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Patterning Non-neural Ectoderm by Organizer-Modulated Homeodomain Factors

  • Thomas D. Sargent
Chapter

Abstract

Embryonic cells must be provided with spatial and temporal information in order for development to occur. Classical embryology suggests two general sources of spatial cues. One is based on specific and oriented distribution of egg cytoplasmic contents to rigidly arranged blastomere lineages determining fate within this architectural context. This was termed “mosaic” development and is exemplified by invertebrates such as C. elegans, certain snails and ascidians. The second classical mode of spatial organization is based on induction between cells. An extreme example of this is the mammalian embryo, which even after disaggregation and prolonged culture in vitro, can still be organized into a completely normal embryo (Gilbert 2000). With its fertilization-triggered cytoplasmic rearrangements and partially defined fate map at early cleavage, Xenopus is somewhere in the middle of this spectrum, but has been particularly useful for studies of induction. The cell—cell interactions that drive this organizational mechanism have been a major topic of investigation for the past 100 years or so, reaching a historical, if not mechanistic, climax in 1924 with the embryological characterization of what became known as the Spemann/Mangold organizer. An important corollary of the organizer model, and the many studies that it inspired, is the concept of intercellular signals, or morphogens, that are generated from local sources, and somehow diffuse or are transported away from this source, leading to a morphogenetic gradient of signal strength that conveys positional information to embryonic cells. Several molecules have been postulated to serve this function with respect to the organizer, most notably members of the bone morphogenetic protein (BMP) subfamily of TGFβ-like growth factors, predominantly ventral in origin, and BMP antagonists secreted by organizer tissue (Balemans and van Hul 2002).

Keywords

Bone Morphogenetic Protein Neural Crest Neural Plate Bone Morphogenetic Protein Signaling Cement Gland 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Balemans W, van Hul W (2002) Extracellular regulation of BMP signaling in vertebrates: a cocktail of modulators. Dev Biol 250: 231–250PubMedCrossRefGoogle Scholar
  2. Beanan MJ, Feledy JA, Sargent TD (2000) Regulation of early expression of Dlx3, a Xenopus anti-neural factor, by beta-catenin signaling. Mech Dev 91: 227–235PubMedCrossRefGoogle Scholar
  3. Bendall AJ, Rincon-Limas DE, Botas J, Abate-Shen C (1998) Protein complex formation between Msxl and Lhx2 homeoproteins is incompatible with DNA binding activity. Differentiation 63: 151–157PubMedCrossRefGoogle Scholar
  4. Blitz IL, Cho KW (1995) Anterior neurectoderm is progressively induced during gastrulation: the role of the Xenopus homeobox gene orthodenticle. Development 121: 993–1004PubMedGoogle Scholar
  5. Catron KM, Zhang H, Marshall SC, Inostroza JA, Wilson JM, Abate C (1995) Transcriptional repression by Msx-1 does not require homeodomain DNA-binding sites. Mol Cell Biol 15: 861–871PubMedGoogle Scholar
  6. Davidson EH (2001) Genomic regulatory systems: development and evolution. Academic Press, San Diego, CAGoogle Scholar
  7. De Robertis EM, Wessely O, Oelgeschlager M, Brizuela B, Pera E, Larrain J, Abreu J, Bachiller D (2001) Molecular mechanisms of cell-cell signaling by the Spemann-Mangold organizer. Int J Dev Biol 45 (1 Spec No): 189–197PubMedGoogle Scholar
  8. Ekker M, Akimenko MA, Bremiller R, Westerfield M (1992) Regional expression of three homeobox transcripts in the inner ear of zebrafish embryos. Neuron 9: 27–35PubMedCrossRefGoogle Scholar
  9. Faure S, Lee MA, Keller T, ten Dijke P, Whitman M (2000) Endogenous patterns of TGFbeta superfamily signaling during early Xenopus development. Development 127: 2917–2931PubMedGoogle Scholar
  10. Feledy JA, Beanan MJ, Sandoval JJ, Goodrich JS, Lim JH, Matsuo-Takasaki M, Sato S, Sargent TD (1999a) Inhibitory patterning of the anterior neural plate in Xenopus by homeodomain factors Dlx3 and Msx1. Dev Biol 212: 455–464PubMedCrossRefGoogle Scholar
  11. Feledy JA, Morasso MI, Jong S-I, Sargent TD (1999b) Transcriptional activation by the homeodomain protein Distal-less 3. Nucleic Acids Res 27: 764–770PubMedCrossRefGoogle Scholar
  12. Gilbert, SF (2000) Developmental biology, 6th edn. Sinauer Associates, Sunderland, MAGoogle Scholar
  13. Hausen P, Riebesell M (1991) The early development of Xenopus laevis: an atlas of the histology. Springer, Berlin Heidelberg New YorkGoogle Scholar
  14. Ishimura A, Maeda R, Takeda M, Kikkawa M, Daar IO, Maeno M (2000) Involvement of BMP-4/ msx-1 and FGF pathways in neural induction in the Xenopus embryo. Dev Growth Differ 42: 307–316PubMedCrossRefGoogle Scholar
  15. LaBonne C, Bronner-Fraser M (1998) Neural crest induction in Xenopus: evidence for a two-signal model. Development 125: 2403–2014PubMedGoogle Scholar
  16. Luo T, Matsuo-Takasaki M, Lim JH, Sargent TD (200la) Differential regulation of Dlx gene expression by a BMP morphogenetic gradient. Int J Dev Biol 45: 681–684Google Scholar
  17. Luo T, Matsuo-Takasaki M, Sargent TD (200 lb) Distinct roles for Distal-less genes Dlx3 and Dlx5 in regulating ectodermal development in Xenopus. Mol Reprod Dev 60: 331–337Google Scholar
  18. Maeda R, Kobayashi A, Sekine R, Lin JJ, Kung H, Maeno M (1997) Xmsx-1 modifies mesodermaltissue pattern along dorsoventral axis in Xenopus laevis embryo. Development 124: 2553–2560PubMedGoogle Scholar
  19. Marchant L, Linker C, Ruiz P, Guerrero N, Mayor R (1998) The inductive properties of mesoderm suggest that the neural crest cells are specified by a BMP gradient. Dev Biol 198: 319–329PubMedGoogle Scholar
  20. Mayor R, Morgan R, Sargent MG (1995) Induction of the prospective neural crest of Xenopus. Development 121: 767–777PubMedGoogle Scholar
  21. Mizuseki K, Kishi M, Matsui M, Nakanishi S, Sasai Y (1998) Xenopus zic-related-1 and Sox2 two factors induced by chordin have distinct activities in the initiation of neural induction. Development 125: 579–587Google Scholar
  22. Morasso MI, Grinberg A, Robinson G, Sargent TD, Mahon KA (1999) Placental failure in mice lacking the homeobox gene Dlx3. Proc Natl Acad Sci USA 96: 162–167PubMedCrossRefGoogle Scholar
  23. Morgan R, Sargent MG (1997) The role in neural patterning of translation initiation factor eIF4AII; induction of neural fold genes. Development 124: 2751–2760PubMedGoogle Scholar
  24. Nakata K, Nagai T, Aruga J, Mikoshiba K (1997) Xenopus Zic3, a primary regulator both in neural and neural crest development. Proc Natl Acad Sci USA 94: 11980–11985Google Scholar
  25. Nguyen VH, Schmid B, Trout J, Connors SA, Ekker M, Mullins MC (1998) Ventral and lateral regions of the zebrafish gastrula, including the neural crest progenitors, are established by a bmp2b/swirl pathway of genes. Dev Biol 199: 93–110PubMedCrossRefGoogle Scholar
  26. Panganiban G, Rubenstein JL (2002) Developmental functions of the Distal-less/Dlx homeobox genes. Development 129: 4371–4386PubMedGoogle Scholar
  27. Pannese M, Polo C, Andreazzoli M, Vignali R, Kablar B, Barsacchi G, Boncinelli E (1995) The Xenopus homologue of Otx2 is a maternal homeobox gene that demarcates and specifies anterior body regions. Development 121: 707–720PubMedGoogle Scholar
  28. Pera E, Stein S, Kessel M (1999) Ectodermal patterning in the avian embryo: epidermis versus neural plate. Development 126: 63–73PubMedGoogle Scholar
  29. Robledo RF, Rajan L, Li X, Lufkin T (2002) The Dlx5 and Dlx6 homeobox genes are essential for craniofacial, axial, and appendicular skeletal development. Genes Dev 16: 1089–1101PubMedCrossRefGoogle Scholar
  30. Saint-Jeannet JP, He X, Varmus HE, Dawid IB (1997) Regulation of dorsal fate in the neuraxis by Wnt-1 and Wnt-3a. Proc Natl Acad Sci USA 94: 13713–13718PubMedCrossRefGoogle Scholar
  31. Sive H, Hattori K, Weintraub H (1989) Progressive determination during formation of the anteroposterior axis in Xenopus laevis. Cell 58: 171–180PubMedCrossRefGoogle Scholar
  32. Solomon KS, Fritz A (2002) Concerted action of two dlx paralogs in sensory placode formation. Development 129: 3127–3136PubMedGoogle Scholar
  33. Suzuki A, Theis RS, Yamaji N, Song JJ, Wozney J, Murakami K, Ueno N (1994) A truncated BMP receptor affects dorsal-ventral patterning in the early Xenopus embryo. Proc Natl Acad Sci USA 91: 10255–10259PubMedCrossRefGoogle Scholar
  34. Suzuki A, Ueno N, Hemmati-Brivanlou A (1997) Xenopus msxl mediates epidermal induction and neural inhibition by BMP4. Development 124: 3037–3044Google Scholar
  35. Vaglia JL, Hall BK (1999) Regulation of neural crest cell populations: occurrence, distribution and underlying mechanisms. Int J Dev Biol 43: 95–110PubMedGoogle Scholar
  36. Wilson PA, Lagna G, Suzuki A, Hemmati-Brivanlou A (1997) Concentration-dependent patterning of the Xenopus ectoderm by BMP4 and its signal transducer Smadl. Development 124: 3177–3184PubMedGoogle Scholar
  37. Yang L, Zhang H, Hu G, Wang H, Abate-Shen C, Shen MM (1998) An early phase of embryonic Dlx5 expression defines the rostral boundary of the neural plate. J Neurosci 18: 8322–8330PubMedGoogle Scholar
  38. Zhang H, Hu G, Wang H, Sciavolino P, 11er N, Shen MM, Abate-Shen C (1997) Heterodimerization of Msx and Dlx homeoproteins results in functional antagonism. Mol Cell Biol 17: 2920–2932PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2004

Authors and Affiliations

  • Thomas D. Sargent
    • 1
  1. 1.Laboratory of Molecular Genetics, National Institute of Child Health and Human DevelopmentNational Institutes of HealthBethesdaUSA

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