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Food odors trigger an endocrine response that affects food ingestion and metabolism

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Abstract

Food odors stimulate appetite and innate food-seeking behavior in hungry animals. The smell of food also induces salivation and release of gastric acid and insulin. Conversely, sustained odor exposure may induce satiation. We demonstrate novel effects of food odors on food ingestion, metabolism and endocrine signaling in Drosophila melanogaster. Acute exposure to attractive vinegar odor triggers a rapid and transient increase in circulating glucose, and a rapid upregulation of genes encoding the glucagon-like hormone adipokinetic hormone (AKH), four insulin-like peptides (DILPs) and some target genes in peripheral tissues. Sustained exposure to food odors, however, decreases food intake. Hunger-induced strengthening of synaptic signaling from olfactory sensory neurons (OSNs) to brain neurons increases food-seeking behavior, and conversely fed flies display reduced food odor sensitivity and feeding. We show that increasing the strength of OSN signaling chronically by genetic manipulation of local peptide neuromodulation reduces feeding, elevates carbohydrates and diminishes lipids. Furthermore, constitutively strengthened odor sensitivity altered gene transcripts for AKH, DILPs and some of their targets. Thus, we show that food odor can induce a transient anticipatory endocrine response, and that boosted sensitivity to this odor affects food intake, as well as metabolism and hormonal signaling.

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Acknowledgments

We thank E. Rulifson (Stanford, CA), K. Yu (Daejeon, Korea), J. H. Park (Knoxville, TN), Ping Shen (Athens, GA) and Bloomington Drosophila Stock Center (BDSC), Bloomington, IN for providing fly stocks. We are grateful to J. A. Veenstra (Bordeaux, France) and Mark Brown (Athens, GA) for providing antisera. Drs Heinrich Dircksen and Jonas Bengtsson (both Stockholm) kindly read and commented on an earlier version of the manuscript. Funding was from the Swedish Research Council (VR) and Karl Trygger Foundation (both to D.R.N.).

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The authors declare that there was no conflict of interest.

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  1. Oleh V. Lushchak

    Present address: Department of Biochemistry and Biotechnology, Vasyl Stefanyk Precarpathian National University, Ivano-Frankivsk, Ukraine

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  1. Department of Zoology, Stockholm University, 10691, Stockholm, Sweden

    Oleh V. Lushchak, Mikael A. Carlsson & Dick R. Nässel

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Fig.S1

Expression of sNPF peptide and receptor in antennal OSNs. A Expression of snpfr-Gal4 in the antennal OSNs coincides to a large extent with sNPF peptide expression (α-sNPF). B Detail (framed area in A2) of OSNs expressing both markers. Scale bars: 25 µm (TIFF 4464 kb)

Fig.S2

Long term effects of sNPF manipulations in OSNs on metabolism (related to Fig. 4). A – D Female flies with sNPF overexpressed or knocked down (sNPF-RNAi) in OSNs (orco-Gal4 driver) were sampled after 25 d of adult life and assayed for carbohydrates and TAG. The results are similar to the effects seen in 3-4 d old flies (see Fig. 4). In all the above experiments data were analyzed by One-way ANOVA followed by Dunnett’s multiple comparison test, *p<0.05, **p<0.01, ***p<0.001, for each treatment n=50-60 (performed in 6 replicates) (TIFF 577 kb)

Fig.S3

Effects of sNPFR and insulin receptor (InR) manipulations in OSNs on metabolism and gene expression (related to Fig. 4 and 5). A – C Expression of sNPFR-RNAi and dInRCA in OSNs (orco-Gal4) does not affect levels of glucose, trehalose or glycogen. D Dilp6 levels are not significantly affected by receptor manipulations. E – H Of other gene transcripts tobi, upd2 and pepck are affected by sNPFR-RNAi and dInRCA expression, whereas 4ebp is not. In the above experiments data were analyzed by One-way ANOVA followed by Dunnett’s multiple comparison test, *p<0.05, **p<0.01, ***p<0.001, for each treatment n= 35-40 flies (measured in 4 replicates) (TIFF 1161 kb)

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Lushchak, O.V., Carlsson, M.A. & Nässel, D.R. Food odors trigger an endocrine response that affects food ingestion and metabolism. Cell. Mol. Life Sci. 72, 3143–3155 (2015). https://doi.org/10.1007/s00018-015-1884-4

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