Handling Editor: Cassandra Extavour
ABSTRACT
Animal steroid hormones initiate signaling by passive diffusion into cells and binding to their nuclear receptors to regulate gene expression. Animal steroid hormones can initiate signaling via G protein-coupled receptors (GPCRs); however, the underlying mechanisms are unclear. Here, we show that a newly discovered ecdysone-responsive GPCR, ErGPCR-3, transmits the steroid hormone 20-hydroxyecdysone (20E) signal by binding 20E and promoting its entry into cells in the lepidopteran insect Helicoverpa armigera. Knockdown of ErGPCR-3 in larvae caused delayed and abnormal pupation, inhibited remodeling of the larval midgut and fat body, and repressed 20E-induced gene expression. Also, 20E induced both the interaction of ErGPCR-3 with G proteins and rapid intracellular increase in calcium, cAMP and protein phosphorylation. ErGPCR-3 was endocytosed by GPCR kinase 2-mediated phosphorylation, and interacted with β-arrestin-1 and clathrin, to terminate 20E signaling under 20E induction. We found that 20E bound to ErGPCR-3 and induced the ErGPCR-3 homodimer to form a homotetramer, which increased 20E entry into cells. Our study revealed that homotetrameric ErGPCR-3 functions as a cell membrane receptor and increases 20E diffusion into cells to transmit the 20E signal and promote metamorphosis.
Footnotes
Competing interests
The authors declare no competing or financial interests.
Author contributions
Conceptualization: X.-L.K., J.-X.W., X.-F.Z.; Methodology: X.-L.K., X.-F.Z.; Software: X.-L.K.; Validation: X.-L.K., Y.-X.L., X.-F.Z.; Formal analysis: X.-L.K.; Investigation: X.-L.K., Y.-X.L., Y.-L.L.; Resources: Y.-L.L., J.-X.W., X.-F.Z.; Data curation: X.-F.Z.; Writing - original draft: X.-L.K.; Writing - review & editing: X.-F.Z.; Supervision: J.-X.W., X.-F.Z.; Project administration: X.-F.Z.; Funding acquisition: X.-F.Z.
Funding
This study was supported by the National Natural Science Foundation of China (31730083).
Supplementary information
Supplementary information available online at https://dev.biologists.org/lookup/doi/10.1242/dev.196667.supplemental
- Received September 3, 2020.
- Accepted February 5, 2021.
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