retinoic acid production and degradation in the zebrafish embryo. Mech Dev 121:339-350.
31. Dolle P, Fraulob V, Kastner P, Chambon P. 1994. Developmental expression of murine retinoid X receptor (RXR) genes. Mech Dev 45:91-104.
32. Dupe V, Davenne M, Brocard J, Dolle P, Mark M, Dierich A, Chambon P, et al. 1997. In vivo functional analysis of the Hoxa-1 3′ retinoic acid response element (3′RARE). Development 124:399-410.
33. Dupe V, Ghyselinck NB, Wendling O, Chambon P, Mark M. 1999. Key roles of retinoic acid receptors alpha and beta in the patterning of the caudal hindbrain, pharyngeal arches and otocyst in the mouse. Development 126:5051-5059.
34. Dupe V, Lumsden A. 2001. Hindbrain patterning involves graded responses to retinoic acid signalling. Development 128:2199-2208.
35. Durston AJ, Timmermans JP, Hage WJ, Hendriks HF, de Vries NJ, Heideveld M, Nieuwkoop PD. 1989. Retinoic acid causes an anteroposterior transformation in the developing central nervous system. Nature 340:140-144.
36. Eichmann A, Grapin-Botton A, Kelly L, Graf T, Le Douarin NM, Sieweke M. 1997. The expression pattern of the mafB/kr gene in birds and mice reveals that the kreisler phenotype does not represent a null mutant. Mech Dev 65:111-122.
37. Emoto Y, Wada H, Okamoto H, Kudo A, Imai Y. 2005. Retinoic acid-metabolizing enzyme Cyp26a1 is essential for determining territories of hindbrain and spinal cord in zebrafish. Dev Biol 278:415-427.
38. Frasch M, Chen X, Lufkin T. 1995. Evolutionary-conserved enhancers direct region-specific expression of the murine Hoxa-1 and Hoxa-2 loci in both mice and Drosophila. Development 121:957-974.
39. Fujii H, Sato T, Kaneko S, Gotoh O, Fujii-Kuriyama Y, Osawa K, Kato S, et al. 1997. Metabolic inactivation of retinoic acid by a novel P450 differentially expressed in developing mouse embryos. Embo J 16:4163-4173.
40. Gale E, Prince V, Lumsden A, Clarke J, Holder N, Maden M. 1996. Late effects of retinoic acid on neural crest and aspects of rhombomere. Development 122:783-793.
41. Gale E, Zile M, Maden M. 1999. Hindbrain respecification in the retinoid-deficient quail. Mech Dev 89:43-54.
42. Gavalas A, Krumlauf R. 2000. Retinoid signalling and hindbrain patterning. Curr Opin Genet Dev 10:380-386.
43. Gavalas A, Studer M, Lumsden A, Rijli FM, Krumlauf R, Chambon P. 1998. Hoxal and Hoxb1 synergize in patterning the hindbrain, cranial nerves and second pharyngeal arch. Development 125:1123-1136.
44. Goldstein JT, Dobrzyn A, Clagett-Dame M, Pike JW, DeLuca HF. 2003. Isolation and characterization of unsaturated fatty acids as natural ligands for the retinoid-X receptor. Arch Biochem Biophys 420:185-193.
45. Gorry P, Lufkin T, Dierich A, Rochette-Egly C, Decimo D, Dolle P, Mark M, et al. 1994. The cellular retinoic acid binding protein I is dispensable. Proc Natl Acad Sci USA 91:9032-9036.
46. Gould A, Itasaki N, Krumlauf R. 1998. Initiation of rhombomeric Hoxb4 expression requires induction by somites and a retinoid pathway. Neuron 21:39-51.
47. Grandel H, Lun K, Rauch GJ, Rhinn M, Piotrowski T, Houart C, Sordino P, et al. 2002. Retinoic acid signalling in the zebrafish embryo is necessary during pre-segmentation stages to pattern the anterior-posterior axis of the CNS and to induce a pectoral fin bud. Development 129:2851-2865.
48. Grapin-Botton A, Bonnin MA, McNaughton LA, Krumlauf R, Le Douarin NM. 1995. Plasticity of transposed rhombomeres: Hox gene induction is correlated with phenotypic modifications. Development 121:2707-2721.
49. Grapin-Botton A, Bonnin MA, Sieweke M, Le Douarin NM. 1998. Defined concentrations of a posteriorizing signal are critical for MafB/Kreisler segmental expression in the hindbrain. Development 125:1173-1181.
50. Gu X, Xu F, Wang X, Gao X, Zhao Q. 2005. Molecular cloning and expression of a novel CYP26 gene (cyp26d1) during zebrafish early development. Gene Expr Patterns 5:733-739.
51. Guidato S, Barrett C, Guthrie S. 2003. Patterning of motor neurons by retinoic acid in the chick embryo hindbrain in vitro. Mol Cell Neurosci 23:81-95.
52. Haselbeck RJ, Hoffmann I, Duester G. 1999. Distinct functions for Aldh1 and Raldh2 in the control of ligand production for embryonic retinoid signaling pathways. Dev Genet 25:353-364.
53. Hernandez RE, Rikhof HA, Bachmann R, Moens CB. 2004. vhnf1 integrates global RA patterning and local FGF signals to direct posterior hindbrain development in zebrafish. Development 131:4511-4520.
54. Hill J, Clarke JD, Vargesson N, Jowett T, Holder N. 1995. Exogenous retinoic acid causes specific alterations in the development of the midbrain and hindbrain of the zebrafish embryo including positional respecification of the Mauthner neuron. Mech Dev 50:3-16.
55. Ho L, Mercola M, Gudas LJ. 1994. Xenopus laevis cellular retinoic acid-binding protein: temporal and spatial expression pattern during early embryogenesis. Mech Dev 47:53-64.
56. Holder N, Hill J. 1991. Retinoic acid modifies development of the midbrain-hindbrain border and affects cranial ganglion formation in zebrafish embryos. Development 113:1159-1170.
57. Hollemann T, Chen Y, Grunz H, Pieler T. 1998. Regionalized metabolic activity establishes boundaries of retinoic acid signalling. EMBO J 17:7361-7372.
58. Hoover F, Glover JC. 1998. Regional pattern of retinoid X receptor-alpha gene expression in the central nervous system of the chicken embryo and its up-regulation by exposure to 9-cis retinoic acid. J Comp Neurol 398:575-586.
59. Hoover F, Gundersen TE, Ulven SM, Michaille JJ, Blanchet S, Blomhoff R, Glover JC. 2001. Quantitative assessment of retinoid signaling pathways in the developing eye and retina of the chicken embryo. J Comp Neurol 436:324-335.
60. Hoover F, Kielland A, Glover JC. 2000. RXR gamma gene is expressed by discrete cell columns within the alar plate of the brainstem of the chicken embryo. J Comp Neurol 416:417-428.
61. Horton C, Maden M. 1995. Endogenous distribution of retinoids during normal development and teratogenesis in the mouse embryo. Dev Dyn 202:312-323.
62. Huang D, Chen SW, Gudas LJ. 2002. Analysis of two distinct retinoic acid response elements in the homeobox gene Hoxb1 in transgenic mice. Dev Dyn 223:353-370.
63. Huang D, Chen SW, Langston AW, Gudas LJ. 1998. A conserved retinoic acid responsive element in the murine Hoxb-1 gene is required for expression in the developing gut. Development 125:3235-3246.
64. Irving C, Mason I. 2000. Signalling by FGF8 from the isthmus patterns anterior hindbrain and establishes the anterior limit of Hox gene expression. Development 127:177-186.
65. Itasaki N, Sharpe J, Morrison A, Krumlauf R. 1996. Reprogramming Hox expression in the vertebrate hindbrain: influence of paraxial mesoderm and rhombomere transposition. Neuron 16:487-500.
66. Jones BB, Ohno CK, Allenby G, Boffa MB, Levin AA, Grippo JF, Petkovich M. 1995. New retinoid X receptor subtypes in zebra fish (Danio rerio) differentially modulate transcription and do not bind 9-cis retinoic acid. Mol Cell Biol 15:5226-5234.
67. Joore J, van der Lans GB, Lanser PH, Vervaart JM, Zivkovic D, Speksnijder JE, Kruijer W. 1994. Effects of retinoic acid on the expression of retinoic acid receptors during zebrafish embryogenesis. Mech Dev 46:137-150.
68. Kalter H, Warkany J. 1959. Experimental production of congenital malformations in mammals by metabolic procedure. Physiol Rev 39:69-115.
69. Kastner P, Messaddeq N, Mark M, Wendung O, Grondona JM, Ward S, Ghyselinck N, et al. 1997. Vitamin A deficiency and mutations of RXRalpha, RXRbeta and RARalpha lead to early differentiation of embryonic ventricular cardiomyocytes. Development 124:4749-4758.
70. Kessel M, Gruss P. 1991. Homeotic transformations of murine vertebrae and concomitant alteration of Hox codes induced by retinoic acid. Cell 67:89-104.
71. Kolm PJ, Apekin V, Sive H. 1997. Xenopus hindbrain patterning requires retinoid signaling. Dev Biol 192:1-16.
72. Kraft JC, Juchau MR. 1995. Xenopus laevis: a model system for the study of embryonic retinoid metabolism. III. Isomerization and metabolism of all-trans-retinoic acid and 9-cis-retinoic acid and their dysmorphogenic effects in embryos during neurulation. Drug Metab Dispos 23:1058-1071.
73. Kraft JC, Schuh T, Juchau M, Kimelman D. 1994. The retinoid X receptor ligand, 9-cis-retinoic acid, is a potential regulator of early Xenopus development. Proc Natl Acad Sci USA 91:3067-3071.
74. Kudoh T, Wilson SW, Dawid IB. 2002. Distinct roles for Fgf, Wnt and retinoic acid in posteriorizing the neural ectoderm. Development 129:4335-4346.
75. Lammer EJ, Armstrong DL. 1992. Malformations of hindbrain structures among humans exposed to isotretinoin 13-cis-retinoic acid during early embryogenesis. In: Morris-Kay GM, editor. Retinoids in Normal Development and Teratogenesis. Oxford: Oxford University Press, pp.281-295.
76. Lampron C, Rochette-Egly C, Gorry P, Dolle P, Mark M, Lufkin T, LeMeur M, et al. 1995. Mice deficient in cellular retinoic acid binding protein II (CRABPII) or in both CRABPI and CRABPII are essentially normal. Development 121:539-548.
77. Langsten AW, Gudas LJ. 1992. Identification of a retinoic acid responsive enhancer 3′ of the murine homeobox gene Hox-1.6. Mech Dev 38:217-227.
78. Li H, Wagner E, McCaffery P, Smith D, Andreadis A, Drager UC. 2000. A retinoic acid synthesizing enzyme in ventral retina and telencephalon of the embryonic mouse. Mech Dev 95:283-289.
79. Liao YP, Ho SY, Liou JC. 2004. Non-genomic regulation of transmitter release by retinoic acid at developing motoneurons in Xenopus cell culture. J Cell Sci 117:2917-2924.
80. Lin M, Zhang M, Abraham M, Smith SM, Napoli JL. 2003. Mouse retinal dehydrogenase 4 (RALDH4), molecular cloning, cellular expression, and activity in 9-cis-retinoic acid biosynthesis in intact cells. J Biol Chem 278:9856-9861.
81. Linville A, Gumusaneli E, Chandraratna RA, Schilling TF. 2004. Independent roles for retinoic acid in segmentation and neuronal differentiation in the zebrafish hindbrain. Dev Biol 270:186-199.
82. Liu JP, Laufer E, Jessell TM. 2001. Assigning the positional identity of spinal motor neurons: rostrocaudal patterning of Hox-c expression by FGFs, Gdf11, and retinoids. Neuron 32:997-1012.
83. Liu RZ, Sharma MK, Sun Q, Thisse C, Thisse B, Denovan-Wright EM, Wright JM. 2005. Retention of the duplicated cellular retinoic acid-binding protein 1 genes (crabp1a and crapb1b) in the zebrafish genome by sub-functionalization of tissue-specific expression. FEBS J 272:3561-3571.
84. Luria A, Furlow JD. 2004. Spatiotemporal retinoid-X receptor activation detected in live vertebrate embryos. Proc Natl Acad Sci USA 101:8987-8992.
85. 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 107:195-201.
86. Maconochie MK, Nonchev S, Studer M, Chan SK, Popperl H, Sham MH, Mann RS, et al. 1997. Cross-regulation in the mouse HoxB complex: the expression of Hoxb2 in rhombomere 4 is regulated by Hoxb1. Genes Dev 11:1885-1895.
87. Maden M. 2002. Retinoid signalling in the development of the central nervous system. Nat Rev Neurosci 3:843-853.
88. Maden M, Hunt P, Eriksson U, Kuroiwa A, Krumlauf R, Summerbell D. 1991. Retinoic acid-binding protein, rhombomeres and the neural crest. Development 111:35-43.
89. Maden M, Sonneveld E, van der Saag PT, Gale E. 1998. The distribution of endogenous retinoic acid in the chick embryo: implications for developmental mechanisms. Development 125:4133-4144.
90. Manns M, Fritzsch B. 1992. Retinoic acid affects the organization of reticulospinal neurons in developing Xenopus. Neurosci Lett 139:253-256.
91. Manzanares M, Bel-Vialar S, Ariza-McNaughton L, Ferretti E, Marshall H, Maconochie MM, Blasi F, et al. 2001. Independent regulation of initiation and maintenance phases of Hoxa3 expression in the vertebrate hindbrain involve auto- and cross-regulatory mechanisms. Development 128:3595-3607.
92. Marklew S, Smith DP, Mason CS, Old RW. 1994. Isolation of a novel RXR from Xenopus that most closely resembles mammalian RXR beta and is expressed throughout early development. Biochim Biophys Acta 1218:267-272.
93. Marshall H, Morrison A, Studer M, Popperl H, Krumlauf R. 1996. Retinoids and Hox genes. FASEB J 10:969-978.
94. Marshall H, Nonchev S, Sham MH, Muchamore I, Lumsden A, Krumlauf R. 1992. Retinoic acid alters hindbrain Hox code and induces transformation of rhombomeres 2/3 into a 4/5 identity. Nature 360:737-741.
95. Marshall H, Studer M, Popperl H, Aparicio S, Kuroiwa A, Brenner S, Krumlauf R. 1994. A conserved retinoic acid response element required for early expression of the homeobox gene Hoxb-1. Nature 370:567-571.
96. Matkovits T, Christakos S. 1995. Ligand occupancy is not required for vitamin D receptor and retinoid receptor-mediated transcriptional activation. Mol Endocrinol 9:232-242.
97. Maves L, Kimmel CB. 2005. Dynamic and sequential patterning of the zebrafish posterior hindbrain by retinoic acid. Dev Biol 285:593-605.
98. McCaffery P, Drager UC. 1994. Hot spots of retinoic acid synthesis in the developing spinal cord. Proc Natl Acad Sci USA 91:7194-7197.
99. Mic FA, Haselbeck RJ, Cuenca AE, Duester G. 2002. Novel retinoic acid generating activities in the neural tube and heart identified by conditional rescue of Raldh2 null mutant mice. Development 129:2271-2282.
100. Mic FA, Molotkov A, Fan X, Cuenca AE, Duester G. 2000. RALDH3, a retinaldehyde dehydrogenase that generates retinoic acid, is expressed in the ventral retina, otic vesicle and olfactory pit during mouse development. Mech Dev 97:227-230.
101. Michaille JJ, Kanzler B, Blanchet S, Gamier JM, Dhouailly D. 1995. Characterization of cDNAs encoding two chick retinoic acid receptor alpha isoforms and distribution of retinoic acid receptor alpha, beta and gamma transcripts during chick skin development. Int J Dev Biol 39:587-596.
102. Moens CB, Cordes SP, Giorgianni MW, Barsh GS, Kimmel CB. 1998. Equivalence in the genetic control of hindbrain segmentation in fish and mouse. Development 125:381-391.
103. Mollard R, Viville S, Ward SJ, Decimo D, Chambon P, Dolle P. 2000. Tissue-specific expression of retinoic acid receptor isoform transcripts in the mouse embryo. Mech Dev 94:223-232.
104. Morrison A, Ariza-McNaughton L, Gould A, Featherstone M, Krumlauf R. 1997. HOXD4 and regulation of the group 4 paralog genes. Development 124:3135-3146.
105. Morrison A, Moroni MC, Ariza-McNaughton L, Krumlauf R, Mavilio F. 1996. In vitro and transgenic analysis of a human HOXD4 retinoid-responsive enhancer. Development 122:1895-1907.
106. Morriss GM. 1972. Morphogenesis of the malformations induced in rat embryos by maternal hypervitaminosis A. J Anat 113:241-250.
107. Morriss GM, Thorogood PVT. 1978. An approach to cranial neural crest cell migration and differentiation in mammalian embryos. In: Johnson MH, editor. Development in Mammals, Vol. 3. North-Holland, Amsterdam: Elsevier, pp. 363-412.
108. Morriss-Kay GM, Murphy P, Hill RE, Davidson DR. 1991. Effects of retinoic acid excess on expression of Hox-2.9 and Krox-20 and on morphological segmentation in the hindbrain of mouse embryos. Embo J 10:2985-2995.
109. Nelson DR. 1999. A second CYP26 P450 in humans and zebrafish: CYP26B1. Arch Biochem Biophys 371:345-347.
110. Niederreither K, Fraulob V, Gamier JM, Chambon P, Dolle P. 2002. Differential expression of retinoic acid-synthesizing (RALDH) enzymes during fetal development and organ differentiation in the mouse. Mech Dev 110:165-171.
111. Niederreither K, McCaffery P, Drager UC, Chambon P, Dolle P. 1997. Restricted expression and retinoic acid-induced downregulation of the retinaldehyde dehydrogenase type 2 (RALDH-2) gene during mouse development. Mech Dev 62:67-78.
112. Niederreither K, Vermot J, Schuhbaur B, Chambon P, Dolle P. 2000. Retinoic acid synthesis and hindbrain patterning in the mouse embryo. Development 127:75-85.
113. Nittenberg R, Patel K, Joshi Y, Krumlauf R, Wilkinson DG, Brickell PM, Tickle C, et al. 1997. Cell movements, neuronal organisation and gene expression in hindbrains lacking morphological boundaries. Development 124:2297-2306.
114. Nolle C, Amores A, Nagy Kovacs E, Postlethwait J, Featherstone M. 2003. The role of a retinoic acid response element in establishing the anterior neural expression border of Hoxd4 transgenes. Mech Dev 120:325-335.
115. Oosterveen T, Niederreither K, Dolle P, Chambon P, Meijlink F, Deschamps J. 2003. Retinoids regulate the anterior expression boundaries of 5′ Hoxb genes in posterior hindbrain. Embo J 22:262-269.
116. Papalopulu N, Clarke JD, Bradley L, Wilkinson D, Krumlauf R, Holder N. 1991. Retinoic acid causes abnormal development and segmental patterning of the anterior hindbrain in Xenopus embryos. Development 113:1145-1158.
117. Perz-Edwards A, Hardison NL, Linney E. 2001. Retinoic acid-mediated gene expression in transgenic reporter zebrafish. Dev Biol 229:89-101.
118. Pijnappel WW, Hendriks HF, Folkers GE, van den Brink CE, Dekker EJ, Edelenbosch C, van der Saag PT, et al. 1993. The retinoid ligand 4-oxo-retinoic acid is a highly active modulator of positional specification. Nature 366:340-344.
119. Popperl H, Bienz M, Studer M, Chan SK, Aparicio S, Brenner S, Mann RS, et al. 1995. Segmental expression of Hoxb-1 is controlled by a highly conserved autoregulatory loop dependent upon exd/pbx. Cell 81:1031-1042.
120. Prince VE, Moens CB, Kimmel CB, Ho RK. 1998. Zebrafish hox genes: expression in the hindbrain region of wild-type and mutants of the segmentation gene, valentine. Development 125:393-406.
121. Ray WJ, Bain G, Yao M, Gottlieb DI. 1997. CYP26, a novel mammalian cytochrome P450, is induced by retinoic acid and defines a new family. J Biol Chem 272:18702-18708.
122. Reijntjes S, Gale E, Maden M. 2004. Generating gradients of retinoic acid in the chick embryo: Cyp26C1 expression and a comparative analysis of the Cyp26 enzymes. Dev Dyn 230:509-517.
123. Renaud JS, Nordheim S, Glover JC. 2004. Retinoic acid gradient establishes and maintains an anteroposterior gradient of dorsoventral patterning in the avian hindbrain. Soc Neurosci Abstr 34:721.7.
124. Rijli FM, Gavalas A, Chambon P. 1998. Segmentation and specification in the branchial region of the head: the role of the Hox selector genes. Int J Dev Biol 42:393-401.
125. Romand R, Sapin V, Ghyselinck NB, Avan P, Le Calvez S, Dolle P, Chambon P, et al. 2000. Spatio-temporal distribution of cellular retinoid binding protein gene transcripts in the developing and the adult cochlea. Morphological and functional consequences in CRABP- and CRBPI-null mutant mice. Eur J Neurosci 12:2793-2804.
126. Rossant J, Zirngibl R, Cado D, Shago M, Giguere V. 1991. Expression of a retinoic acid response element-hsplacZ transgene defines specific domains of transcriptional activity during mouse embryogenesis. Genes Dev 5:1333-1344.
127. Rowe A, Brickell PM. 1993. The nuclear retinoid receptors. Int J Exp Pathol 74:117-126.
128. Ruberte E, Dolle P, Chambon P, Morriss-Kay G. 1991. Retinoic acid receptors and cellular retinoid binding proteins. II. Their differential pattern of transcription during early morphogenesis in mouse embryos. Development 111:45-60.
129. Ruberte E, Dolle P, Krust A, Zelent A, Morriss-Kay G, Chambon P. 1990. Specific spatial and temporal distribution of retinoic acid receptor gamma transcripts during mouse embryogenesis. Development 108:213-222.
130. Ruberte E, Friederich V, Chambon P, Morriss-Kay G. 1993. Retinoic acid receptors and cellular retinoid binding proteins. III. Their differential transcript distribution during mouse nervous system development. Development 118:267-282.
131. Ruberte E, Friederich V, Morriss-Kay G, Chambon P. 1992. Differential distribution patterns of CRABP I and CRABP II transcripts during mouse embryogenesis. Development 115:973-987.
132. Sakai Y, Meno C, Fujii H, Nishino J, Shiratori H, Saijoh Y, Rossant J, et al. 2001. The retinoic acid-inactivating enzyme CYP26 is essential for establishing an uneven distribution of retinoic acid along the anterio-posterior axis within the mouse embryo. Genes Dev 15:213-225.
133. Scadding SR, Maden M. 1994. Retinoic acid gradients during limb regeneration. Dev Biol 162:608-617.
134. Serpente P, Tumpel S, Ghyselinck NB, Niederreither K, Wiedemann LM, Dolle P, Chambon P, et al. 2005. Direct crossregulation between retinoic acid receptor {beta} and Hox genes during hindbrain segmentation. Development 132:503-513.
135. Sharma MK, Denovan-Wright EM, Boudreau ME, Wright JM. 2003. A cellular retinoic acid-binding protein from zebrafish (Danio rerio): cDNA sequence, phylogenetic analysis, mRNA expression, and gene linkage mapping. Gene 311:119-128.
136. Sharma MK, Saxena V, Liu RZ, Thisse C, Thisse B, Denovan-Wright EM, Wright JM. 2005. Differential expression of the duplicated cellular retinoic acid-binding protein 2 genes (crabp2a and crapb2b) during zebrafish embryonic development. Gene Expr Patterns 5:371-379.
137. Sharpe C, Goldstone K. 2000. The control of Xenopus embryonic primary neurogenesis is mediated by retinoid signalling in the neurectoderm. Mech Dev 91:69-80.
138. Sharpe CR. 1992. Two isoforms of retinoic acid receptor alpha expressed during Xenopus development respond to retinoic acid. Mech Dev 39:81-93.
139. Sharpe CR. 1994. The expression of retinoic acid receptors in Xenopus development. Biochem Soc Trans 22:575-579.
140. Shiotsugu J, Katsuyama Y, Arima K, Baxter A, Koide T, Song J, Chandraratna RA, et al. 2004. Multiple points of interaction between retinoic acid and FGF signaling during embryonic axis formation. Development 131:2653-2667.
141. Simeone A, Acampora D, Arcioni L, Andrews PW, Boncinelli E, Mavilio F. 1990. Sequential activation of HOX2 homeobox genes by retinoic acid in human embryonal carcinoma cells. Nature 346:763-766.
142. Simeone A, Acampora D, Nigro V, Faiella A, D'Esposito M, Stornaiuolo A, Mavilio F, et al. 1991. Differential regulation by retinoic acid of the homeobox genes of the four HOX loci in human embryonal carcinoma cells. Mech Dev 33:215-227.
143. Sirbu IO, Gresh L, Barra J, Duester G. 2005. Shifting boundaries of retinoic acid activity control hindbrain segmental gene expression. Development 132:2611-2622.
144. Smith DP, Mason CS, Jones EA, Old RW. 1994. A novel nuclear receptor superfamily member in Xenopus that associates with RXR, and shares extensive sequence similarity to the mammalian vitamin D3 receptor. Nucleic Acids Res 22:66-71.
145. Smith SM, Eichele G. 1991. Temporal and regional differences in the expression pattern of distinct retinoic acid receptor-beta transcripts in the chick embryo. Development 111:245-252.
146. Solomin L, Johansson CB, Zetterstrom RH, Bissonnette RP, Heyman RA, Olson L, Lendahl U, et al. 1998. Retinoid-X receptor signalling in the developing spinal cord. Nature 395:398-402.
147. Studer M, Gavalas A, Marshall H, Ariza-McNaughton L, Rijli FM, Chambon P, Krumlauf R. 1998. Genetic interactions between Hoxa1 and Hoxb1 reveal new roles in regulation of early hindbrain patterning. Development 125:1025-1036.
148. Studer M, Popperl H, Marshall H, Kuroiwa A, Krumlauf R. 1994. Role of a conserved retinoic acid response element in rhombomere restriction of Hoxb-1. Science 265:1728-1732.
149. Sundin O, Eichele G. 1992. An early marker of axial pattern in the chick embryo and its respecification by retinoic acid. Development 114:841-852.
150. Sundin OH, Busse HG, Rogers MB, Gudas LJ, Eichele G. 1990. Region-specific expression in early chick and mouse embryos of Ghox-lab and Hox 1.6, vertebrate homeobox-containing genes related to Drosophila labial. Development 108:47-58.
151. Swindell EC, Thaller C, Sockanathan S, Petkovich M, Jessell TM, Eichele G. 1999. Complementary domains of retinoic acid production and degradation in the early chick embryo. Dev Biol 216:282-296.
152. 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 3:449-454.
153. Thaller C, Eichele G. 1987. Identification and spatial distribution of retinoids in the developing chick limb bud. Nature 327:625-628.
154. Thompson JN, Howell JM, Pitt GA, McLaughlin CI. 1969. The biological activity of retinoic acid in the domestic fowl and the effects of vitamin A deficiency on the chick embryo. Br J Nutr 23:471-490.
155. Trainor PA, Krumlauf R. 2000. Patterning the cranial neural crest: hindbrain segmentation and Hox gene plasticity. Nat Rev Neurosci 1:116-124.
156. Ulven SM, Gundersen TE, Sakhi AK, Glover JC, Blomhoff R. 2001. Quantitative axial profiles of retinoic acid in the embryonic mouse spinal cord: 9-cis retinoic acid only detected after all-trans-retinoic acid levels are super-elevated experimentally. Dev Dyn 222:341-353.
157. van der Wees J, Schilthuis JG, Koster CH, Diesveld-Schipper H, Folkers GE, van der Saag PT, Dawson MI, et al. 1998. Inhibition of retinoic acid receptor-mediated signalling alters positional identity in the developing hindbrain. Development 125:545-556.
158. Wagner E, Luo T, Drager UC. 2002. Retinoic acid synthesis in the postnatal mouse brain marks distinct developmental stages and functional systems. Cereb Cortex 12:1244-1253.
159. Wagner M, Han B, Jessell TM. 1992. Regional differences in retinoid release from embryonic neural tissue detected by an in vitro reporter assay. Development 116:55-66.
160. Wagner M, Thaller C, Jessell T, Eichele G. 1990. Polarizing activity and retinoid synthesis in the floor plate of the neural tube. Nature 345:819-822.
161. Wang Y, Zolfaghari R, Ross AC. 2002. Cloning of rat cytochrome P450RAI (CYP26) cDNA and regulation of its gene expression by all-trans-retinoic acid in vivo. Arch Biochem Biophys 401:235-243.
162. Wendling O, Ghyselinck NB, Chambon P, Mark M. 2001. Roles of retinoic acid receptors in early embryonic morphogenesis and hindbrain patterning. Development 128:2031-2038.
163. Weston AD, Blumberg B, Underhill TM. 2003. Active repression by unliganded retinoid receptors in development: less is sometimes more. J Cell Biol 161:223-228.
164. White JA, Guo YD, Baetz K, Beckett-Jones B, Bonasoro J, Hsu KE, Dilworth FJ, et al. 1996. Identification of the retinoic acid-inducible all-trans-retinoic acid 4-hydroxylase. J Biol Chem 271:29922-29927.
165. White JC, Highland M, Kaiser M, Clagett-Dame M. 2000. Vitamin A deficiency results in the dose-dependent acquisition of anterior character and shortening of the caudal hindbrain of the rat embryo. Dev Biol 220:263-284.
166. Wilkinson DG, Bhatt S, Cook M, Boncinelli E, Krumlauf R. 1989. Segmental expression of Hox-2 homeobox-containing genes in the developing mouse hindbrain. Nature 341:405-409.
167. Wilson JG, Roth CB, Warkany J. 1953. An analysis of the syndrome of malformations induced by maternal vitamin A deficiency. Effects of restoration of vitamin A at various times during gestation. Am J Anat 92:189-217.
168. Wilson L, Gale E, Chambers D, Maden M. 2004. Retinoic acid and the control of dorsoventral patterning in the avian spinal cord. Dev Biol 269:433-446.
169. Wood H, Pall G, Morriss-Kay G. 1994. Exposure to retinoic acid before or after the onset of somitogenesis reveals separate effects on rhombomeric segmentation and 3′ HoxB gene expression domains. Development 120:2279-2285.
170. Yamamoto M, Drager UC, McCaffery P. 1998. A novel assay for retinoic acid catabolic enzymes shows high expression in the developing hindbrain. Brain Res Dev Brain Res 107:103-111.
171. Yamamoto M, Fujinuma M, Hirano S, Hayakawa Y, Clagett-Dame M, Zhang J, McCaffery P. 2005. Retinoic acid influences the development of the inferior olivary nucleus in the rodent. Dev Biol 280:421-433.
172. Yamamoto M, Ullman D, Drager UC, McCaffery P. 1999. Postnatal effects of retinoic acid on cerebellar development. Neurotoxicol Teratol 21:141-146.
173. Zhang F, Nagy Kovacs E, Featherstone MS. 2000. Murine hoxd4 expression in the CNS requires multiple elements including a retinoic acid response element. Mech Dev 96:79-89.
174. Zhang F, Popperl H, Morrison A, Kovacs EN, Prideaux V, Schwarz L, Krumlauf R, et al. 1997. Elements both 5′ and 3′ to the murine Hoxd4 gene establish anterior borders of expression in mesoderm and neurectoderm. Mech Dev 67:49-58.
175. Zhang J, Smith D, Yamamoto M, Ma L, McCaffery P. 2003. The meninges is a source of retinoic acid for the late-developing hindbrain. J Neurosci 23:7610-7620.
176. Zhang Z, Balmer JE, Lovlie A, Fromm SH, Blomhoff R. 1996. Specific teratogenic effects of different retinoic acid isomers and analogs in the developing anterior central nervous system of zebrafish. Dev Dyn 206:73-86.
177. Zhao D, McCaffery P, Ivins KJ, Neve RL, Hogan P, Chin WW, Drager UC. 1996. Molecular identification of a major retinoic-acid-synthesizing enzyme, a retinaldehyde-specific dehydrogenase. Eur J Biochem 240:15-22.
178. Zhao Q, Dobbs-McAuliffe B, Linney E. 2005. Expression of CYP26b1 during zebrafish early development. Gene Expr Patterns 5:363-369.