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Immunocytochemical localization of the L1 and N-CAM cell adhesion molecules and their shared carbohydrate epitope L2/HNK-1 in the developing and differentiated gustatory papillae of the mouse tongue

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Journal of Neurocytology

Summary

The localization of the cell adhesion molecules L1 and N-CAM, and their shared carbohydrate epitope L2/HNK-1, was investigated at the light and electron microscopic levels in developing and adult fungiform and circumvallate gustatory papillae of the mouse tongue.

At embryonic day 13, the earliest stage investigated, the tongue epithelium was still undifferentiated and was not yet innervated by sensory fibres. At this stage none of the three molecules was detectable within the tongue epithelium. At embryonic day 15 the primordia of the gustatory papilla became unequivocally discernible when the papillary epithelium was already innervated by few sensory axons. At this stage N-CAM was the first molecule expressed on epithelial cells and was confined to those parts of the papillary epithelium destined to become the chemosensory cells of the taste buds. The sensory axons were N-CAM-, L1- and L2/HNK-1-positive when fasciculating or contacting their accompanying Schwann cells or the cells of the papillary epithelium. Contacts between Schwann cells were also prominently labelled by antibodies to the three antigens. The mesenchymal tissue underlying the prospective sensory epithelium expressed N-CAM at all embryonic stages, but ceased to be N-CAM positive within the first six postnatal days. From embryonic day 16 onward a weak L1 immunoreactivity was detectable within the basal and intermediate layers of the lingual epithelium and remained present in adulthood.

Cytodifferentiation of epithelial cells into spindle-shaped sensory cells and organization into taste buds began at postnatal day two. Simultaneously, L1 and L2/HNK-1 immunoreactivity increased on taste bud cells and N-CAM disappeared from the non-sensory extragemmal parts of the papillary epithelium. At approximately postnatal day six, taste bud formation was complete and the pattern of cell adhesion molecule expression was comparable to that found in the adult in that L1 was strongly expressed on the apposing surfaces of all cells, whereas N-CAM was confined to cell contacts between a subpopulation of intragemmal cells. The L2/HNK-1 epitope was visible on the surfaces of taste bud cells, on intragemmal axons, and in a small portion of extracellular matrix directly underlying the taste buds, but was no longer expressed on those parts of the sensory fibres embedded in the subepithelial mesenchyme. The L2/HNK-1 epitope may thus be regarded as a cell surface marker for the cellular elements of mature taste buds. The highly sialylated form of N-CAM was not detectable at any stage investigated.

The observations suggest that the expression of the three molecules within the papillary epithelium follows rather than precedes the innervation by sensory axons and does not, therefore, reflect the gustatory epithelium's susceptibility to innervation as found for N-CAM in the neuromuscular system. The spatio-temporal expression of N-CAM, however, is suggestive of its influence on the differentiation of taste bud cells. Apart from axon-axon and axon-Schwann cell interactions L1 might be involved in interactions between gustatory cells and sensory nerve terminals and, surprisingly, also between non-sensory epithelial cells, whereas the L2/HNK-1 epitope may be implicated in the maintenance of the characteristic cytoarchitecture of the differentiated taste buds.

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  1. R. Martini

    Present address: Department of Neurobiology, Swiss Federal Institute of Technology, 8093, Hönggerberg, Zürich, Switzerland

  2. C. Nolte

    Present address: Department of Biochemical Pharmacology, Schering AG, Müllerstr. 170–178, 1000, Berlin 65, FRG

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  1. Department of Neurobiology, University of Heidelberg, Im Neuenheimer Feld 364, 6900, Heidelberg, FRG

    C. Nolte & R. Martini

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Nolte, C., Martini, R. Immunocytochemical localization of the L1 and N-CAM cell adhesion molecules and their shared carbohydrate epitope L2/HNK-1 in the developing and differentiated gustatory papillae of the mouse tongue. J Neurocytol 21, 19–33 (1992). https://doi.org/10.1007/BF01206895

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