Review
Peptide regulators of peripheral taste function

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Abstract

The peripheral sensory organ of the gustatory system, the taste bud, contains a heterogeneous collection of sensory cells. These taste cells can differ in the stimuli to which they respond and the receptors and other signaling molecules they employ to transduce and encode those stimuli. This molecular diversity extends to the expression of a varied repertoire of bioactive peptides that appear to play important functional roles in signaling taste information between the taste cells and afferent sensory nerves and/or in processing sensory signals within the taste bud itself. Here, we review studies that examine the expression of bioactive peptides in the taste bud and the impact of those peptides on taste functions. Many of these peptides produced in taste buds are known to affect appetite, satiety or metabolism through their actions in the brain, pancreas and other organs, suggesting a functional link between the gustatory system and the neural and endocrine systems that regulate feeding and nutrient utilization.

Highlights

► Taste cells express a number of bioactive peptides. ► These peptides are differentially distributed in the taste bud. ► Many have been implicated in the regulation of feeding or nutrient metabolism. ► Cognate receptors are also expressed in taste cells or on associated nerves. ► These peptides likely modulate taste function through local actions at the taste bud.

Introduction

Sensory perceptions are not exact representations of the environment. Rather, these perceptions result from several layers of neural processing that occur after a stimulus is detected by sensory receptors. In this way, the recognition of specific sensory stimuli can be understood in the context of other sensory information as well as the animal's experience, motivation, and physiological state. While the central nervous system plays a fundamental role in sensory processing, the peripheral sensory organ can also critically shape the neural signals that are sent to the brain. The visual [1], [2], [3], olfactory [4], [5], [6], nociceptive [7], auditory [8], [9], vestibular [10] and somatosensory [11] systems all process sensory information to varying degrees at the level of the sensory organ. There is also growing evidence indicating that taste information undergoes significant processing within the gustatory sensory organ, the taste bud, as well as between the taste bud and the cranial nerves that carry gustatory information to the central nervous system. Recent reviews have done an excellent job of describing the roles of classical and non-classical small molecule neurotransmitters such as serotonin and adenosine triphosphate (ATP) in shaping peripheral taste responses [12], [13]. Here, we will focus on the emerging understanding of the role that peptide-mediated signaling may play in shaping gustatory responses in the taste bud.

Cells of the mammalian taste bud express a number of diverse peptide receptors and often their cognate ligands. All of these peptides have important roles outside the gustatory system, where they often act on nervous or endocrine tissues to regulate physiological responses. However, there is now an emerging view that these peptides, whether produced in the taste bud or in distant tissues, are impacting peripheral taste responsiveness through autocrine, paracrine and even endocrine signaling. Below, we discuss several peptides that are produced by taste bud cells as well as the evidence supporting roles for these peptides in regulating peripheral gustatory function.

Section snippets

The taste bud

Taste buds are collections of gustatory sensory cells, supporting cells and progenitor cells, and can be found on the dorsal surface of the tongue (on fungiform, foliate or circumvallate papillae) or on the soft palate [12], [13]. Taste cells are also found in the oropharynx. Taste cells can be differentiated based on morphology and ultrastructure, the expression of specific molecules, or their responses to taste stimuli that elicit distinct perceptual qualities (i.e., sweet, umami, bitter,

Glucagon-like peptide 1

Glucagon-like peptide 1 (GLP-1) is a 30-amino acid peptide hormone produced upon the cleavage of the prohormone proglucagon by the proprotein convertase PC1/3 (other peptides, including GLP-2 and glucagon, are also processed from proglucagon) [62]. GLP-1 is secreted from intestinal enteroendocrine L cells after meal ingestion [62]. Fats and sugars are both potent stimulators of GLP-1 secretion from the gut [63]. A major role of GLP-1 in the body is to regulate glucose homeostasis by stimulating

Summary

It is now clear that taste cells express a number of bioactive peptides. Furthermore, there is growing evidence that these peptides can impact taste function at the level of the gustatory periphery. However, we only have a cursory understanding of the conditions under which these peptides are released, the contributions they make to sensory coding, and the mechanisms by which they exert their effects. For example, is peptide signaling in taste cells linked to activation of the cells by

Acknowledgement

This work was supported by the National Institute on Deafness and Other Communication Disorders (DC010110, DC010364).

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