Review

Authors: Tianqi Xu, Xin Jiang, Donna Denton...

The removal of superfluous and unwanted cells is a critical part of animal development. In insects the steroid hormone ecdysone, the focus of this review, is an essential regulator of developmental transitions, including molting and metamorphosis. Like other steroid hormones, ecdysone works via nuclear hormone receptors to direct spatial and temporal regulation of gene transcription including genes required for cell death. During insect metamorphosis, pulses of ecdysone orchestrate the deletion of obsolete larval tissues, including the larval salivary glands and the midgut. In this review we discuss the molecular machinery and mechanisms of ecdysone-dependent cell and tissue removal, with a focus on studies in Drosophila and Lepidopteran insects.

Topics: Animals; Cell Death; Drosophila; Ecdysone; Lepidoptera; Metamorphosis, Biological; Molting

PubMed: 31745213
DOI: 10.1038/s41418-019-0456-9

Authors: Jennifer M Clark, Allen G Gibbs

Previous studies have shown that selection for starvation resistance in Drosophila melanogaster results in delayed eclosion and increased adult fat stores. It is assumed that these traits are caused by the starvation selection pressure, but its mechanism is unknown. We found that our starvation-selected (SS) population stores more fat during larval development and has extended larval development and pupal development time. Developmental checkpoints in the third instar associated with ecdysteroid hormone pulses are increasingly delayed. The delay in the late larval period seen in the SS population is indicative of reduced and delayed ecdysone signaling. An enzyme immunoassay for ecdysteroids (with greatest affinity to the metabolically active 20-hydroxyecdysone and the α-ecdysone precursor) confirmed that the SS population had reduced and delayed hormone production compared with that of fed control (FC) flies. Feeding third instar larvae on food supplemented with α-ecdysone partially rescued the developmental delay and reduced subsequent adult starvation resistance. This work suggests that starvation selection causes reduced and delayed production of ecdysteroids in the larval stage and affects the developmental delay phenotype that contributes to subsequent adult fat storage and starvation resistance.

Topics: Animals; Ecdysone; Ecdysteroids; Drosophila melanogaster; Larva; Phenotype

PubMed: 37671530
DOI: 10.1242/jeb.246144

Review

Authors: Klaus-Dieter Spindler, C Hönl, Ch Tremmel...

Several reviews devoted to various aspects of ecdysone research have been published during the last few years. Therefore, this article concentrates mainly on the considerable progress in ecdysone research observed recently, and will cover the results obtained during the last 2 years. The main emphasis is put on the molecular mode of ecdysteroid receptor-mediated hormone action. Two examples of interaction with other hormonal signalling pathways are described, namely crosstalk with juvenile hormone and insulin. Some selected, recently investigated examples of the multitude of hormonal responses are described. Finally, ecological aspects and some practical applications are discussed.

Topics: Animals; Arthropods; Ecdysone; Ecdysteroids; Models, Biological; Receptors, Steroid; Sesquiterpenes; Signal Transduction

PubMed: 19669094
DOI: 10.1007/s00018-009-0112-5

Review

Authors: Hannah Morrow, Christen K Mirth

Specifically timed pulses of the moulting hormone ecdysone are necessary for developmental progression in insects, guiding development through important milestones such as larval moults, pupation and metamorphosis. It also coordinates the acquisition of cell identities, known as cell patterning, and growth in a tissue-specific manner. In the absence of ecdysone, the ecdysone receptor heterodimer Ecdysone Receptor and Ultraspiracle represses expression of target primary response genes, which become de-repressed as the ecdysone titre rises. However, ecdysone signalling elicits both repressive and activating responses in a temporal and tissue-specific manner. To understand how ecdysone achieves such specificity, this review explores the layers of gene regulation involved in stage-appropriate ecdysone responses in Drosophila fruit flies.

Topics: Animals; Drosophila; Ecdysone; Drosophila Proteins; Steroids; Gene Expression Regulation; Larva; Gene Expression Regulation, Developmental; Drosophila melanogaster

PubMed: 38271845
DOI: 10.1016/j.gde.2023.102148

Authors: Lewis V Hun, Naoki Okamoto, Eisuke Imura...

The primary insect steroid hormone ecdysone requires a membrane transporter to enter its target cells. Although an organic anion-transporting polypeptide (OATP) named Ecdysone Importer (EcI) serves this role in the fruit fly and most likely in other arthropod species, this highly conserved transporter is apparently missing in mosquitoes. Here we report three additional OATPs that facilitate cellular incorporation of ecdysone in and the yellow fever mosquito . These additional ecdysone importers (EcI-2, -3, and -4) are dispensable for development and reproduction in , consistent with the predominant role of EcI. In contrast, in , EcI-2 is indispensable for ecdysone-mediated development, whereas EcI-4 is critical for vitellogenesis induced by ecdysone in adult females. Altogether, our results indicate unique and essential functions of these additional ecdysone importers in mosquito development and reproduction, making them attractive molecular targets for species- and stage-specific control of ecdysone signaling in mosquitoes.

Topics: Aedes; Animals; Drosophila; Drosophila melanogaster; Ecdysone; Female; Insect Proteins; Organic Anion Transporters; Vitellogenesis

PubMed: 35696563
DOI: 10.1073/pnas.2202932119

Review

Authors: Richard W Carthew, Pamela Agbu, Ritika Giri...

Over the last decade, microRNAs have emerged as critical regulators in the expression and function of animal genomes. This review article discusses the relationship between microRNA-mediated regulation and the biology of the fruit fly Drosophila melanogaster. We focus on the roles that microRNAs play in tissue growth, germ cell development, hormone action, and the development and activity of the central nervous system. We also discuss the ways in which microRNAs affect robustness. Many gene regulatory networks are robust; they are relatively insensitive to the precise values of reaction constants and concentrations of molecules acting within the networks. MicroRNAs involved in robustness appear to be nonessential under uniform conditions used in conventional laboratory experiments. However, the robust functions of microRNAs can be revealed when environmental or genetic variation otherwise has an impact on developmental outcomes.

Topics: Animals; Cell Differentiation; Central Nervous System; Drosophila Proteins; Drosophila melanogaster; Ecdysone; Female; Gene Expression Regulation, Developmental; Gene Regulatory Networks; Germ Cells; Intercellular Signaling Peptides and Proteins; Male; MicroRNAs; Morphogenesis; Neurons; Protein Isoforms; Signal Transduction; Synapses

PubMed: 27000418
DOI: 10.1016/j.semcdb.2016.03.015

Time- and temperature-dependent dynamics of prothoracicotropic hormone and ecdysone sensitivity co-regulate pupal diapause in the green-veined white butterfly Pieris napi.

Authors: Philip Süess, Heinrich Dircksen, Kevin T Roberts...

Diapause, a general shutdown of developmental pathways, is a vital adaptation allowing insects to adjust their life cycle to adverse environmental conditions such as winter. Diapause in the pupal stage is regulated by the major developmental hormones prothoracicotropic hormone (PTTH) and ecdysone. Termination of pupal diapause in the butterfly Pieris napi depends on low temperatures; therefore, we study the temperature-dependence of PTTH secretion and ecdysone sensitivity dynamics throughout diapause, with a focus on diapause termination. While PTTH is present throughout diapause in the cell bodies of two pairs of neurosecretory cells in the brain, it is absent in the axons, and the PTTH concentration in the haemolymph is significantly lower during diapause than during post diapause development, indicating that the PTTH signaling is reduced during diapause. The sensitivity of pupae to ecdysone injections is dependent on diapause stage. While pupae are sensitive to ecdysone during early diapause initiation, they gradually lose this sensitivity and become insensitive to non-lethal concentrations of ecdysone about 30 days into diapause. At low temperatures, reflecting natural overwintering conditions, diapause termination propensity after ecdysone injection is precocious compared to controls. In stark contrast, at high temperatures reflecting late summer and early autumn conditions, sensitivity to ecdysone does not return. Thus, here we show that PTTH secretion is reduced during diapause, and additionally, that the low ecdysone sensitivity of early diapause maintenance is lost during termination in a temperature dependent manner. The link between ecdysone sensitivity and low-temperature dependence reveals a putative mechanism of how diapause termination operates in insects that is in line with adaptive expectations for diapause.

Topics: Animals; Butterflies; Diapause; Diapause, Insect; Ecdysone; Insect Hormones; Insecta; Pupa; Temperature

PubMed: 36084800
DOI: 10.1016/j.ibmb.2022.103833

Review

Authors: Jade R Kannangara, Christen K Mirth, Coral G Warr...

In both mammals and insects, steroid hormones play a major role in directing the animal's progression through developmental stages. To maximize fitness outcomes, steroid hormone production is regulated by the environmental conditions experienced by the animal. In insects, the steroid hormone ecdysone mediates transitions between developmental stages and is regulated in response to environmental factors such as nutrition. These environmental signals are communicated to the ecdysone-producing gland via the action of neuropeptide and peptide hormone signalling pathways. While some of these pathways have been well characterized, there is evidence to suggest more signalling pathways than has previously been thought function to control ecdysone production, potentially in response to a greater range of environmental conditions. Here, we review the neuropeptide and peptide hormone signalling pathways known to regulate the production of ecdysone in the model genetic insect , as well as what is known regarding the environmental signals that trigger these pathways. Areas for future research are highlighted that can further contribute to our overall understanding of the complex orchestration of environmental, physiological and developmental cues that together produce a functioning adult organism.

Topics: Animals; Drosophila Proteins; Drosophila melanogaster; Ecdysone; Gene Expression Regulation, Developmental; Neuropeptides

PubMed: 33593157
DOI: 10.1098/rsob.200373

Review

Authors: Shannon Nicolson, Donna Denton, Sharad Kumar...

During Drosophila development, the steroid hormone ecdysone plays a key role in the transition from embryo into larva and then into pupa. It is during larval-pupal metamorphosis that extensive programmed cell death occurs to remove large obsolete larval tissues. During this transition, ecdysone pulses control the expression of specific transcription factors which drive the expression of key genes involved in cell death, thus spatially and temporally controlling programmed cell death. Ecdysone also controls cell death in specific larval and adult tissues. This review focuses on the current knowledge of ecdysone-mediated cell death in Drosophila.

Topics: Animals; Apoptosis; Autophagy; Drosophila; Ecdysone; Gene Expression Regulation, Developmental; Larva; Metamorphosis, Biological; Pupa

PubMed: 26374522
DOI: 10.1387/ijdb.150055sk

Review

Authors: Gyunghee Lee, Jae H Park

Metamorphosis is fascinating and dramatic stage of postembryonic development in insects [1]. The most prominent metamorphic changes seen in holometabolous insects involve destruction of most larval structures and concomitant generation of adult ones. Such diverse cellular events are orchestrated by ecdysone. The central nervous system (CNS) is also extensively remodeled to process new sensory inputs; to coordinate new types of locomotion; and to perform higher-order decision making [2]. Programmed cell death (PCD) is an integral part of the metamorphic development. It eliminates obsolete larval tissues and extra cells that are generated from the morphogenesis of adult tissues. In the CNS, PCD of selected neurons and glial cells as well as reshaping of persistent larval cells are essential for establishing the adult CNS. In this review, we summarize the ecdysone signaling, and then molecular and cellular events associated with PCD primarily in the metamorphosing CNS of Drosophila melanogaster.

Topics: Animals; Apoptosis; Central Nervous System; Drosophila melanogaster; Ecdysone; Gene Expression Regulation, Developmental; Insecta; Metamorphosis, Biological

PubMed: 33065339
DOI: 10.1016/j.cois.2020.09.015