High Dietary Sugar Reshapes Sweet Taste to Promote Feeding Behavior in Drosophila melanogaster

Christina E May,Anoumid Vaziri,Yong Qi Lin,Olga Grushko,Morteza Khabiri,Qiao-Ping Wang,Kristina J Holme,Scott D Pletcher,Peter L Freddolino,G Gregory Neely,Monica Dus

doi:10.1016/j.celrep.2019.04.027

Christina E May, Anoumid Vaziri + Show 9 more

Open Access

https://doi.org/10.1016/j.celrep.2019.04.027

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Abstract

Recent studies find that sugar tastes less intense to humans with obesity, but whether this sensory change is a cause or a consequence of obesity is unclear. To tackle this question, we study the effects of a high sugar diet on sweet taste sensation and feeding behavior in Drosophila melanogaster. On this diet, fruit flies have lower taste responses to sweet stimuli, overconsume food, and develop obesity. Excess dietary sugar, but not obesity or dietary sweetness alone, caused taste deficits and overeating via the cell-autonomous action of the sugar sensor O-linked N-Acetylglucosamine (O-GlcNAc) transferase (OGT) in the sweet-sensing neurons. Correcting taste deficits by manipulating the excitability of the sweet gustatory neurons or the levels of OGT protected animals from diet-induced obesity. Our work demonstrates that the reshaping of sweet taste sensation by excess dietary sugar drives obesity and highlights the role of glucose metabolism in neural activity and behavior.

Highlights

Many arguments about the underlying cause in the rise of obesity point toward the increased availability of highly palatable foods
Do changes in taste sensation occur with diet-induced obesity? Are these changes a consequence of the altered physiology of the obese state or do they result from chronic exposure to a high nutrient diet? And, if changes in taste function occur, what role do they play in the etiology of obesity?
We tested genetically lean flies to ask if a decrease in taste responses was linked to high dietary sugar, instead of obesity. perilipin2 is a gene essential for fat mobilization (Beller et al, 2010) (Figure 2A); despite remaining lean (Figure 2B) and maintaining normal Drosophila insulin-like peptide transcript levels on a SD (Figures S2A and S2B), plin2 mutants experienced a comparable decrease in taste responses relative to that of control and bmm mutant flies (Figure 2C). These results suggest that obesity is neither necessary nor sufficient for the reduction in sweet taste, and that, instead, excess dietary sugar—but not just dietary sweetness, since a sweet sucralose diet did not dull sweet taste—may alter taste directly

Summary

Introduction

Many arguments about the underlying cause in the rise of obesity point toward the increased availability of highly palatable foods. Such foods are thought to alter the activity of reward pathways at least partly via their taste properties, and this leads to overconsumption and weight gain (Small, 2009; Volkow et al, 2011). No doubt the perception of palatable food qualities such as sweetness plays a key role in eating behaviors. This hypothesis does not fit with a growing body of evidence that associates obesity with reduced taste perceptions (Bartoshuk et al, 2006; Berthoud and Zheng, 2012; Rodin et al, 1976). Do changes in taste sensation occur with diet-induced obesity? Are these changes a consequence of the altered physiology of the obese state or do they result from chronic exposure to a high nutrient diet? And, if changes in taste function occur, what role do they play in the etiology of obesity?

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Discussion

Conclusion