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The distribution of mesenchyme proteoglycan (PG-M) during wing bud outgrowth

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Summary

This study utilizes immunofluorescence to describe the distribution of several extracellular matrix molecules in the chick embryo during the process of limb outgrowth and the formation of precartilage condensations. A large chondroitin sulfate proteoglycan (PG-M) is detected at the wing level at Hamburger and Hamilton stage 14 in and under the dorsal ectoderm, and is associated with the basement membranes around the neural tube, notochord and pronephros, but not with other basement membranes. The galactose-specific leetin, peanut agglutinin (PNA), has a similar distribution except that it also binds to the dorsal side of the neural tube. PG-M is not detected in the limb mesenchyme until after stage 17, when it is present in the distal region, as is PNA-binding material. With further development of the wing bud, PG-M is present in the subectodermal mesenchyme, the mesenchyme at the distal tip and in the prechondrogenic core. After stage 22 PNA-binding material becomes localized in the prechondrogenic core, the basement membranes under the apical ectodermal ridge, and the ventral sulcus. The distribution of these components (PG-M and PNA binding material) overlaps, but differs from that of type I collagen and fibronectin and basement membrane components, such as laminin, basement membrane heparan sulfate proteoglycan, and type IV collagen. Tenascin, on the other hand, is not detected in the limb bud until stage 25, after the appearance of cartilage matrix components such as type II collagen and cartilage proteoglycan (PG-H). These results are considered in relation to the formation of precartilage aggregates, and indicate that PNA binds to components in precartilage aggregates other than PG-M or tenascin.

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References

  • Aulthouse AL, Solursh M (1987) The detection of a precartilage, blastema-specific marker. Dev Biol 120:377–384

    Google Scholar 

  • Bayne EK, Anderson MJ, Fambrough DM (1984) Extracellular matrix organization in developing muscle: correlation with acetylcholine receptor aggregates. J Cell Biol 99:1486–1501

    Google Scholar 

  • Chiquet M, Fambrough DM (1984) Chick myotendinous antigen. I. A monoclonal antibody as a marker for tendon and muscle morphogenesis. J Cell Biol 98:1926–1936

    Google Scholar 

  • Chiquet M, Eppenberger HM, Turner DC (1981) Muscle morphogenesis: Evidence for an organizing function of exogenous fibronectin. Dev Biol 88:220–235

    Google Scholar 

  • Chiquet-Ehrismann R, Kalla P, Pearson CA, Beck K, Chiquet M (1988) Tenascin interferes with fibronectin action. Cell 53:383–390

    Google Scholar 

  • Cottrill CP, Archer CW, Hornbruch A, Wolpert L (1987) The differentiation of normal and muscle-free distal chick limb bud mesenchyme in micromass culture. Dev Biol 119:143–151

    Google Scholar 

  • Dessau W, von der Mark H, von der Mark K, Fischer S (1980) Change in the patterns of collagens and fibronectin during limbbud chondrogenesis. J Embryol Exp Morphol 57:51–60

    Google Scholar 

  • Duband JL, Thiery JP (1987) Distribution of laminin and collagens during avian neural crest development. Development 101:461–478

    Google Scholar 

  • Fell HB (1925) The histogenesis of cartilage and bone in the long bones of the embryonic fowl. J Morphol 40:417–451

    Google Scholar 

  • Fitch JM, Gibney E, Sandersan RD, Mayne R, Linsenmayer TF (1982) Domain and basement membrane specificity of a monoclonal antibody against chicken type IV collagen. J Cell Biol 95:461–467

    Google Scholar 

  • Gallera J (1966) Mise en evidence du role de l'ectoblaste dans la differenciation des somites chez les Oiseaux. Rev Suisse Zool 73:492–502

    Google Scholar 

  • Gardner JM, Fambrough DM (1983) Fibronectin expression during myogenesis. J Cell Biol 96:474–485

    Google Scholar 

  • Gould R, Day A, Wolpert L (1972) Mesenchymal condensations and cell contact in early morphogenesis of the chick limb. Exp Cell Res 72:325–336

    Google Scholar 

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

    Google Scholar 

  • Jurand A (1965) Ultrastructural aspects of early development of the fore-limb buds in the chick and the mouse. Proc R Soc Lond 162:387–405

    Google Scholar 

  • Kimata K, Oike Y, Tani K, Shinomura T, Yamagata M, Uritani M, Suzuki S (1986) A large chondroitin sulfate proteoglycan (PG-M) synthesized before chondrogenesis in the limb bud of chick embryo. J Biol Chem 261:13517–13525

    Google Scholar 

  • Kosher RA, Kordasey HW, Ledger PW (1982) Temporal and spatial distribution of fibronectin during development of the embryonic chick limb bud. Cell Differ 11:217–228

    Google Scholar 

  • Linsenmayer TF, Hendrix MJC, Little CD (1979) Production and characterization of a monoclonal antibody to chicken type I collagen. Proc Natl Acad Sci USA 76:3703–3707

    Google Scholar 

  • Mackie EJ, Thesleff I, Chiquet-Ehrismann R (1987) Tenascin is associated with chondrogenic and osteogenic differentiation in vivo and promotes chondrogenesis in vitro. J Cell Biol 105:2569–2579

    Google Scholar 

  • Melnick M, Jaskoll T, Brownell AG, Macdougall M, Bessern C, Slavkin HC (1981) Spatiotemporal patterns of fibronectin distribution during embryonic development I. Chick limbs. J Embryol Exp Morphol 63:193–206

    Google Scholar 

  • Oettinger HF, Thal G, Sasse J, Holtzer H, Pacifici M (1985) Immunological analysis of chick notochord and cartilage matrix development with antisera to cartilage matrix macromolecules. Dev Biol 109:63–71

    Google Scholar 

  • Saunders JW (1948) The proximo-distal sequence of origin of the parts of the chick wing and the role of the ectoderm. J Exp Zool 108:363–403

    Google Scholar 

  • Shinomura T, Kimata K, Oike Y, Maedam N, Yano S, Suzuki S (1984) Appearance of distinct types of proteoglycan in a well defined temporal and spatial pattern during early cartilage formation in the chick limb. Dev Biol 103:211–220

    Google Scholar 

  • Singley CT, Solursh M (1981) The spatial distribution of hyaluronic acid and mesenchymal condensation in the embryonic chick wing. Dev Biol 84:102–120

    Google Scholar 

  • Solursh M (1984) Cell matrix interactions during limb chondrogenesis. In: Kemp RB, Hinchliffe JR (eds) Matrices and Cell Differentiation, pp 47–60. A R Liss, New York

    Google Scholar 

  • Solursh M, Jensen KL (1988) The accumulation of basement membrane components during the onset of chondrogenesis and myogenesis in the chick wing bud. Development 104:41–49

    Google Scholar 

  • Solursh M, Fisher M, Singley CT (1979) The synthesis of hyaluronic acid by ectoderm during early organogenesis in the chick embryo. Differentiation 14:77–85

    Google Scholar 

  • Summerbell D, Lewis JH, Wolpert L (1973) Positional information in chick limb bud morphogenesis. Nature 224:492–496

    Google Scholar 

  • Swalla BJ, Owens EM, Linsenmayer TF, Solursh M (1983) Two distinct classes of prechondrogenic cell types in the embryonic limb bud. Dev Biol 97:59–69

    Google Scholar 

  • Swalla BJ, Solursh M (1989) Differences in chondrogenesis by proximal and distal chick wing bud cell subpopulations. (Submitted)

  • Thiery JP, Duband JL, Delouvee A (1982) Pathways and mechanisms of avian trunk neural crest cell migration and localization. Dev Biol 93:324–343

    Google Scholar 

  • Thorogood PV, Hinchliffe JR (1975) An analysis of the condensation process during chondrogenesis in the embryonic chick hind limb. J Embryol Exp Morphol 33:581–606

    Google Scholar 

  • Tomasek JJ, Mazurkiewicz JE, Newman SA (1982) Nonuniform distribution of fibronectin during avian limb development. Dev Biol 90:118–126

    Google Scholar 

  • von der Mark H, von der Mark K, Gay S (1976) Study of differential collagen synthesis during development of the chick embryo by immunofluorescence. Dev Biol 48:237–249

    Google Scholar 

  • Yamagata M, Yamada KM, Yoneda M, Suzuki S, Kimata K (1986) Chondroitin sulfate proteoglycan (PG-M-like proteoglycan) is involved in the binding of hyaluronic acid to cellular fibronectin. J Biol Chem 261:13526–13535

    Google Scholar 

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Shinomura, T., Jensen, K.L., Yamagata, M. et al. The distribution of mesenchyme proteoglycan (PG-M) during wing bud outgrowth. Anat Embryol 181, 227–233 (1990). https://doi.org/10.1007/BF00174617

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  • DOI: https://doi.org/10.1007/BF00174617

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