The impact of FOXO on dopamine and octopamine metabolism in Drosophila under normal and heat stress conditions.

Nataly E Gruntenko,Elena V Burdina,Inga Yu Rauschenbach,Olga V Andreenkova,Daniil V Gladkikh,Evgenia K Karpova,Natalya V Adonyeva,Yury Y Ilinsky

doi:10.1242/bio.022038

Abstract

ABSTRACTThe forkhead boxO transcription factor (FOXO) is a component of the insulin signalling pathway and plays a role in responding to adverse conditions, such as oxidative stress and starvation. In stressful conditions, FOXO moves from the cytosol to the nucleus where it activates gene expression programmes. Here, we show that FOXO in Drosophila melanogaster responds to heat stress as it does to other stressors. The catecholamine signalling pathway is another component of the stress response. In Drosophila, dopamine and octopamine levels rise steeply under heat, nutrition and mechanical stresses, which are followed by a decrease in the activity of synthesis enzymes. We demonstrate that the nearly twofold decline of FOXO expression in foxoBG01018 mutants results in dramatic changes in the metabolism of dopamine and octopamine and the overall response to stress. The absence of FOXO increases tyrosine decarboxylase activity, the first enzyme in octopamine synthesis, and decreases the enzymatic activity of enzymes in dopamine synthesis, alkaline phosphatase and tyrosine hydroxylase, in young Drosophila females. We identified the juvenile hormone as a mediator of FOXO regulation of catecholamine metabolism. Our findings suggest that FOXO is a possible trigger for endocrinological stress reactions.

Highlights

The endocrinological aspects of the stress response in insects include hormonal and neurotransmitter levels, and these parameters change sharply when an insect faces a stressor, such as adverse temperatures, mechanical and chemical stimuli, high population density, nutrient deprivation or immobilization (Peric-́ Mataruga et al, 2006; Gruntenko and Rauschenbach, 2008; Even et al, 2012)
Increased levels of DA and OA are accompanied by a decrease in the activity of the enzyme alkaline phosphatase (ALP), that regulates the pool of the DA and OA precursor, tyrosine (Wright, 1987), continuing for up to 140 min of stress exposure (Sukhanova et al, 1996; Bogomolova et al, 2010); and a decrease in the activity of the enzyme tyrosine decarboxylase (TDC) (Livingstone and Tempel, 1983), involved in OA synthesis, continuing for up to 120 min of stress exposure (Sukhanova et al, 1997; Gruntenko et al, 2004, 2009; Neckameyer and Weinstein, 2005)
Under normal conditions (Fig. 1A), antibody-labelled dFOXO was distributed throughout the cytoplasm in all cells, and no signal was detected in the nucleus

Summary

Introduction

The endocrinological aspects of the stress response in insects include hormonal and neurotransmitter levels, and these parameters change sharply when an insect faces a stressor, such as adverse temperatures, mechanical and chemical stimuli, high population density, nutrient deprivation or immobilization (Peric-́ Mataruga et al, 2006; Gruntenko and Rauschenbach, 2008; Even et al, 2012). Increased levels of DA and OA were accompanied by a decrease in the activity of the enzyme tyrosine hydroxylase (TH), that catalyses the first and rate-limiting step in DA synthesis (Neckameyer, 1996), continuing for up to 60 min of stress exposure (Rauschenbach et al, 1995). Increased levels of DA and OA are accompanied by a decrease in the activity of the enzyme alkaline phosphatase (ALP), that regulates the pool of the DA and OA precursor, tyrosine (Wright, 1987), continuing for up to 140 min of stress exposure (Sukhanova et al, 1996; Bogomolova et al, 2010); and a decrease in the activity of the enzyme tyrosine decarboxylase (TDC) (Livingstone and Tempel, 1983), involved in OA synthesis, continuing for up to 120 min of stress exposure (Sukhanova et al, 1997; Gruntenko et al, 2004, 2009; Neckameyer and Weinstein, 2005)

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