Juvenile hormone membrane signaling phosphorylates USP and thus potentiates 20-hydroxyecdysone action in Drosophila

Yue Gao, Suning Liu, Qiangqiang Jia, Lixian Wu, Dongwei Yuan, Emma Y. Li, Qili Feng, Guirong Wang, Subba R. Palli, Jian Wang, Sheng Li

Research output: Contribution to journalArticlepeer-review

7 Scopus citations

Abstract

Juvenile hormone (JH) and 20-hydroxyecdysone (20E) coordinately regulate development and metamorphosis in insects. Two JH intracellular receptors, methoprene-tolerant (Met) and germ-cell expressed (Gce), have been identified in the fruit fly Drosophila melanogaster. To investigate JH membrane signaling pathway without the interference from JH intracellular signaling, we characterized phosphoproteome profiles of the Met gce double mutant in the absence or presence of JH in both chronic and acute phases. Functioning through a potential receptor tyrosine kinase and phospholipase C pathway, JH membrane signaling activated protein kinase C (PKC) which phosphorylated ultraspiracle (USP) at Ser35, the PKC phosphorylation site required for the maximal action of 20E through its nuclear receptor complex EcR-USP. The uspS35A mutant, in which Ser was replaced with Ala at position 35 by genome editing, showed decreased expression of Halloween genes that are responsible for ecdysone biosynthesis and thus attenuated 20E signaling that delayed developmental timing. The uspS35A mutant also showed lower Yorkie activity that reduced body size. Altogether, JH membrane signaling phosphorylates USP at Ser35 and thus potentiates 20E action that regulates the normal fly development. This study helps better understand the complex JH signaling network.

Original languageEnglish
Pages (from-to)186-197
Number of pages12
JournalScience Bulletin
Volume67
Issue number2
DOIs
StatePublished - Jan 30 2022

Bibliographical note

Funding Information:
Thanks to Dr. Jianquan Ni (Tsinghua University) for designing CRISPR/Cas9-mediated genome editing, and Drs. Jie Shen (China Agricultural University, Shian Wu (Nankai University), Zizhang Zhou (Shandong Agicultural University), Haiyun Song (Shanghai Jiao Tong University), Lei Zhang (University of Chinese Academy of Sciences), Fengwei Yu (National University of Singapore), and Bloomington Drosophila Stock Center for providing stocks and reagents. This work was supported by the National Natural Science Foundation of China (31620103917, 31970459, 32070441, 31702054, and 31930014), the Shenzhen Science and Technology Program (20180411143628272), and the Natural Science Foundation of Guangdong Province (2019A1515011899). Sheng Li and Jian Wang designed and conceived the study. Yue Gao, Suning Liu, Qiangqiang Jia, Lixian Wu, Dongwei Yuan, and Emma Y. Li performed experiments. Qili Feng, Guirong Wang, and Subba R. Palli analyzed data. Sheng Li, Jian Wang, Yue Gao, and Suning Liu wrote the manuscript, with contributions from other authors.

Funding Information:
Thanks to Dr. Jianquan Ni (Tsinghua University) for designing CRISPR/Cas9-mediated genome editing, and Drs. Jie Shen (China Agricultural University, Shian Wu (Nankai University), Zizhang Zhou (Shandong Agicultural University), Haiyun Song (Shanghai Jiao Tong University), Lei Zhang (University of Chinese Academy of Sciences), Fengwei Yu (National University of Singapore), and Bloomington Drosophila Stock Center for providing stocks and reagents. This work was supported by the National Natural Science Foundation of China ( 31620103917 , 31970459 , 32070441 , 31702054 , and 31930014 ), the Shenzhen Science and Technology Program (20180411143628272), and the Natural Science Foundation of Guangdong Province (2019A1515011899).

Publisher Copyright:
© 2021 Science China Press

Keywords

  • 20-Hydroxyecdysone action
  • Juvenile hormone
  • Phosphoproteomics
  • Receptor tyrosine kinase
  • USP
  • Yorkie activity

ASJC Scopus subject areas

  • General

Fingerprint

Dive into the research topics of 'Juvenile hormone membrane signaling phosphorylates USP and thus potentiates 20-hydroxyecdysone action in Drosophila'. Together they form a unique fingerprint.

Cite this