Skip to main content
Top
Published in: Brain Structure and Function 3/2006

01-06-2006 | Original Article

Role of Wnt-6 in limb myogenesis

Authors: Poongodi Geetha-Loganathan, Suresh Nimmagadda, Ruijin Huang, Martin Scaal, Bodo Christ

Published in: Brain Structure and Function | Issue 3/2006

Login to get access

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.
Literature
go back to reference Amprino R, Amprino-Bonetti D (1967) Experimental observations in the development of ectoderm-free mesoderm of the limb bud in chick embryos. Nature 214:826–827PubMedCrossRef Amprino R, Amprino-Bonetti D (1967) Experimental observations in the development of ectoderm-free mesoderm of the limb bud in chick embryos. Nature 214:826–827PubMedCrossRef
go back to reference Amthor H, Christ B, Weil M, Patel K (1998) The importance of timing differentiation during limb muscle development. Curr Biol 8:642–652CrossRefPubMed Amthor H, Christ B, Weil M, Patel K (1998) The importance of timing differentiation during limb muscle development. Curr Biol 8:642–652CrossRefPubMed
go back to reference 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 376:768–771PubMedCrossRef 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 376:768–771PubMedCrossRef
go back to reference 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 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
go back to reference Chevallier A, Kieny M, Mauger A (1977) Limb-somite relationship: origin of the limb musculature. J Embryol Exp Morphol 41:245–258PubMed Chevallier A, Kieny M, Mauger A (1977) Limb-somite relationship: origin of the limb musculature. J Embryol Exp Morphol 41:245–258PubMed
go back to reference Christ B, Jacob HJ, Jacob M (1974) Die Somitogenese beim Hühnerembryo. Zur Determination der Segmentierungsrichtung. Verh Anat Ges 68:573–579PubMed Christ B, Jacob HJ, Jacob M (1974) Die Somitogenese beim Hühnerembryo. Zur Determination der Segmentierungsrichtung. Verh Anat Ges 68:573–579PubMed
go back to reference Christ B, Jacob HJ, Jacob M (1977) Experimental analysis of the origin of the wing musculature in avian embryos. Anat Embryol 150:171–186CrossRefPubMed Christ B, Jacob HJ, Jacob M (1977) Experimental analysis of the origin of the wing musculature in avian embryos. Anat Embryol 150:171–186CrossRefPubMed
go back to reference 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 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
go back to reference 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 43:175–186CrossRefPubMed 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 43:175–186CrossRefPubMed
go back to reference Dietrich S, Schubert FR, Healy C, Sharpe PT, Lumsden A (1998) Specification of the hypaxial musculature. Development 125:2235–2249PubMed Dietrich S, Schubert FR, Healy C, Sharpe PT, Lumsden A (1998) Specification of the hypaxial musculature. Development 125:2235–2249PubMed
go back to reference Flickinger RA (1974) Muscle and cartilage differentiation in small and large explants from the chick embryo limb bud. Dev Biol 41:202–208CrossRefPubMed Flickinger RA (1974) Muscle and cartilage differentiation in small and large explants from the chick embryo limb bud. Dev Biol 41:202–208CrossRefPubMed
go back to reference Galceran J, Farinas I, Depew MJ, Clevers H, Grosschedl R (1999) Wnt 3a -/- like phenotype and limb deficiency in Lef 1(-/-) mice. Genes Dev 13:709–717PubMedCrossRef Galceran J, Farinas I, Depew MJ, Clevers H, Grosschedl R (1999) Wnt 3a -/- like phenotype and limb deficiency in Lef 1(-/-) mice. Genes Dev 13:709–717PubMedCrossRef
go back to reference Gasseling MT, Saunders JW Jr (1961) Effects of the apical ectodermal ridge on growth of the versene-stripped chick limb bud. Dev Biol 3:1–25CrossRefPubMed Gasseling MT, Saunders JW Jr (1961) Effects of the apical ectodermal ridge on growth of the versene-stripped chick limb bud. Dev Biol 3:1–25CrossRefPubMed
go back to reference 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 4:2319–2332PubMedCrossRef 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 4:2319–2332PubMedCrossRef
go back to reference 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 288:221–233CrossRefPubMed 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 288:221–233CrossRefPubMed
go back to reference Hamburger V, Hamilton HL (1951) A series of normal stages in the development of chick embryo. J Morphol 88:49–92CrossRef Hamburger V, Hamilton HL (1951) A series of normal stages in the development of chick embryo. J Morphol 88:49–92CrossRef
go back to reference 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):179–193CrossRef 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):179–193CrossRef
go back to reference 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 104:891–900CrossRefPubMed 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 104:891–900CrossRefPubMed
go back to reference Kengaku M, Capdevila J, Rodriguez-Esteban C (1998) Distinct WNT pathways regulating AER formation and dorsoventral polarity in the chick limb bud. Science 280:1274–1277CrossRefPubMed Kengaku M, Capdevila J, Rodriguez-Esteban C (1998) Distinct WNT pathways regulating AER formation and dorsoventral polarity in the chick limb bud. Science 280:1274–1277CrossRefPubMed
go back to reference 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 50:75–97PubMed 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 50:75–97PubMed
go back to reference Le Douarin NM (1982) The neural crest. Cambridge University Press, London Le Douarin NM (1982) The neural crest. Cambridge University Press, London
go back to reference 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 123:195–201CrossRefPubMed 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 123:195–201CrossRefPubMed
go back to reference MacCabe JA, Errick J, Saunders JW Jr (1974) Ectodermal control of the dorsoventral axis in the leg bud of the chick embryo. Dev Biol 39:69–82PubMedCrossRef MacCabe JA, Errick J, Saunders JW Jr (1974) Ectodermal control of the dorsoventral axis in the leg bud of the chick embryo. Dev Biol 39:69–82PubMedCrossRef
go back to reference Ordahl CP, Le Douarin NM (1992) Two myogenic lineages within the developing somite. Development 114:339–53PubMed Ordahl CP, Le Douarin NM (1992) Two myogenic lineages within the developing somite. Development 114:339–53PubMed
go back to reference 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 119:247–261PubMed 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 119:247–261PubMed
go back to reference Parr BA, McMahon AP (1995) Dorsalizing signal Wnt-7a required for normal polarity of D-V and A-P axes of mouse limb. Nature 374:350–353CrossRefPubMed Parr BA, McMahon AP (1995) Dorsalizing signal Wnt-7a required for normal polarity of D-V and A-P axes of mouse limb. Nature 374:350–353CrossRefPubMed
go back to reference Pardanaud L, Dieterlen-Lièvre F (1993) Emergence of endothelial and hemopoietic cells in the avian embryo. Anat Embryol 187:107–114CrossRefPubMed Pardanaud L, Dieterlen-Lièvre F (1993) Emergence of endothelial and hemopoietic cells in the avian embryo. Anat Embryol 187:107–114CrossRefPubMed
go back to reference 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 100:339–349PubMed 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 100:339–349PubMed
go back to reference 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 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
go back to reference 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 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
go back to reference Searls RL (1976) Effect of dorsal and ventral limb ectoderm on the development of the limb of the embryonic chick. J Embryol Exp Morphol 35:369–381PubMed Searls RL (1976) Effect of dorsal and ventral limb ectoderm on the development of the limb of the embryonic chick. J Embryol Exp Morphol 35:369–381PubMed
go back to reference Searls RL, Smith AA (1982) Evidence that ectoderm influences the differentiation of muscle in the limb of the embryonic chick. J Exp Zool 220:343–351CrossRefPubMed Searls RL, Smith AA (1982) Evidence that ectoderm influences the differentiation of muscle in the limb of the embryonic chick. J Exp Zool 220:343–351CrossRefPubMed
go back to reference 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 38:51–63CrossRefPubMed 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 38:51–63CrossRefPubMed
go back to reference Serra JA (1946) Histochemical tests for protein and amino acids: the characterization of basic proteins. Stain Technol 21:5–18 Serra JA (1946) Histochemical tests for protein and amino acids: the characterization of basic proteins. Stain Technol 21:5–18
go back to reference Solursh M, Drake C, Meier S (1987) The migration of myogenic cells from the somites at the wing level in avian embryos. Dev Biol 121:389–396CrossRefPubMed Solursh M, Drake C, Meier S (1987) The migration of myogenic cells from the somites at the wing level in avian embryos. Dev Biol 121:389–396CrossRefPubMed
go back to reference Wilting J, Brand-Saberi B, Huang R, Zhi Q, Kontges G, Ordahl CP, Christ B(1995) Angiogenic potential of the avian somite. Dev Dyn 202:165–171PubMed Wilting J, Brand-Saberi B, Huang R, Zhi Q, Kontges G, Ordahl CP, Christ B(1995) Angiogenic potential of the avian somite. Dev Dyn 202:165–171PubMed
go back to reference Wilting J, Papoutsi M, Schneider M, Christ B (2000) The lymphatic endothelium of the avian wing is of somite origin. Dev Dyn 217:271–278CrossRefPubMed Wilting J, Papoutsi M, Schneider M, Christ B (2000) The lymphatic endothelium of the avian wing is of somite origin. Dev Dyn 217:271–278CrossRefPubMed
go back to reference 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 194:327–339CrossRefPubMed 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 194:327–339CrossRefPubMed
go back to reference Zwilling E (1964) Development of fragmented and of dissociated limb bud mesoderm. Dev Biol 9:20–37CrossRef Zwilling E (1964) Development of fragmented and of dissociated limb bud mesoderm. Dev Biol 9:20–37CrossRef
Metadata
Title
Role of Wnt-6 in limb myogenesis
Authors
Poongodi Geetha-Loganathan
Suresh Nimmagadda
Ruijin Huang
Martin Scaal
Bodo Christ
Publication date
01-06-2006
Publisher
Springer-Verlag
Published in
Brain Structure and Function / Issue 3/2006
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-005-0069-6

Other articles of this Issue 3/2006

Brain Structure and Function 3/2006 Go to the issue