Skip to main content
Log in

Role of Wnt-6 in limb myogenesis

  • Original Article
  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Abstract

Cells from the ventrolateral lip of the dermomyotome at limb levels undergo epithelio-mesenchymal transition and migrate as individual and undifferentiated cells into the limb buds. The precursor cells are under the influence of various signaling factors in the limb. Dorsal and ventral ectoderm influences various aspects of limb development. In addition to our previous studies, we investigated the influence of ectoderm and Wnt-6 on somitic cells in the limb bud. We show that in the absence of ectoderm the precursor cells never form muscle cells but differentiate into endothelial cells. In addition, we show that Wnt-6 that is secreted from the ectoderm influences the precursor cells to form muscle even in the absence of ectoderm. This indicates that Wnt-6 is an ectodermal signal that induces somite-derived progenitor cells to form muscle cells during limb development.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Amprino R, Amprino-Bonetti D (1967) Experimental observations in the development of ectoderm-free mesoderm of the limb bud in chick embryos. Nature 214:826–827

    Article  PubMed  CAS  Google Scholar 

  • Amthor H, Christ B, Weil M, Patel K (1998) The importance of timing differentiation during limb muscle development. Curr Biol 8:642–652

    Article  PubMed  CAS  Google Scholar 

  • Bladt F, Riethnacher D, Isenmann S, Aguzzi A, Birchmeier C (1995) Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature 376:768–771

    Article  PubMed  CAS  Google Scholar 

  • Bolender DL, Lawrence J, Krug EL, Markwald RR (1993) Effects of ectoderm co-culture and conditioned medium on the limb mesoderm in vitro. Prog Clin Biol Res 383:141–151

    Google Scholar 

  • Chevallier A, Kieny M, Mauger A (1977) Limb-somite relationship: origin of the limb musculature. J Embryol Exp Morphol 41:245–258

    PubMed  CAS  Google Scholar 

  • Christ B, Jacob HJ, Jacob M (1974) Die Somitogenese beim Hühnerembryo. Zur Determination der Segmentierungsrichtung. Verh Anat Ges 68:573–579

    PubMed  CAS  Google Scholar 

  • Christ B, Jacob HJ, Jacob M (1977) Experimental analysis of the origin of the wing musculature in avian embryos. Anat Embryol 150:171–186

    Article  PubMed  CAS  Google Scholar 

  • Christ B, Jacob H, Brand-Saberi B, Grim M (1993) On the development of the human hand. In: Preuschoft H, Chivers DJ (eds) Hands of primates. Springer, Berlin Heidelberg Wein New York, pp 405–421

    Google Scholar 

  • Christ B, Ordahl CP, (1995) Early stages of chick somite development. Anat Embryol 191:381–396

    Article  PubMed  CAS  Google Scholar 

  • Dealy CN, Roth A, Ferrari D, Brown AM, Kosher RA (1993) Wnt-5a and Wnt-7a are expressed in the developing chick limb bud in a manner suggesting roles in pattern formation along the proximodistal and dorsoventral axes. Mech Dev 43:175–186

    Article  PubMed  CAS  Google Scholar 

  • Dietrich S, Schubert FR, Healy C, Sharpe PT, Lumsden A (1998) Specification of the hypaxial musculature. Development 125:2235–2249

    PubMed  CAS  Google Scholar 

  • Flickinger RA (1974) Muscle and cartilage differentiation in small and large explants from the chick embryo limb bud. Dev Biol 41:202–208

    Article  PubMed  CAS  Google Scholar 

  • Galceran J, Farinas I, Depew MJ, Clevers H, Grosschedl R (1999) Wnt 3a -/- like phenotype and limb deficiency in Lef 1(-/-) mice. Genes Dev 13:709–717

    Article  PubMed  CAS  Google Scholar 

  • Gasseling MT, Saunders JW Jr (1961) Effects of the apical ectodermal ridge on growth of the versene-stripped chick limb bud. Dev Biol 3:1–25

    Article  PubMed  CAS  Google Scholar 

  • Gavin BJ, McMahon JA, McMahon AP (1990) Expression of multiple novel Wnt-1/int-1-related genes during fetal and adult mouse development. Genes Dev 4:2319–2332

    Article  PubMed  CAS  Google Scholar 

  • Geetha-Loganathan P, Nimmagadda S, Prols F, Patel K, Scaal M, Huang R, Christ B (2005) Ectodermal Wnt-6 promotes Myf5-dependent avian limb myogenesis. Dev Biol 288:221–233

    Article  PubMed  CAS  Google Scholar 

  • Hamburger V, Hamilton HL (1951) A series of normal stages in the development of chick embryo. J Morphol 88:49–92

    Article  Google Scholar 

  • Jacob M, Christ B, Jacob HJ (1978) On the migration of myogenic stem cells into the prospective wing region of chick embryos. A scanning and transmission electron microscope study. Anat Embryol (Ber) 153(2):179–193

    Article  CAS  Google Scholar 

  • Kawakami Y, Capdevila J, Buscher D, Itoh T, Esteban CR, Belmonte JCI (2001) WNT signals control FGF-dependent limb initiation and AER induction in the chick embryo. Cell 104:891–900

    Article  PubMed  CAS  Google Scholar 

  • Kengaku M, Capdevila J, Rodriguez-Esteban C (1998) Distinct WNT pathways regulating AER formation and dorsoventral polarity in the chick limb bud. Science 280:1274–1277

    Article  PubMed  CAS  Google Scholar 

  • Kosher RA, Savage MP, Chan SC (1979) In vitro studies on the morphogenesis and differentiation of the mesoderm subjacent to the apical ectodermal ridge of the embryonic chick limb-bud. J Embryol Exp Morphol 50:75–97

    PubMed  CAS  Google Scholar 

  • Le Douarin NM (1982) The neural crest. Cambridge University Press, London

    Google Scholar 

  • Loganathan PG, Nimmagadda S, Huang R, Scaal M, Christ B (2005) Comparative analysis of the expression patterns of Wnts during chick limb development. Histochem Cell Biol 123:195–201

    Article  PubMed  CAS  Google Scholar 

  • MacCabe JA, Errick J, Saunders JW Jr (1974) Ectodermal control of the dorsoventral axis in the leg bud of the chick embryo. Dev Biol 39:69–82

    Article  PubMed  CAS  Google Scholar 

  • Ordahl CP, Le Douarin NM (1992) Two myogenic lineages within the developing somite. Development 114:339–53

    PubMed  CAS  Google Scholar 

  • Parr BA, Shea MJ, Vassileva G, McMahon AP (1993) Mouse Wnt genes exhibit discrete domains of expression in the early embryonic CNS and limb buds. Development 119:247–261

    PubMed  CAS  Google Scholar 

  • Parr BA, McMahon AP (1995) Dorsalizing signal Wnt-7a required for normal polarity of D-V and A-P axes of mouse limb. Nature 374:350–353

    Article  PubMed  CAS  Google Scholar 

  • Pardanaud L, Dieterlen-Lièvre F (1993) Emergence of endothelial and hemopoietic cells in the avian embryo. Anat Embryol 187:107–114

    Article  PubMed  CAS  Google Scholar 

  • Pardanaud L, Altmann C, Kitos P, Dieterlen-Lièvre F, Buck CA (1987) Vasculogenesis in the early quail blastodisc as studied with a monoclonal antibody recognizing endothelial cells. Development 100:339–349

    PubMed  CAS  Google Scholar 

  • Pautou MP, Kieny M (1973) Interaction ecto-mesodermique dans l’etablissement de la polarite dorso-ventrale du pied de l’embryon de poulet. C R Acad Sci Ser D 277:1225–1228

    CAS  Google Scholar 

  • Rodriguez-Niedenführ M, Dathe V, Jacob HJ, Prols F, Christ B (2003) Spatial and temporal pattern of Wnt-6 expression during chick development. Anat Embryol (Berl) 206:447–451

    Google Scholar 

  • Searls RL (1976) Effect of dorsal and ventral limb ectoderm on the development of the limb of the embryonic chick. J Embryol Exp Morphol 35:369–381

    PubMed  CAS  Google Scholar 

  • Searls RL, Smith AA (1982) Evidence that ectoderm influences the differentiation of muscle in the limb of the embryonic chick. J Exp Zool 220:343–351

    Article  PubMed  CAS  Google Scholar 

  • Stark RJ, Searls RL (1974) The establishment of the cartilage pattern in the embryonic chick wing, and evidence for a role of the dorsal and ventral ectoderm in normal wing development. Dev Biol 38:51–63

    Article  PubMed  CAS  Google Scholar 

  • Serra JA (1946) Histochemical tests for protein and amino acids: the characterization of basic proteins. Stain Technol 21:5–18

    Google Scholar 

  • Solursh M, Drake C, Meier S (1987) The migration of myogenic cells from the somites at the wing level in avian embryos. Dev Biol 121:389–396

    Article  PubMed  CAS  Google Scholar 

  • Wilting J, Brand-Saberi B, Huang R, Zhi Q, Kontges G, Ordahl CP, Christ B(1995) Angiogenic potential of the avian somite. Dev Dyn 202:165–171

    PubMed  CAS  Google Scholar 

  • Wilting J, Papoutsi M, Schneider M, Christ B (2000) The lymphatic endothelium of the avian wing is of somite origin. Dev Dyn 217:271–278

    Article  PubMed  CAS  Google Scholar 

  • Zhi Q, Huang R, Christ B, Brand-Saberi B (1996) Participation of individual brachial somites in the skeletal muscles of the avian distal wing. Anat Embryol 194:327–339

    Article  PubMed  CAS  Google Scholar 

  • Zwilling E (1964) Development of fragmented and of dissociated limb bud mesoderm. Dev Biol 9:20–37

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank Mrs. L. Koschny, Mrs. M. Schüttoff and Mr. G. Frank for excellent technical assistance. This study was supported by the Deutsche Forschungsgemeinschaft (SFB-592, A1 to B.C & M.S) and the European Network of Excellence, MYORES (B.C. and M.S.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bodo Christ.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Geetha-Loganathan, P., Nimmagadda, S., Huang, R. et al. Role of Wnt-6 in limb myogenesis. Anat Embryol 211, 183–188 (2006). https://doi.org/10.1007/s00429-005-0069-6

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-005-0069-6

Keywords

Navigation