Antagonism between PTP1B and PTK Mediates Adults’ Insulin-Like Signaling Regulation of Egg Diapause in the Migratory Locust

Diapause is a physiological development arrest state that helps insects to adapt to seasonality and overcome adverse environmental conditions. Numerous reports have indicated that insulinlike and fork head transcription factor (FOXO) are involved in the regulation of diapause in insects. However, th...

Full description

Bibliographic Details
Main Authors: Shuang Li, Jie Wang, Dongnan Cui, Kun Hao, Jun Chen, Xiongbing Tu, Zehua Zhang
Format: Article
Language:English
Published: MDPI AG 2021-03-01
Series:Insects
Subjects:
Online Access:https://www.mdpi.com/2075-4450/12/3/253
_version_ 1797540959753338880
author Shuang Li
Jie Wang
Dongnan Cui
Kun Hao
Jun Chen
Xiongbing Tu
Zehua Zhang
author_facet Shuang Li
Jie Wang
Dongnan Cui
Kun Hao
Jun Chen
Xiongbing Tu
Zehua Zhang
author_sort Shuang Li
collection DOAJ
description Diapause is a physiological development arrest state that helps insects to adapt to seasonality and overcome adverse environmental conditions. Numerous reports have indicated that insulinlike and fork head transcription factor (FOXO) are involved in the regulation of diapause in insects. However, the upstream modulators of the insulin-like signaling pathway (ISP) involved in diapause regulation are still unknown. Here, we used RNAi and an inhibitor to treat PTK and PTP1B in adult tissues and injected Prx V or RNAi Prx V under both short and long photoperiod conditions and monitored effects on the expression of ISP genes, the phosphorylation levels for IR and IRS, the activity of NADPH oxidase, the accumulation of reactive oxygen species (ROS) and energy metabolism, seeking to identify both proteins and broader cellular metabolism influences on diapause regulation. We found that under short photoperiod conditions PTP1B in female adults induces egg diapause, whereas PTK in female adults inhibits egg diapause. Intriguingly, we also found that the antioxidant enzyme Prx V is a negative regulator of NADPH oxidizing reaction and apparently decreases ROS production and NADPH-OX activity. In contrast, all the eggs laid by adults that were treated with a series of knockdown or purified-protein injection experiments or inhibitor studies and that were reared under long photoperiod conditions hatched successfully. Thus, our results suggest a mechanism wherein diapause-related proteins (PTP1B, PTK, and Prx V) of female adults are the upstream modulators that regulate offspring eggs’ diapause process through the insulin-like signaling pathway under short photoperiod conditions.
first_indexed 2024-03-10T13:08:30Z
format Article
id doaj.art-2ddac4d3624944eca7f825c1fddf929d
institution Directory Open Access Journal
issn 2075-4450
language English
last_indexed 2024-03-10T13:08:30Z
publishDate 2021-03-01
publisher MDPI AG
record_format Article
series Insects
spelling doaj.art-2ddac4d3624944eca7f825c1fddf929d2023-11-21T10:55:01ZengMDPI AGInsects2075-44502021-03-0112325310.3390/insects12030253Antagonism between PTP1B and PTK Mediates Adults’ Insulin-Like Signaling Regulation of Egg Diapause in the Migratory LocustShuang Li0Jie Wang1Dongnan Cui2Kun Hao3Jun Chen4Xiongbing Tu5Zehua Zhang6State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, ChinaState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, ChinaState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, ChinaState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, ChinaState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, ChinaState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, ChinaState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, ChinaDiapause is a physiological development arrest state that helps insects to adapt to seasonality and overcome adverse environmental conditions. Numerous reports have indicated that insulinlike and fork head transcription factor (FOXO) are involved in the regulation of diapause in insects. However, the upstream modulators of the insulin-like signaling pathway (ISP) involved in diapause regulation are still unknown. Here, we used RNAi and an inhibitor to treat PTK and PTP1B in adult tissues and injected Prx V or RNAi Prx V under both short and long photoperiod conditions and monitored effects on the expression of ISP genes, the phosphorylation levels for IR and IRS, the activity of NADPH oxidase, the accumulation of reactive oxygen species (ROS) and energy metabolism, seeking to identify both proteins and broader cellular metabolism influences on diapause regulation. We found that under short photoperiod conditions PTP1B in female adults induces egg diapause, whereas PTK in female adults inhibits egg diapause. Intriguingly, we also found that the antioxidant enzyme Prx V is a negative regulator of NADPH oxidizing reaction and apparently decreases ROS production and NADPH-OX activity. In contrast, all the eggs laid by adults that were treated with a series of knockdown or purified-protein injection experiments or inhibitor studies and that were reared under long photoperiod conditions hatched successfully. Thus, our results suggest a mechanism wherein diapause-related proteins (PTP1B, PTK, and Prx V) of female adults are the upstream modulators that regulate offspring eggs’ diapause process through the insulin-like signaling pathway under short photoperiod conditions.https://www.mdpi.com/2075-4450/12/3/253insulin-like signalingPI3KAktembryo diapauseinsectdiapause related protein
spellingShingle Shuang Li
Jie Wang
Dongnan Cui
Kun Hao
Jun Chen
Xiongbing Tu
Zehua Zhang
Antagonism between PTP1B and PTK Mediates Adults’ Insulin-Like Signaling Regulation of Egg Diapause in the Migratory Locust
Insects
insulin-like signaling
PI3K
Akt
embryo diapause
insect
diapause related protein
title Antagonism between PTP1B and PTK Mediates Adults’ Insulin-Like Signaling Regulation of Egg Diapause in the Migratory Locust
title_full Antagonism between PTP1B and PTK Mediates Adults’ Insulin-Like Signaling Regulation of Egg Diapause in the Migratory Locust
title_fullStr Antagonism between PTP1B and PTK Mediates Adults’ Insulin-Like Signaling Regulation of Egg Diapause in the Migratory Locust
title_full_unstemmed Antagonism between PTP1B and PTK Mediates Adults’ Insulin-Like Signaling Regulation of Egg Diapause in the Migratory Locust
title_short Antagonism between PTP1B and PTK Mediates Adults’ Insulin-Like Signaling Regulation of Egg Diapause in the Migratory Locust
title_sort antagonism between ptp1b and ptk mediates adults insulin like signaling regulation of egg diapause in the migratory locust
topic insulin-like signaling
PI3K
Akt
embryo diapause
insect
diapause related protein
url https://www.mdpi.com/2075-4450/12/3/253
work_keys_str_mv AT shuangli antagonismbetweenptp1bandptkmediatesadultsinsulinlikesignalingregulationofeggdiapauseinthemigratorylocust
AT jiewang antagonismbetweenptp1bandptkmediatesadultsinsulinlikesignalingregulationofeggdiapauseinthemigratorylocust
AT dongnancui antagonismbetweenptp1bandptkmediatesadultsinsulinlikesignalingregulationofeggdiapauseinthemigratorylocust
AT kunhao antagonismbetweenptp1bandptkmediatesadultsinsulinlikesignalingregulationofeggdiapauseinthemigratorylocust
AT junchen antagonismbetweenptp1bandptkmediatesadultsinsulinlikesignalingregulationofeggdiapauseinthemigratorylocust
AT xiongbingtu antagonismbetweenptp1bandptkmediatesadultsinsulinlikesignalingregulationofeggdiapauseinthemigratorylocust
AT zehuazhang antagonismbetweenptp1bandptkmediatesadultsinsulinlikesignalingregulationofeggdiapauseinthemigratorylocust