The Steroid Molting Hormone Ecdysone Regulates Sleep in Adult Drosophila Melanogaster

By Ishimoto, Hiroshi; Kitamoto, Toshihiro | Genetics, May 2010 | Go to article overview

The Steroid Molting Hormone Ecdysone Regulates Sleep in Adult Drosophila Melanogaster


Ishimoto, Hiroshi, Kitamoto, Toshihiro, Genetics


ABSTRACT

Ecdysone is the major steroid hormone in insects and plays essential roles in coordinating developmental transitions such as larval molting and metamorphosis through its active metabolite 20-hydroxyecdysone (20E). Although ecdysone is present throughout life in both males and females, its functions in adult physiology remain largely unknown. In this study we demonstrate that ecdysone-mediated signaling in the adult is intimately involved in transitions between the physiological states of sleep and wakefulness. First, administering 20E to adult Drosophila melanogaster promoted sleep in a dose-dependent manner, and it did so primarily by altering the length of sleep and wake bouts without affecting waking activity. Second, mutants for ecdysone synthesis displayed the "short-sleep phenotype," and this was alleviated by administering 20E at the adult stage. Third, mutants for nuclear ecdysone receptors showed reduced sleep, and conditional overexpression of wild-type ecdysone receptors in the adult mushroom bodies resulted in an isoform-specific increase in sleep. Finally, endogenous ecdysone levels increased after sleep deprivation, and mutants defective for ecdysone signaling displayed little sleep rebound, suggesting that ecdysone is involved in homeostatic sleep regulation. In light of the recent finding that lethargus-a period at larval-stage transitions in the nematode worm Caenorhabditis elegans-is a sleep-like state, our results suggest that sleep is functionally and mechanistically linked to a genetically programmed, quiescent behavioral state during development.

STEROID hormones have a wide variety of effects on the development, physiology and behavior of evolutionarily diverse organisms. The major steroid hormone in the fruit fly Drosophila melanogaster is ecdysone. Extensive studies in Drosophila and other insects have revealed that ecdysone plays vital roles in orchestrating major transitions during development-for example, during larval molting and metamorphosis-through its active metabolite 20-hydroxyecdysone (20E) (Truman and Riddiford 2002). The actions of ecdysone are primarily mediated by ecdysone receptors (EcRs), members of an evolutionarily conserved nuclear hormone receptor family. EcRs form heterodimers with the retinoid X receptor homolog ultraspiracle (USP), and these EcR/USP complexes function as ligand-activated transcription factors to regulate the expression of downstream genes in a tightly coordinated manner (Evans 1988; Aranda and Pascual 2001). Homozygous loss-offunction mutations in the EcR gene (EcR) are lethal, demonstrating that nuclear receptor-mediated ecdysone signaling is indispensable for development. Ecdysone is present throughout life in both males and females (Handler 1982). In adult females, ecdysone signaling is critical for reproduction, as it mediates eggchamber maturation during mid-oogenesis (Buszczak et al. 1999). However, other functions of ecdysone in mature adult flies have received less attention and remain largely elusive.

Unlike flies homozygous for loss-of-function mutations in EcR, those that are heterozygous for such mutations (EcR/1) develop into adult flies with no apparent deficit in morphology, activity, or fertility. Interestingly, EcR/1 adult flies show enhanced resistance to oxidative stress, heat, and dry starvation (Simon et al. 2003). In addition, under regular laboratory conditions, EcR/1 adult flies exhibit remarkable increases in life span, surviving 40-50% longer than wildtype controls (Simon et al. 2003). Other studies have demonstrated that the levels of 20E are increased in adult flies when they are exposed to unfavorable environmental conditions, such as nutrient restriction and heat treatment (Rauschenbach et al. 2000; Terashima et al. 2005). These findings indicate that ecdysone signaling indeed occurs in adult flies and that it is likely involved in endocrinologic regulation of their physiological and behavioral states in response to the internal and external environments. …

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The Steroid Molting Hormone Ecdysone Regulates Sleep in Adult Drosophila Melanogaster
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