Summary
The distribution of complex carbohydrate structures during the embryonic development of the rat palate was analysed by examining lectin-binding patterns in serial paraffin and cryostat sections. With few exceptions, the binding patterns showed a general increase in lectin receptors in the more developed stages of palatogenesis. High mannose oligosaccharides were especially amplified during development. Terminal fucose molecules were not expressed. In contrast, terminal sialic acid molecules were ubiquitously distributed in epithelial and mesenchymal tissues. Non-sialylated terminal N-acetylglucosamine was specifically restricted to evolving bone matrix. Before palatal fusion, quantitative but not qualitative differences were detected between oral, nasal, and medial-edge epithelial surfaces. The only exception was LCA, which specifically marked epithelial cells at the tip of palatal shelves. A very selective affinity for Jacalin was demonstrated in the oral epithelium of the palate after day 16, suggesting the presence of sialylated terminal galactose-(β-1,3)-N-acetylgalactosamine. PNA specifically marked the basal lamina of the oral side of palatal processes. The binding patterns of DBA, GSL IA, SBA, and VVA indicated that the epithelium of the tongue is characterized by terminal α- and β-galactose residues, whereas palatine cells possess only molecules with β-anomery. During palatogenesis, glycosaminoglycans patterns were significantly modified. Our data suggest that alteration of complex carbohydrate structures may play a central role in modulating cell-cell and cell-matrix interactions. The significance of these findings, however, remains to be elucidated.
Similar content being viewed by others
References
ALROY, J., UCCI, A. A., GOYAL, V. & WOODS, W. (1984) Lectin histochemistry of glycolipid storage diseases on frozen and paraffin-embedded tissue sections. J. Histochem. Cytochem. 34, 501–5.
ALROY, J., UCCI, A. A. & PERIERA, M. E. (1988) Lectin histochemistry. In Advances in Immunohistochemistry (edited by DELELLIS, R. A.), pp. 93–131. New York: Raven Press.
AULTHOUSE, A. L. & SOLURSH, M. (1987) The detection of a precartilage, blastema-specific marker. Dev. Biol. 120, 377–84.
BAKER, D. A., KABAT, S. S., RATCLIFFE, R. M., HERMENTIN, P. & LEMIEUX, R. U. (1983) Immunochemical studies on the combining sites of Forssman hapten reactive hemagglutinins from Dolichos biflorus, Helix pomata, and Wistaria floribunda. Biochemistry 22, 2741–50.
BERNHARD, W. & AVREMEAS, S. (1971) Ultrastructural visualization of cellular carbohydrate components by means of concanavalin A. Exp. Cell Res. 64, 232–6.
COOK, H. C. (1990) Carbohydrates. In Theory and Practice of Histological Techniques (edited by BANCROFT, J. D. & STEVENS, A.), pp. 177–213. Edinburgh: Churchill Livingstone.
CUMMINGS, R. D. & KORNFELD, S. (1982) Characterization of the structural determinants required for the high affinity interaction of asparagine-linked oligosaccharides with immobilized Phaseolus vulgaris leukagglutinin and erythroagglutinating lectins. J. Biol. Chem. 257, 11 230–4.
DAMJANOV, I. (1987) Lectin cytochemistry and histochemistry. Lab. Invest. 57, 5–20.
DEBRAY, H., DECOUT, D., STRECKER, G., SPIK, G. & MONTREUIL, J. (1981) Specifity of twelve lectins towards oligosaccharides and glycopeptides related to N-glycosylproteins. Eur. J. Biochem. 117, 41–55.
FRANK, J. D., BALENA, R., MASRACHIA, P., SEEDOR, J. G. & CARTWRIGHT, M. E. (1992) The effect of three different demineralization agents on osteopontin localization in adult rat bone using immunohistochemistry. Histochemistry 99, 295–301.
GABIUS, H. J. (1991) Detection and functions of mammalian lectins - with emphasis on membrane lectins. Biochim. Biophys. Acta. 1071, 1–18.
GIRARD, N., DELPECH, A. & DELPECH, B. (1986) Characterization of hyaluronic acid on tissue sections with hyaluronectin. J. Histochem. Cytochem. 34, 539–41.
GREENE, R. M. & PRATT, R. M. (1977) Inhibition by diazo-oxonorleucine. (DON) of rat palatal glycoprotein synthesis and epithelial cell adhesion in vitro. Exp. Cell Res. 105, 27–37.
HENNIGAR, R. A., SCHULTE, B. A. & SPICER, S. S. (1986) Histochemical detection of glycogen using Griffonia simplicifolia agglutinin II. Histochem. J. 18, 589–96.
HENNIGAR, L. M., HENNIGAR, R. A. & SCHULTE, B. A. (1987) Histochemical specifity of β-galactose binding lectins from Arachis hypogea (peanut) and Ricinus communis (castor bean). Stain Technol. 62, 317–25.
KNUDSEN, T. B., BULLEIT, R. F. & ZIMMERMAN, R. F. (1985) Histochemical localization of glycosaminoglycans during morphogenesis of the secondary palate in mice. Anat. Embryol. 173, 137–42.
KORNFELD, K., REITMAN, M. L. & KORNFELD, R. (1981) The carbohydrate-binding specifity of pea and lentil lectins. Fucose is an important determinant. J. Biol. Chem. 256, 6633–40.
MONSIGNY, M., ROCHE, A. C., SENE, C., MAGET-DANA, R. & DELMOTTE, F. (1980) Sugar-lectin interactions, how does wheat-germ agglutinin bind sialoglycoconjugates. Eur. J. Biochem. 104, 147–53.
MORRIS-WIMAN, J. & BRINKLEY, L. (1992) An extracellular matrix infrastructure provides support for murine secondary palatal shelf remodelling. Anat. Rec. 234, 575–86.
PEREIRA, M. E., KISAILUS, E. L., KRUEZO, F. & KABAT, E. (1978) Immunochemical studies on the combining sites of blood groups H-specific lectin I from Ulex europaeus seeds. Arch. Biochem. Biophys. 185, 108–15.
PERRIS, R., KROTOSKI, D., LALLIER, T., DOMINGO, C., SORRELL, J. M. & BRONNER-FRASER, M. (1991) Spatial and temporal changes of proteoglycans during avian neural crest development. Development 111, 583–99.
PETERS, B. P. & GOLDSTEIN, I. J. (1979) The use of fluoresceinconjugated Bandeireaea simplicifolia B4-isolectin as a histochemical reagent for the detection of α-D-galactopyranosyl groups. Exp. Cell Res. 120, 321–34.
PRATT, R. M. & HASSEL, J. R. (1975) Appearance and distribution of carbohydrate-rich macromolecules on the epithelial surface of the developing rat palate shelf. Dev. Biol. 45, 192–8.
PRATT, R. M., GIBSON, W. A. & HASSEL, J. R. (1973) Concanavalin A binding to the secondary palate of the embryonic rat. J. Dent. Res. 52, 111–23.
RAMBOURG, A. (1971) Morphological and histochemical aspects of glycoprotein at the surface of animal cells. Int. Rev. Cytol. 31, 57–106.
SÉNÉCHAL, H., DELAIN, D., SHAPIRA, G. & WAHRMANN, J. P. (1983) Alterations in glycolysation of plasma membrane proteins during myogenesis. Exp. Cell Res. 147, 341–50.
SHARPE, P. M., BRUNET, C. L., FOREMAN, D. M. & FERGUSON, M. W. (1993) Localisation of acidic and basic fibroblast growth factors during mouse palate development and their effects on mouse palate mesenchyme cells in vitro. Roux's Arch. Dev. Biol. 202, 132–43.
SLAVKIN, H. C. (1984) Morphogenesis of a complex organ, vertebrate palate development. Curr. Top. Dev. Biol. 19, 1–16.
SPICER, S. S. & SCHULTE, B. A. (1992) Diversity of cell glycoconjugates shown histochemically, a perspective. J. Histochem. Cytochem. 40, 1–38.
STOWARD, P. J., SPICER, S. S. & MILLER, R. L. (1980) Histochemical reactivity of peanut lectin-horseradish peroxidase conjugate. J. Histochem. Cytochem. 28, 979–90.
STURGESS, J. M., MITRANIC, M. M. & MOSCARELLO, M. A. (1978) Extraction of glycoproteins during tissue preparation for electron microscopy. J. Microsc. 114, 101–5.
TOLLEFSEN, S. E. & KORNFELD, R. (1983) The B4 lectin from Vicia villosa seeds interacts with N-acetylgalactosamine residues α-linked to serine or threonine residues in cell surface glycoproteins. J. Biol. Chem. 258, 5172–6.
TOOLE, B. P. & UNDERHILL, C. B. (1982) Regulation of the morphogenesis by the pericellular matrix. In Cell Interactions and Development, Molecular Mechanisms (edited by YAMADA, K. M.), pp. 203–230. New York: J. Wiley & Sons.
WALKER, R. A. (1989) The use of lectins in histopathology. Path. Res. Pract. 185, 826–35.
ZSCHÄBITZ, A., GABIUS, H. J., STOFFT, E. & REICHEL, W. (1992) Demonstration of endogenous lectins in synovial tissue. Scand. J. Rheumatol. 20, 242–51.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Zschäbitz, A.R., Biesalski, H.K., Krahn, V. et al. Distribution patterns in glycoconjugate expression during the development of the rat palate. Histochem J 26, 705–720 (1994). https://doi.org/10.1007/BF00158203
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF00158203