Autocrine and Paracrine Roles for ATP and Serotonin in Mouse Taste Buds

Huang, Yung Kai; Dando, Robin; Roper, Stephen D.

doi:10.1523/jneurosci.2351-09.2009

Cited by 142 publications

(183 citation statements)

References 42 publications

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“…Consistently, taste cells of the type II have been demonstrated to release ATP into intercellular space upon gustatory and electrical stimulation (Huang et al, 2007;Romanov et al, 2007). This entails activation of P2X2/P2X3 receptors on afferent taste nerves (Bo et al, 1999;Kataoka et al, 2006) and a variety of P2X and P2Y receptors on taste cells (Baryshnikov et al, 2003;Kataoka et al, 2004;Bystrova et al, 2006;Huang et al, 2009;Huang et al, 2011). Taste cells of the type II lack conventional synapses (Royer and Kinnamon, 1991;Tabata et al, 1995), but instead release ATP via voltage-gated channels (Huang et al, 2007;Huang et al, 2011;Romanov et al, 2007;Romanov et al, 2008).…”

Section: Introductionmentioning

confidence: 94%

Dispensable ATP permeability of Pannexin 1 channels in a heterologous system and in mammalian taste cells

Romanov

Bystrova

Rogachevskaya

et al. 2012

Journal of Cell Science

154

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SummaryAfferent output in type II taste cells is mediated by ATP liberated through ion channels. It is widely accepted that pannexin 1 (Panx1) channels are responsible for ATP release in diverse cell types, including taste cells. While biophysical evidence implicates slow deactivation of ion channels following ATP release in taste cells, recombinant Panx1 activates and deactivates rapidly. This inconsistency could indicate that the cellular context specifies Panx1 functioning. We cloned Panx1 from murine taste tissue, and heterologously expressed it in three different cell lines: HEK-293, CHO and neuroblastoma SK-N-SH cells. In all three cell lines, Panx1 transfection yielded outwardly rectifying anion channels that exhibited fast gating and negligible permeability to anions exceeding 250 Da. Despite expression of Panx1, the host cells did not liberate ATP upon stimulation, making it unclear whether Panx1 is involved in taste-related ATP secretion. This issue was addressed using mice with genetic ablation of the Panx1 gene. The ATP-biosensor assay revealed that, in taste cells devoid of Panx1, ATP secretion was robust and apparently unchanged compared with the control. Our data suggest that Panx1 alone forms a channel that has insufficient permeability to ATP. Perhaps, a distinct subunit and/or a regulatory circuit that is absent in taste cells is required to enable a high ATP-permeability mode of a native Panx1-based channel.

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Section: Introductionmentioning

confidence: 94%

Dispensable ATP permeability of Pannexin 1 channels in a heterologous system and in mammalian taste cells

Romanov

Bystrova

Rogachevskaya

et al. 2012

Journal of Cell Science

154

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“…However, no studies have yet resolved whether the salty and sour responses observed in type III taste cells arise from two distinct populations of cells or whether receptors for sour and salty taste are coexpressed in the same type III cells. Much of the difficulty in resolving this question arises from the prevalence of cell-to-cell communication in the intact taste bud, which makes it difficult to determine whether the response of a taste cell to a tastant is attributable to the tastant interacting with receptors/channels expressed by the cell itself or whether the cell is being activated indirectly through cell-to-cell communication (Caicedo et al, 2002;Tomchik et al, 2007;Huang et al, 2009;Roper, 2013). This difficulty is of particular concern for type III taste cells, which commonly respond to multiple taste qualities, including sweet, bitter, and umami (Tomchik et al, 2007), de- Ca 2ϩ responses to taste stimuli and KCl depolarization in isolated CV taste cells can be used to reliably identify AI salt-responsive type III taste cells.…”

Section: B)mentioning

confidence: 99%

Amiloride-Insensitive Salt Taste Is Mediated by Two Populations of Type III Taste Cells with Distinct Transduction Mechanisms

et al. 2016

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Responses in the amiloride-insensitive (AI) pathway, one of the two pathways mediating salty taste in mammals, are modulated by the size of the anion of a salt. This "anion effect" has been hypothesized to result from inhibitory transepithelial potentials (TPs) generated across the lingual epithelium as cations permeate through tight junctions and leave their larger and less permeable anions behind (Ye et al., 1991). We tested directly the necessity of TPs for the anion effect by measuring responses to NaCl and Na-gluconate (small and large anion sodium salts, respectively) in isolated taste cells from mouse circumvallate papillae. Using calcium imaging, we identified AI salt-responsive type III taste cells and demonstrated that they compose a subpopulation of acid-responsive taste cells. Even in the absence of TPs, many (66%) AI salt-responsive type III taste cells still exhibited the anion effect, demonstrating that some component of the transduction machinery for salty taste in type III cells is sensitive to anion size. We hypothesized that osmotic responses could explain why a minority of type III cells (34%) had AI salt responses but lacked anion sensitivity. All AI type III cells had osmotic responses to cellobiose, which were significantly modulated by extracellular sodium concentration, suggesting the presence of a sodium-conducting osmotically sensitive ion channel. However, these responses were significantly larger in AI type III cells that did not exhibit the anion effect. These findings indicate that multiple mechanisms could underlie AI salt responses in type III taste cells, one of which may contribute to the anion effect.

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“…43 Upon secretion, ATP acts as a neurotransmitter on nearby sensory afferent fibers 44,45 ; ATP also acts as a paracrine/autocrine hormone, binding with receptors expressed on neighboring taste receptor cells. [46][47][48][49][50] Type III cells release serotonin, c-amino butyric acid, and norepinephrine and are most notable for possessing synapses. [51][52][53][54] These cells, also termed presynaptic cells, express voltage-gated calcium channels associated with neurotransmitter release, enzymes for serotonin, and c-amino butyric acid, as well as uptake transporters for biogenic amines.…”

Section: Taste Bud Anatomy and Physiologymentioning

confidence: 99%

Taste perception, associated hormonal modulation, and nutrient intake

et al. 2015

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It is well known that taste perception influences food intake. After ingestion, gustatory receptors relay sensory signals to the brain, which segregates, evaluates, and distinguishes the stimuli, leading to the experience known as "flavor." It is well accepted that five taste qualities -sweet, salty, bitter, sour, and umami -can be perceived by animals. In this review, the anatomy and physiology of human taste buds, the hormonal modulation of taste function, the importance of genetic chemosensory variation, and the influence of gustatory functioning on macronutrient selection and eating behavior are discussed. Individual genotypic variation results in specific phenotypes of food preference and nutrient intake. Understanding the role of taste in food selection and ingestive behavior is important for expanding our understanding of the factors involved in body weight maintenance and the risk of chronic diseases including obesity, atherosclerosis, cancer, diabetes, liver disease, and hypertension.

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Autocrine and Paracrine Roles for ATP and Serotonin in Mouse Taste Buds

Abstract: Receptor (type II)

Cited by 142 publications

References 42 publications

Dispensable ATP permeability of Pannexin 1 channels in a heterologous system and in mammalian taste cells

Dispensable ATP permeability of Pannexin 1 channels in a heterologous system and in mammalian taste cells

Amiloride-Insensitive Salt Taste Is Mediated by Two Populations of Type III Taste Cells with Distinct Transduction Mechanisms

Taste perception, associated hormonal modulation, and nutrient intake

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