PGC1α Controls Sucrose Taste Sensitization in Drosophila

Qiao-Ping Wang,Yong Qi Lin,Mei-Ling Lai,Zhiduan Su,Lisa J Oyston,Teleri Clark,Scarlet J Park,Thang M Khuong,Man-Tat Lau,Victoria Shenton,Yan-Chuan Shi,David E James,William W Ja,Herbert Herzog,Stephen J Simpson,G Gregory Neely

doi:10.1016/j.celrep.2020.03.044

Abstract

Perceived palatability of food controls caloric intake. Sweet taste is the primary means of detecting the carbohydrate content of food. Surprisingly, sweet taste sensitivity is responsive to extrinsic factors like diet, and this occurs by unknown mechanisms. Here, we describe an unbiased proteomic investigation into sweet taste sensitivity in the fruit fly. We identify a dopamine/cyclic AMP (cAMP)/CREB axis acting within sweet taste neurons that controls taste perception but is largely dispensable for acute taste transduction. This pathway modulates sweet taste perception in response to both sensory- and nutrient-restricted diets and converges on PGC1α, a critical regulator of metabolic health and lifespan. By electrophysiology, we found that enhanced sucrose taste sensitivity was the result of heightened sweet taste intensity and that PGC1α was both necessary and sufficient for this effect. Together, we provide the first molecular insight into how diet-induced taste perception is regulated within the sweet taste neuron.

Highlights

Sweet taste is used to estimate the nutritional value of foods, with the detection of simple carbohydrate content achieved primarily through sweet taste
The energy contained within dietary carbohydrates are fixed, sweet taste perception is dynamically regulated according to internal nutritional state, albeit through unclear mechanisms
After 6 days of exposure to each diet, animals were tested for sucrose taste sensitivity by using the proboscis extension response (PER) assay

Summary

Introduction

Sweet taste is used to estimate the nutritional value of foods, with the detection of simple carbohydrate content achieved primarily through sweet taste. The energy contained within dietary carbohydrates are fixed, sweet taste perception is dynamically regulated according to internal nutritional state, albeit through unclear mechanisms. Classical studies suggest internal nutritional state is a key factor for acute taste modulation to guide immediate nutritional requirements. In humans, fasting rapidly enhances sweet taste perception, whereas feeding acutely suppresses sweet sensitivity (Zverev, 2004). Modulation of taste sensitivity can be rapid and specific, with gustatory sensitivity to sweet tastes enhanced by short periods of carbohydrate deprivation and depressed by carbohydrate repletion and responses to amino acids independently modulated by dietary protein content (Simpson et al, 1991)

Results

Discussion

Conclusion