Diofenolan induces male offspring production through binding to the juvenile hormone receptor in Daphnia magna

Abe, Ryosuke; Toyota, Kenji; Miyakawa, Hitoshi; Watanabe, Haruna; Oka, Tomohiro; Miyagawa, Shinichi; Nishide, Hiroyo; Uchiyama, Ikuo; Tollefsen, Knut Erik; Iguchi, Taisen; Tatarazako, Norihisa

doi:10.1016/j.aquatox.2014.11.015

Cited by 37 publications

(35 citation statements)

References 46 publications

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“…, low-density lipoprotein receptors containing Ca 2+ -binding EGF-like domains) were differentially expressed in whole body with log 2 -transformed FC values between 2.11 and 9.06 (Additional files 3 and 4 ). Further, candidate genes in the whole body contained several serine protease and hemoglobin-related genes, known as MF-responsive genes in daphnids [ 36 , 37 ], implying that this experimental design possesses higher reliability to select factors involved in downstream of MF signaling. In addition, more than 50% of the candidate genes could not be attributed to any annotations (Figure 2 C, F), suggesting that those genes might be novel candidates for sexual fate determination via MF signaling in D. pulex (Additional files 8 and 9 ).…”

Section: Resultsmentioning

confidence: 99%

NMDA receptor activation upstream of methyl farnesoate signaling for short day-induced male offspring production in the water flea, Daphnia pulex

et al. 2015

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BackgroundThe cladoceran crustacean Daphnia pulex produces female offspring by parthenogenesis under favorable conditions, but in response to various unfavorable external stimuli, it produces male offspring (environmental sex determination: ESD). We recently established an innovative system for ESD studies using D. pulex WTN6 strain, in which the sex of the offspring can be controlled simply by changes in the photoperiod: the long-day and short-day conditions can induce female and male offspring, respectively. Taking advantage of this system, we demonstrated that de novo methyl farnesoate (MF) synthesis is necessary for male offspring production. These results indicate the key role of innate MF signaling as a conductor between external environmental stimuli and the endogenous male developmental pathway. Despite these findings, the molecular mechanisms underlying up- and downstream signaling of MF have not yet been well elucidated in D. pulex.ResultsTo elucidate up- and downstream events of MF signaling during sex determination processes, we compared the transcriptomes of daphnids reared under the long-day (female) condition with short-day (male) and MF-treated (male) conditions. We found that genes involved in ionotropic glutamate receptors, known to mediate the vast majority of excitatory neurotransmitting processes in various organisms, were significantly activated in daphnids by the short-day condition but not by MF treatment. Administration of specific agonists and antagonists, especially for the N-methyl-D-aspartic acid (NMDA) receptor, strongly increased or decreased, respectively, the proportion of male-producing mothers. Moreover, we also identified genes responsible for male production (e.g., protein kinase C pathway-related genes). Such genes were generally shared between the short-day reared and MF-treated daphnids.ConclusionsWe identified several candidate genes regulating ESD which strongly suggests that these genes may be essential factors for male offspring production as an upstream regulator of MF signaling in D. pulex. This study provides new insight into the fundamental mechanisms underlying how living organisms alter their phenotypes in response to various external environments.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1392-9) contains supplementary material, which is available to authorized users.

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Section: Resultsmentioning

confidence: 99%

NMDA receptor activation upstream of methyl farnesoate signaling for short day-induced male offspring production in the water flea, Daphnia pulex

et al. 2015

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“…Juvenile hormone analogues like methoprene and later pyriproxyfen have initially been designed to interfere with insect development and are broadly used to fight insect pests such as Aedes , a vector for dengue, chikungunya, Zika, and yellow fever viruses (reviewed in Henrick, 2007). The discovery the sesquiterpenoid MF in crustaceans by Laufer et al (1987) already raised concerns if the effect of juvenile hormone analogues is restricted to insect development (Walker et al, 2005; Abe et al, 2015), calling for more specific tests with non-target species. Our results argue that aquatic lophotrochozoans should also be systematically included in specificity tests for compounds targeting sesquiterpenoid signalling pathway, and that such tests should not be restricted to mortality (Henrick, 2007), but include assays on reproductive fitness.…”

Section: Discussionmentioning

confidence: 99%

Discovery of methylfarnesoate as the annelid brain hormone reveals an ancient role of sesquiterpenoids in reproduction

Schenk

Krauditsch

Frühauf

et al. 2016

eLife

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Animals require molecular signals to determine when to divert resources from somatic functions to reproduction. This decision is vital in animals that reproduce in an all-or-nothing mode, such as bristle worms: females committed to reproduction spend roughly half their body mass for yolk and egg production; following mass spawning, the parents die. An enigmatic brain hormone activity suppresses reproduction. We now identify this hormone as the sesquiterpenoid methylfarnesoate. Methylfarnesoate suppresses transcript levels of the yolk precursor Vitellogenin both in cell culture and in vivo, directly inhibiting a central energy–costly step of reproductive maturation. We reveal that contrary to common assumptions, sesquiterpenoids are ancient animal hormones present in marine and terrestrial lophotrochozoans. In turn, insecticides targeting this pathway suppress vitellogenesis in cultured worm cells. These findings challenge current views of animal hormone evolution, and indicate that non-target species and marine ecosystems are susceptible to commonly used insect larvicides.DOI: http://dx.doi.org/10.7554/eLife.17126.001

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“…We had not previously evaluated hydroprene and diofenolan in vivo , while, others had reported high potency of these compounds with respect to stimulating male sex determination 40, 44 . Therefore, we evaluated these compounds in the present study.…”

Section: Discussionmentioning

confidence: 99%

Ligand-Mediated Receptor Assembly as an End Point for High-Throughput Chemical Toxicity Screening

Kakaley

Eytcheson

LeBlanc

2017

Environ. Sci. Technol.

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The high throughput screening of chemicals for interaction with intracellular targets is gaining prominence in the toxicity evaluation of environmental chemicals. We describe ligand-mediated receptor assembly as an early event in receptor signaling and its application to the screening of chemicals for interaction with targeted receptors. We utilized bioluminescence resonance energy transfer (BRET) to detect and quantify assembly of the methyl farnesoate receptor (MfR) in response to various high-production volume and other chemicals. The hormone methyl farnesoate binds to the MfR to regulate various aspects of reproduction and development in crustaceans. The MfR protein subunits Met and SRC, cloned from Daphnia pulex, were fused to the fluorophore, mAmetrine and the photon generator, Rluc2, respectively. Ligand-mediated receptor assembly was measured by photon transfer from the photon donor to the fluorophore resulting in fluorescence emission. Overall, the BRET assay had comparable or greater sensitivity as compared to a traditional reporter gene assay. Further, chemicals that screened positive in the BRET assay also stimulated phenotypic outcomes in daphnids that result from MfR signaling. We concluded the BRET assay is an accurate, sensitive, and cost/time efficient alternative to traditional screening assays.

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Diofenolan induces male offspring production through binding to the juvenile hormone receptor in Daphnia magna

Cited by 37 publications

References 46 publications

NMDA receptor activation upstream of methyl farnesoate signaling for short day-induced male offspring production in the water flea, Daphnia pulex

NMDA receptor activation upstream of methyl farnesoate signaling for short day-induced male offspring production in the water flea, Daphnia pulex

Discovery of methylfarnesoate as the annelid brain hormone reveals an ancient role of sesquiterpenoids in reproduction

Ligand-Mediated Receptor Assembly as an End Point for High-Throughput Chemical Toxicity Screening

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