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First published online March 31, 2007
Journal of Experimental Biology 210, 1424-1434 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02755
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Regulation of feeding behaviour and locomotor activity by takeout in Drosophila

Nicolas Meunier*,{dagger}, Yesser Hadj Belgacem{dagger} and Jean-René Martin{ddagger}

Equipe: Bases Neurales des Comportements chez la Drosophile, Laboratoire de Neurobiologie Cellulaire et Moléculaire (NBCM), CNRS, Unité UPR-9040, 1 Avenue de la Terrasse (Bat. 32/33), F-91198 Gif-sur-Yvette Cedex, France


Figure 1
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  		Fig. 1. Food intake under normal and starved conditions. (A) Under normal conditions, both male and female to1 flies eat more than wild type [Canton Special (CS)]. Directed expression of the takeout (to) gene within to-producing cells (tim-GAL4/UAS-to in a to1 genetic background) fully rescues the phenotype in to1 females (rescue), but only partially in males. (B) To quantify the difference in feeding between CS and to1 flies under normal conditions, the amount of Blue dye ingested was indexed on CS. to1 males or females eat eight or three times more food than CS males or females, respectively. (C) After a 16-h period of starvation, the increase in food intake in CS flies (40-fold in males, eightfold in females) is significantly higher than in to1 flies (twofold in both males and females). Targeted expression of to rescues food intake in males, but only partially in females. The determination of the total food ingested, measured as the total amount of Blue dye ingested (OD, optic density), was performed on groups of 10 flies. The number in each box represents the number of fly groups used for each genotype. Rescue, tim-GAL4/UAS-to in a to1 genetic background; to1, to mutant. *P<0.05; **P<0.001; ***P<0.0001. Mean ± s.e.m.

 

Figure 2
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  		Fig. 2. Triglyceride and trehalose levels before and after starvation. (A) The total amount of triglycerides was quantified for each genotype before and after starvation. Prior to starvation, female and male to1 flies display an increase in the total amount of triglycerides. This phenotype is fully rescued by directed genetic expression of takeout (rescue) in both sexes. After 16 h starvation, the triglyceride level is reduced for all genotypes but the amount of triglycerides remains higher for to1. This phenotype was also rescued in males, but not in females. (B) The total amount of trehalose was quantified for each genotype before and after starvation. Female and male wild-types displayed a decrease in their level of trehalose after starvation. However, starvation had no effect on trehalose level in to1 flies. As for the triglyceride level, this phenotype was rescued genetically. The total amount of triglycerides and trehalose was determined on groups of 10 flies. The number in each box represents the number of fly groups used for each genotype. In B, for the statistical analysis, the comparison was performed, for the same genotype, before and after starvation. CS, Canton Special; rescue, tim-GAL4/UAS-to in a to1 genetic background; to1, to mutant. *P<0.05; **P<0.001; ***P<0.0001. Mean ± s.e.m.

 

Figure 3
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  		Fig. 3. Presence of Takeout (TO) in the head fat body, which is hypertrophic in to1. (A) Immunohistological staining using an anti-TO antibody. (Ai,Aii) TO is detected in the head fat body (arrows) of a wild-type Canton Special (CS) male, whereas in a to1 mutant it is not detected (10x; scale bar, 100 µm). (Aiii,Aiv) In wild-type CS, TO is also detected in the gustatory sensilla (arrows) (Aiii: 20x; scale bar, 50 µm. Aiv: 40x; scale bar, 25 µm). (B) Hematoxylin-Eosin (HE) staining reveals that under normal feeding conditions, to flies exhibit a hypertrophic head fat body (outlined in red). The 40x field corresponds to the 10x outlined area. The head fat body cells in to1 exhibit large lipid vacuoles (40x image). This phenotype is rescued by directed genetic expression of to within the to-producing cells. (40x: scale bar, 25 µm; 10x: scale bar, 100 µm). (C) After a 16-h period of starvation, the head fat body is reduced in wild-type flies, because they have mobilized their energy resource. The HE staining is more intense in the head fat body of wild-type flies as cells have shrunk and cell membranes are tightly regrouped. In to1 flies, the fat body is also reduced, but less so than in wild type. This phenotype is also rescued by directed genetic expression of to within TO-producing cells. Rescue, tim-GAL4/UAS-to in a to1 genetic background; to1, to mutant.

 

Figure 4
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  		Fig. 4. Modulation of taste sensitivity of gustatory neurons to sugar after starvation. The response of the gustatory neurons sensitive to sugar is estimated by the number of spikes during the first second after stimulation with 100 mmol l–1 glucose. Results are normalized on response prior to starvation for each genotype. After starvation, the activity of neurons sensitive to sugars is increased by approximately 20% in wild type, whereas it remains unchanged for to1 (takeout mutant), suggesting that to1 gustatory neurons do not modulate their activity after a starvation period. This phenotype is rescued by directed genetic expression of to within the to-producing cells. The number in each box represents the number of sensilla recorded for each genotype. CS, Canton Special; rescue, tim-GAL4/UAS-to in a to1 genetic background. Data presented are recorded from males. *P<0.05; **P<0.001. Mean ± s.e.m.

 

Figure 5
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  		Fig. 5. takeout mutants (to1) displayed disturbed locomotor activity. Total distance traveled by flies during a 5-h period of recording of locomotor activity, as measured by video-tracking. Male and female to1 flies displayed lower total distance traveled, which can be correlated to lower foraging activity. This phenotype is fully rescued in males, whereas it is only partially rescued in females. The number in each box represents the number of flies recorded for each genotype. CS, Canton Special; rescue, tim-GAL4/UAS-to in a to1 genetic background. *P<0.05; **P<0.001. Mean ± s.e.m.

 

Figure 6
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  		Fig. 6. to1 (takeout mutant) defects in sexual dimorphism of locomotor activity are related to juvenile hormone (JH) level. (A) Wild-type flies present a sexual dimorphism in locomotor activity, as the males do not have the same number of start/stop phases compared with females. This sexual dimorphism is absent in to1. This phenotype is rescued by directed genetic expression of to within the to-producing cells. (B) The normal number of start/stop phases is rescued by local application of methoprene (a JH analog) compared with the vehicle alone (ethanol), suggesting that to serves as a JH carrier. The number in each box represents the number of flies recorded for each genotype. CS, Canton Special; rescue, tim-GAL4/UAS-to in a to1 genetic background. *P<0.05; **P<0.001. Mean ± s.e.m.

 

Figure 7
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  		Fig. 7. Proposed model of Takeout (TO) action. Juvenile hormone (JH) produced by corpus allatum could have pleiotropic effects according to the circulating juvenile hormone binding proteins (JHBPs). During starvation, TO level is increased and the binding of JH-TO could act specifically on target cells to regulate feeding behavior.

 

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© The Company of Biologists Ltd 2007