Skip to main content
SpringerLink
Log in

Transcriptional Regulation at the Neural Plate Border

  • Chapter
Neural Crest Induction and Differentiation

Part of the book series: Advances in Experimental Medicine and Biology ((volume 589))

Abstract

The neural crest (NC) is usually defined as a cell type arising at the border of the neural plate and the epidermis in vertebrate embryos. While accurate, this definition implies that the border exists as a distinct boundary, which is not really the case. Like other domains in the early embryo, the NC is not a sharply delimited territory, but rather is an overlapping zone of specification that has characteristics of both epidermis and neural plate, with additional characteristics of its own. This can be seen in the spatial pattern of regulatory factors that have been implicated in NC induction, many of which are shared.1 For example Msx1 and AP2 are also expressed in the epidermis, at lower levels, and c-myc is likewise transcribed in neural plate in addition to NC. Nor is this limited to regulatory factors. The epidermal keratins, which constitute the intermediate filament cytoskeleton of epidermal cells are also expressed in NC, at a lower level than the epidermis. This can be seen by in situ hybridization (Fig. 1A) as a region of relatively weak but significant signal in the cranial neural crest region. Another indication of the fuzzy nature of NC comes from lineage mapping experiments in the chick embryo, which show that cells fated to differentiate as NC, neural plate, epidermis and placodal derivatives are all intermingled in the neural-epidermal boundary region.2 Nor is there always a clear gap visible between neural plate and epidermal gene expression domains, for example in a double in situ with epidermal keratin and the pan-neural marker NCAM the two domains are contiguous (Fig. 1B). Expression of keratin genes is also evident in animal caps that have been dissected from embryos injected with BMP antagonists, such as chordin, along with a canonical Wnt signal molecule, such as Wnt3a.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Similar content being viewed by others

References

  1. Huang X, Saint-Jeannet JP. Induction of the neural crest and the opportunities of life on the edge. Developmental Biology 2004; 275(1):1–11.

    Article  PubMed  CAS  Google Scholar 

  2. Streit A. Extensive cell movements accompany formation of the otic placode. Dev Biol 2002; 249(2):237–254.

    Article  PubMed  CAS  Google Scholar 

  3. Meulemans D, Bronner-Fraser M. Gene-regulatory interactions in neural crest evolution and development. Developmental Cell 2004; 7(3):291–299.

    Article  PubMed  CAS  Google Scholar 

  4. Cohen SM, Bronner G, Kuttner F et al. Distal-less encodes a homoeodomain protein required for limb development in Drosophila. Nature 1989; 338(6214):432–434.

    Article  PubMed  CAS  Google Scholar 

  5. Bendall AJ, Abate-Shen C. Roles for Msx and Dlx homeoproteins in vertebrate development. Gene 2000; 247(1–2):17–31.

    Article  PubMed  CAS  Google Scholar 

  6. Feledy JA, Morasso MI, Jang SI et al. Transcriptional activation by the homeodomain protein distal-less 3. Nucleic Acids Res 1999; 27(3):764–770.

    Article  PubMed  CAS  Google Scholar 

  7. Stock DW, Ellies DL, Zhao Z et al. The evolution of the vertebrate Dlx gene family. Proc Natl Acad Sci USA 1996; 93(20):10858–10863.

    Article  PubMed  CAS  Google Scholar 

  8. Luo T, Matsuo-Takasaki M, Lim JH et al. Differential regulation of Dlx gene expression by a BMP morphogenetic gradient. Int J Dev Biol 2001; 45(4):681–684.

    PubMed  CAS  Google Scholar 

  9. Luo T, Matsuo-Takasaki M, Sargent TD. Distinct roles for Distal-less genes Dlx3 and Dlx5 in regulating ectodermal development in Xenopus. Mol Reprod Dev 2001; 60(3):331–337.

    Article  PubMed  CAS  Google Scholar 

  10. Papalopulu N, Kintner C. Xenopus Distal-less related homeobox genes are expressed in the developing forebrain and are induced by planar signals. Development 1993; 117(3):961–975.

    PubMed  CAS  Google Scholar 

  11. Panganiban G, Rubenstein JL. Developmental functions of the Distal-less/Dlx homeobox genes. Development 2002; 129(19):4371–4386.

    PubMed  CAS  Google Scholar 

  12. Zhang H, Catron KM, Abate-Shen C. A role for the Msx-1 homeodomain in transcriptional regulation: Residues in the N-terminal arm mediate TATA binding protein interaction and transcriptional repression. Proc Natl Acad Sci USA 1996; 93(5):1764–1769.

    Article  PubMed  CAS  Google Scholar 

  13. Lee H, Habas R, Abate-Shen C. MSX1 cooperates with histone H1b for inhibition of transcription and myogenesis. Science 2004; 304(5677):1675–1678.

    Article  PubMed  CAS  Google Scholar 

  14. Zhang H, Hu G, Wang H et al. Heterodimerization of Msx and Dlx homeoproteins results in functional antagonism. Mol Cell Biol 1997; 17(5):2920–2932.

    PubMed  CAS  Google Scholar 

  15. Bryan JT, Morasso MI. The Dlx3 protein harbors basic residues required for nuclear localization, transcriptional activity and binding to Msx1. J Cell Sci 2000; 113 (Pt 22):4013–4023.

    PubMed  CAS  Google Scholar 

  16. Alvarez Martinez CE, Binato R, Gonzalez S et al. Characterization of a Smad motif similar to Drosophila mad in the mouse Msx 1 promoter. Biochem Biophys Res Commun 2002; 291(3):655–662.

    Article  PubMed  CAS  Google Scholar 

  17. Suzuki A, Ueno N, Hemmati-Brivanlou A. Xenopus msx1 mediates epidermal induction and neural inhibition by BMP4. Development 1997; 124(16):3037–3044.

    PubMed  CAS  Google Scholar 

  18. Brugger SM, Merrill AE, Torres-Vazquez J et al. A phylogenetically conserved cis-regulatory module in the Msx2 promoter is sufficient for BMP-dependent transcription in murine and Drosophila embryos. Development 2004; 131(20):5153–5165.

    Article  PubMed  CAS  Google Scholar 

  19. Jaynes JB, O’Farrell PH. Active repression of transcription by the engrailed homeodomain protein. EMBO J 1991; 10(6):1427–1433.

    PubMed  CAS  Google Scholar 

  20. Miyama K, Yamada G, Yamamoto TS et al. A BMP-inducible gene, dlx5, regulates osteoblast differentiation and mesoderm induction. Dev Biol 1999; 208(1):123–133.

    Article  PubMed  CAS  Google Scholar 

  21. Feledy JA, Beanan MJ, Sandoval JJ et al. Inhibitory patterning of the anterior neural plate in Xenopus by homeodomain factors Dlx3 and Msx1. Dev Biol 1999; 212(2):455–464.

    Article  PubMed  CAS  Google Scholar 

  22. Beanan MJ, Feledy JA, Sargent TD. Regulation of early expression of Dlx3, a Xenopus anti-neural factor, by beta-catenin signaling. Mech Dev 2000; 91(1–2):227–235.

    Article  PubMed  CAS  Google Scholar 

  23. Woda JM, Pastagia J, Mercola M et al. Dlx proteins position the neural plate border and determine adjacent cell fates. Development 2003; 130(2):331–342.

    Article  PubMed  CAS  Google Scholar 

  24. Saint-Germain N, Lee YH, Zhang YH et al. Specification of the otic placode depends on Sox9 function in Xenopus. Development 2004; 131(8):1755–1763.

    Article  PubMed  CAS  Google Scholar 

  25. Solomon KS, Fritz A. Concerted action of two dlx paralogs in sensory placode formation. Development 2002; 129(13):3127–3136.

    PubMed  CAS  Google Scholar 

  26. McLarren KW, Litsiou A, Streit A. DLX5 positions the neural crest and preplacode region at the border of the neural plate. Dev Biol 2003; 259(1):34–47.

    Article  PubMed  CAS  Google Scholar 

  27. Kolm PJ, Sive HL. Efficient hormone-inducible protein function in Xenopus laevis. Dev Biol 1995; 171(1):267–272.

    Article  PubMed  CAS  Google Scholar 

  28. Kaji T, Artinger KB. dlx3b and dlx4b function in the development of Rohon-Beard sensory neurons and trigeminal placode in the zebrafish neurula. Dev Biol 2004; 276(2):523–540.

    Article  PubMed  CAS  Google Scholar 

  29. Tribulo C, Aybar MJ, Nguyen VH et al. Regulation of Msx genes by a Bmp gradient is essential for neural crest specification. Development 2003; 130(26):6441–6452.

    Article  PubMed  CAS  Google Scholar 

  30. Mayor R, Young R, Vargas A. Development of neural crest in Xenopus. Curr Top Dev Biol 1999; 43:85–113.

    PubMed  CAS  Google Scholar 

  31. Willert J, Epping M, Pollack JR et al. A transcriptional response to Wnt protein in human embryonic carcinoma cells. BMC Dev Biol 2002; 2(1):8.

    Article  PubMed  Google Scholar 

  32. Tribulo C, Aybar MJ, Sanchez SS et al. A balance between the anti-apoptotic activity of Slug and the apoptotic activity of msx1 is required for the proper development of the neural crest. Dev Biol 2004; 275(2):325–342.

    Article  PubMed  CAS  Google Scholar 

  33. Mohibullah N, Donner A, Ippolito JA et al. SELEX and missing phosphate contact analyses reveal flexibility within the AP-2[alpha] protein: DNA binding complex. Nucleic Acids Res 1999; 27(13):2760–2769.

    Article  PubMed  CAS  Google Scholar 

  34. Satoda M, Zhao F, Diaz GA et al. Mutations in TFAP2B cause Char syndrome, a familial form of patent ductus arteriosus. Nat Genet 2000; 25(1):42–46.

    Article  PubMed  CAS  Google Scholar 

  35. Hilger-Eversheim K, Moser M, Schorle H et al. Regulatory roles of AP-2 transcription factors in vertebrate development, apoptosis and cell-cycle control. Gene 2000; 260(1–2): 1–12.

    Article  PubMed  CAS  Google Scholar 

  36. Luo T, Matsuo-Takasaki M, Thomas ML et al. Transcription factor AP-2 is an essential and direct regulator of epidermal development in Xenopus. Dev Biol 2002; 245(1):136–144.

    Article  PubMed  CAS  Google Scholar 

  37. Maconochie M, Krishnamurthy R, Nonchev S et al. Regulation of Hoxa2 in cranial neural crest cells involves members of the AP-2 family. Development 1999; 126(7):1483–1494.

    PubMed  CAS  Google Scholar 

  38. Knight RD, Javidan Y, Nelson S et al. Skeletal and pigment cell defects in the lockjaw mutant reveal multiple roles for zebrafish tfap2a in neural crest development. Dev Dyn 2004; 229(1):87–98.

    Article  PubMed  CAS  Google Scholar 

  39. Mitchell PJ, Timmons PM, Hebert JM et al. Transcription factor AP-2 is expressed in neural crest cell lineages during mouse embryogenesis. Genes Dev 1991; 5(1):105–119.

    Article  PubMed  CAS  Google Scholar 

  40. Schorle H, Meier P, Buchert M et al. Transcription factor AP-2 essential for cranial closure and craniofacial development. Nature 1996; 381(6579):235–238.

    Article  PubMed  CAS  Google Scholar 

  41. Zhang J, Hagopian-Donaldson S, Serbedzija G et al. Neural tube, skeletal and body wall defects in mice lacking transcription factor AP-2. Nature 1996; 381(6579):238–241.

    Article  PubMed  CAS  Google Scholar 

  42. Moser M, Pscherer A, Roth C et al. Enhanced apoptotic cell death of renal epithelial cells in mice lacking transcription factor AP-2beta. Genes Dev 1997; 11(15):1938–1948.

    PubMed  CAS  Google Scholar 

  43. Auman HJ, Nottoli T, Lakiza O et al. Transcription factor AP-2gamma is essential in the extra-embryonic lineages for early postimplantation development. Development 2002; 129(11):2733–2747.

    PubMed  CAS  Google Scholar 

  44. Brewer S, Jiang X, Donaldson S et al. Requirement for AP-2alpha in cardiac outflow tract morphogenesis. Mech Dev 2002; 110(1–2):139–149.

    Article  PubMed  CAS  Google Scholar 

  45. Brewer S, Feng W, Huang J et al. Wnt1-Cremediated deletion of AP-2alpha causes multiple neural crest-related defects. Dev Biol 2004; 267(1):135–152.

    Article  PubMed  CAS  Google Scholar 

  46. Danielian PS, Muccino D, Rowitch DH et al. Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Curr Biol 1998; 8(24):1323–1326.

    Article  PubMed  CAS  Google Scholar 

  47. Neuhauss SC, Solnica-Krezel L, Schier AF et al. Mutations affecting craniofacial development in zebrafish. Development 1996; 123:357–367.

    PubMed  CAS  Google Scholar 

  48. Schilling TF, Piotrowski T, Grandel H et al. Jaw and branchial arch mutants in zebrafish I: Branchial arches. Development 1996; 123:329–344.

    PubMed  CAS  Google Scholar 

  49. Barrallo-Gimeno A, Holzschuh J, Driever W et al. Neural crest survival and differentiation in zebrafish depends on mont blanc/tfap2a gene function. Development 2004; 131(7):1463–1477.

    Article  PubMed  CAS  Google Scholar 

  50. Knight RD, Nair S, Nelson SS et al. lockjaw encodes a zebrafish tfap2a required for early neural crest development. Development 2003; 130(23):5755–5768.

    Article  PubMed  CAS  Google Scholar 

  51. Luo T, Lee YH, Saint-Jeannet JP et al. Induction of neural crest in Xenopus by transcription factor AP2alpha. Proc Natl Acad Sci USA 2003; 100(2):532–537.

    Article  PubMed  CAS  Google Scholar 

  52. Dagle JM, Littig JL, Sutherland LB et al. Targeted elimination of zygotic messages in Xenopus laevis embryos by modified oligpnucleotides possessing terminal cationic linkages. Nucleic Acids Res 2000; 28(10):2153–2157.

    Article  PubMed  CAS  Google Scholar 

  53. Dagle JM, Weeks DL. Selective degradation of targeted mRNAs using partially modified oligonucleotides. Methods Enzymol 2000; 313:420–436.

    Article  PubMed  CAS  Google Scholar 

  54. Saint-Jeannet JP, He X, Varmus HE et al. Regulation of dorsal fate in the neuraxis by Wnt-1 and Wnt-3a. Proc Natl Acad Sci USA 1997; 94(25):13713–13718.

    Article  PubMed  CAS  Google Scholar 

  55. LaBonne C, Bronner-Fraser M. Neural crest induction in Xenopus: Evidence for a two-signal model. Development 1998; 125(13):2403–2414.

    PubMed  CAS  Google Scholar 

  56. Monsoro-Burq AH, Fletcher RB, Harland RM. Neural crest induction by paraxial mesoderm in Xenopus embryos requires FGF signals. Development 2003; 130(14):3111–3124.

    Article  PubMed  CAS  Google Scholar 

  57. Vallin J, Thuret R, Giacomello E et al. Cloning and characterization of three Xenopus slug promoters reveal direct regulation by Lef/beta-catenin signaling. J Biol Chem 2001; 276(32):30350–30358.

    Article  PubMed  CAS  Google Scholar 

  58. Locascio A, Manzanares M, Blanco MJ et al. Modularity and reshuffling of Snail and Slug expression during vertebrate evolution. Proc Nad Acad Sci USA 2002; 99(26):16841–16846.

    Article  CAS  Google Scholar 

  59. Satokata I, Ma L, Ohshima H et al. Msx2 deficiency in mice causes pleiotropic defects in bone growth and ectodermal organ formation. Nat Genet 2000; 24(4):391–395.

    Article  PubMed  CAS  Google Scholar 

  60. Satokata I, Maas R. Msx1 deficient mice exhibit cleft palate and abnormalities of craniofacial and tooth development. Nat Genet 1994; 6(4):348–356.

    Article  PubMed  CAS  Google Scholar 

  61. Kishi M, Mizuseki K, Sasai N et al. Requirement of Sox2-mediated signaling for differentiation of early Xenopus neuroectoderm. Development 2000; 127(4):791–800.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Molecular Genetics, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland, USA

    Thomas D. Sargent

Authors
  1. Thomas D. Sargent
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Department of Animal Biology, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA

    Jean-Pierre Saint-Jeannet Ph.D.

Rights and permissions

Reprints and permissions

Copyright information

© 2006 Landes Bioscience and Springer Science+Business Media

About this chapter

Cite this chapter

Sargent, T.D. (2006). Transcriptional Regulation at the Neural Plate Border. In: Saint-Jeannet, JP. (eds) Neural Crest Induction and Differentiation. Advances in Experimental Medicine and Biology, vol 589. Springer, Boston, MA. https://doi.org/10.1007/978-0-387-46954-6_3

Download citation

Publish with us

Policies and ethics

Search

Navigation