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Ultraspiracle-independent anti-apoptotic function of ecdysone receptors is required for the survival of larval peptidergic neurons via suppression of grim expression in Drosophila melanogaster.

ABSTRACT: In Drosophila melanogaster a significant number of heterogenous larval neurons in the central nervous system undergo metamorphosis-associated programmed cell death, termed metamorphoptosis. Interestingly distinct groups of doomed larval neurons are eliminated at different metamorphic phases. Although ecdysone hormonal signaling via nuclear ecdysone receptors (EcRs) is known to orchestrate the neuronal metamorphoptosis, little is known about how this signaling controls such diverse neuronal responses. Crustacean cardioactive peptide (CCAP)-producing neurons in the ventral nerve cord are developmentally programmed to die shortly after adult emergence. In this study, we show that disruption of endogenous EcR function by ectopic expression of dominant negative forms of EcRs (EcRDN) causes premature death of larval CCAP neurons in a caspase-dependent manner. This event is rescued by co-expression of individual EcR isoforms. Furthermore, larval CCAP neurons are largely normal in ecr mutants lacking either EcR-A or EcR-B isoforms, suggesting that EcR isoforms redundantly function to protect larval CCAP neurons. Of surprise, a role of Ultraspiracle (Usp), a canonical partner of EcR, is dispensable in the protection of CCAP neurons, whereas both EcR and Usp are required for inducing metamorphoptosis of vCrz neurons shortly after prepupal formation. As a downstream, grim is an essential cell death gene for the EcRDN-mediated CCAP neuronal death, while either hid or rpr function is dispensable. Together, our results suggest that Usp-independent EcR actions protect CCAP neurons from their premature death by repressing grim expression until their normally scheduled apoptosis at post-emergence. Our studies highlight two opposite roles played by EcR function for metamorphoptosis of two different peptidergic neuronal groups, proapoptotic (vCrz) versus antiapoptotic (CCAP), and propose that distinct death timings of doomed larval neurons are determined by differential signaling mechanisms involving EcR.

SUBMITTER: Lee G

PROVIDER: S-EPMC6486403 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

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Ultraspiracle-independent anti-apoptotic function of ecdysone receptors is required for the survival of larval peptidergic neurons via suppression of grim expression in Drosophila melanogaster.

Lee Gyunghee G Sehgal Ritika R Wang Zixing Z Park Jae H JH

Apoptosis : an international journal on programmed cell death 20190401 3-4

In Drosophila melanogaster a significant number of heterogenous larval neurons in the central nervous system undergo metamorphosis-associated programmed cell death, termed metamorphoptosis. Interestingly distinct groups of doomed larval neurons are eliminated at different metamorphic phases. Although ecdysone hormonal signaling via nuclear ecdysone receptors (EcRs) is known to orchestrate the neuronal metamorphoptosis, little is known about how this signaling controls such diverse neuronal respo ...[more]

PMID: 30637539

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Project description:Recent studies on Drosophila melanogaster and other insects have revealed important insights into the functions and evolution of neuropeptide signaling. In contrast, in- and output connections of insect peptidergic circuits are largely unexplored. Existing morphological descriptions typically do not determine the exact spatial location of peptidergic axonal pathways and arborizations within the neuropil, and do not identify peptidergic in- and output compartments. Such information is however fundamental to screen for possible peptidergic network connections, a prerequisite to understand how the CNS controls the activity of peptidergic neurons at the synaptic level. We provide a precise 3D morphological description of peptidergic neurons in the thoracic and abdominal neuromeres of the Drosophila larva based on fasciclin-2 (Fas2) immunopositive tracts as landmarks. Comparing the Fas2 "coordinates" of projections of sensory or other neurons with those of peptidergic neurons, it is possible to identify candidate in- and output connections of specific peptidergic systems. These connections can subsequently be more rigorously tested. By immunolabeling and GAL4-directed expression of marker proteins, we analyzed the projections and compartmentalization of neurons expressing 12 different peptide genes, encoding approximately 75% of the neuropeptides chemically identified within the Drosophila CNS. Results are assembled into standardized plates which provide a guide to identify candidate afferent or target neurons with overlapping projections. In general, we found that putative dendritic compartments of peptidergic neurons are concentrated around the median Fas2 tracts and the terminal plexus. Putative peptide release sites in the ventral nerve cord were also more laterally situated. Our results suggest that i) peptidergic neurons in the Drosophila ventral nerve cord have separated in- and output compartments in specific areas, and ii) volume transmission is a prevailing way of peptidergic communication within the CNS. The data can further be useful to identify colocalized transmitters and receptors, and develop peptidergic neurons as new landmarks.

Project description:Conopomorpha sinensis Bradley (Lepidoptera: Gracilariidae) is the dominant insect pest of litchi (chinensis Sonn.) and longan (Euphoria longan Lour.) fruit trees. Management of this pest species is a challenging task due to its cryptic borer behavior. Controlling C. sinensis at the egg stage is the best alternative strategy to chemical control of C. sinensis adults. However, thorough studies regarding the indirect and sublethal effects of chemicals on the different developmental stages of C. sinensis are insufficient. In this study, the effect of some insecticides was evaluated on C. sinensis eggs. The ovicidal activity of chlorbenzuron, abamectin, chlorantraniliprole, and ?-cyhalothrin was confirmed by morphological observation of the defects in C. sinensis eggs. Moreover, we characterized four essential ecdysone receptor proteins in insects [i.e., two isoform ecdysone receptors (EcR: CsEcRA. CsEcRB) and two isoform ultraspiracle proteins (USP: CsUSP1, CsUSP2)] from C. sinensis eggs. The CsEcRA, CsEcRB, CsUSP1, and CsUSP2 genes consisted of 1521-, 1614-, 1410-, and 1236-bp open reading frames which encoded proteins of 506, 527, 469, and 413 amino acid residues, respectively. Furthermore, the embryonic differential responses of CsEcRs, CsUSPs, and vitellogenin receptor (VgR: CsVgR) to insecticides were evaluated by qRT-PCR. Among the five tested genes, CsVgR and CsUSP1 were the most sensitive to all the tested insecticides, with fold change of the expression diminished by 4.27-8.70 times compared with untreated control insects. The data suggests that these insecticidal compounds regulate the expression of these specific proteins, which might eventually lead to reduced viability of C. sinensis eggs. We present here the first data providing molecular elucidation of ecdysone receptor genes and their differential responses to insecticides in C. sinensis eggs. Together with our previous report of insecticide sublethal effects on two reproduction-related genes in C. sinensis adults, CsVgR and CsUSP1 seem to be appropriate molecular parameters for the evaluation of insecticide impact on C. sinensis. This study exemplifies the potential utility of transcriptional measurement of nuclear receptors as the molecular biomarkers for ecotoxicological evaluations of ovicidal impact of insecticides.

Dataset Information

Ultraspiracle-independent anti-apoptotic function of ecdysone receptors is required for the survival of larval peptidergic neurons via suppression of grim expression in Drosophila melanogaster.

Publications

Ultraspiracle-independent anti-apoptotic function of ecdysone receptors is required for the survival of larval peptidergic neurons via suppression of grim expression in Drosophila melanogaster.

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