Merkel cells and the mechanosensitivity of normal and regenerating nerves in Xenopus skin
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abstract
We have investigated some of the physiological, morphological and trophic characteristics of the Merkel cell-neurite complexes in the skin of Xenopus laevis. The Merkel cells, which are specialized sensory cells, occur in groups of 2-4 around the openings of the cutaneous gland ducts. A voltage-controlled mechanical stimulator was used to determine the distribution of mechanosensory thresholds across the skin; an analysis of the results revealed the presence of a single population of rapidly adapting, low threshold mechanoreceptors, whose locations coincided with those of the epidermal Merkel cell-neurite complexes. The possible role of the Merkel cell in the mechanosensory process, and its trophic interactions with the sensory nerve, were examined (i) by following the development of mechanosensitivity when sensory nerves regenerated into denervated, or newly regenerated, skin; (ii) by looking for possible correlations between the expression of physiological function and the appearance of morphological features characteristic of the Merkel cell-neurite complex; and (iii) by investigating the mechanosensitivity that remained after elimination of the Merkel cells. Not only did Merkel cells survive denervation without obvious changes in their fine structure, but they developed with normal morphology in new skin that had regenerated in nerve free limbs. Ingrowing sensory nerves contacted these Merkel cells, and eventually normal mechanosensory function was established; thus the Merkel cells act as targets for these nerves. The full recovery of the normal pattern of mechanosensitivity in the skin following nerve regeneration was correlated with the redevelopment of the specialized contacts between the nerve endings and Merkel cells, that eventually included reciprocal synapses. However, following the mechanical removal of the epidermis by enzymatic treatment, or the selective elimination of the Merkel cells by irradiation after they had taken up the fluorescent dye quinacrine, essentially normal mechanosensory responses could be initiated, though with somewhat increased thresholds. The results indicate that the Merkel cells are not involved in mechanosensory transduction; they do, however, act as targets for the growing nerves, thereby ensuring the appropriate distribution of low threshold mechanosensitivity, and they may have a role in enhancing and even inducing the excitability of the mechanosensitive nerve endings.
