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

doi:10.1016/j.scib.2021.06.019

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 journal › Article › peer-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 usp^S35A 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 usp^S35A 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 language	English
Pages (from-to)	186-197
Number of pages	12
Journal	Science Bulletin
Volume	67
Issue number	2
DOIs	https://doi.org/10.1016/j.scib.2021.06.019
State	Published - 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

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10.1016/j.scib.2021.06.019

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@article{f9d04fe573e64efbb588d899ebfcef41,

title = "Juvenile hormone membrane signaling phosphorylates USP and thus potentiates 20-hydroxyecdysone action in Drosophila",

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.",

keywords = "20-Hydroxyecdysone action, Juvenile hormone, Phosphoproteomics, Receptor tyrosine kinase, USP, Yorkie activity",

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

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: {\textcopyright} 2021 Science China Press",

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doi = "10.1016/j.scib.2021.06.019",

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T1 - Juvenile hormone membrane signaling phosphorylates USP and thus potentiates 20-hydroxyecdysone action in Drosophila

AU - Gao, Yue

AU - Liu, Suning

AU - Jia, Qiangqiang

AU - Wu, Lixian

AU - Yuan, Dongwei

AU - Li, Emma Y.

AU - Feng, Qili

AU - Wang, Guirong

AU - Palli, Subba R.

AU - Wang, Jian

AU - Li, Sheng

N1 - 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

PY - 2022/1/30

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N2 - 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.

AB - 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.

KW - 20-Hydroxyecdysone action

KW - Juvenile hormone

KW - Phosphoproteomics

KW - Receptor tyrosine kinase

KW - USP

KW - Yorkie activity

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

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Bibliographical note

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