Abstract
Taste buds are gustatory endorgans which use an uncommon purinergic signalling system to transmit information to afferent gustatory nerve fibres. In mammals, ATP is a crucial neurotransmitter released by the taste cells to activate the afferent nerve fibres. Taste buds in mammals display a characteristic, highly specific ecto-ATPase (NTPDase2) activity, suggesting a role in inactivation of the neurotransmitter. The purpose of this study was to test whether the presence of markers of purinergic signalling characterize taste buds in anamniote vertebrates and to test whether similar purinergic systems are employed by other exteroceptive chemosensory systems. The species examined include several teleosts, elasmobranchs, lampreys and hagfish, the last of which lacks vertebrate-type taste buds. For comparison, Schreiner organs of hagfish and solitary chemosensory cells (SCCs) of teleosts, both of which are epidermal chemosensory end organs, were also examined because they might be evolutionarily related to taste buds. Ecto-ATPase activity was evident in elongate cells in all fish taste buds, including teleosts, elasmobranchs and lampreys. Neither SCCs nor Schreiner organs show specific ecto-ATPase activity, suggesting that purinergic signalling is not crucial in those systems as it is for taste buds. These findings suggest that the taste system did not originate from SCCs but arose independently in early vertebrates.
Highlights
Taste buds are the gustatory end organs in vertebrates ranging from lamprey to mammals [1]
Taste buds can be recognized by three key features. (i) Taste buds are an aggregate of elongate taste cells of multiple morphological and functional types. (ii) Taste cells extend from the basal lamina to an apical pore or other opening in the epithelium. (iii) taste buds are innervated by sensory fibres of the & 2013 The Authors
Is the presence of ecto-ATPase coincident with the appearance of vertebrate taste buds, or is ecto-ATPase present in or around other epithelial chemosensory endorgans suggestive of a more ancient origin for ATP neurotransmission by chemosensory systems? The present results show that ectoATPase is present in taste buds of fish including lamprey but not at all in Schreiner organs in hagfish, nor is it associated with solitary chemosensory cells (SCCs) of any vertebrate
Summary
Taste buds are the gustatory end organs in vertebrates ranging from lamprey to mammals [1]. SCCs share some features with taste buds, i.e. they are elongate, span the height of the epithelium, form synapses with afferent nerves and even may express common receptors [4,5]; but SCCs are not merely dispersed taste cells. Some have speculated that SCCs may even be phylogenetic forerunners of taste buds [8] Hagfish possess another distinct chemosensory endorgan, the Schreiner organ, which shares many features with taste buds, but again is not identical to taste buds [4]. Schreiner organs are an assembly of several cell types and form functional contacts with nerve fibres entering from their basal aspect. Schreiner organs do not extend to the basal lamina and can be innervated by non-gustatory nerves, e.g. the trigeminal nerve [4]. Schreiner organs are not considered to be taste buds, but may be functionally or phylogenetically related to taste buds
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