Ecdysteroid signalling in insects—From biosynthesis to gene expression regulation

Yamanaka, Naoaki

doi:10.1016/bs.aiip.2021.03.002

Cited by 16 publications

(13 citation statements)

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“…Insects comprise 80% of the estimated species biodiversity on earth [ 18 , 19 ], with pivotal roles as pollinators, agricultural pests, and infectious disease vectors; as such, their impacts on global human health are vast and far-reaching. Unlike vertebrates, insects possess only 1 major class of steroid hormone, the ecdysteroids, predominated by the most biologically active hormone 20-hydroxyecdysone (20E) [ 20 ]. Similarly to vertebrate steroids, 20E regulates many physiological and organismal insect traits, including juvenile-to-adult developmental transitions [ 3 , 21 , 22 ], reproductive maturation [ 23 ], energy metabolism [ 24 ], behavior [ 25 ], stress responses [ 26 ], and longevity [ 26 , 27 ].…”

Section: Introductionmentioning

confidence: 99%

“…The best-studied role of 20E is driving major developmental transitions during the insect juvenile growth period, including key stages of embryogenesis [ 28 , 29 ], the molts between larval instars [ 3 , 21 ], and, in holometabolous insects, the onset of puparium formation and metamorphosis [ 20 , 30 , 31 ]. Peaks in 20E production and circulating titers initiate the irreversible cellular and morphological changes that constitute progression through the insect life stages [ 20 ]. In addition to these well-studied developmental effects, specific 20E peaks are also accompanied by activation of immune processes in a variety of insect taxa as detailed below.…”

Section: Introductionmentioning

confidence: 99%

“… (A) Schematic illustrating the temporal dynamics of 20E titer and immune gene induction during insect pupariation. Distinct peaks in hemolymph 20E levels drive developmental transitions including the onset of metamorphosis in Drosophila and other holometabolous insects [ 20 , 30 , 31 ]. A dramatic, microbe-independent up-regulation of immune gene transcripts, including AMPs, also occurs at pupariation [ 40 , 45 ].…”

Section: Introductionmentioning

confidence: 99%

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Steroid hormone regulation of innate immunity in Drosophila melanogaster

Keith

2023

PLoS Genet

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Endocrine signaling networks control diverse biological processes and life history traits across metazoans. In both invertebrate and vertebrate taxa, steroid hormones regulate immune system function in response to intrinsic and environmental stimuli, such as microbial infection. The mechanisms of this endocrine-immune regulation are complex and constitute an ongoing research endeavor facilitated by genetically tractable animal models. The 20-hydroxyecdysone (20E) is the major steroid hormone in arthropods, primarily studied for its essential role in mediating developmental transitions and metamorphosis; 20E also modulates innate immunity in a variety of insect taxa. This review provides an overview of our current understanding of 20E-mediated innate immune responses. The prevalence of correlations between 20E-driven developmental transitions and innate immune activation are summarized across a range of holometabolous insects. Subsequent discussion focuses on studies conducted using the extensive genetic resources available in Drosophila that have begun to reveal the mechanisms underlying 20E regulation of immunity in the contexts of both development and bacterial infection. Lastly, I propose directions for future research into 20E regulation of immunity that will advance our knowledge of how interactive endocrine networks coordinate animals’ physiological responses to environmental microbes.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Steroid hormone regulation of innate immunity in Drosophila melanogaster

Keith

2023

PLoS Genet

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“…At the same time, βFTZ-F1 is part of the dynamic feedback regulation of 20E-EcR signaling, enhancing ecdysteroid biosynthesis in the prothoracic gland and probably in the ovaries [8]. The role of 20E in reproduction has been reported in both holometabolous and hemimetabolous insects, including Bombyx mori, Aedes aegypti, Drosophila melanogaster, Nilaparvata lugens, and Schistocerca gregaria, where 20E is involved in aspects of oogenesis [26][27][28][29]. Ecdysone response genes are required for vitellogenesis, with ecdysone receptor binding sites and transcriptional regulators E74 and E75 identified in the 5 0 upstream regulatory region of the vitellogenin (Vg) gene [30,31].…”

Section: Introductionmentioning

confidence: 99%

A critical role for ecdysone response genes in regulating egg production in adult female Rhodnius prolixus

2023

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Ecdysteroids control ovary growth and egg production through a complex gene hierarchy. In the female Rhodnius prolixus, a blood-gorging triatomine and the vector of Chagas disease, we have identified the ecdysone response genes in the ovary using transcriptomic data. We then quantified the expression of the ecdysone response gene transcripts (E75, E74, BR-C, HR3, HR4, and FTZ-F1) in several tissues, including the ovary, following a blood meal. These results confirm the presence of these transcripts in several tissues in R. prolixus and show that the ecdysone response genes in the ovary are mostly upregulated during the first three days post blood meal (PBM). Knockdown of E75, E74, or FTZ-F1 transcripts using RNA interference (RNAi) was used to understand the role of the ecdysone response genes in vitellogenesis and egg production. Knockdown significantly decreases the expression of the transcripts for the ecdysone receptor and Halloween genes in the fat body and the ovaries and reduces the titer of ecdysteroid in the hemolymph. Knockdown of each of these transcription factors typically alters the expression of the other transcription factors. Knockdown also significantly decreases the expression of vitellogenin transcripts, Vg1 and Vg2, in the fat body and ovaries and reduces the number of eggs produced and laid. Some of the laid eggs have an irregular shape and smaller volume, and their hatching rate is decreased. Knockdown also influences the expression of the chorion gene transcripts Rp30 and Rp45. The overall effect of knockdown is a decrease in number of eggs produced and a severe reduction in number of eggs laid and their hatching rate. Clearly, ecdysteroids and ecdysone response genes play a significant role in reproduction in R. prolixus.

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“…Activated nuclear receptors in turn direct expression of a series of genes and alter cellular functions ( McKenna and O’Malley, 2002 ). In arthropods, ecdysteroids are the class of steroid hormones that regulate development through controlling molting and metamorphosis ( Riddiford et al, 2000 ; Hill et al, 2013 ; Truman, 2019 ; Yamanaka, 2021 ). Ecdysteroid actions are mediated by intracellular nuclear receptors, the ecdysone receptor (EcR) and Ultraspiracle (USP; Yao et al, 1992 , 1993 ; Thomas et al, 1993 ).…”

Section: Introductionmentioning

confidence: 99%

Rapid Assessment of Insect Steroid Hormone Entry Into Cultured Cells

et al. 2022

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Steroid hormones control development and homeostasis in a wide variety of animals by interacting with intracellular nuclear receptors. Recent discoveries in the fruit fly Drosophila melanogaster revealed that insect steroid hormones or ecdysteroids are incorporated into cells through a membrane transporter named Ecdysone Importer (EcI), which may become a novel target for manipulating steroid hormone signaling in insects. In this study, we established an assay system that can rapidly assess EcI-mediated ecdysteroid entry into cultured cells. Using NanoLuc Binary Technology (NanoBiT), we first developed an assay to detect ligand-dependent heterodimerization of the ecdysone receptor (EcR) and retinoid X receptor (RXR) in human embryonic kidney (HEK) 293T cells. We also developed HEK293 cells that stably express EcI. By combining these tools, we can monitor ecdysteroid entry into the cells in real time, making it a reliable system to assess EcI-mediated steroid hormone incorporation into animal cells.

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Ecdysteroid signalling in insects—From biosynthesis to gene expression regulation

Cited by 16 publications

References 351 publications

Steroid hormone regulation of innate immunity in Drosophila melanogaster

Steroid hormone regulation of innate immunity in Drosophila melanogaster

A critical role for ecdysone response genes in regulating egg production in adult female Rhodnius prolixus

Rapid Assessment of Insect Steroid Hormone Entry Into Cultured Cells

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