ReviewDeveloping a sense of taste
Highlights
► Early induction and patterning of taste buds occur via processes inherent to the developing tongue. ► Interactions of the Wnt, BMP, Shh and FGF pathways regulate early taste bud formation. ► Signals from the mesenchyme to the overlying epithelium are important regulators of taste bud pattern. ► FGF, Notch and miR-200 signaling control cell fate decisions within multicellular taste buds. ► Molecular genetic approaches in both mouse and zebrafish underlie recent advances in our understanding of taste development.
Introduction
Taste is a primary sense of all vertebrates, reliably conveying important chemical information from the mouth to the brain to regulate ingestion. For most animals, sweet, moderately salty or certain amino acid stimuli trigger appetitive behavior, while bitter or sour substances typically are rejected. The ability of animals to distinguish between nutritional, versus potentially lethal, fermented or unripe food items may mean the difference between survival and death. Human beings also rely on the taste system to select delicious foods and beverages based, in part, on taste preferences for the 5 basic taste stimuli; sweet, sour, salt, bitter, and umami (the taste of glutamate). Because taste is involved in ingestive behavior, this sensory system is inherently linked to human diseases that result from obesity, such as stroke, heart disease and diabetes.
Taste buds are multicellular receptor organs that transduce taste stimuli in the oral cavity. Multiple taste cells within buds are innervated by cranial nerve fibers, which in turn convey taste information to the brain. For nearly a century, taste buds were thought to be induced by nerve contact late in embryonic development. Over the past decade, however, this view has shifted dramatically. A host of studies now indicate that taste bud development is initiated and proceeds via processes that are nerve-independent, occur long before birth, and are governed by cellular and molecular mechanisms intrinsic to the developing tongue. Thus our primary focus here is a review of recent advances in our understanding of the molecular and cellular mechanisms of taste bud development that occur in the embryonic oropharynx.
Another aspect of our review is to emphasize the progress made in detailed mapping of the fates of embryonic cell populations that contribute to the developing taste periphery. In large part, these studies have entailed use of cutting edge molecular genetic mouse models, and each has provided new insights into the cellular mechanisms governing specification and differentiation of taste epithelium. These types of genetic tools have also been instrumental in revealing fundamental molecular machinery involved in these early processes.
Finally, while the focus of the field has for decades been on rodent model systems, more recently amphibian embryos, and now the genetic zebrafish and medaka systems are providing new insights and accelerating the pace of discovery. Here we highlight the newest molecular genetic data concerning taste bud development in fish.
Section snippets
The anatomy of the taste system of vertebrates
The sense of taste or gustation is mediated by multicellular taste buds, which reside primarily within the oral and pharyngeal cavities. Taste receptor cells transduce taste stimuli, i.e. sweet, bitter, sour, salt and umami, into electrochemical signals and transmit these signals to afferent nerve fibers of the VIIth, IXth and Xth cranial nerve ganglia, which in turn convey taste information to the first central taste relay located in the hindbrain, the nucleus of the solitary tract. To date,
Taste bud cellular composition in mice and fish
Each taste bud is composed of a heterogeneous population of fusiform cells, which parse into 3 morphological types (I, II and III), but physiologically likely represent at least 5 distinct functional classes (sweet, sour, salt, bitter and umami). Enormous advances have been made in our understanding of taste receptor cell function in the past decade, and these are reviewed elsewhere in this review volume (I. Matsumoto et al and references there in). Here we focus briefly on the conserved
Defining the embryonic origin of vertebrate taste buds
Taste buds are found in the epithelia lining the oral and pharyngeal cavity, and like epidermis of the skin, taste cells are continually renewed throughout adult life [37], [38]. Based on their location and this regenerative feature, taste bud cells have long been considered to be modified epithelial cells which therefore were presumed to arise directly from the local epithelium [39], [40]. Subsequently, this hypothesis was addressed experimentally; in axolotl (a type of salamander) [41]
Nerve-dependent induction
The prevailing model of taste bud development has been neural induction, where late in embryogenesis taste nerves invade the lingual epithelium and induce taste bud precursors from an otherwise homogeneously competent epithelium [47], [61], [62]. However, over the past 20 years, experimental tests have firmly rejected this hypothesis. Using both grafting and culture approaches combined with molecular marker expression, we showed that amphibian taste buds differentiate without innervation,
Molecular mechanisms of taste bud development
The focus of studies of taste bud development has now shifted from a neural induction model to processes intrinsic to the tongue, and in particular to investigations of the molecular mechanisms involved. To date, regulation of taste bud development involves a number of pathways known to play critical roles in a variety of tissues throughout development, as well as in adult homeostasis and disease. Foremost among these are the Shh and Wnt/β-catenin pathways. Here we review new data on the role
Conclusion
The sense of taste plays a key role in our ability to select palatable and nutritious foods, as well as to reject those substances that are toxic or decomposing. While our understanding of taste system function has expanded dramatically over the past 2 decades, how this system develops embryonically is only now receiving increased attention and study. Molecular genetic tools in mouse have become steadily more numerous and sophisticated, as well as more tractable for use in the taste system;
Acknowledgements
We are grateful to Frederic Rosa and IBENS (MK), and to the Rocky Mountain Taste and Smell Center (P30 DC004657) for support (LAB). This work was funded by the ANR-09-BLAN-077 (MK) and NIH/NIDCD DC008373 and DC003947 (LAB).
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Possible functional proximity of various organisms based on the bioinformatics analysis of their taste receptors
2022, International Journal of Biological MacromoleculesCitation Excerpt :Each bud is garlic shaped and is composed of 50–100 cells [7]. Taste buds are found in structures called papillae on the tongue, palate and on the wall of the throat [8,9]. Taste buds in the anterior two thirds of the tongue reside in the fungiform papillae, each containing one or a few taste buds.
Three-dimensional ultrastructure and histomorphology of mouse circumvallate papillary taste buds before and after birth using focused ion beam-scanning electron microscope tomography
2022, Tissue and CellCitation Excerpt :Zhang and colleagues reported that in the mouse CVP, no matured taste buds with taste pores are found at birth; however, the taste pores gradually form after birth (Zhang et al., 2008). Instead, taste buds fully differentiate in the postnatal week (Barlow, 2015; Kapsimali and Barlow, 2013). Nevertheless, immunohistological studies have shown that taste cells are differentiated before birth (Golden et al., 2021; Thirumangalathu and Barlow, 2015).
Nkx2-2 expressing taste cells in endoderm-derived taste papillae are committed to the type III lineage
2021, Developmental BiologyCitation Excerpt :Although several cell signaling pathways and transcription factors critical for the development of the taste system and adult taste cell renewal have been identified, our understanding of these processes is far from complete (Barlow, 2015). Intriguingly, cell signaling pathways such as SHH and Wnt/β-catenin can have varying effects in different taste fields and in embryonic and adult stages (Kapsimali and Barlow, 2013). However, the mechanisms underlying these differences are not known.
Age-related taste cell generation in circumvallate papillae organoids via regulation of multiple signaling pathways
2020, Experimental Cell ResearchCitation Excerpt :In mice, taste placodes develop as early as at E12, and taste papillae are well formed by E18.5 [1,11]. However, until the first postnatal week, taste buds do not express specific taste cell markers, especially in CV and FF papillae [6,11,12]. Multiple pathways are involved in regulating taste cells development [13].
Transcriptome analysis of axolotl oropharyngeal explants during taste bud differentiation stages
2020, Mechanisms of DevelopmentPolycomb Repressive Complex 1 Controls Maintenance of Fungiform Papillae by Repressing Sonic Hedgehog Expression
2019, Cell ReportsCitation Excerpt :It is organized as a patterned array of lingual papillae called fungiform and filiform papillae (Mbiene and Roberts, 2003; Okubo et al., 2006). The fungiform papillae harbor the taste cells (Barlow and Klein, 2015; Kapsimali and Barlow, 2013; Mistretta and Kumari, 2017) and are surrounded by non-gustatory filiform papillae that provide protective barrier functions and help in food intake (Manabe et al., 1999). During development, the lingual papillae originate from a single layer of lingual epithelial progenitors.