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Bitter taste receptors confer diverse functions to neurons.

Delventhal R, Carlson JR - Elife (2016)

Bottom Line: Expression of individual Grs conferred strikingly different effects in different neurons.The results support a model in which bitter Grs interact, exhibiting competition, inhibition, or activation.The results have broad implications for the problem of how taste systems evolve to detect new environmental dangers.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, United States.

ABSTRACT
Bitter compounds elicit an aversive response. In Drosophila, bitter-sensitive taste neurons coexpress many members of the Gr family of taste receptors. However, the molecular logic of bitter signaling is unknown. We used an in vivo expression approach to analyze the logic of bitter taste signaling. Ectopic or overexpression of bitter Grs increased endogenous responses or conferred novel responses. Surprisingly, expression of Grs also suppressed many endogenous bitter responses. Conversely, deletion of an endogenous Gr led to novel responses. Expression of individual Grs conferred strikingly different effects in different neurons. The results support a model in which bitter Grs interact, exhibiting competition, inhibition, or activation. The results have broad implications for the problem of how taste systems evolve to detect new environmental dangers.

No MeSH data available.


Related in: MedlinePlus

Findings and models.Four findings of this study are indicated, along with one possible model to explain each. i) Expression of a Gr, indicated by the blue sphere, decreases the response to a tastant, represented by the traces below. One possible model is that the expressed Gr (blue sphere) interacts with another, active Gr (green) and inhibits it (represented by its conversion from a green, active Gr to a red, inactive Gr). ii) Deletion of Gr59c (blue sphere with X) leads to an increased response. One possible model is that in wild type, the Gr inhibits an endogenous Gr (red). Removal of the Gr allows the inactive Gr (red) to become active (green). iii) Overexpression of a Gr, in a neuron that contains the Gr endogenously, induces a response that is not observed in wild type. One model is that above a certain concentration threshold of the Gr, it is able to bind and convert another Gr from an inactive (red) to an active (green) form. iv) Expression of a Gr in two different neurons, 'A' and 'B,' produces different results. The neuron at left shows an increase in response to a tastant whereas the neuron at the right shows a decrease. One model is that in the A neuron, the expressed Gr (blue) binds to an inactive Gr (red) specific to neuron A, and activates it (green). By contrast, in the B neuron, the expressed Gr (blue) binds to a different Gr (green) specific to neuron B, and inactivates it (red).DOI:http://dx.doi.org/10.7554/eLife.11181.019
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fig12: Findings and models.Four findings of this study are indicated, along with one possible model to explain each. i) Expression of a Gr, indicated by the blue sphere, decreases the response to a tastant, represented by the traces below. One possible model is that the expressed Gr (blue sphere) interacts with another, active Gr (green) and inhibits it (represented by its conversion from a green, active Gr to a red, inactive Gr). ii) Deletion of Gr59c (blue sphere with X) leads to an increased response. One possible model is that in wild type, the Gr inhibits an endogenous Gr (red). Removal of the Gr allows the inactive Gr (red) to become active (green). iii) Overexpression of a Gr, in a neuron that contains the Gr endogenously, induces a response that is not observed in wild type. One model is that above a certain concentration threshold of the Gr, it is able to bind and convert another Gr from an inactive (red) to an active (green) form. iv) Expression of a Gr in two different neurons, 'A' and 'B,' produces different results. The neuron at left shows an increase in response to a tastant whereas the neuron at the right shows a decrease. One model is that in the A neuron, the expressed Gr (blue) binds to an inactive Gr (red) specific to neuron A, and activates it (green). By contrast, in the B neuron, the expressed Gr (blue) binds to a different Gr (green) specific to neuron B, and inactivates it (red).DOI:http://dx.doi.org/10.7554/eLife.11181.019

Mentions: The effects observed in this study are difficult to reconcile with this simple model of Gr function. A more complex model is required to explain, for example, the findings that: i) expression of some Grs decreased endogenous responses; ii) deletion of Gr59c increased the response to certain tastants; iii) expression of some Grs in neurons in which they are endogenously expressed caused novel responses; iv) the effects of expression of a Gr differed among neuron types (Figures 11, 12, Figure 11—figure supplement 1). Below we consider mechanisms that could explain these findings.10.7554/eLife.11181.019Figure 12.Findings and models.


Bitter taste receptors confer diverse functions to neurons.

Delventhal R, Carlson JR - Elife (2016)

Findings and models.Four findings of this study are indicated, along with one possible model to explain each. i) Expression of a Gr, indicated by the blue sphere, decreases the response to a tastant, represented by the traces below. One possible model is that the expressed Gr (blue sphere) interacts with another, active Gr (green) and inhibits it (represented by its conversion from a green, active Gr to a red, inactive Gr). ii) Deletion of Gr59c (blue sphere with X) leads to an increased response. One possible model is that in wild type, the Gr inhibits an endogenous Gr (red). Removal of the Gr allows the inactive Gr (red) to become active (green). iii) Overexpression of a Gr, in a neuron that contains the Gr endogenously, induces a response that is not observed in wild type. One model is that above a certain concentration threshold of the Gr, it is able to bind and convert another Gr from an inactive (red) to an active (green) form. iv) Expression of a Gr in two different neurons, 'A' and 'B,' produces different results. The neuron at left shows an increase in response to a tastant whereas the neuron at the right shows a decrease. One model is that in the A neuron, the expressed Gr (blue) binds to an inactive Gr (red) specific to neuron A, and activates it (green). By contrast, in the B neuron, the expressed Gr (blue) binds to a different Gr (green) specific to neuron B, and inactivates it (red).DOI:http://dx.doi.org/10.7554/eLife.11181.019
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Related In: Results  -  Collection

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fig12: Findings and models.Four findings of this study are indicated, along with one possible model to explain each. i) Expression of a Gr, indicated by the blue sphere, decreases the response to a tastant, represented by the traces below. One possible model is that the expressed Gr (blue sphere) interacts with another, active Gr (green) and inhibits it (represented by its conversion from a green, active Gr to a red, inactive Gr). ii) Deletion of Gr59c (blue sphere with X) leads to an increased response. One possible model is that in wild type, the Gr inhibits an endogenous Gr (red). Removal of the Gr allows the inactive Gr (red) to become active (green). iii) Overexpression of a Gr, in a neuron that contains the Gr endogenously, induces a response that is not observed in wild type. One model is that above a certain concentration threshold of the Gr, it is able to bind and convert another Gr from an inactive (red) to an active (green) form. iv) Expression of a Gr in two different neurons, 'A' and 'B,' produces different results. The neuron at left shows an increase in response to a tastant whereas the neuron at the right shows a decrease. One model is that in the A neuron, the expressed Gr (blue) binds to an inactive Gr (red) specific to neuron A, and activates it (green). By contrast, in the B neuron, the expressed Gr (blue) binds to a different Gr (green) specific to neuron B, and inactivates it (red).DOI:http://dx.doi.org/10.7554/eLife.11181.019
Mentions: The effects observed in this study are difficult to reconcile with this simple model of Gr function. A more complex model is required to explain, for example, the findings that: i) expression of some Grs decreased endogenous responses; ii) deletion of Gr59c increased the response to certain tastants; iii) expression of some Grs in neurons in which they are endogenously expressed caused novel responses; iv) the effects of expression of a Gr differed among neuron types (Figures 11, 12, Figure 11—figure supplement 1). Below we consider mechanisms that could explain these findings.10.7554/eLife.11181.019Figure 12.Findings and models.

Bottom Line: Expression of individual Grs conferred strikingly different effects in different neurons.The results support a model in which bitter Grs interact, exhibiting competition, inhibition, or activation.The results have broad implications for the problem of how taste systems evolve to detect new environmental dangers.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, United States.

ABSTRACT
Bitter compounds elicit an aversive response. In Drosophila, bitter-sensitive taste neurons coexpress many members of the Gr family of taste receptors. However, the molecular logic of bitter signaling is unknown. We used an in vivo expression approach to analyze the logic of bitter taste signaling. Ectopic or overexpression of bitter Grs increased endogenous responses or conferred novel responses. Surprisingly, expression of Grs also suppressed many endogenous bitter responses. Conversely, deletion of an endogenous Gr led to novel responses. Expression of individual Grs conferred strikingly different effects in different neurons. The results support a model in which bitter Grs interact, exhibiting competition, inhibition, or activation. The results have broad implications for the problem of how taste systems evolve to detect new environmental dangers.

No MeSH data available.


Related in: MedlinePlus