Cholecystokinin-like peptide mediates satiety by inhibiting sugar attraction.

Di Guo,Jian Li,Dick R Nässel,Su Zhang,Chao Guo,Yu-Feng Pan,Cong-Fen Gao,Shun-Fan Wu,Yi-Jie Zhang,Chen-Yu Li,Ya-Long Jia,Chen-Xi Liu,Jun-Yu Ma,Ning Zhang

doi:10.1371/journal.pgen.1009724

Abstract

Feeding is essential for animal survival and reproduction and is regulated by both internal states and external stimuli. However, little is known about how internal states influence the perception of external sensory cues that regulate feeding behavior. Here, we investigated the neuronal and molecular mechanisms behind nutritional state-mediated regulation of gustatory perception in control of feeding behavior in the brown planthopper and Drosophila. We found that feeding increases the expression of the cholecystokinin-like peptide, sulfakinin (SK), and the activity of a set of SK-expressing neurons. Starvation elevates the transcription of the sugar receptor Gr64f and SK negatively regulates the expression of Gr64f in both insects. Interestingly, we found that one of the two known SK receptors, CCKLR-17D3, is expressed by some of Gr64f-expressing neurons in the proboscis and proleg tarsi. Thus, we have identified SK as a neuropeptide signal in a neuronal circuitry that responds to food intake, and regulates feeding behavior by diminishing gustatory receptor gene expression and activity of sweet sensing GRNs. Our findings demonstrate one nutritional state-dependent pathway that modulates sweet perception and thereby feeding behavior, but our experiments cannot exclude further parallel pathways. Importantly, we show that the underlying mechanisms are conserved in the two distantly related insect species.

Highlights

Neuronal control of feeding is interesting for at least two reasons: in the human population there is a growing problem with excess food consumption causing obesity and associated severe health problems, and secondly, pest insects consume large amounts of our crops worldwide
After 24h we compared the food uptake to a control group, which was injected with phosphate-buffered saline (PBS)
N. lugens injected with sNlSK1 or sNlSK2 consumed 50%-70% less food than the PBS-injected control

Summary

Introduction

Neuronal control of feeding is interesting for at least two reasons: in the human population there is a growing problem with excess food consumption causing obesity and associated severe health problems, and secondly, pest insects consume large amounts of our crops worldwide. Both problems are very costly to society. Satiety signals lower the attractive sensory thresholds and act on neuronal circuits that regulate feeding behavior, thereby stopping further food intake [12,15]

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Conclusion