Neuronal influence on peripheral circadian oscillators in pupal Drosophila prothoracic glands

Morioka, Eri; Matsumoto, Akira; Ikeda, Masayuki

doi:10.1038/ncomms1922

Cited by 33 publications

(51 citation statements)

References 39 publications

(61 reference statements)

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“…The regulatory group comprises a total of 13 DNA-binding proteins. Of these, molting defective ( mld ), vvl, ouija board ( ouib , aka CG11762 ), snail , and timeless ( tim ) were already known to have specific expression in the RG (Cheng et al, 2014; Danielsen et al, 2014; Komura-Kawa et al, 2015; Morioka et al, 2012; Neubueser et al, 2005;Sánchez-Higueras et al, 2014), while tinman has been linked to the embryonic development of the CC, but no expression in the RG has been demonstrated (Park et al, 2011). Among the identified transcription factors are Escargot, which is related to Snail, and Hand, which ranks among the 50 most highly enriched mRNAs in the RG (Table S2), as well as pdm3 , which encodes—like vvl —a POU-domain transcription factor.…”

Section: Resultsmentioning

confidence: 99%

The Insect Prothoracic Gland as a Model for Steroid Hormone Biosynthesis and Regulation

Zeng

Yamanaka

et al. 2016

Cell Reports

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SUMMARY Steroid hormones are ancient signaling molecules found in vertebrates and insects alike. Both taxa show intriguing parallels with respect to how steroids function and how their synthesis is regulated. As such, insects are excellent models for studying universal aspects of steroid physiology. Here, we present a comprehensive genomic and genetic analysis of the principal steroid hormone-producing organs in two popular insect models, Drosophila and Bombyx. We identified 173 genes with previously unknown specific expression in steroid-producing cells, 15 of which had critical roles in development. The insect neuropeptide PTTH and its vertebrate counterpart ACTH both regulate steroid production, but molecular targets of these pathways remain poorly characterized. Identification of PTTH-dependent gene sets identified the nuclear receptor HR4 as a highly conserved target in both Drosophila and Bombyx. We consider this study to be a critical step toward understanding how steroid hormone production and release are regulated in all animal models.

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Section: Resultsmentioning

confidence: 99%

The Insect Prothoracic Gland as a Model for Steroid Hormone Biosynthesis and Regulation

Zeng

Yamanaka

et al. 2016

Cell Reports

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“…; Morioka et al . ). Therefore, gene expression levels of a certain set of genes in the PG might be transcriptionally oscillated under the control of the central clock network.…”

Section: Discussionmentioning

confidence: 97%

“…No validated targets of HLH54F in the PG have been reported. More interestingly, the central circadian clock genes period and timeless, which do not encode actual TFs but regulatory proteins modulating transcription, are rhythmically expressed in the pupal PG and play a role in controlling eclosion rhythms (Myers et al 2003;Morioka et al 2012). Therefore, gene expression levels of a certain set of genes in the PG might be transcriptionally oscillated under the control of the central clock network.…”

Section: Discussionmentioning

confidence: 99%

Transcriptional regulation of insect steroid hormone biosynthesis and its role in controlling timing of molting and metamorphosis

Niwa

2015

Dev Growth Differ

113

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The developmental transition from juvenile to adult is often accompanied by many systemic changes in morphology, metabolism, and reproduction. Curiously, both mammalian puberty and insect metamorphosis are triggered by a pulse of steroid hormones, which can harmonize gene expression profiles in the body and thus orchestrate drastic biological changes. However, understanding of how the timing of steroid hormone biosynthesis is regulated at the molecular level is poor. The principal insect steroid hormone, ecdysteroid, is biosynthesized from dietary cholesterol in the specialized endocrine organ called the prothoracic gland. The periodic pulses of ecdysteroid titers determine the timing of molting and metamorphosis. To date, at least nine families of ecdysteroidogenic enzyme genes have been identified. Expression levels of these genes correlate well with ecdysteroid titers, indicating that the transcriptional regulatory network plays a critical role in regulating the ecdysteroid biosynthesis pathway. In this article, we summarize the transcriptional regulation of ecdysteroid biosynthesis. We first describe the development of prothoracic gland cells during Drosophila embryogenesis, and then provide an overview of the transcription factors that act in ecdysteroid biosynthesis and signaling. We also discuss the external signaling pathways that target these transcriptional regulators. Furthermore, we describe conserved and/or diverse aspects of steroid hormone biosynthesis in insect species as well as vertebrates.

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“…This gland produces the hormone ecdysone, which declines in levels, presumably in response to circadian signals, just prior to eclosion. Although weak autonomous oscillations of clock genes in PG cells can be seen in the absence of brain input, input from the central nervous system (dependent on PDF and LNs) dramatically amplifies and synchronizes oscillations in this tissue (Myers et al 2003;Morioka et al 2012). On the other hand, a clock in the Malphigian Tubules, equivalent to the kidney, appears to be entirely autonomous and directly entrained by light, presum-ably by CRY expression in this tissue (Giebultowicz et al 2000).…”

Section: Peripheral Clocksmentioning

confidence: 99%

Circadian Rhythms and Sleep in Drosophila melanogaster

2017

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The advantages of the model organism Drosophila melanogaster, including low genetic redundancy, functional simplicity, and the ability to conduct large-scale genetic screens, have been essential for understanding the molecular nature of circadian (24 hr) rhythms, and continue to be valuable in discovering novel regulators of circadian rhythms and sleep. In this review, we discuss the current understanding of these interrelated biological processes in Drosophila and the wider implications of this research. Clock genes period and timeless were first discovered in large-scale Drosophila genetic screens developed in the 1970s. Feedback of period and timeless on their own transcription forms the core of the molecular clock, and accurately timed expression, localization, post-transcriptional modification, and function of these genes is thought to be critical for maintaining the circadian cycle. Regulators, including several phosphatases and kinases, act on different steps of this feedback loop to ensure strong and accurately timed rhythms. Approximately 150 neurons in the fly brain that contain the core components of the molecular clock act together to translate this intracellular cycling into rhythmic behavior. We discuss how different groups of clock neurons serve different functions in allowing clocks to entrain to environmental cues, driving behavioral outputs at different times of day, and allowing flexible behavioral responses in different environmental conditions. The neuropeptide PDF provides an important signal thought to synchronize clock neurons, although the details of how PDF accomplishes this function are still being explored. Secreted signals from clock neurons also influence rhythms in other tissues. SLEEP is, in part, regulated by the circadian clock, which ensures appropriate timing of sleep, but the amount and quality of sleep are also determined by other mechanisms that ensure a homeostatic balance between sleep and wake. Flies have been useful for identifying a large set of genes, molecules, and neuroanatomic loci important for regulating sleep amount. Conserved aspects of sleep regulation in flies and mammals include wake-promoting roles for catecholamine neurotransmitters and involvement of hypothalamus-like regions, although other neuroanatomic regions implicated in sleep in flies have less clear parallels. Sleep is also subject to regulation by factors such as food availability, stress, and social environment. We are beginning to understand how the identified molecules and neurons interact with each other, and with the environment, to regulate sleep. Drosophila researchers can also take advantage of increasing mechanistic understanding of other behaviors, such as learning and memory, courtship, and aggression, to understand how sleep loss impacts these behaviors. Flies thus remain a valuable tool for both discovery of novel molecules and deep mechanistic understanding of sleep and circadian rhythms.

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Neuronal influence on peripheral circadian oscillators in pupal Drosophila prothoracic glands

Cited by 33 publications

References 39 publications

The Insect Prothoracic Gland as a Model for Steroid Hormone Biosynthesis and Regulation

The Insect Prothoracic Gland as a Model for Steroid Hormone Biosynthesis and Regulation

Transcriptional regulation of insect steroid hormone biosynthesis and its role in controlling timing of molting and metamorphosis

Circadian Rhythms and Sleep in Drosophila melanogaster

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