Cross communication between signaling pathways: Juvenoid hormones modulate ecdysteroid activity in a crustacean

Abstract

Methyl farnesoate is a juvenoid hormone that regulates a variety of processes in crustaceans including male sex determination among daphnids (Branchiopoda, Cladocera). The synthetic juvenoids pyriproxyfen and fenoxycarb mimic the action of methyl farnesoate in daphnids. In the present study we tested the hypothesis that juvenoids also can regulate ecdysteroid activity in a crustacean (Daphnia magna). Methyl farnesoate, pyriproxyfen, and fenoxycarb all disrupted ecdysteroid-regulated aspects of embryo development in daphnids. Exposure of ecdysteroid-responsive cells to 20-hydroxyecdysone reduced cell proliferation and increased mRNA levels of the ecdysone receptor and its partner protein ultraspiracle. Co-treatment of cells with the juvenoid pyriproxyfen attenuated all of these ecdysteroid mediated responses. While juvenoids functioned as anti-ecdysteroids in both intact embryos and in cultured cells, 20-hydroxyecdysone showed no evidence of acting as an anti-juvenoid. The combined effects of pyroproxyfen with the ecdysteroid synthesis inhibitor fenarimol and the ecdysteroid receptor antagonist testosterone were evaluated in an effort to discern whether the action of the juvenoids were additive with those of know anti-ecdysteroids. The anti-ecdysteroid effects of pyriproxyfen were non-additive with those of either anti-ecdysteroid. Rather, joint effects conformed to a model of synergy. These results demonstrated that juvenoids elicit anti-ecdysteroidal activity in a crustacean through a unique mechanism of action. A model involving receptor partner deprivation is proposed that explains the synergistic interactions observed.

Cloning and characterization of the ecdysone receptor and ultraspiracle protein from the water flea Daphnia magna

“…It has been reported that Ec is responsible for embryo development, larval molts, pupation, and metamorphosis in Drosophila, Bombyx mori and other arthropods (Riddiford 1993, Subramoniam 2000, Sekimoto et al 2006. The Ec is known to regulate a number of biological processes by coordinating with juvenile hormone (JH; Dubrovsky 2005) and cross talk between them has been reported in Daphnia and other arthropods (Mu & LeBlanc 2004).…”

Endocrine regulation of the reproduction in crustaceans: Identification of potential targets for toxicants and environmental contaminants

“…Similarly, other two xeno-ecdysteroids, strong fytoecdysterone agonist Ponasterone A and synthetic ecdysone agonist bisacylhydrazine RG-102240, are potent lignads for EcR (that heterodimerizes with RXR) in U. pugilator (Wu et al 2004). Xenobiotics can also affect EcR levels in target cells as was documented for synthetic juvenoids pyriproxifen and fenoxycarb that attenuated expression of mRNA encoding EcR (and its heterodimer partner USP) in the insect in vitro model with Drosophila Kc cells (Mu & LeBlanc 2004).…”

Ecological genomics in Daphnia: stress responses and environmental sex determination

“…Physiological and biochemical studies would be useful to uncover such systemic changes in metabolism in response to JHA treatment. Furthermore, alteration of chitin metabolism underscores connections between MF and ecdysis due to genetic crosstalk with ecdysone pathways (Mu and LeBlanc, 2004). Third, involvement of the rheb receptor in response to MF is, to our knowledge, a novel observation linking this protein to a crustacean hormonal response.…”

“…Third, as a classic example of phenotypic plasticity and epigenetic regulation, it offers the possibility of uncovering molecular mechanisms responsible for these ecologically and evolutionarily central mechanisms. Fourth, evidence indicates important couplings between juvenile hormone (JH) pathways and ecdysone pathways in Daphnia (Mu and LeBlanc, 2004), which are likely to be useful for genetic and genomic analyses of these pathways across the Ecdysozoa. Olmstead and LeBlanc (2002) were first to demonstrate production of male broods of D. magna in response to the sesquiterpenoid hormone methyl farnesoate (MF), the unepoxidated form of insect JH III.…”

“…For further discussion, see Laufer and Biggers (2001) and Mu and LeBlanc (2004). Arrows (induction or production) and blocked lines (repression) may be direct or indirect effects (possibly both, indicated by dashed lines).…”