Skip to main content
Log in

Retinoic acid and mammalian craniofacial morphogenesis

  • Published:
Journal of Biosciences Aims and scope Submit manuscript

Abstract

Retinoic acid is a morphogenetic signalling molecule in vertebrate embryos, one being known to perform a specific function in organizing the body pattern along the anteroposterior axis. This molecule has especially attracted research attention because retinoic acid treatment will also induce abnormal morphogenesis, particularly in the craniofacial structures. The present review discusses recent molecular insights revealing how the retinoic acid signal is transduced within a cell, specifically focusing on the involvement of cranial neural crest cells in retinoic acid-induced abnormal morphogenesis in the mammalian head

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Arcioni L, Simeone A, Guazzii S, Zappavigna V, Boncinelli E and Mavilio F 1992 The upstream region of the human homeobox gene HOX3D is a target for regulation by retinoic acid and HOX homeoproteins;EMBO J. 11 265–277

    PubMed  CAS  Google Scholar 

  • Adelman H B 1925 The development of the neural folds and cranial ganglia of the rat;J. Comp. Neural. 39 19–171

    Article  Google Scholar 

  • Balkan W, Colbert M, Brock C and Linney E 1992 Transgenic indicator mice for studying activated retinoic acid receptors during development;Proc. Natil. Acad. Sci. USA 89 3347–3351

    Article  CAS  Google Scholar 

  • Bartelmez G W 1923 The subdivisions of the neural folds in man;J. Comp. Neural. 35 231–247

    Article  Google Scholar 

  • Bartelmez G W and Evans H M 1925 Development of the human embryo during the period of somite formation, including embryos with 2 to 16 pairs of somites;Contrib. Embryol. 17 1–67

    Google Scholar 

  • Brown N A, Hunt P and Krumlauf R 1992 Craniofacial developmental abnormalities induced by triazoles a comparison of homeobox gene expression and stage-specificity with retinoic acid-induced defects;Teratology 45 456

    Google Scholar 

  • Cohlan S Q 1953 Excessive intake of vitamin A as a cause of congenital anomalies in the rat;Science 117 535–536

    Article  PubMed  CAS  Google Scholar 

  • Conlon R A and Rossant J 1992 Exogenous retinoic acid rapidly induces anterior ectopic expression of murinHox-2 genes in vivo;Development 116 357–368

    PubMed  CAS  Google Scholar 

  • Cooney A J, Tsai S Y, O’Malley B W and Tsai M J 1992 Chicken ovalbumin upstream promoter transcription factor (COUP-TF) dimers bind to different GGTCA response elements, allowing COUP-TF to repress hormonal induction of the vitamin D3, thyroid hormone, and retinoic acid receptors;Mol. Cell. Biol. 12 4153–4163

    PubMed  CAS  Google Scholar 

  • Dencker L, Annerwell E, Busch C and Eriksson U 1990 Localization of specific retinoid-binding sites and expression of cellular retinoic acid-binding protein (CRABP) in the early mouse embryo;Development 110 343–352

    PubMed  CAS  Google Scholar 

  • Dencker L, D’Argy R, Danielsson B R G, Ghantous H and Sperber G O 1987 Saturable accumulation of retinoic acid in neural and neural crest derived cells in early embryonic development;Dec. Pharmacol. Ther. 10 212–223

    CAS  Google Scholar 

  • Dencker L, Gustafson A L, Annerwell E, Bush C and Eriksson U 1991 Retinoid-binding proteins in craniofacial development;J. Craniof. Genet. Dev. Biol. 11 303–314

    CAS  Google Scholar 

  • de The A, del Mar Vivanco-Ruiz M, Tiollais, Stunnen berg H and Dejean A 1990 Identification of a retinoic acid responsive element in the retinoic acid receptorβ gene;Nature (London) 343 177–180

    Article  Google Scholar 

  • Dolle P, Ruberte E, Leroy P, Morriss-Kay G and Chambon P 1990 Retinoic acid receptors and cellular retinoid binding proteins. I. A systematic study of their differential pattern of transcription during mouse organ ogenesis;Development 110 1133–1151

    PubMed  CAS  Google Scholar 

  • Durand B, Saunders M, Leroy P, Leid M and Chambon P 1992 All-trans and 9-cis retinoic acid induction of CRABP 11 transcriptionis mediated by RAR/RXR heterodimers bound to DR1 and DR2 repeated motifs;Cell 71 73–85

    Article  PubMed  CAS  Google Scholar 

  • Eichele G 1989 Retinoids: signalling molecules in vertebrate limb pattern formation;Trends Genet. 5 246–251

    Article  PubMed  CAS  Google Scholar 

  • Evans R M 1988 The steroid and thyroid hormone receptor superfamily;Science 240 889–895

    Article  PubMed  CAS  Google Scholar 

  • Fawcett D, Pasceri P, Fraser R, Colbert M, Rossant J and Giguere V 1995 Postaxial polydactyly in forelimbs of CRABP-II mutant mice;Development 121 671–679

    PubMed  CAS  Google Scholar 

  • Fukiishi Y and Morriss-Kay G M 1992 Migration of cranial neural crest cells to the pharyngeal arches and heart in rat embryos;Cell Tissue Res. 268 1–8

    Article  PubMed  CAS  Google Scholar 

  • Geelen JAG 1979 Hypervitaminosis A induced teratogenesis;Crit. Rev. Toxicol. 6 351–375

    CAS  Google Scholar 

  • Goulding E H and Pratt R M 1986 Isotretinoin teratogenicity in mouse whole embryo culture;J. Craniof. Gene. Den. Biol. 6 99–112

    CAS  Google Scholar 

  • Green S and Chambon P 1988 Nuclear receptors enhance our understanding of transcriptional regulation;Trends Genet. 4 309–314

    Article  PubMed  CAS  Google Scholar 

  • Gustafson A L, Dencker L and Eriksson U 1993 Non-overlapping expression of CRBP I and CRABP I during pattern formation of limbs and craniofacial structures in the early mouse embryo;Development 117 451–460

    PubMed  CAS  Google Scholar 

  • Harnish D C, Jiang H, Soprano K J, Kochhar D M and Soprano D R 1992 Retinoic acid receptor β2 mRNA is elevated by retinoic acid in vivo in susceptible regions of mid-gestation mouse embryos;Dev. Dyn. 194 239–246

    PubMed  CAS  Google Scholar 

  • Heyman R A, Mangelsdorf D J, Dyck J A, Stein R B, Eichele G, Evans R M and Thaller C 1992 9-cis retinoic acid is a high affinity ligand for the retinoid X receptor;Cell 68 397–406

    Article  PubMed  CAS  Google Scholar 

  • Hale F 1937 The relation of maternal vitamin A deficiency to microphthalmia in pigs;Texas State J. Med. 33 228–232

    Google Scholar 

  • Hoffmann C and Eichele G 1994 Retinoids in development; inThe Retinoids: Biology, chemistry. and medicine, 2nd edition (eds) M B Spporn, A B Roberts and D S Goodman (New York: Raven Press) pp 387–441

    Google Scholar 

  • Hogan B G M, Thaller C and Eichele G 1992 Evidence that Hensenls node is a site of retinoic acid synthesis;Nature (London) 359 237–241

    Article  CAS  Google Scholar 

  • Horton C and Maden M 1995 Endogenous distribution of retinoids during normal development and terotogenesis in the mouse embryo;Dev. Dyn. 202 312–323

    PubMed  CAS  Google Scholar 

  • Huber J, Cholnoky P and Zoethout H E 1967 Congenital aplasia of parathyroid glands and thymus;Arch. Dis. Child. 42 190–192

    Article  PubMed  CAS  Google Scholar 

  • Hunt P and Krumlauf R 1991 Deciphering theHox code: clues to patterning pharyngeal regions of the head;Cell 66 1075–1078

    Article  PubMed  CAS  Google Scholar 

  • Kastner P, Grondona J M, Mark M, Gansmuller A, LeMeur M, Decimo D, Vonesch J L, Dolle P and Chambon P 1994 Genetic analysis of RXRa developmental function: convergence of RXR and RAR signaling pathways in heart and eye morphogenesis;Cell 78 987–1003

    Article  PubMed  CAS  Google Scholar 

  • Kirby M L 1987 Cardiac morphogenesis—Recent research advances;Pediatr. Res. 21 219–224

    Article  PubMed  CAS  Google Scholar 

  • Kliewer S A, Umesono K, Mangelsdorf D J and Evans R M 1992a Retinoid X receptor interacts with nuclear receptors in retinoic acid, thyroid hormone, and vitamin D3 signalling;Nature (London) 355 446–449

    Article  CAS  Google Scholar 

  • Kliewer S A, Umesono K, Nooman D J, Heyman R A and Evans R M 1992b Convergence of 9-cis retinoic acid and peroxisome proliferator signalling pathways through heterodimer formation of their receptors;Nature (London) 358 771–774

    Article  CAS  Google Scholar 

  • Kliewer S A, Umesono K, Heyman R A, Mangelsdorf D J, Dyck J A and Evans R M 1992c Retinoid X receptor-COUP-TF interactions modulate retinoic acid signalling;Proc. Nail. Acad. Sci. USA 89 1448–1452

    Article  CAS  Google Scholar 

  • Krumlauf R 1993Hox genes and pattern formation in the branchial region of the vertebrate head;Trends Genet. 9 106–112

    Article  PubMed  CAS  Google Scholar 

  • Lammer E J, Chen D T, Hoar R M, Agnish N D, Benke P J, Braun J T, Curry C J, Fernhoff M, Grix A W, Lott I T, Richard J M and Sun S C 1985 Retinoic acid embryopathy;N. Engl. J. Med. 313 837–841

    Article  PubMed  CAS  Google Scholar 

  • Lee Y M, Osumi-Yamashita N, Ninomiya Y, Moon C K, Eriksson U and Eto K 1995 Retinoic acid stage-dependently alters the migrationpattern and identity of hindbrain neural crest cells;Development 121 825–837

    PubMed  CAS  Google Scholar 

  • Leid M, Kastner R, Mendelsohn C, Zelent A and Chambon P 1992 Retinoic acid receptors; inRetinoids in normal development and teratogenesis (ed) G M Morriss-Kay (Oxford: Oxford University Press) pp 7–25

    Google Scholar 

  • Leonard L, Horton C, Maden M and Pizzey J A 1995 Anteriorization of CRABP-I expression by retinoic acid in the developing mouse central nervous system and its relationship to teratogenesis;Dev. Biol. 168 514–528

    Article  PubMed  CAS  Google Scholar 

  • Leroy P, Krust A, Kastner R, Lyons R 1, Nakshatri H, Saunders M, Zacharewski T, Chen J-Y, Staub A, Gamier J-M, Mader S and Chambon P 1992 Purification, cloning, and RXR identity of the HeLa cell factor with which RAR or TR heterodimerizes to bind target sequences efficiently;Cell 68 377–395

    Article  Google Scholar 

  • Levin A A, Sturzenbecker L J, Kazmer S, Bosakowski T, Huselton C, Allenby G, Speck J, Kratzeisen C, Rosenberger M, Lovey A and Grippo J F 1992 9-cis retinoic acid sterioisomer binds and activates the nuclear receptor RXRcςNature (London) 355 359–361

    Article  CAS  Google Scholar 

  • Li E, Sucov H M, Lee K F, Evans R M and Jaenisch R 1993 Normal development and growth of mice carrying a targeted disruption of the a l retinoic acid receptor gene;Proc. Nail. Acid. Sei. USA 90 1590–1594

    Article  CAS  Google Scholar 

  • Lohhnes D, Kastner P, Dierich A, Mark M, LeMeur M and Chanbon P 1993 Function of retinoic acid receptor y in the mouse;Cell 73 643–658

    Article  Google Scholar 

  • Lufkin T, Lohnes D, Mark M, Dierich A, Gorry P, Gaub M P, LeMeur M and Chambon P 1993 High postnatal lethality and testis degeneration in retinoic acid receptor alpha mutant mice;Proc. Natl. Acad. Sci. USA 90 7225–7229

    Article  PubMed  CAS  Google Scholar 

  • Luo J, Pasceri P, Conlon R A, Rossant J and Giguêre V 1995 Mice lacking all isoforms of retinoic acid receptor β develop normally and are susceptible to the teratogenic effects of retinoic acid;Mech. Dev. 53 61–71

    Article  PubMed  CAS  Google Scholar 

  • Luo J, Sucov 1-I M, Bader J -A, Evans R M and Gigere V 1996 Compound mutants for retinoic acid receptor (RAR)β and RAR al reveal developmental functions for multiple RAR isoforms;Mech. Dev. 55 33–44

    Article  PubMed  CAS  Google Scholar 

  • Maden M 1982 Vitamin A and pattern formation in the regenerating limb;Nature (London) 295 672–675

    Article  CAS  Google Scholar 

  • Maden M, Horton C, Graham A, Leonard L and Pizzey J, Siegenthaler G, Lumsden A and Eriksson U 1992 Domains of cellular-retinoic-acid-binding protein I (CRABP I) expression in the hindbrain and neural crest of the mouse embryo;Mech. Dev. 37 13–23

    Article  PubMed  CAS  Google Scholar 

  • Mangelsdorf D J, Borgmeyer U, Heyman R A, Zhou J Y, Ong E S, Oro A E, Kakizukia A and Evans R M 1992 Characterization of three RXR genes that mediate the action of 9-cis retinoic acid;Genes Dev. 6 329–344

    Article  PubMed  CAS  Google Scholar 

  • Mangelsdorf D J, Umesono K and Evans R M 1994 The retinoid receptors; inRetinoids: Biology, chemistry, and medicine 2nd edition (eds) M B Spporn, A B Roberts and D S Goodman (New York: Raven Press) pp 319–385

    Google Scholar 

  • Marshall FL Nochev S, Sham M Fl, Muchamore 1, Lumsden A and Krumlauf R 1992 Retinoic acid alters hindbrainHox code and induces transformation of rhombomeres 2/3 into a 4/5 identity;Nature (London) 360 737–741

    Article  CAS  Google Scholar 

  • Marshall H, Studer M, Popperl H, Aparicio S, Kuroiwa A, Brenner S and Krumlauf R 1994 A conserved retinoic acid response element required for early expression of the homeobox geneHoxb-1;Nature (London) 370 567–571

    Article  CAS  Google Scholar 

  • Matsuo T, Osumi-Yamashita N, Noji S, Ohuchi H, Koyama E, Myokai F, Matsuo N, Taniguchi S, Doi H, Iseki S, Ninomiya Y, Fujiwara M, Watanabe T and Eto K 1993 A mutation in thePax-6 gene in ratsmall eye is associated with impaired migration of midbrain crest cells;Nature Genet. 3 299–304

    Article  PubMed  CAS  Google Scholar 

  • McGinnis W and Krumlauf R 1992 Homeobox genes and axial patterning;Cell 68 283–302

    Article  PubMed  CAS  Google Scholar 

  • Meier S and Tam PPL 1982 Metameric pattern development in the embryonic axis of the mouse;Differentiation 21 95–108

    Article  PubMed  CAS  Google Scholar 

  • Mendelsohn C, Mark M, Dolle P, Dierich A, Gaub M P, Krust A, Lamron C and Chambon P 1994 Retinoic acid receptor beta 2 (RARβ2) null mutant mice appear normal;Dev. Biol. 166 246–258

    Article  PubMed  CAS  Google Scholar 

  • Morriss G M 1972 Morphogenesis of the malformations induced in rat embryos by maternal hypervitaminosis A;J.Anat. 113 241

    PubMed  CAS  Google Scholar 

  • Morriss G M and Thorogood P V 1978 An approach to cranial neural crest cell migration and differentiation in mammalian embryos; inDevelopment in mammals (ed.) M Johnson (Cambridge: Cambridge Univ. Press) Vol. 3, pp 363–412

    Google Scholar 

  • Morriss-Kay G M 1992aRetinoids in normal development and teratogenesis (Oxford: Oxford Univ. Press)

    Google Scholar 

  • Morriss-Kay G M 1992b Retinoic acid receptors in normal growth and development;Cancer Surv. 14 181–193

    PubMed  CAS  Google Scholar 

  • Morriss-Kay G M 1993 Retinoic acid and craniofacial development: Molecules and morphogenesis;BioEssays 15 9–15

    Article  PubMed  CAS  Google Scholar 

  • Morriss-Kay G M, Murphy P, Hill R E and Davidson D R 1991 Effects of retinoic acid excess on expression of Hox-2.9 andKrox-20 and on morphological segmentation in the hindbrain of mouse embryos;EMBOJ. 10 2985–2995

    CAS  Google Scholar 

  • Morriss-Kay G M and Tan S S 1987 Mapping cranial neural crest cell migration pathways in mammalian embryos;Trends Genet. 3 257–261

    Article  Google Scholar 

  • Motoyama J, Eto K 1994 Antisense retinoic acid recetor g-1 ologonucleotide enhances chondrogenesis of mouse limb mesenchymal cells in vitro;FEBS Lett. 228 319–322

    Article  Google Scholar 

  • Motoyama J, Taki K, Osumi-Yamashita N and Eto K 1994 Retinoic acid treatment induces cell death and the protein expression of retinoic acid receptor fi in the mesenchymal cells of mouse facial primordia in vitro;Dev. Growth Differ. 36 281–288

    Article  CAS  Google Scholar 

  • Niazi I A and Saxena S 1978 Abnormal hind limb regeneration in tadpoles of the toad,Bufo andersoni exposed to excess vitamin A;Folio Biol. (Krakow) 26 3–8

    CAS  Google Scholar 

  • Nichols D H 1981 Neural crest formation in the head of the mouse embryos as observed using a new histological technique;J. Embryol. Exp. Morphol. 6 105–120

    Google Scholar 

  • Nichols D H 1986 Formation and distribution of neural crest mesenchyme to the first pharyngeal arch region of the mouse embryo;Am. J. Anat. 176 221–231

    Article  PubMed  CAS  Google Scholar 

  • Noden D M 1983 The role of the neural crest in patterning of avian cranial skeletal, connective and muscle tissues;Der. Biol. 96 144–165

    CAS  Google Scholar 

  • Ong D E, Newcdomer M E and Chytil F 1994 Cellular retinoid-binding proteins; inRetinoids: Biology. chemistry and medicine, 2nd edition (eds) M B Spporn, A B Roberts and D S Goodman (New York: Raven Press)pp 283–317

    Google Scholar 

  • Osumi-Yamashita N and Etc K 1990 Mammalian cranial neural crest cells and facial development;Dev. Growth Differ. 32 451–459

    Article  Google Scholar 

  • Osumi-Yamashita N, Iseki S, Noji S, Nohno T, Koyama E, Taniguchi S, Doi H and Eto K 1992 Retinoic acid treatment induces the ectopic expression of retinoic acid receptor β gene and excessive cell death in the embryonic mouse face;Dev. Growth Differ. 34 199–209

    Article  CAS  Google Scholar 

  • Osumi-Yamashita N, Ninomiya Y N, Doi H and Eto K 1994 The contribution of both forebrain and midbrain crest cells to the mesenchyme in the frontonasal mass of mouse embryos;Dev. Biol. 164 409–419

    Article  PubMed  CAS  Google Scholar 

  • Osumi-Yamashita N, Ninomiya Y N, Doi H and Eto K 1996 Rh ombomere formation and hindbrain crest cell migration from prorhombomeric origins in mouse embryos;Dev. Growth Differ. 38 107–118

    Article  Google Scholar 

  • Osumi-Yamashita N, Noji S, Nohno T, Koyama E, Doi H, Eto K and Taniguchi S 1990 Expression of retinoic acid receptor genes in the neural crest derived cells during mouse facial development;FEBS Lett. 264 71–74

    Article  PubMed  CAS  Google Scholar 

  • Papalopulu N, Lovell-Badge R and Krumlauf 1991 The expression of murineHox-2 genes is dependent on the differentiation pathway and displays a collinear sensitivity to retionic acid in F9 cells and Xenopus embryos;Nucleic Acids Res. 19 5497–5506

    Article  PubMed  CAS  Google Scholar 

  • Qiu Y, Cooney A j, Kuratani S, DeMayo F J, Tsai S Y and Tsai M J 1994 Spatiotemporal expression patterns of chicken ovalbumin upstream promoter-transcription factors in the developing mouse central nervous system: evidence for a role in segmental patterning of the diencephalon;Proc. Natl. Acad. Sci. USA 91 4451–4455

    Article  PubMed  CAS  Google Scholar 

  • Rijli F M, Mark M, Lakkaraju S, Dierich A, Dolle P and Chambon P 1993 A homeotic transformation is generated in the rostral branchial region of the head by disruption ofHoxa-2, which acts as a selector gene;Cell 75 1333–1349

    Article  PubMed  CAS  Google Scholar 

  • Rossant J, Zirngiblle R, Cado D, Shago M and Giguere V 1991 Expression of a retinoic acid response element-hspplacZ transgene defines specific domains of transcriptional activity during mouse embryogenesis;Genes Dee. 5 1333–1344

    Article  CAS  Google Scholar 

  • Rowe A, Richman J and Brickell P M 1991 A member of the RXR nuclear receptor family is expressed in neural-crest-derived cells of the developing chick peripheral nervous system;Development 111 771–778

    PubMed  CAS  Google Scholar 

  • Ruberte E, Dolle P, Chambon P and 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

    PubMed  CAS  Google Scholar 

  • Ruberte E, Dolle P, Krust A, Zelent A, Morriss-Kay G and Chambon P 1990 Specific spatial and temporal distribution of retinoic acid receptor y transcripts during mouse embryogenesis;Development 108 213–222

    PubMed  CAS  Google Scholar 

  • Ruberte E, Friederich V, Morriss-Kay G and Chambon P 1992 Differential distribution patterns of CRABP I and CRABP II transcripts during mouse embryogenesis;Development 115 973–987

    PubMed  CAS  Google Scholar 

  • Schuh T and Kimelman D 1992 COUP-TFI is a potential regulator of retinoic acid-modulated developmentin Xenopus embryos;Mech. Dev. 51 39 -49

    Article  Google Scholar 

  • Serbedzija G N, Bonner-Fraser M and Fraser S E 1992 Vital dye analysis of cranial neural crest cell migration in the mouse embryo;Development 116 297–307

    PubMed  CAS  Google Scholar 

  • Shenefelt R E 1972 Morphogenesis of malformations in hamsters caused by retinoic acid: Relation of dose and stage at treatment;Teratology 5 103–118

    Article  PubMed  CAS  Google Scholar 

  • Siebert J R, Graham J M Jr and MacDonald C 1985 Pathologic features of the CHARGE association: support for involvement of the neural crest;Teratology 31 331–336

    Article  PubMed  CAS  Google Scholar 

  • Simeone A, Acampora D, Arcioni L, Andrew P W, Boncinelli E and Mavilio F 1990 Sequential activation ofHox2 homeobox genes by retinoic acid in human embryonal carcinoma cells;Nature (London) 346 764–767

    Article  Google Scholar 

  • Simeone A, Acampora D, Nigro V, Faiella A, D’Esposito M, Stornainolo A, Mavilio F and Boncinelli E 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

    Article  PubMed  CAS  Google Scholar 

  • Simeone A, Avantaggiato V, Moroni M C, Mavilio F, Arra C, Cotelli F, Nigro V and Acamora D 1995 Retinoic acid induces stage-specific atnero-posterior transformation of rostral central nervous system;Mech. Dev. 51 83–98

    Article  PubMed  CAS  Google Scholar 

  • Studer M, Nipped H, Marshall H, Kuroiwa A and Krumlauf R 1994 Role of conserved retinoic acid response element in rhombomere restriction ofHoxb-1;Science 265 1728–1732

    Article  PubMed  CAS  Google Scholar 

  • Sucov H M, Dyson E, Gumeringer C L, Price J, Chien K R and Evans R M 1994 RXRa mutant mice establish a genetic basis for vitamin A signaling in hear morphogenesis;GenesDev. 8 1007–1018

    CAS  Google Scholar 

  • Sucov H M, IzpisUa-Belmonte J-C, Gaflan Y and Evans RM 1995 Mouse embryos lacking RXRa are resistent to retinoic acid-reduced limb defects;Development 121 3997–4003

    PubMed  CAS  Google Scholar 

  • Sucov H M, Murakami K K and Evans R M 1990 Characterization of an autoregulated response element in the mouse retinoic acid receptor type β gene;Proc. Natl. Acad. Sci. USA 87 5392–5396

    Article  PubMed  CAS  Google Scholar 

  • Sundin O, Janocha R and Eichele G 1993 Retinoids and pattern formation in vertebrate embryos; inCell-cell signalling in vertebrate development (eds) E Robertson, R R Maxfield and H J Vogel (New York: Academic Press) pp 157–319

    Google Scholar 

  • Tan S S and Morriss-Kay G M 1985 The development and distribution of the cranial neural crest in the rat embryo;Cell Tissue Res. 240 403–416

    Article  PubMed  CAS  Google Scholar 

  • Tabin C 1991 Retinoids homeoboxes, and growth factors: toward molecular models for limb development;Cell 66 199–217

    Article  PubMed  CAS  Google Scholar 

  • Thorogood P 1988 The developmental specification of the vertebrate skull;Development Suppl. 103 141–153

    Google Scholar 

  • Tickle C, Summerbell D and Wolppert L 1975 Positional signalling and specification of digits in chick limb morphogenesis;Nature (London) 254 199–202

    Article  CAS  Google Scholar 

  • Trainor P A and Tam PPL 1995 Cranial paraxial mesoderm and neural crest cells of the mouse embryo: co-distribution in the craniofacial mesenchyme but distinct segregation in branchial arches;Development 121 2569–2582

    PubMed  CAS  Google Scholar 

  • Webster W S, Johnston M C, Lammer E J and Sulik K K 1986 Isotretinoin embryopathy and the cranial neural crest: Anin vivo andin vitro study;J. Craniof. Gene. Dev. Biol. 6 211–222

    CAS  Google Scholar 

  • Wedden S E, Ralphs J R and Tickle C 1988 Pattern formation in the facial primordia;Development Suppl. 103 31–40

    Google Scholar 

  • Wilkinson D G 1990 Segmental gene expression in the developing mouse hindbrain;Seminars Dev. Biol. 1 127–134

    Google Scholar 

  • Wood H, Pall G and Morriss-Kay G M 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 2279–2286

    PubMed  CAS  Google Scholar 

  • Yu V C, Delsert C, Anderson B, Holloway J M, Devary 0 V, Naar A M, Kim S Y, Boutin J-M, Glass C K and Rosenfeld MG 1991 RXR β: A coregulator that enhances binding of retinoic acid, thyroid hormone, and vitamin D receptors to their cognate response elements;Cell 67 1251–1266

    Article  PubMed  CAS  Google Scholar 

  • Zimmer A and Zimmer A 1992 Induction of a RARb2-lacZ transgene by retinoic acid reflects the neuromeridic organization of the central nervous system;Development 116 977–983

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Osumi-Yamashita, N. Retinoic acid and mammalian craniofacial morphogenesis. J Biosci 21, 313–327 (1996). https://doi.org/10.1007/BF02703091

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02703091

Keywords

Navigation