Diuretic hormone 31 activates two G protein-coupled receptors with differential second messengers for diuresis in Drosophila suzukii

Authors: YOON, HOJUNG - Oregon State University; Price, Briana; PARKS, RYSSA - Oregon State University; AHN, SEUNG-JOON - Mississippi State University; Choi, Man-Yeon

Submitted to: Insect Biochemistry and Molecular Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/6/2023
Publication Date: 10/9/2023
Citation: Yoon, H., Price, B.E., Parks, R., Ahn, S., Choi, M.Y. 2023. Diuretic hormone 31 activates two G protein-coupled receptors with differential second messengers for diuresis in Drosophila suzukii. Insect Biochemistry and Molecular Biology. 162:104025. https://doi.org/10.1016/j.ibmb.2023.104025.
DOI: https://doi.org/10.1016/j.ibmb.2023.104025

Interpretive Summary: Diuresis, the increased production of urine, is one of the most important physiological processes to maintain water and osmotic homeostasis in insects for environmental adaptation and survival. In this study, a diuretic hormone (DH) and two corresponding receptors were identified and characterized by differential gene expression, 3D structures of their receptors, and cell signaling mechanisms in the Malpighian tubules (similar to the kidney in mammals) of the spotted wing drosophila (SWD), Drosophila suzukii. SWD is an invasive vinegar fly that is a major threat to the small fruits and cherry industries worldwide. The primary control methods for SWD rely on conventional insecticides, mostly chemical applications. Our results provide a fundamental characterization of the diuretic physiology of SWD to facilitate the identification of potential biological targets for SWD control.

Technical Abstract: Diuretic hormones (DHs) bind to G protein-coupled receptors (GPCRs) to control water and ion balance to maintain essential homeostasis in animals. Insect DHs are two distinct hormones, diuretic calcitonin (CT)-like DH31 and corticotropin-releasing factor (CRF)-like DH44. In this study, we identified and characterized DH31 and two DH31 GPCR variants, DH31-Ra and DH31-Rb, from the spotted wing drosophila, Drosophila suzukii, a worldwide pest of vinegar fly that causes severe damage to small fruits. Both GPCRs are active, but DH31-Ra is the dominant receptor based on gene expression and DH31 binding affinities. A notable difference between the two variants is in 1) the GPCR structure in the C-terminus and 2) the second messenger usage. The amino acid sequences of the two variants are identical except for the C-terminal portions. DH31-Ra has a 12-AA longer C-terminus, providing different intracellular forms of its 3D. DH31-Ra uses both cAMP and Ca2+ as second messengers, whereas DH31-Rb uses only cAMP as second messenger, this is the first time for the insect CT-like DH31 peptide in insects. The fly injected with DH31 secreted the fluid, which was increased by the peptide in a dose-dependent manner. However, when the fly was injected with a mixture of DH31 and CAPA, an anti-diuretic hormone, fluid secretion was suppressed. We discussed the structures of the DH receptors and the various signaling pathways, including second messengers, involved in fly diuresis. The results fundamentally characterized D. suzukii DH31 and DH31-Rs to facilitate the identification of potential biological targets for D. suzukii control.